In the United States, colorectal cancer (CRC) is the second leading cause of cancer deaths for men and women combined (1). Of the estimated 132,700 new cases expected to be diagnosed in 2015 (1), 70–80% will undergo surgical resection with curative intent (2, 3) and up to 40% of patients with locoregional disease will develop recurrent cancer, of which 90% will occur within 5 years (4). The postoperative surveillance of patients treated for CRC is intended to prolong survival by diagnosing recurrent and metachronous cancers at a curable stage, and to prevent metachronous cancer by detection and removal of precancerous polyps.
Surveillance strategies employ a combination of modalities, including history and physical examination, carcinoembryonic antigen (CEA), computed tomography (CT) scans, and endoluminal imaging, including colonoscopy, sigmoidoscopy, endoscopic ultrasound (EUS), and CT colonography (CTC). Although the optimal surveillance strategy is still not clearly defined, the role of colonoscopy is primarily to clear the colon of synchronous cancers and polyps and prevent metachronous neoplasms.
In 2006, the US Multi-Society Task Force (USMSTF) published a consensus guideline to address the use of endoscopy for patients after CRC resection (5). This updated document focuses on the role of colonoscopy in patients after CRC resection. Additionally, based on a comprehensive literature review updated from the 2006 recommendations, we review the possible adjunctive roles of fecal testing (e.g., fecal immunochemical testing for hemoglobin) and CTC. The use of CEA, CT scans of the liver, as well as chest radiographs are beyond the scope of this document and are not reviewed. The goal of this consensus document is to provide a critical review of the literature and recommendations regarding the role of colonoscopy, flexible sigmoidoscopy, EUS, fecal testing, and CTC in surveillance after surgical resection of CRC.
The English-language medical literature was searched using MEDLINE (2005 to September 30, 2015), EMBASE (2005 to September 30, 2015), the Database of Abstracts of Reviews and Effects (2005 to October 7, 2015), and the Cochrane Database of Systematic Reviews (2005 to October 7, 2015). In MEDLINE, subject headings for colorectal neoplasms were combined with the subheading for surgery, resection, postoperative, colectomy, curative, survivor, survival, neoplasm recurrence, second primary neoplasms, and treatment outcome. The resulting set was combined with subject and keywords for colonoscopy or follow- up studies. Similar searches were performed in EMBASE, the Database of Abstracts of Reviews and Effects, and the Cochrane Database of Systematic Reviews. Case reports and studies performed in patients with inflammatory bowel disease, prior CRC, or hereditary CRC syndromes were excluded. Review papers, meta-analyses, gastroenterology textbooks, and editorials were searched manually for additional references. Data from studies with no explicit documentation that perioperative colonoscopic clearing had been performed were not included in the overall summary tables, but some of these studies are referred to in the discussion of the evidence. The review includes studies published since 2005, but also incorporates older evidence used to draft the 2006 guidelines (5). Evidence-based recommendations are provided with supporting discussion to help guide clinicians in the management of these patients.
Abbreviations used in this paper:CEA, carcinoembryonic antigen; CI, confidence interval; CRC, colorectal cancer; CT, computed tomography; CTC, computed tomographic colonography; EUS, endoscopic ultrasound; FIT, fecal immunochemical test; GRADE, Grading of Recommendations Assessment, Development and Evaluation; OR, odds ratio; RCT, randomized controlled trial; RR, relative risk; SPS, serrated polyposis syndrome; USMSTF, US Multi-Society Task Force.
The review focused on the use of colonoscopy after surgical resection in patients with TNM stages I-III (or Dukes A-C) CRC, and selected patients with resected stage IV cancer (6). When available, we included studies with specific reporting of overall and cancer-specific survival, and rates of second primary (metachronous) cancers and anastomotic recurrences. Although significant variability exists in the terminology of the reviewed studies, the following general definitions were employed: metachronous cancer refers to CRC diagnosed as a second primary after surgical resection and perioperative clearing, and anastomotic recurrence includes CRC which recurs intraluminally at or within close proximity of the surgical anastomosis.
Rectal cancer is generally associated with a higher risk of local recurrence than cancer in other segments of the colon, and requires additional considerations for surveillance, which are discussed in more detail in a separate section.
Throughout the document, reference is made to “high-quality” colonoscopy for perioperative clearing and surveillance for metachronous neoplasms. A high-quality colonoscopy assumes completeness (cecum or anastomosis is reached), adequate bowel preparation, and meticulous examination by appropriately trained operators who meet adenoma detection benchmarks (i.e., frequency of conventional adenoma detection of >25% in average-risk screening colonoscopies) (7, 8).
