Clinical Review & Education
Review
Modern Multidisciplinary Perioperative Management of Rectal Cancer Mariana Berho, MD; Rahul Narang, MD; Julie Ann M. Van Koughnett, MD, MEd; Steven D. Wexner, MD, PhD(Hon)
IMPORTANCE The management of care for rectal cancer has undergone many changes and
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improvements in recent decades. A multidisciplinary approach to this complex disease is essential to ensure high-quality treatment and outcomes. OBJECTIVE To present a current, evidence-based approach to the multidisciplinary team management of rectal cancer with a review of the diagnosis, staging, and treatment of the disease by radiologists, oncologists, surgeons, and pathologists. EVIDENCE REVIEW The literature review was conducted through online searches of MEDLINE
and PubMed. Articles published between January 1, 2000, and June 2014 and pertaining to staging modalities, surgical approaches, pathologic assessment, and medical treatments of rectal cancer were considered. All studies were reviewed, with preferential inclusion of larger or randomized trials. The review focused on changing paradigms and current controversies in rectal cancer management. FINDINGS A multidisciplinary approach to the patient with rectal cancer includes many health care professionals. Although treatments continue to evolve and improve, clear evidence-based principles have been well studied. The important roles of various specialists must be acknowledged and utilized. Within each role, new and emerging treatment approaches require critical review by experts in their fields. CONCLUSIONS AND RELEVANCE Many new technologies and treatment options will continue to advance the treatment of rectal cancer, further emphasizing the need for a multidisciplinary approach to achieve optimal care.
Corresponding Author: Steven D. Wexner, MD, PhD(Hon), Digestive Disease Center, Cleveland Clinic Florida, 2950 Cleveland Clinic Blvd, Weston, FL 33331 ([email protected]).
JAMA Surg. 2015;150(3):260-266. doi:10.1001/jamasurg.2014.2887 Published online January 28, 2015.
T
he pivotal work of Sir Ernest Miles in 1908 revolutionized the surgical treatment of rectal cancer. However, this was only possible in large part owing to the advances in other disciplines, including anesthesia, anatomy, pathology, and the understanding of sepsis and antisepsis (eAppendix in the Supplement).1 Although every physician seeks to provide patients with the best possible care, unilateral medical decisions may be influenced by personal perceptions and often lack an evidence-based rationale. The first organized attempt to measure the effect of a multispecialty group was successfully undertaken in the United Kingdom for breast cancer. Kesson and colleagues2 demonstrated that patients with breast cancer who were receiving the care of a multidisciplinary team had better outcomes. This benefit persisted after adjustment for age, cancer stage, and access to health care. Burton et al3 showed that multidisciplinary review of imaging in patients with colorectal cancer resulted in improved staging and curative resection rates. The surgeon no longer carries the sole responsibility of deciding the appropriate therapy; instead, medical care relies on a group of experts, including surgeons, radiotherapy oncologists, medical oncologists, and pathologists. The various components and roles of the 260
Author Affiliations: Department of Pathology and Laboratory Medicine, Cleveland Clinic Florida, Weston (Berho); Digestive Disease Center, Cleveland Clinic Florida, Weston (Narang, Van Koughnett, Wexner).
multidisciplinary team in rectal cancer are summarized in the Table. This review is focused on changing paradigms in the management of rectal cancer, with emphasis on the importance of the multidisciplinary team on achieving optimal oncologic outcomes. A literature review of MEDLINE and PubMed was conducted, and highquality studies were selected for inclusion. Articles published between January 1, 2000, and June 2014 and pertaining to staging modalities, surgical approaches, pathologic assessment, and medical treatments of rectal cancer were considered. All studies were reviewed, with preferential inclusion of larger or randomized trials.
Role of the Radiologist The American Society of Clinical Oncology guidelines to preoperatively stage rectal cancer require examination using colonoscopy; contrast-enhanced computed tomography of the abdomen, pelvis, and chest; and serum carcinoembryonic antigen level.4 A complete colonoscopy should be performed to evaluate the tumor location and identify and treat any synchronous lesions. The incidence
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Table. Multidisciplinary Team for Perioperative Management of Rectal Cancer Characteristic
Surgeon
Radiologist
Oncologist
Endoscopist/Primary Care Physician
Pathologist
•
•
Allied Healtha
Diagnosis
•
Staging
•
Preoperative planning
•
•
•
•
Preoperative counseling
•
•
•
•
•
Neoadjuvant treatmentb •
Specimen evaluation
•
Postoperative management
•
• •
Adjuvant therapyb
•
•
• •
a
Includes office coordinators and stoma nurses.
b
If applicable.
•
•
of synchronous cancers ranges from 1% to 3%, and the incidence of synchronous polyps is approximately 30%.5 If colonoscopy cannot be performed, alternative means of imaging (ie, contrast enema or computed tomography colonography) should be performed. Digital rectal examination alone is not enough to assess the location and degree of fixation (and, by extension, tumor invasion). Digital rectal examination for low rectal lesions is largely inaccurate in assessing the location of the lesion relative to the anal verge.6 Digital rectal examination has been shown6 to have only 65% agreement with the pathologic specimen when predicting tumor characteristics. Carcinoembryonic antigen levels should be recorded, although high preoperative levels are not an independent indication for adjuvant treatment. Staging modalities to evaluate the primary rectal tumor have 4 objectives: assessment of tumor depth within the wall of the rectum (T stage), examination of lymph node status (N stage), detection of metastatic disease (M stage), and determination of the distance of the tumor from the circumferential resection margin (CRM). Magnetic resonance imaging (MRI) and endorectal ultrasonography (ERUS) can determine the accurate depth of tumor penetration in 60% to 92% of patients.7 The advantages of one of these methods over the other have been the subject of debate.8 Magnetic resonance imaging is very accurate in predicting T stage, with agreements with pathologic staging well above 80%.9 The primary role of MRI in staging is to assess the CRM. The importance of CRM status was presented by the Magnetic Resonance Imaging and Rectal Cancer European Equivalence (MERCURY) study as a predictor of recurrence and need for neoadjuvant therapy.10 The results showed that CRM-involved tumors identified by MRI had lower 5-year disease-free and recurrence-free survivals.11 In addition, CRM involvement was associated with metastatic disease.11 A positive CRM identified in the pathologic specimen is associated with local and distant recurrence as well as lower overall and disease-free survival.12,13 A negative margin of only 1 to 2 mm has recurrence and survival benefits.13 Magnetic resonance imaging has a specificity of 94% in predicting CRM involvement.14 Endorectal ultrasonography can be performed in the office setting and has been shown15 to have an overall accuracy of 87% in predicting T stage. A prospective Scandinavian study16 found T-stage accuracy to be slightly lower at 74% and N-stage accuracy to be 65%. The sensitivity of perirectal tissue invasion was higher at 82%. Garciajamasurgery.com
•
•
Surgery
Surveillance
•
•
Aguilar et al17 found overall accuracy of ERUS to be 69% for T stage, finding 18% of the tumors to be overstaged and 13% to be understaged. Overstaging resulted from difficulties in differentiating perirectal fat inflammation from tumor infiltration. Brown and colleagues18 found the agreement of ERUS and pathologic staging to be 69% and advocated for the use of MRI in its place. Although both modalities depend on reader interpretation, ERUS is more operator dependent in its accuracy and MRI is the preferred local staging modality. Unfortunately, the positive predictive value of MRI and ERUS in detecting positive lymph nodes is only approximately 60%.9 This low level of accuracy has led some surgeons to advocate for complementary use of both ERUS and MRI.19 A survey by the International Rectal Cancer Study Group20 found very poor agreement on the best staging regimen among surgeons performing rectal cancer surgery. However, the recent introduction of high-resolution phasedarray MRI along with fast spin-echo T2-weighted sequencing has significantly improved preoperative imaging.21 In addition, highresolution MRI is exceptionally sensitive and specific in detecting extramural vascular invasion, which is an independent prognostic marker. In addition, computed tomography or positron emission tomography imaging can exclude distant metastatic disease. Thus, MRI has replaced ERUS as the preferred local staging modality.