Process and levels of evidence
The USMSTF includes gastroenterology experts with specific interest in CRC. These members represent the American College of Gastroenterology, the American Gastroenterological Association, and the American Society for Gastrointestinal Endoscopy. Summary tables and a draft document were circulated to members of the Task Force, and final guidelines were developed by consensus during a joint teleconference. The document underwent committee review and governing board approval by all 3 societies. The USMSTF grades the quality of evidence and strength of recommendations using an adaptation of the Grading of Recommendations Assessment, Development and Evaluation (GRADE) approach (9). The GRADE process categorizes the quality of the evidence as high, moderate, low, or very low (Table 1). This categorization is based on an assessment of the study design (e.g., randomized controlled trial or observational study), study limitations, inconsistency of results, indirectness of evidence, imprecision, and publication bias. The USMSTF members conduct literature searches to identify published papers that address the key issues discussed within these recommendations. These publications are supplemented both by review of citations from the identified papers as well as other key references elicited from the subject matter experts on the Task Force. The GRADE process involves the collection of literature, analysis, summary (often as meta-analysis), and a separate review of the quality of evidence and strength of recommendations. The USMSTF members employ a modified, qualitative approach for this assessment based on exhaustive and critical review of evidence, without a traditional meta-analysis. The GRADE process separates evaluation of the quality of the evidence to support a recommendation from the strength of that recommendation. This is done in recognition of the fact that, although the quality of the evidence impacts the strength of the recommendation, other factors can influence a recommendation, such as side effects, patient preferences, values, and cost. Strong recommendations mean that most informed patients would choose the recommended management and that clinicians can structure their interactions with patients accordingly. Weak recommendations mean that patients' choices will vary according to their values and preferences, and clinicians must ensure that patients' care is in keeping with their values and preferences (9). Weaker recommendations are indicated by phrases such as “we suggest,” whereas stronger recommendations are stated as “we recommend.”
RESULTS OF LITERATURE REVIEW
Effect of surveillance colonoscopy on survival
Observational studies utilizing large administrative databases (10, 11, 12) and meta-analysis of randomized controlled trials (RCTs) (13, 14) show that patients who receive surveillance colonoscopy after CRC resection have lower overall (10, 11, 12, 13, 14), but not disease-specific (11, 14) mortality. Cancer-specific mortality is considered the most important outcome in cancer trials (15). Possible explanations for the discrepancies between all-cause and CRC-specific mortality are unmeasured comorbidity leading physicians to select healthier patients for colonoscopic surveillance, cancer survivors tending to be more closely scrutinized and receiving more non-oncologic medical care, and inaccurate adjudication of cause of death (3, 16).
Colonoscopy is one of several modalities used in the surveillance of CRC patients after curative-intent surgical resection, and the impact of colonoscopy on patient outcomes cannot be discussed without considering the broader context of other co-interventions. The modalities used for surveillance include a combination of medical examinations, CEA measurements, radiologic imaging, and colonoscopy. To date, 11 RCTs that enrolled >4000 patients have compared different surveillance regimens (17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27). The surveillance strategies (test selection and frequency of administration) used in these RCTs were heterogeneous, complicating the drawing of definitive conclusions regarding the optimal use of individual tests and their effect on patient outcomes (28, 29). Furthermore, some the findings may be less relevant to contemporary surveillance recommendations because several of the RCTs enrolled patients in the 1980s and 1990s. Since then, there have been important improvements in surgical technique (such as total mesorectal excision for rectal cancer), CT imaging technology to detect recurrences earlier, and the use of chemotherapy (for stage III and certain stage II patients, and to downstage patients with previously unresectable disease) (30, 31). Three ongoing RCTs (27, 32, 33) should better clarify the impact of CRC surveillance regimens on patient outcomes (Table 2).
Despite these limitations, meta-analyses and systematic reviews (13, 14, 34, 35, 36) incorporating evidence from the RCTs have been conducted. A Cochrane review showed that patients undergoing more intensive follow-up (variably defined between studies) had reduced all-cause 5-year mortality (odds ratio [OR]=0.73; 95% confidence interval [CI]: 0.59–0.91), and reduced mean time until recurrence (−6.75 months, 95% CI: −11.06 to −2.44 months) (35). A meta-analysis that included 7 RCTs (17, 18, 19, 20, 21, 22, 23) and preliminary results of an ongoing RCT (27) reported comparable findings (13). This analysis also found that colonoscopy (vs. no colonos- copy) was associated with improved overall survival; however, the frequency of colonoscopy had no significant effect on survival (13). The most recent meta-analysis (14) included 11 RCTs and reported that patients undergoing more intensive follow-up had reduced overall mortality (hazard ratio=0.75; 95% CI: 0.66–0.86), higher probability of detection of asymptomatic recurrences (RR=2.59; 95% CI: 1.66–4.06), curative surgery attempted at recurrences (RR=1.98; 95% CI: 1.51–2.60), survival after recurrences (RR=2.13; 95% CI: 1.24–3.69), and a shorter time to detecting recurrences (mean difference, −5.23 months; 95% CI: −9.58 to −0.88 months). There was, however, no significant difference in cancer-specific mortality. It is important to note that although intensive multimodality surveillance is associated with increased overall survival and earlier detection of cancer recurrence, these benefits are most apparent in studies using frequent CEA measurements to detect recurrent disease (13, 14, 34, 35, 36). The performance of radiologic imaging (such as CT to detect liver metastases) has been associated with improved overall mortality when compared with no imaging in most (14, 34, 35, 36), but not all (13), analyses. The recently published FACS (Follow Up After Colorectal Surgery) (25) RCT reported that intensive imaging with CT of the chest, abdomen, and pelvis, and CEA measurement were each associated with increased rates of surgical resection of recurrences with curative intent, but not improved survival compared with minimal follow-up. Conversely, annual or more frequent surveillance colonoscopy has not been shown to improve survival (13, 22, 26, 36). This is not surprising because the rates of intraluminal or anastomotic recurrences are low, particularly for cancer proximal to the rectum, and usually associated with extraluminal disease that is not amenable to curative surgical resection. Increasing the intensity of surveillance colonoscopy solely to detect intraluminal disease is unlikely beneficial (5, 36).
A recently published RCT conducted in China provides additional information regarding colonoscopy surveillance after CRC resection (26). In this trial, 326 patients undergoing surgery for CRC were randomized to either intensive colonoscopic surveillance (i.e., colonoscopy at 3-month intervals for 1 year, at 6-month intervals for the next 2 years, and once a year subsequently), or routine colonoscopic surveillance (i.e., colonoscopy at 6, 30, and 60 months postoperatively). All patients underwent preoperative colonoscopy (or within 6 months postoperatively), and similar non-colonoscopic surveillance (i.e., medical history and examination, CEA, chest x-ray, and CT or ultrasound of the liver), and were followed until the date of last visit or death. There were no differences in overall 5-year survival rates (77% in the intensive colonoscopic surveillance group vs. 72% in the routine colonoscopic surveillance group; P=0.25). Although the authors stated that intensive colo- noscopic surveillance improved the prognosis of patients with symptomatic postoperative CRC, others have suggested lead-time bias as explanation (37). Furthermore, the higher E rate of reoperation has been observed in other studies O comparing intensity of surveillance strategies; this might be due to intervention bias, which can occur when clinicians not blinded to randomization arm make decisions regarding the selection of patients for reoperation (16). Of note, there were 3 complications in the intensive colonoscopic surveillance group (2 cases of hemorrhage requiring hospitalization and 1 perforation requiring laparotomy) and none in the routine colonoscopic surveillance group. These rates are similar to those reported in an older RCT (22). Thus, increased intensity of surveillance colonoscopy after curative resection of CRC (38) does not produce better outcomes, and might increase harm to some patients.
In summary, the evidence shows that although postoperative colonoscopy is associated with improved overall survival, there is no effect on cancer-specific death, and no survival benefit associated with frequent performance of surveillance colonoscopy. The role of postoperative colonoscopy is confined primarily to perioperative clearing and prevention of metachronous colon cancer, which are discussed in the following sections. The possible role of intraluminal imaging and EUS in improving survival from rectal cancer are discussed.
COLONOSCOPY AND PERIOPERATIVE CLEARING IN PATIENTS WITH CANCER OF THE COLON OR RECTUM
The critical importance of a complete high-quality colonoscopy to exclude synchronous tumors and find and resect polyps in patients with CRC cannot be overemphasized. In patients with CRC, the prevalence of synchronous cancers ranges from 0.7% to about 7% (39, 40, 41, 42, 43, 44, 45, 46, 47, 48). Colonoscopy is preferably performed preoperatively (49); however, it can be deferred for 3 to 6 months postoperatively if colonoscopy is incomplete due to malignant obstruction. The 3-month lower limit is intended to provide patients with sufficient time for postoperative recovery. Intraoperative colonoscopy has been proposed as an alternative approach (50), although not commonly practiced.