Role of the Oncologist Patients with locally advanced distal rectal cancer are candidates for neoadjuvant treatment. Two Cochrane Database reviews22,23 concluded that there is a reduction in local recurrence after chemoradiotherapy vs radiotherapy alone for stage II and stage III rectal cancer (odds ratios, 0.39-0.72). Neither review found a significant difference in overall survival, sphincter preservation, or anastomotic leaks. If MRI reveals a negative CRM, neoadjuvant treatment may not be needed, as demonstrated in the MERCURY study. The decision as to whether neoadjuvant treatment is needed must be individualized to each patient and depends on agreement between the multidisciplinary team members.11 After neoadjuvant treatment for locally advanced rectal cancer, when should surgery be performed? Traditionally, rectal cancer trials have used a 6- to 8-week interval between the last radio(Reprinted) JAMA Surgery March 2015 Volume 150, Number 3
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therapy session and surgery. A randomized trial24 comparing 4-week with 8-week intervals in node-negative rectal cancers did not find a significant advantage to waiting longer before surgery. However, prolonging the interval may result in increased tumor regression prior to surgery. Påhlman25 reviewed wait-time intervals and found that tumor regression, sphincter preservation, local recurrence, and overall survival were not different with time intervals of less than or greater than 41 days. Habr-Gama et al26 found no statistically significant differences in 5-year overall or disease-free survival between patients according to time to surgery (ⱕ12 vs >12 weeks). A recent systematic review27 found that, in studies reporting complete pathologic response after chemoradiotherapy, 4 of 7 studies found higher rates of complete pathologic response after longer intervals. This result was confirmed in a meta-analysis28 reporting that the complete pathologic response rates increased from 13.7% to 19.5% when the interval was longer than 6 to 8 weeks. Additional studies are needed to delineate the ideal interval and to predict which patients may benefit from a longer interval. Nevertheless, the time between the completion of neoadjuvant therapy and surgery appears to be getting longer.
Role of the Surgeon When possible, a restorative proctectomy should be performed without jeopardizing oncologic integrity. To help optimize function, a stapled anastomosis should be performed if the anastomosis does not require a mucosectomy or intersphincteric dissection. The types of reconstruction performed for a restorative distal anastomosis include an end-to-side (Baker) anastomosis, colonic J pouch, coloplasty, and straight coloanal anastomosis. Multiple series29 have clearly demonstrated that the colonic J pouch confers better functional results with fewer bowel movements and less incontinence 1 year after surgery. However, longer-term sustainment of these benefits varies in the literature.30 A colonic J pouch should be no longer than 6 to 8 cm per limb to provide good function. Coloplasty and end-to-side anastomoses are also alternatives to a straight anastomosis. Comparisons of colonic J pouch with transverse coloplasty have found minimal differences in functional outcomes but have found coloplasty to have a statistically significantly higher complication rate.31 In addition, the colonic J pouch provides faster recovery of function after surgery than does the transverse coloplasty.32 A 2008 systematic review33 concluded that, although the colonic J pouch was superior to a straight anastomosis in most studies, larger studies were required to better define the roles of the end-to-side and transverse coloplasty. However, in practical terms and pending such studies, the colonic J pouch has been much more widely clinically used, whereas the coloplasty has been largely abandoned. However, end-to-side anastomosis seems to be experiencing a surge in popularity as an alternate technique. There are risks and benefits of a diverting stoma at the time of rectal cancer resection. A database review34 of the American College of Surgeons’ National Surgical Quality Improvement Project found that a stoma resulted in a higher incidence of acute renal failure but protected the patient from postoperative sepsis and need for reoperation. Most studies35 describe a decreased anastomotic leak rate with diverting stoma as well as a decreased need for reoperation to repair an anastomotic leak. A meta-analysis 36 per262
formed in 2009 showed overall benefit of an ileostomy over a colostomy. Ileostomy was associated with less sepsis and fewer stoma complications, although it carried a higher risk of dehydration. Detailed patient instructions and postoperative follow-up are needed for the patient with fecal diversion, but overall the risk of morbidity of an anastomotic leak and delayed adjuvant chemotherapy usually outweigh the risk of fecal diversion. Early nonrandomized studies found that oncologic surgical outcomes were comparable between open and laparoscopic surgery for rectal cancer. Laparoscopy is associated with less blood loss, quicker return of bowel function, and shorter hospital stay.37 In addition, early postoperative quality of life was repeatedly demonstrated to be superior after laparoscopic rectal cancer resection.38 Even in laparoscopic converted to open cases, oncologic outcomes are equivalent to those of open cases.39 Results of randomized trials40,41 have also shown equivalent oncologic outcomes, less blood loss, and faster recovery findings at the expense of only longer operative times. Sexual, bladder, and anal sphincter function may be adversely affected after proctectomy. The risk of fecal incontinence depends mainly on the tumor level and height of the anastomosis. Morino et al42 evaluated male sexual and urinary function after laparoscopic total mesorectal excision (TME) and found that sexual desire was maintained in 55.6% of the patients and the ability to engage in intercourse was maintained in 57.8% of the patients. The role of robotic-assisted surgery is unclear, and pelvic dissection is believed by many to be the best use for the roboticassisted approach in colorectal surgery. Robotic-assisted proctectomy has been shown43 to be a safe alternative with similar oncologic outcomes and morbidities. However, it is also associated with increased cost and longer operative times.44 Although laparoscopic and robotic-assisted surgery have benefits over open proctectomy for rectal cancer, the robotic approach has failed to demonstrate any significant advantage while the several above-cited disadvantages have been repeatedly and clearly demonstrated. Transanal excision and transanal endoscopic surgery (TES) have been used for early rectal cancers. The advent of TES platforms in particular has improved the surgeon’s ability to perform a complete one-piece resection with wide margins. Transanal endoscopic surgery does not carry the morbidity of a transabdominal resection. Numerous studies45,46 have shown that for carefully selected patients with favorable T1 and perhaps T2 lesions with very low risk features, various TES platforms can achieve clear margins, good oncologic outcomes, and low morbidity. The main concern with TES for rectal cancer is that lymphadenectomy is not performed, leaving the patient with up to a 25% chance of retained lymph node metastasis in T2 lesions.47 Cancer recurrence after local resection ranges between 4% and 18% for T1 lesions and 27% to 67% for T2 lesions after TES.48 To reduce the risk of local recurrence, various studies are investigating the role of radiotherapy and/or chemotherapy. The Alliance Z6041 and Transanal Endoscopic Microsurgery and Radiotherapy in Early Rectal Cancer trials are underway to determine the best treatment plan for locally excisable tumors. Results from trials49,50 using conventional neoadjuvant chemoradiotherapy followed by TES show good overall oncologic and survival outcomes. Although long-term data are not yet available, an even newer approach is transanal endoscopic TME combined with laparoscopic assistance.51 In pa-
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tients who have undergone this procedure, results show complete mesorectal excision with negative margins and no intraoperative complications.51 Although more data are needed, this hybrid technique may shift the paradigm in upcoming years. A complete clinical response will be noted in approximately 10% of patients during subsequent physical examination and restaging after neoadjuvant treatment. Habr-Gama and colleagues52 in Brazil have written extensively on the watch-and-wait approach, in which the patient does not proceed to surgical resection but rather undergoes regimented close monitoring for recurrent disease. The investigators have also found that, with an extended course of chemoradiotherapy with additional fluorouracil and leucovorin calcium, many patients with T2-T4/N0 distal rectal cancer were able to avoid surgery. With close monitoring, salvage surgery was possible in 90% of the patients with local recurrence.53 The nonoperative approach after complete clinical response has become more accepted in a greater number of centers as further data from around the world have become available. With the watch-and-wait approach, careful patient selection and close monitoring using digital rectal examination, proctoscopy, carcinoembryonic antigen levels, computed tomography and/or MRI, and biopsies of suspicious lesions is recommended. Recurrent disease should be treated with surgical resection. Routine scar biopsies are not recommended because they have a negative predictive value of 11%.54 In a study of rectal cancer pathologic specimens of patients who received chemoradiotherapy followed by proctectomy, 25% of the specimens were pathologic tumor stage 0.55 However, 74% of these specimens had a visible mucosal lesion and therefore were not deemed a complete clinical response.55 Patients must be aware of the potential risks and benefits of the watch-and-wait approach in the setting of complete clinical response and understand that surgical resection is, at this time, still the standard of care. Nonetheless, there are undoubtedly good candidates for the watchand-wait approach. The challenges are in correctly identifying these patients and ensuring appropriate follow-up evaluations for them. It has long been known that surgeon volume and specialization in colorectal surgery affects practice patterns. A 1998 study56 found that colorectal-trained surgeons treated more mid and distal rectal tumors and yet performed significantly fewer abdominoperineal resections than did surgeons without colorectal training who treat rectal cancer (27% vs 47% abdominoperineal resections, respectively). A recent Cochrane Database57 review concluded that surgeons with higher volumes and colorectal training had better 5-year survival outcomes, lower postoperative mortality, and lower rates of permanent stomas. In the United States, a database study found that 39% of surgeons performing proctectomies performed only abdominoperineal resections, and surgeons who completed both nonrestorative and restorative proctectomies had better patient outcomes.58 Specialization and regionalization of care are controversial in many areas within surgery, and rectal cancer treatment is no exception.
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sitivity to neoadjuvant radiotherapy and chemotherapy. Intraoperative frozen sections are occasionally performed at the request of the surgeon.Traditionally,pathologictumorandnodalstageswerethesole predictors of outcomes; however, several studies59 have concluded that the integrity of the mesorectum is an independent prognostic factor of both disease-free and overall survival. The quality of the mesorectum is assessed by the pathologist and can be divided into complete (intact with minimal irregularities), near complete (defects >5 mm but without exposure of the muscularis propria), and incomplete (deep defects in the mesorectal fat that expose the muscularis propria).60 The pathologist is responsible for providing accurate and unbiased feedback to the surgeon and oncologist. Several studies61,62 have shown that a complete or near-complete pathologic response (few residual malignant cells in the surgical specimen) correlates with better outcomes; therefore, it is imperative that the tumor regression grade is documented in the pathologist’s report. In addition to the assessment of the mesorectal quality, the margins of resection should be recorded. The acceptable length of the distal resection margin for rectal cancer has been a matter of debate during the past decade. The desire for a restorative proctectomy has resulted in studies that challenged the traditional 2-cm rule for rectal cancer. Initial studies63 indicated that a distal margin of 1 cm or more provided the same survival and local recurrence estimates as a 2-cm margin. Subsequent studies64 have demonstrated that a subcentemeric margin, as low as 5 mm, did not affect local recurrence or survival outcomes. In addition to adequate proximal and distal margins, the importance of the circumferential margin in predicting recurrence cannot be overstated. The criterion standard of 12 lymph nodes used on colon cancer pathologic specimens as a marker of adequate surgical resection may not apply for rectal cancer. Studies65,66 have demonstrated that fewer lymph nodes are found in specimens after neoadjuvant chemoradiotherapy compared with surgery alone. A recent study67 of the Surveillance, Epidemiology, and End Results database found that, to prevent stage migration of the proctectomy specimen, 18 and 16 lymph nodes were needed in patients undergoing surgery alone and neoadjuvant treatment followed by surgery, respectively. One way to improve lymph node yield is through surgical technique and proper TME. Laparoscopic TME, for example, has been shown68 to significantly increase lymph node yield compared with the open approach. High ligation of the inferior mesentery artery ensures clearance of its associated lymph nodes, which negatively affect survival if positive for malignancy.69 In addition, improved fat clearance and lymph node–revealing solutions improve lymph node yield when used by pathologists.70 Lymph node assessment in the rectum tends to be more challenging since the mesorectal nodes are smaller, and preoperative radiotherapy leads to a decreased number of perirectal lymph nodes.71 The use of cancer synoptic reports is strongly recommended because they standardize reporting of data and avoid omission of important information.
Role of the Pathologist
Working Together: Effect of the Multidisciplinary Team
Confirmation of malignancy on tissue biopsies prior to a radical cancer operation is essential. In addition, although not yet a standard of care, preoperative tissue may be used in the future to test tumor sen-
The responsibility of all physicians treating rectal cancer is to coordinate care to optimize survival while minimizing morbidity and maximizingqualityoflife.TheNationalInstituteforClinicalExcellenceinLon-
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don published guidelines to help organize multidisciplinary care.72 The multidisciplinary approach has been well studied and validated for breast cancer. Frost et al73 evaluated patients with newly diagnosed breast cancer and found that those who received a multidisciplinary approachtotreatmenthadhigherlevelsofphysicalfunction(P = .003) and satisfaction with their health (P < .01), physician (P < .001), and nursing care (P = .004). In addition, breast cancer–related mortality decreased after multidisciplinary care was established.2 Implementation of multidisciplinary teams in rectal cancer has resulted in improved postoperative mortality in Denmark74 and Spain.75 To improve rectal cancer care, many European countries have set strict national guidelines to regionalize rectal cancer care to centers of excellence, resulting in better short- and long-term outcomes.76 In England, rectal cancer care is centralized with surgical techniques standardization and multidisciplinary tumor boards. Similar efforts in Scandinavian countries have resulted in more patients undergoing TME, reduced local recurrence, and improved 5-year survival.77,78 The Consortium for Optimizing Surgical Treatment of Rectal Cancer (OSTRiCh) group is seeking to improve the quality of rectal cancer care delivery in the United States in a similar manner.76,79 The principles of the group include TME, pathologic assessment of surgical quality, effective use of imaging, evidencebased use of medical and radiotherapy oncology in addition to surgery, and the multidisciplinary team approach. The OSTRiCh group has demonstrated wide variability in both treatment and outcome of rectal cancer in the United States. In addition to the efforts of the OSTRiCh group, the American College of Surgeons’ Commission on Cancer accredits more than 1500 cancer programs nationwide to provide state-of-the-art pretreatment evaluation, staging, treatment, and clinical follow-up for patients with cancer. The OSTRiCh group has been working in collaboration with the Commission on Cancer and the American College of Surgeons to implement accreditation programs for rectal cancer surgery in the USA. ARTICLE INFORMATION Accepted for Publication: August 26, 2014. Published Online: January 28, 2015. doi:10.1001/jamasurg.2014.2887. Author Contributions: Drs Berho and Wexner had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: All authors. Acquisition, analysis, or interpretation of data: All authors. Drafting of the manuscript: All authors. Critical revision of the manuscript for important intellectual content: All authors. Administrative, technical, or material support: Van Koughnett, Wexner. Study supervision: Wexner. Conflict of Interest Disclosures: None reported. REFERENCES 1. Miles WE. A method of performing abdomino-perineal excision for carcinoma of the rectum and of the terminal portion of the pelvic colon. Lancet. 1908;2:1812-1813. 2. Kesson EM, Allardice GM, George WD, Burns HJ, Morrison DS. Effects of multidisciplinary team working on breast cancer survival: retrospective,
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It is essential that patients with newly diagnosed rectal cancer undergo thorough preoperative counseling. Mayo et al80 reported on a randomized trial comparing 2 “prehabilitation” programs; patients who did well during prehabilitation were more likely to recover postoperatively to their baseline function. Patients should also be counseled by the enterostomal therapist about a potential ostomy, including proper care, management of high output, and quality-of-life expectations.
Conclusions The treatment of rectal cancer has made significant gains in recent decades. To achieve optimal outcomes, the team of health care workers and the patient must be aware of shifting paradigms in the standard of care (eTable in the Supplement). Preoperative local staging with MRI and/or ERUS will provide essential information on both the type of surgery needed and the role of neoadjuvant chemoradiation. Important studies continue to be conducted on minimally invasive approaches to expedite recovery without compromising oncologic outcomes. Local excision and the watch-and-wait approach appear to be safe, but patient selection is essential. The multidisciplinary care of the patient with rectal cancer must include the surgeon, pathologist, oncologist, radiologist, and endoscopist/ primary care physician in the pursuit of excellence in rectal cancer outcomes. The advantages of multidisciplinary care are clear, and a specialized team is essential given the complexity of the many facets of rectal cancer care. Positive results can be achieved if the OSTRiCh group, working with the American College of Surgeons, College of American Pathologists, American College of Radiology, and Commission on Cancer, can introduce the same multidisciplinary rectal cancer centers of excellence program in North America that has so greatly benefitted patients in Europe.
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3. Burton S, Brown G, Daniels IR, Norman AR, Mason B, Cunningham D; Royal Marsden Hospital, Colorectal Cancer Network. MRI directed multidisciplinary team preoperative treatment strategy: the way to eliminate positive circumferential margins? Br J Cancer. 2006;94(3): 351-357.
9. Park JS, Jang YJ, Choi GS, et al. Accuracy of preoperative MRI in predicting pathology stage in rectal cancers: node-for-node matched histopathology validation of MRI features. Dis Colon Rectum. 2014;57(1):32-38.