Available evidence indicates that perioperative colonos- copy should be meticulous, with the goal of detecting both synchronous cancers and precancerous lesions. Finding and resecting synchronous precancerous polyps in patients with CRC to prevent metachronous neoplasia is highly relevant. Considerable evidence indicates that significant neoplastic lesions can be missed during colonoscopy. The quality of the baseline examination, measured by the adenoma detection rate, is directly associated with the risk of development of, and death from, interval CRC (51, 52). Variable colonoscopy quality has also been demonstrated with respect to the completeness of polypectomy (53). In fact, the great majority of interval CRC cases are attributed to missed lesions or incomplete polyp resection (54). The issues regarding variability in colonoscopy quality, and the negative impact of this variability on protection from CRC described in average-risk cohorts, are potentially even more relevant in the higher-risk CRC patients. A large population-based study utilizing the Netherlands Cancer Registry employed an adjudication algorithm to ascribe likely etiology for metachronous CRC in a cohort of 5157 patients with CRC (47). There were 93 (1.8%) metachronous cancers diagnosed between 7 and 356 months after the initial CRC diagnosis (40.8% diagnosed within 36 months), and these were attributed to missed lesions in 43%, nonadherence to surveillance recommendations in 43%, and incomplete resection in 5.4%; de novo cancers accounted for only 5.4%. Several studies show that patients with CRC and synchronous adenomas or advanced adenomas have a higher risk of developing metachronous adenomas (12, 40, 42, 46, 55, 56, 57, 58, 59) and advanced neoplasms, including cancer (40, 56, 57, 58, 59, 60, 61) after surgery, underscoring the importance of adequate perioperative colonoscopy. The role of CTC in the perioperative setting is discussed in the section “Alternatives and Adjuncts to Colonoscopy,” but the case of obstructive CRC precluding preoperative colonoscopy and perioperative clearing done by CTC deserves additional comment. In this context, choosing colonoscopy instead of CTC for the first postoperative examination is prudent because synchronous diminutive and flat neoplastic lesions, which might be missed or not reported by CTC, are potentially highly relevant in a patient with CRC. Recently, serrated polyposis syndrome (SPS) has been recognized as the most common polyp syndrome, and is associated with an increased risk of CRC in both the right and left colon. In patients with SPS and CRC, SPS has usually been recognized at the colonoscopy that diagnosed CRC or during surveillance after CRC resec- tion (62). Because patients with SPS should undergo colonos- copy at more frequent intervals (63, 64), this underscores the importance of colonoscopist awareness of SPS and consideration of SPS diagnosis in patients with multiple and/or large serrated lesions.
We recommend that patients with CRC undergo high-quality perioperative clearing with colonoscopy. The procedure should be performed preoperatively, or within a 3- to 6-month interval after surgery in the case of obstructive CRC. The goals of perioperative clearing colonoscopy are detection of synchronous cancer and detection and complete resection of precancerous polyps.
Strong recommendation, low-quality evidence
COLONOSCOPY AND PREVENTION OF METACHRONOUS CANCER AFTER SURGERY FOR COLON AND FOR RECTAL CANCER
Colonoscopy is the procedure of choice for the detection of intraluminal metachronous CRCs. Pooled data from studies selected for this review (Supplementary Tables 1 and 2) show that approximately two-thirds of metachronous cancers are asymptomatic, TNM stage I or II (or Dukes stage A or B), and reoperated with curative intent. Data from population-based registries suggest that metachronous CRCs are being diagnosed at earlier stages, possibly reflecting the effect of increased surveillance (48, 65). The cumulative incidence of metachronous cancers of the colon and rectum is estimated to be about 0.3–0.35% per year (5, 60, 66), presenting at any time, even decades after the index malig-nancy (4, 18, 19, 20, 39, 41, 42, 43, 45, 55, 66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80). All colorectal segments are at increased risk for a metachronous cancer, although some studies suggest that among older survivors, the risk remains elevated only in the proximal colon (81). Thus, postoperative colonoscopic surveillance in CRC patients is indicated long term, or until the benefit is outweighed by decreased life expectancy due to age and/or competing comorbidity.