4. National Comprehensive Cancer Network Guidelines, version 2013: rectal cancer. 2012. http://www.nccn.org/professionals/physician_gls/f _guidelines.asp. Accessed December 12, 2014. 5. Barillari P, Ramacciato G, De Angelis R, et al. Effect of preoperative colonoscopy on the incidence of synchronous and metachronous neoplasms. Acta Chir Scand. 1990;156(2):163-166. 6. Brown G, Davies S, Williams GT, et al. Effectiveness of preoperative staging in rectal cancer: digital rectal examination, endoluminal ultrasound or magnetic resonance imaging? Br J Cancer. 2004;91(1):23-29. 7. Schaffzin DM, Wong WD. Endorectal ultrasound in the preoperative evaluation of rectal cancer. Clin Colorectal Cancer. 2004;4(2):124-132. 8. Bipat S, Glas AS, Slors FJ, Zwinderman AH, Bossuyt PM, Stoker J. Rectal cancer: local staging and assessment of lymph node involvement with
10. Taylor FG, Quirke P, Heald RJ, et al; MERCURY study group. Preoperative high-resolution magnetic resonance imaging can identify good prognosis stage I, II, and III rectal cancer best managed by surgery alone: a prospective, multicenter, European study. Ann Surg. 2011;253(4):711-719. 11. Taylor FG, Quirke P, Heald RJ, et al; Magnetic Resonance Imaging in Rectal Cancer European Equivalence Study Study Group. Preoperative magnetic resonance imaging assessment of circumferential resection margin predicts disease-free survival and local recurrence: 5-year follow-up results of the MERCURY study. J Clin Oncol. 2014;32(1):34-43. 12. Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer? J Clin Oncol. 2008;26(2):303-312. 13. Trakarnsanga A, Gonen M, Shia J, et al. What is the significance of the circumferential margin in
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locally advanced rectal cancer after neoadjuvant chemoradiotherapy? Ann Surg Oncol. 2013;20(4): 1179-1184. 14. Al-Sukhni E, Milot L, Fruitman M, et al. Diagnostic accuracy of MRI for assessment of T category, lymph node metastases, and circumferential resection margin involvement in patients with rectal cancer: a systematic review and meta-analysis. Ann Surg Oncol. 2012;19(7): 2212-2223. 15. Xu D, Ju HX, Qian CW, Jiang F. The value of TRUS in the staging of rectal carcinoma before and after radiotherapy and comparison with the staging postoperative pathology. Clin Radiol. 2014;69(5): 481-484. 16. Nesbakken A, Løvig T, Lunde OC, Nygaard K. Staging of rectal carcinoma with transrectal ultrasonography. Scand J Surg. 2003;92(2): 125-129. 17. Garcia-Aguilar J, Pollack J, Lee SH, et al. Accuracy of endorectal ultrasonography in preoperative staging of rectal tumors. Dis Colon Rectum. 2002;45(1):10-15. 18. Brown G. Staging rectal cancer: endoscopic ultrasound and pelvic MRI. Cancer Imaging. 2008;8 (special issue A):S43-S45. 19. Samdani T, Garcia-Aguilar J. Imaging in rectal cancer: magnetic resonance imaging versus endorectal ultrasonography. Surg Oncol Clin N Am. 2014;23(1):59-77. 20. Augestad KM, Lindsetmo RO, Stulberg J, et al; International Rectal Cancer Study Group (IRCSG). International preoperative rectal cancer management: staging, neoadjuvant treatment, and impact of multidisciplinary teams. World J Surg. 2010;34(11):2689-2700. 21. Curvo-Semedo L, Lambregts DM, Maas M, Beets GL, Caseiro-Alves F, Beets-Tan RG. Diffusion-weighted MRI in rectal cancer: apparent diffusion coefficient as a potential noninvasive marker of tumor aggressiveness. J Magn Reson Imaging. 2012;35(6):1365-1371. 22. De Caluwé L, Van Nieuwenhove Y, Ceelen WP. Preoperative chemoradiation versus radiation alone for stage II and III resectable rectal cancer [update of Cochrane Database Syst Rev. 2009;(1): CD006041]. Cochrane Database Syst Rev. 2013;2: CD006041. 23. McCarthy K, Pearson K, Fulton R, Hewitt J. Pre-operative chemoradiation for non-metastatic locally advanced rectal cancer. Cochrane Database Syst Rev. 2012;12:CD008368. doi:10.1002 /14651858.CD008368.pub2. 24. Saglam S, Bugra D, Saglam EK, et al. Fourth versus eighth week surgery after neoadjuvant radiochemotherapy in T3-4/N0+ rectal cancer: Istanbul R-01 study. J Gastrointest Oncol. 2014;5(1): 9-17. 25. Påhlman L. Optimal timing of surgery after preoperative chemoradiotherapy for rectal cancer. Nat Clin Pract Oncol. 2009;6(3):128-129. 26. Habr-Gama A, Perez RO, Proscurshim I, et al. Interval between surgery and neoadjuvant chemoradiation therapy for distal rectal cancer: does delayed surgery have an impact on outcome? Int J Radiat Oncol Biol Phys. 2008;71(4):1181-1188. 27. Foster JD, Jones EL, Falk S, Cooper EJ, Francis NK. Timing of surgery after long-course neoadjuvant chemoradiotherapy for rectal cancer:
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a systematic review of the literature. Dis Colon Rectum. 2013;56(7):921-930. 28. Petrelli F, Sgroi G, Sarti E, Barni S. Increasing the interval between neoadjuvant chemoradiotherapy and surgery in rectal cancer: a meta-analysis of published studies [published online November 3, 2013]. Ann Surg. doi:10.1097 /SLA.0000000000000368. 29. Heriot AG, Tekkis PP, Constantinides V, et al. Meta-analysis of colonic reservoirs versus straight coloanal anastomosis after anterior resection. Br J Surg. 2006;93(1):19-32. 30. Joo JS, Latulippe JF, Alabaz O, Weiss EG, Nogueras JJ, Wexner SD. Long-term functional evaluation of straight coloanal anastomosis and colonic J-pouch: is the functional superiority of colonic J-pouch sustained? Dis Colon Rectum. 1998; 41(6):740-746. 31. Biondo S, Frago R, Codina Cazador A, et al. Long-term functional results from a randomized clinical study of transverse coloplasty compared with colon J-pouch after low anterior resection for rectal cancer. Surgery. 2013;153(3):383-392. 32. Jiang JK, Yang SH, Lin JK. Transabdominal anastomosis after low anterior resection: a prospective, randomized, controlled trial comparing long-term results between side-to-end anastomosis and colonic J-pouch. Dis Colon Rectum. 2005;48(11):2100-2108. 33. Brown CJ, Fenech DS, McLeod RS. Reconstructive techniques after rectal resection for rectal cancer. Cochrane Database Syst Rev. 2008; (2):CD006040.
II (COLOR II) Study Group. Laparoscopic versus open surgery for rectal cancer (COLOR II): short-term outcomes of a randomised, phase 3 trial. Lancet Oncol. 2013;14(3):210-218. 42. Morino M, Allaix ME, Giraudo G, Corno F, Garrone C. Laparoscopic versus open surgery for extraperitoneal rectal cancer: a prospective comparative study. Surg Endosc. 2005;19(11): 1460-1467. 43. Xiong B, Ma L, Zhang C, Cheng Y. Robotic versus laparoscopic total mesorectal excision for rectal cancer: a meta-analysis. J Surg Res. 2014;188 (2):404-414. 44. Scarpinata R, Aly EH. Does robotic rectal cancer surgery offer improved early postoperative outcomes? Dis Colon Rectum. 2013;56(2):253-262. 45. Lezoche G, Guerrieri M, Baldarelli M, et al. Transanal endoscopic microsurgery for 135 patients with small nonadvanced low rectal cancer (iT1-iT2, iN0): short- and long-term results. Surg Endosc. 2011;25(4):1222-1229. 46. Albert MR, Atallah SB, deBeche-Adams TC, Izfar S, Larach SW. Transanal minimally invasive surgery (TAMIS) for local excision of benign neoplasms and early-stage rectal cancer: efficacy and outcomes in the first 50 patients. Dis Colon Rectum. 2013;56(3):301-307. 47. Sengupta S, Tjandra JJ. Local excision of rectal cancer: what is the evidence? Dis Colon Rectum. 2001;44(9):1345-1361. 48. Paty PB, Nash GM, Baron P, et al. Long-term results of local excision for rectal cancer. Ann Surg. 2002;236(4):522-529.
34. Nurkin S, Kakarla VR, Ruiz DE, Cance WG, Tiszenkel HI. The role of faecal diversion in a low rectal cancer: a review of 1791 patients having rectal resection with anastomosis for cancer, with and without a proximal stoma. Colorectal Dis. 2013;15 (6):e309-e316. doi:10.1111/codi.12248.
49. Lezoche E, Baldarelli M, Lezoche G, Paganini AM, Gesuita R, Guerrieri M. Randomized clinical trial of endoluminal locoregional resection versus laparoscopic total mesorectal excision for T2 rectal cancer after neoadjuvant therapy. Br J Surg. 2012; 99(9):1211-1218.
35. Seo SI, Yu CS, Kim GS, et al. The role of diverting stoma after an ultra-low anterior resection for rectal cancer. Ann Coloproctol. 2013;29(2):66-71.
50. Pucciarelli S, De Paoli A, Guerrieri M, et al. Local excision after preoperative chemoradiotherapy for rectal cancer: results of a multicenter phase II clinical trial. Dis Colon Rectum. 2013;56(12):1349-1356.
36. Rondelli F, Reboldi P, Rulli A, et al. Loop ileostomy versus loop colostomy for fecal diversion after colorectal or coloanal anastomosis: a meta-analysis. Int J Colorectal Dis. 2009;24(5): 479-488. 37. Seshadri RA, Srinivasan A, Tapkire R, Swaminathan R. Laparoscopic versus open surgery for rectal cancer after neoadjuvant chemoradiation: a matched case-control study of short-term outcomes. Surg Endosc. 2012;26(1):154-161. 38. Ng SS, Leung WW, Wong CY, et al. Quality of life after laparoscopic vs open sphincter-preserving resection for rectal cancer. World J Gastroenterol. 2013;19(29):4764-4773. 39. Keller DS, Khorgami Z, Swendseid B, et al. Laparoscopic and converted approaches to rectal cancer resection have superior long-term outcomes: a comparative study by operative approach. Surg Endosc. 2014;28(6):1940-1948. 40. Kang SB, Park JW, Jeong SY, et al. Open versus laparoscopic surgery for mid or low rectal cancer after neoadjuvant chemoradiotherapy (COREAN trial): short-term outcomes of an open-label randomised controlled trial. Lancet Oncol. 2010;11 (7):637-645. 41. van der Pas MH, Haglind E, Cuesta MA, et al; Colorectal Cancer Laparoscopic or Open Resection
51. de Lacy AM, Rattner DW, Adelsdorfer C, et al. Transanal natural orifice transluminal endoscopic surgery (NOTES) rectal resection: “down-to-up” total mesorectal excision (TME)—short-term outcomes in the first 20 cases. Surg Endosc. 2013; 27(9):3165-3172. 52. Habr-Gama A, Sabbaga J, Gama-Rodrigues J, et al. Watch and wait approach following extended neoadjuvant chemoradiation for distal rectal cancer: are we getting closer to anal cancer management? Dis Colon Rectum. 2013;56(10): 1109-1117. 53. Habr-Gama A, Gama-Rodrigues J, São Julião GP, et al. Local recurrence after complete clinical response and watch and wait in rectal cancer after neoadjuvant chemoradiation: impact of salvage therapy on local disease control. Int J Radiat Oncol Biol Phys. 2014;88(4):822-828. 54. Perez RO, Habr-Gama A, Pereira GV, et al. Role of biopsies in patients with residual rectal cancer following neoadjuvant chemoradiation after downsizing: can they rule out persisting cancer? Colorectal Dis. 2012;14(6):714-720. 55. Smith FM, Wiland H, Mace A, Pai RK, Kalady MF. Clinical criteria underestimate complete pathological response in rectal cancer treated with
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neoadjuvant chemoradiotherapy. Dis Colon Rectum. 2014;57(3):311-315. 56. Porter GA, Soskolne CL, Yakimets WW, Newman SC. Surgeon-related factors and outcome in rectal cancer. Ann Surg. 1998;227(2):157-167. 57. Archampong D, Borowski D, Wille-Jørgensen P, Iversen LH. Workload and surgeon’s specialty for outcome after colorectal cancer surgery. Cochrane Database Syst Rev. 2012;3:CD005391. doi:10.1002 /14651858.CD005391.pub3. 58. Ricciardi R, Roberts PL, Read TE, Baxter NN, Marcello PW, Schoetz DJ. Who performs proctectomy for rectal cancer in the United States? Dis Colon Rectum. 2011;54(10):1210-1215. 59. García-Granero E, Faiz O, Muñoz E, et al. Macroscopic assessment of mesorectal excision in rectal cancer: a useful tool for improving quality control in a multidisciplinary team. Cancer. 2009; 115(15):3400-3411. 60. Nagtegaal ID, van de Velde CJ, van der Worp E, Kapiteijn E, Quirke P, van Krieken JH; Cooperative Clinical Investigators of the Dutch Colorectal Cancer Group. Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control. J Clin Oncol. 2002;20 (7):1729-1734. 61. Yeo SG, Kim DY, Kim TH, et al. Pathologic complete response of primary tumor following preoperative chemoradiotherapy for locally advanced rectal cancer: long-term outcomes and prognostic significance of pathologic nodal status (KROG 09-01). Ann Surg. 2010;252(6):998-1004. 62. Topova L, Hellmich G, Puffer E, et al. Prognostic value of tumor response to neoadjuvant therapy in rectal carcinoma. Dis Colon Rectum. 2011;54(4): 401-411. 63. Moore HG, Riedel E, Minsky BD, et al. Adequacy of 1-cm distal margin after restorative rectal cancer resection with sharp mesorectal excision and preoperative combined-modality therapy. Ann Surg Oncol. 2003;10(1):80-85.
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64. Kiran RP, Lian L, Lavery IC. Does a subcentimeter distal resection margin adversely influence oncologic outcomes in patients with rectal cancer undergoing restorative proctectomy? Dis Colon Rectum. 2011;54(2):157-163. 65. Miller ED, Robb BW, Cummings OW, Johnstone PA. The effects of preoperative chemoradiotherapy on lymph node sampling in rectal cancer. Dis Colon Rectum. 2012;55(9):1002-1007. 66. Wang H, Safar B, Wexner S, Zhao R, Cruz-Correa M, Berho M. Lymph node harvest after proctectomy for invasive rectal adenocarcinoma following neoadjuvant therapy: does the same standard apply? Dis Colon Rectum. 2009;52(4): 549-557. 67. Bhangu A, Kiran RP, Brown G, Goldin R, Tekkis P. Establishing the optimum lymph node yield for diagnosis of stage III rectal cancer. Tech Coloproctol. 2014;18(8):709-717. 68. Boutros M, Hippalgaonkar N, Silva E, Allende D, Wexner SD, Berho M. Laparoscopic resection of rectal cancer results in higher lymph node yield and better short-term outcomes than open surgery: a large single-center comparative study. Dis Colon Rectum. 2013;56(6):679-688.
Improving Outcomes in Colorectal Cancers: Manual Update. London, England: National Institute for Clinical Excellence; 2004. 73. Frost MH, Arvizu RD, Jayakumar S, Schoonover A, Novotny P, Zahasky K. A multidisciplinary healthcare delivery model for women with breast cancer: patient satisfaction and physical and psychosocial adjustment. Oncol Nurs Forum. 1999; 26(10):1673-1680. 74. Wille-Jørgensen P, Sparre P, Glenthøj A, et al. Result of the implementation of multidisciplinary teams in rectal cancer. Colorectal Dis. 2013;15(4): 410-413. 75. Ortiz H, Wibe A, Ciga MA, Lujan J, Codina A, Biondo S; Spanish Rectal Cancer Project. Impact of a multidisciplinary team training programme on rectal cancer outcomes in Spain. Colorectal Dis. 2013;15(5):544-551. 76. Dietz DW; Consortium for Optimizing Surgical Treatment of Rectal Cancer (OSTRiCh). Multidisciplinary management of rectal cancer: the OSTRiCH. J Gastrointest Surg. 2013;17(10):1863-1868. 77. Khani MH, Smedh K. Centralization of rectal cancer surgery improves long-term survival. Colorectal Dis. 2010;12(9):874-879.
69. Kanemitsu Y, Hirai T, Komori K, Kato T. Survival benefit of high ligation of the inferior mesenteric artery in sigmoid colon or rectal cancer surgery. Br J Surg. 2006;93(5):609-615.
78. Bülow S, Harling H, Iversen LH, Ladelund S; Danish Colorectal Cancer Group. Improved survival after rectal cancer in Denmark. Colorectal Dis. 2010; 12(7 online):e37-e42.
70. Wang H, Safar B, Wexner SD, Denoya P, Berho M. The clinical significance of fat clearance lymph node harvest for invasive rectal adenocarcinoma following neoadjuvant therapy. Dis Colon Rectum. 2009;52(10):1767-1773.