The optimal intervals of surveillance colonoscopy after CRC resection are not established by RCTs. However, several studies report an increased incidence of cancers diagnosed within the first few years after surgery, despite seemingly adequate perioperative colonoscopic clearance. In the postCRC resection studies included in this review, there were 253 (1.6%) metachronous cancers in 15,803 patients; when timing could be determined, about 30% were detected within 2 years of resection of the index malignancy (Supplementary Table 2). Several of these studies did not explicitly identify patients with Lynch syndrome, and inclusion of these patients could have inflated some of the estimates of the rates of early metachronous cancers (60, 82). The USMSTF recently recommended that all CRCs be studied for evidence of Lynch syndrome (83). The impact of not accounting for these patients is uncertain (a similar concern exists for unrecognized SPS); however, when the analysis was restricted to studies stating that patients with Lynch syndrome were excluded (26, 42, 46, 71, 76), the rate of metachronous cancers diagnosed within 3 years of surgery was about 33%. Recently published, large, population-based cancer registry studies, including ones that specifically excluded patients with Lynch syndrome (47, 66), report a high incidence of metachronous CRC within the first few years after surgery (47, 66, 81, 84). The most plausible explanation is that many early, apparently metachronous cancers are actually due to prevalent cancers or advanced adenomas missed at the time of the primary malignancy diagnosis. The factors involved in the occurrence of interval CRC are presumably the same in the case of missed synchronous cancers and missed synchronous advanced adenomas, and are likely related to the quality of the baseline clearing examination. The consensus 2006 USMSTF guidelines recommended colonoscopy at 1 year after surgery (or after the perioperative clearing colonoscopy), in addition to high-quality perioperative clearing to exclude synchronous neoplasia (5). Studies published since 2005 show that the 1-year examination is high-yield and cost-effective (85). In a study conducted in a large health maintenance organization, 652 patients with curative resection for CRC and at least 1 colo- noscopy were evaluated. Of those, 20 patients (3.1%) were diagnosed with a second primary CRC, including 9 cancers that were detected within 18 months of the initial cancer diagnosis (12). In the 5-year follow-up of the VA Cooperative Study 380, 5 cancers were detected in patients who had CRC diagnosed at baseline (n=23), and 4 of 5 were found within 18 months (86). One study (87) challenged the concept of performing a colonoscopy at the 1-year interval: A review of a subgroup of 155 CRC patients in a cancer registry with both a complete preoperative and at least one complete postoperative colonoscopy (performed at mean of 478±283 days) revealed no metachronous CRC cases. However, there were 3 anastomotic recurrences and 24 patients with 28 adenomatous polyps; 5 of which were >1 cm. In the RCT published by Wang et al. (26), 5 of 9 metachronous cancers were diagnosed within 3 years after surgery. This study provides additional evidence that even with appropriate perioperative clearing of the colon, some patients present a short time after surgery with a second primary cancer, strengthening the recommendation to perform colonoscopy 1 year after surgical resection of CRC.
The timing of subsequent surveillance examinations is supported by weaker evidence, and is based largely on the approach to post-polypectomy surveillance of patients with high-risk adenomas (63). If the 1-year examination reveals no neoplasia, colonoscopy should be performed after 3 years (4 years from CRC diagnosis or perioperative colonoscopy) and if this examination finds no neoplasia, 5 years later (9 years from CRC diagnosis or perioperative colonoscopy). Subsequent surveillance intervals should not exceed 5 years. If polyps are found during any of the examinations, then the interval for the next colonoscopy can be shortened, based on guidelines for post-polypectomy surveillance (63). Patients with known or suspected Lynch syndrome due to tumor testing, age at diagnosis, family history, and/or tumor characteristics should be distinguished from patients with sporadic CRC and referred for genetic counseling and appropriate surveillance based on USMSTF recommendations (88).
We recommend that patients who have undergone curative resection of either colon or rectal cancer receive their first surveillance colonoscopy 1 year after surgery (or 1 year after the clearing perioperative colonoscopy). Additional surveillance recommendations apply to patients with rectal cancer (see “Additional Considerations in Surveillance of Rectal Cancer”).
Strong recommendation, low-quality evidence
We recommend that, after the 1-year colonoscopy, the interval to the next colonoscopy should be 3 years (i.e., 4 years after surgery or perioperative colonoscopy) and then 5 years (i.e., 9 years after surgery or perioperative colonoscopy). Subsequent colonoscopies should occur at 5-year intervals until the benefit of continued surveillance is outweighed by diminishing life expectancy. If neoplastic polyps are detected, the intervals between colonoscopies should be in accordance with published guidelines for polyp surveillance intervals. These intervals do not apply to patients with Lynch syndrome.