79. Monson JR, Probst CP, Wexner SD, et al; Consortium for Optimizing the Treatment of Rectal Cancer (OSTRiCh). Failure of evidence-based cancer care in the United States: the association between rectal cancer treatment, cancer center volume, and geography. Ann Surg. 2014;260(4):625-632.
71. Thakur S, Somashekar U, Chandrakar SK, Sharma D. Anatomic study of distribution, numbers, and size of lymph nodes in mesorectum in Indians: a autopsy study. Int J Surg Pathol. 2011;19(3):315-320. 72. National Institute for Clinical Excellence Improving Outcomes in Colorectal Cancers.
80. Mayo NE, Feldman L, Scott S, et al. Impact of preoperative change in physical function on postoperative recovery: argument supporting prehabilitation for colorectal surgery. Surgery. 2011; 150(3):505-514.
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Modern Multidisciplinary Perioperative Management of Rectal Cancer Mariana Berho, MD; Rahul Narang, MD; Julie Ann M. Van Koughnett, MD, MEd; Steven D. Wexner, MD, PhD(Hon)
IMPORTANCE The management of care for rectal cancer has undergone many changes and
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improvements in recent decades. A multidisciplinary approach to this complex disease is essential to ensure high-quality treatment and outcomes. OBJECTIVE To present a current, evidence-based approach to the multidisciplinary team management of rectal cancer with a review of the diagnosis, staging, and treatment of the disease by radiologists, oncologists, surgeons, and pathologists. EVIDENCE REVIEW The literature review was conducted through online searches of MEDLINE
and PubMed. Articles published between January 1, 2000, and June 2014 and pertaining to staging modalities, surgical approaches, pathologic assessment, and medical treatments of rectal cancer were considered. All studies were reviewed, with preferential inclusion of larger or randomized trials. The review focused on changing paradigms and current controversies in rectal cancer management. FINDINGS A multidisciplinary approach to the patient with rectal cancer includes many health care professionals. Although treatments continue to evolve and improve, clear evidence-based principles have been well studied. The important roles of various specialists must be acknowledged and utilized. Within each role, new and emerging treatment approaches require critical review by experts in their fields. CONCLUSIONS AND RELEVANCE Many new technologies and treatment options will continue to advance the treatment of rectal cancer, further emphasizing the need for a multidisciplinary approach to achieve optimal care.
Corresponding Author: Steven D. Wexner, MD, PhD(Hon), Digestive Disease Center, Cleveland Clinic Florida, 2950 Cleveland Clinic Blvd, Weston, FL 33331 ([email protected]).
JAMA Surg. 2015;150(3):260-266. doi:10.1001/jamasurg.2014.2887 Published online January 28, 2015.
T
he pivotal work of Sir Ernest Miles in 1908 revolutionized the surgical treatment of rectal cancer. However, this was only possible in large part owing to the advances in other disciplines, including anesthesia, anatomy, pathology, and the understanding of sepsis and antisepsis (eAppendix in the Supplement).1 Although every physician seeks to provide patients with the best possible care, unilateral medical decisions may be influenced by personal perceptions and often lack an evidence-based rationale. The first organized attempt to measure the effect of a multispecialty group was successfully undertaken in the United Kingdom for breast cancer. Kesson and colleagues2 demonstrated that patients with breast cancer who were receiving the care of a multidisciplinary team had better outcomes. This benefit persisted after adjustment for age, cancer stage, and access to health care. Burton et al3 showed that multidisciplinary review of imaging in patients with colorectal cancer resulted in improved staging and curative resection rates. The surgeon no longer carries the sole responsibility of deciding the appropriate therapy; instead, medical care relies on a group of experts, including surgeons, radiotherapy oncologists, medical oncologists, and pathologists. The various components and roles of the 260
Author Affiliations: Department of Pathology and Laboratory Medicine, Cleveland Clinic Florida, Weston (Berho); Digestive Disease Center, Cleveland Clinic Florida, Weston (Narang, Van Koughnett, Wexner).
multidisciplinary team in rectal cancer are summarized in the Table. This review is focused on changing paradigms in the management of rectal cancer, with emphasis on the importance of the multidisciplinary team on achieving optimal oncologic outcomes. A literature review of MEDLINE and PubMed was conducted, and highquality studies were selected for inclusion. Articles published between January 1, 2000, and June 2014 and pertaining to staging modalities, surgical approaches, pathologic assessment, and medical treatments of rectal cancer were considered. All studies were reviewed, with preferential inclusion of larger or randomized trials.
Role of the Radiologist The American Society of Clinical Oncology guidelines to preoperatively stage rectal cancer require examination using colonoscopy; contrast-enhanced computed tomography of the abdomen, pelvis, and chest; and serum carcinoembryonic antigen level.4 A complete colonoscopy should be performed to evaluate the tumor location and identify and treat any synchronous lesions. The incidence
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Table. Multidisciplinary Team for Perioperative Management of Rectal Cancer Characteristic
Surgeon
Radiologist
Oncologist
Endoscopist/Primary Care Physician
Pathologist
•
•
Allied Healtha
Diagnosis
•
Staging
•
Preoperative planning
•
•
•
•
Preoperative counseling
•
•
•
•
•
Neoadjuvant treatmentb •
Specimen evaluation
•
Postoperative management
•
• •
Adjuvant therapyb
•
•
• •
a
Includes office coordinators and stoma nurses.
b
If applicable.
•
•
of synchronous cancers ranges from 1% to 3%, and the incidence of synchronous polyps is approximately 30%.5 If colonoscopy cannot be performed, alternative means of imaging (ie, contrast enema or computed tomography colonography) should be performed. Digital rectal examination alone is not enough to assess the location and degree of fixation (and, by extension, tumor invasion). Digital rectal examination for low rectal lesions is largely inaccurate in assessing the location of the lesion relative to the anal verge.6 Digital rectal examination has been shown6 to have only 65% agreement with the pathologic specimen when predicting tumor characteristics. Carcinoembryonic antigen levels should be recorded, although high preoperative levels are not an independent indication for adjuvant treatment. Staging modalities to evaluate the primary rectal tumor have 4 objectives: assessment of tumor depth within the wall of the rectum (T stage), examination of lymph node status (N stage), detection of metastatic disease (M stage), and determination of the distance of the tumor from the circumferential resection margin (CRM). Magnetic resonance imaging (MRI) and endorectal ultrasonography (ERUS) can determine the accurate depth of tumor penetration in 60% to 92% of patients.7 The advantages of one of these methods over the other have been the subject of debate.8 Magnetic resonance imaging is very accurate in predicting T stage, with agreements with pathologic staging well above 80%.9 The primary role of MRI in staging is to assess the CRM. The importance of CRM status was presented by the Magnetic Resonance Imaging and Rectal Cancer European Equivalence (MERCURY) study as a predictor of recurrence and need for neoadjuvant therapy.10 The results showed that CRM-involved tumors identified by MRI had lower 5-year disease-free and recurrence-free survivals.11 In addition, CRM involvement was associated with metastatic disease.11 A positive CRM identified in the pathologic specimen is associated with local and distant recurrence as well as lower overall and disease-free survival.12,13 A negative margin of only 1 to 2 mm has recurrence and survival benefits.13 Magnetic resonance imaging has a specificity of 94% in predicting CRM involvement.14 Endorectal ultrasonography can be performed in the office setting and has been shown15 to have an overall accuracy of 87% in predicting T stage. A prospective Scandinavian study16 found T-stage accuracy to be slightly lower at 74% and N-stage accuracy to be 65%. The sensitivity of perirectal tissue invasion was higher at 82%. Garciajamasurgery.com
•
•
Surgery
Surveillance
•
•
Aguilar et al17 found overall accuracy of ERUS to be 69% for T stage, finding 18% of the tumors to be overstaged and 13% to be understaged. Overstaging resulted from difficulties in differentiating perirectal fat inflammation from tumor infiltration. Brown and colleagues18 found the agreement of ERUS and pathologic staging to be 69% and advocated for the use of MRI in its place. Although both modalities depend on reader interpretation, ERUS is more operator dependent in its accuracy and MRI is the preferred local staging modality. Unfortunately, the positive predictive value of MRI and ERUS in detecting positive lymph nodes is only approximately 60%.9 This low level of accuracy has led some surgeons to advocate for complementary use of both ERUS and MRI.19 A survey by the International Rectal Cancer Study Group20 found very poor agreement on the best staging regimen among surgeons performing rectal cancer surgery. However, the recent introduction of high-resolution phasedarray MRI along with fast spin-echo T2-weighted sequencing has significantly improved preoperative imaging.21 In addition, highresolution MRI is exceptionally sensitive and specific in detecting extramural vascular invasion, which is an independent prognostic marker. In addition, computed tomography or positron emission tomography imaging can exclude distant metastatic disease. Thus, MRI has replaced ERUS as the preferred local staging modality.
Role of the Oncologist Patients with locally advanced distal rectal cancer are candidates for neoadjuvant treatment. Two Cochrane Database reviews22,23 concluded that there is a reduction in local recurrence after chemoradiotherapy vs radiotherapy alone for stage II and stage III rectal cancer (odds ratios, 0.39-0.72). Neither review found a significant difference in overall survival, sphincter preservation, or anastomotic leaks. If MRI reveals a negative CRM, neoadjuvant treatment may not be needed, as demonstrated in the MERCURY study. The decision as to whether neoadjuvant treatment is needed must be individualized to each patient and depends on agreement between the multidisciplinary team members.11 After neoadjuvant treatment for locally advanced rectal cancer, when should surgery be performed? Traditionally, rectal cancer trials have used a 6- to 8-week interval between the last radio(Reprinted) JAMA Surgery March 2015 Volume 150, Number 3
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therapy session and surgery. A randomized trial24 comparing 4-week with 8-week intervals in node-negative rectal cancers did not find a significant advantage to waiting longer before surgery. However, prolonging the interval may result in increased tumor regression prior to surgery. Påhlman25 reviewed wait-time intervals and found that tumor regression, sphincter preservation, local recurrence, and overall survival were not different with time intervals of less than or greater than 41 days. Habr-Gama et al26 found no statistically significant differences in 5-year overall or disease-free survival between patients according to time to surgery (ⱕ12 vs >12 weeks). A recent systematic review27 found that, in studies reporting complete pathologic response after chemoradiotherapy, 4 of 7 studies found higher rates of complete pathologic response after longer intervals. This result was confirmed in a meta-analysis28 reporting that the complete pathologic response rates increased from 13.7% to 19.5% when the interval was longer than 6 to 8 weeks. Additional studies are needed to delineate the ideal interval and to predict which patients may benefit from a longer interval. Nevertheless, the time between the completion of neoadjuvant therapy and surgery appears to be getting longer.
Role of the Surgeon When possible, a restorative proctectomy should be performed without jeopardizing oncologic integrity. To help optimize function, a stapled anastomosis should be performed if the anastomosis does not require a mucosectomy or intersphincteric dissection. The types of reconstruction performed for a restorative distal anastomosis include an end-to-side (Baker) anastomosis, colonic J pouch, coloplasty, and straight coloanal anastomosis. Multiple series29 have clearly demonstrated that the colonic J pouch confers better functional results with fewer bowel movements and less incontinence 1 year after surgery. However, longer-term sustainment of these benefits varies in the literature.30 A colonic J pouch should be no longer than 6 to 8 cm per limb to provide good function. Coloplasty and end-to-side anastomoses are also alternatives to a straight anastomosis. Comparisons of colonic J pouch with transverse coloplasty have found minimal differences in functional outcomes but have found coloplasty to have a statistically significantly higher complication rate.31 In addition, the colonic J pouch provides faster recovery of function after surgery than does the transverse coloplasty.32 A 2008 systematic review33 concluded that, although the colonic J pouch was superior to a straight anastomosis in most studies, larger studies were required to better define the roles of the end-to-side and transverse coloplasty. However, in practical terms and pending such studies, the colonic J pouch has been much more widely clinically used, whereas the coloplasty has been largely abandoned. However, end-to-side anastomosis seems to be experiencing a surge in popularity as an alternate technique. There are risks and benefits of a diverting stoma at the time of rectal cancer resection. A database review34 of the American College of Surgeons’ National Surgical Quality Improvement Project found that a stoma resulted in a higher incidence of acute renal failure but protected the patient from postoperative sepsis and need for reoperation. Most studies35 describe a decreased anastomotic leak rate with diverting stoma as well as a decreased need for reoperation to repair an anastomotic leak. A meta-analysis 36 per262
formed in 2009 showed overall benefit of an ileostomy over a colostomy. Ileostomy was associated with less sepsis and fewer stoma complications, although it carried a higher risk of dehydration. Detailed patient instructions and postoperative follow-up are needed for the patient with fecal diversion, but overall the risk of morbidity of an anastomotic leak and delayed adjuvant chemotherapy usually outweigh the risk of fecal diversion. Early nonrandomized studies found that oncologic surgical outcomes were comparable between open and laparoscopic surgery for rectal cancer. Laparoscopy is associated with less blood loss, quicker return of bowel function, and shorter hospital stay.37 In addition, early postoperative quality of life was repeatedly demonstrated to be superior after laparoscopic rectal cancer resection.38 Even in laparoscopic converted to open cases, oncologic outcomes are equivalent to those of open cases.39 Results of randomized trials40,41 have also shown equivalent oncologic outcomes, less blood loss, and faster recovery findings at the expense of only longer operative times. Sexual, bladder, and anal sphincter function may be adversely affected after proctectomy. The risk of fecal incontinence depends mainly on the tumor level and height of the anastomosis. Morino et al42 evaluated male sexual and urinary function after laparoscopic total mesorectal excision (TME) and found that sexual desire was maintained in 55.6% of the patients and the ability to engage in intercourse was maintained in 57.8% of the patients. The role of robotic-assisted surgery is unclear, and pelvic dissection is believed by many to be the best use for the roboticassisted approach in colorectal surgery. Robotic-assisted proctectomy has been shown43 to be a safe alternative with similar oncologic outcomes and morbidities. However, it is also associated with increased cost and longer operative times.44 Although laparoscopic and robotic-assisted surgery have benefits over open proctectomy for rectal cancer, the robotic approach has failed to demonstrate any significant advantage while the several above-cited disadvantages have been repeatedly and clearly demonstrated. Transanal excision and transanal endoscopic surgery (TES) have been used for early rectal cancers. The advent of TES platforms in particular has improved the surgeon’s ability to perform a complete one-piece resection with wide margins. Transanal endoscopic surgery does not carry the morbidity of a transabdominal resection. Numerous studies45,46 have shown that for carefully selected patients with favorable T1 and perhaps T2 lesions with very low risk features, various TES platforms can achieve clear margins, good oncologic outcomes, and low morbidity. The main concern with TES for rectal cancer is that lymphadenectomy is not performed, leaving the patient with up to a 25% chance of retained lymph node metastasis in T2 lesions.47 Cancer recurrence after local resection ranges between 4% and 18% for T1 lesions and 27% to 67% for T2 lesions after TES.48 To reduce the risk of local recurrence, various studies are investigating the role of radiotherapy and/or chemotherapy. The Alliance Z6041 and Transanal Endoscopic Microsurgery and Radiotherapy in Early Rectal Cancer trials are underway to determine the best treatment plan for locally excisable tumors. Results from trials49,50 using conventional neoadjuvant chemoradiotherapy followed by TES show good overall oncologic and survival outcomes. Although long-term data are not yet available, an even newer approach is transanal endoscopic TME combined with laparoscopic assistance.51 In pa-
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tients who have undergone this procedure, results show complete mesorectal excision with negative margins and no intraoperative complications.51 Although more data are needed, this hybrid technique may shift the paradigm in upcoming years. A complete clinical response will be noted in approximately 10% of patients during subsequent physical examination and restaging after neoadjuvant treatment. Habr-Gama and colleagues52 in Brazil have written extensively on the watch-and-wait approach, in which the patient does not proceed to surgical resection but rather undergoes regimented close monitoring for recurrent disease. The investigators have also found that, with an extended course of chemoradiotherapy with additional fluorouracil and leucovorin calcium, many patients with T2-T4/N0 distal rectal cancer were able to avoid surgery. With close monitoring, salvage surgery was possible in 90% of the patients with local recurrence.53 The nonoperative approach after complete clinical response has become more accepted in a greater number of centers as further data from around the world have become available. With the watch-and-wait approach, careful patient selection and close monitoring using digital rectal examination, proctoscopy, carcinoembryonic antigen levels, computed tomography and/or MRI, and biopsies of suspicious lesions is recommended. Recurrent disease should be treated with surgical resection. Routine scar biopsies are not recommended because they have a negative predictive value of 11%.54 In a study of rectal cancer pathologic specimens of patients who received chemoradiotherapy followed by proctectomy, 25% of the specimens were pathologic tumor stage 0.55 However, 74% of these specimens had a visible mucosal lesion and therefore were not deemed a complete clinical response.55 Patients must be aware of the potential risks and benefits of the watch-and-wait approach in the setting of complete clinical response and understand that surgical resection is, at this time, still the standard of care. Nonetheless, there are undoubtedly good candidates for the watchand-wait approach. The challenges are in correctly identifying these patients and ensuring appropriate follow-up evaluations for them. It has long been known that surgeon volume and specialization in colorectal surgery affects practice patterns. A 1998 study56 found that colorectal-trained surgeons treated more mid and distal rectal tumors and yet performed significantly fewer abdominoperineal resections than did surgeons without colorectal training who treat rectal cancer (27% vs 47% abdominoperineal resections, respectively). A recent Cochrane Database57 review concluded that surgeons with higher volumes and colorectal training had better 5-year survival outcomes, lower postoperative mortality, and lower rates of permanent stomas. In the United States, a database study found that 39% of surgeons performing proctectomies performed only abdominoperineal resections, and surgeons who completed both nonrestorative and restorative proctectomies had better patient outcomes.58 Specialization and regionalization of care are controversial in many areas within surgery, and rectal cancer treatment is no exception.
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sitivity to neoadjuvant radiotherapy and chemotherapy. Intraoperative frozen sections are occasionally performed at the request of the surgeon.Traditionally,pathologictumorandnodalstageswerethesole predictors of outcomes; however, several studies59 have concluded that the integrity of the mesorectum is an independent prognostic factor of both disease-free and overall survival. The quality of the mesorectum is assessed by the pathologist and can be divided into complete (intact with minimal irregularities), near complete (defects >5 mm but without exposure of the muscularis propria), and incomplete (deep defects in the mesorectal fat that expose the muscularis propria).60 The pathologist is responsible for providing accurate and unbiased feedback to the surgeon and oncologist. Several studies61,62 have shown that a complete or near-complete pathologic response (few residual malignant cells in the surgical specimen) correlates with better outcomes; therefore, it is imperative that the tumor regression grade is documented in the pathologist’s report. In addition to the assessment of the mesorectal quality, the margins of resection should be recorded. The acceptable length of the distal resection margin for rectal cancer has been a matter of debate during the past decade. The desire for a restorative proctectomy has resulted in studies that challenged the traditional 2-cm rule for rectal cancer. Initial studies63 indicated that a distal margin of 1 cm or more provided the same survival and local recurrence estimates as a 2-cm margin. Subsequent studies64 have demonstrated that a subcentemeric margin, as low as 5 mm, did not affect local recurrence or survival outcomes. In addition to adequate proximal and distal margins, the importance of the circumferential margin in predicting recurrence cannot be overstated. The criterion standard of 12 lymph nodes used on colon cancer pathologic specimens as a marker of adequate surgical resection may not apply for rectal cancer. Studies65,66 have demonstrated that fewer lymph nodes are found in specimens after neoadjuvant chemoradiotherapy compared with surgery alone. A recent study67 of the Surveillance, Epidemiology, and End Results database found that, to prevent stage migration of the proctectomy specimen, 18 and 16 lymph nodes were needed in patients undergoing surgery alone and neoadjuvant treatment followed by surgery, respectively. One way to improve lymph node yield is through surgical technique and proper TME. Laparoscopic TME, for example, has been shown68 to significantly increase lymph node yield compared with the open approach. High ligation of the inferior mesentery artery ensures clearance of its associated lymph nodes, which negatively affect survival if positive for malignancy.69 In addition, improved fat clearance and lymph node–revealing solutions improve lymph node yield when used by pathologists.70 Lymph node assessment in the rectum tends to be more challenging since the mesorectal nodes are smaller, and preoperative radiotherapy leads to a decreased number of perirectal lymph nodes.71 The use of cancer synoptic reports is strongly recommended because they standardize reporting of data and avoid omission of important information.
Role of the Pathologist
Working Together: Effect of the Multidisciplinary Team
Confirmation of malignancy on tissue biopsies prior to a radical cancer operation is essential. In addition, although not yet a standard of care, preoperative tissue may be used in the future to test tumor sen-
The responsibility of all physicians treating rectal cancer is to coordinate care to optimize survival while minimizing morbidity and maximizingqualityoflife.TheNationalInstituteforClinicalExcellenceinLon-
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don published guidelines to help organize multidisciplinary care.72 The multidisciplinary approach has been well studied and validated for breast cancer. Frost et al73 evaluated patients with newly diagnosed breast cancer and found that those who received a multidisciplinary approachtotreatmenthadhigherlevelsofphysicalfunction(P = .003) and satisfaction with their health (P < .01), physician (P < .001), and nursing care (P = .004). In addition, breast cancer–related mortality decreased after multidisciplinary care was established.2 Implementation of multidisciplinary teams in rectal cancer has resulted in improved postoperative mortality in Denmark74 and Spain.75 To improve rectal cancer care, many European countries have set strict national guidelines to regionalize rectal cancer care to centers of excellence, resulting in better short- and long-term outcomes.76 In England, rectal cancer care is centralized with surgical techniques standardization and multidisciplinary tumor boards. Similar efforts in Scandinavian countries have resulted in more patients undergoing TME, reduced local recurrence, and improved 5-year survival.77,78 The Consortium for Optimizing Surgical Treatment of Rectal Cancer (OSTRiCh) group is seeking to improve the quality of rectal cancer care delivery in the United States in a similar manner.76,79 The principles of the group include TME, pathologic assessment of surgical quality, effective use of imaging, evidencebased use of medical and radiotherapy oncology in addition to surgery, and the multidisciplinary team approach. The OSTRiCh group has demonstrated wide variability in both treatment and outcome of rectal cancer in the United States. In addition to the efforts of the OSTRiCh group, the American College of Surgeons’ Commission on Cancer accredits more than 1500 cancer programs nationwide to provide state-of-the-art pretreatment evaluation, staging, treatment, and clinical follow-up for patients with cancer. The OSTRiCh group has been working in collaboration with the Commission on Cancer and the American College of Surgeons to implement accreditation programs for rectal cancer surgery in the USA. ARTICLE INFORMATION Accepted for Publication: August 26, 2014. Published Online: January 28, 2015. doi:10.1001/jamasurg.2014.2887. Author Contributions: Drs Berho and Wexner had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: All authors. Acquisition, analysis, or interpretation of data: All authors. Drafting of the manuscript: All authors. Critical revision of the manuscript for important intellectual content: All authors. Administrative, technical, or material support: Van Koughnett, Wexner. Study supervision: Wexner. Conflict of Interest Disclosures: None reported. REFERENCES 1. Miles WE. A method of performing abdomino-perineal excision for carcinoma of the rectum and of the terminal portion of the pelvic colon. Lancet. 1908;2:1812-1813. 2. Kesson EM, Allardice GM, George WD, Burns HJ, Morrison DS. Effects of multidisciplinary team working on breast cancer survival: retrospective,
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It is essential that patients with newly diagnosed rectal cancer undergo thorough preoperative counseling. Mayo et al80 reported on a randomized trial comparing 2 “prehabilitation” programs; patients who did well during prehabilitation were more likely to recover postoperatively to their baseline function. Patients should also be counseled by the enterostomal therapist about a potential ostomy, including proper care, management of high output, and quality-of-life expectations.
Conclusions The treatment of rectal cancer has made significant gains in recent decades. To achieve optimal outcomes, the team of health care workers and the patient must be aware of shifting paradigms in the standard of care (eTable in the Supplement). Preoperative local staging with MRI and/or ERUS will provide essential information on both the type of surgery needed and the role of neoadjuvant chemoradiation. Important studies continue to be conducted on minimally invasive approaches to expedite recovery without compromising oncologic outcomes. Local excision and the watch-and-wait approach appear to be safe, but patient selection is essential. The multidisciplinary care of the patient with rectal cancer must include the surgeon, pathologist, oncologist, radiologist, and endoscopist/ primary care physician in the pursuit of excellence in rectal cancer outcomes. The advantages of multidisciplinary care are clear, and a specialized team is essential given the complexity of the many facets of rectal cancer care. Positive results can be achieved if the OSTRiCh group, working with the American College of Surgeons, College of American Pathologists, American College of Radiology, and Commission on Cancer, can introduce the same multidisciplinary rectal cancer centers of excellence program in North America that has so greatly benefitted patients in Europe.
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