Strong recommendation, low-quality evidence
ADDITIONAL CONSIDERATIONS IN SURVEILLANCE OF RECTAL CANCER
An important distinction is made between colon and rectal cancer because of the latter's higher propensity for local recurrence. In the studies compiled for this review that reported on colon and rectal cancer separately, >80% of anastomotic recurrences involved patients with cancer of the rectum or distal colon (18, 20, 26, 39, 40, 41, 44, 76, 89). In the RCT by Wang et al. (26), recurrent cancers diagnosed in the colon had higher resectability than rectal malignancies. The local recurrence rate of rectal cancer depends on accurate preoperative staging, neoadjuvant chemoradiation for locally advanced disease, and surgical technique. Rectal cancer recurrence is decreased by total mesorectal excision in which the rectum and mesorectal fascia are resected en bloc by precise sharp dissection (90). Excision of the rectum and mesorectum, via the low anterior abdominoperineal approach, has historically been the preferred surgical approach to low rectal cancer. Concerns about increased mortality and morbidity and decreased quality of life post-operatively have spurred interest in less invasive local excision options for early rectal cancer (T1 and some T2 tumors), such as transanal excision or transanal endoscopic microsurgery, however, these techniques are associated with higher local recurrence rate than radical surgery (91, 92, 93, 94, 95, 96). Endoscopic submucosal dissection is used in some centers as definitive treatment of selected rectal cancers with superficial submucosal invasion (97, 98, 99). In cases where total mesorectal excision is not performed (including transanal excision methods), there is a rationale for periodic examination of the rectum using sigmoidoscopy or endoscopic ultrasound. Presently, it is unclear which of these 2 modalities is better, or what the ideal surveillance intervals should be, although EUS has the potential for detection of extraluminal recurrence before development of intraluminal endoscopic findings. The use of EUS allows for sampling of suspicious subepithelial lesions or lymph nodes and detects recurrences at earlier stages. Some studies also report that approximately 10% of rectal cancer recurrences are diagnosed by EUS only, and missed by other modalities, including proctoscopy (100, 101). However, there are no controlled trials evaluating whether intensive EUS improves the survival of patients with rectal cancer. The optimal approach to luminal surveillance in an individual patient with resected rectal cancer requires a multidisciplinary collaboration between gastroenterologist, colorectal surgeon, and oncologist. The 2006 USMSTF guidelines suggested sigmoidoscopy or rectal EUS every 3 to 6 months for the first 2 or 3 years after surgery, in addition to colono- scopic surveillance for metachronous neoplasms, and this suggestion is maintained in the current document.
Patients with localized rectal cancer who have undergone surgery without total mesorectal excision, those who have undergone transanal local excision (i.e., transanal excision or transanal endoscopic microsurgery), or endoscopic submucosal dissection, and those with locally advanced rectal cancer who did not receive neoadjuvant chemoradiation and then surgery using total mesorectal excision techniques, are at increased risk for local recurrence. In these situations, we suggest local surveillance with flexible sigmoidoscopy or EUS every 3–6 months for the first 2–3 years after surgery. These surveillance measures are in addition to recommended colonoscopic surveillance for metachronous neoplasia.
Weak recommendation, low-quality evidence
Alternatives and adjuncts to colonoscopy
Computed tomographic colonography
CTC is a USMSTF guideline-endorsed option for CRC screening (102), and its role in patients with CRC is evolving. CTC is an appropriate option in patients with obstructing CRC in whom preoperative colonoscopy to examine the colon proximal to the obstruction is not feasible. One large case series included 284 patients with obstructing CRC and reported sensitivity of 88.6% and negative predictive value of 97.4% for synchronous advanced neoplasia (including advanced adenomas and cancer) proximal to the obstructing cancer (103). The use of CTC with intravenous contrast can be considered preoperatively to exclude both synchronous neoplasia and distant metastases, although caution is advised in cases with complete colonic obstruction due to increased perforation risk associated with gas insufflation. In unselected patients, CTC outperforms double-contrast barium enema at all polyp size ranges (104, 105). A large multicenter UK study (106) randomized 3838 patients with symptoms suggestive of CRC to barium enema or CTC. The detection rate of CRC or large polyps was significantly higher in the CTC group (7.3 vs. 5.6%; RR=1.31; 95% CI: 1.01–1.68; P=0.039), and CTC missed 3 of 45 CRC, while barium enema missed 12 of 85. Thus, CTC is preferred over barium enema for preoperative patients with obstructing cancers; however, barium enema remains an option if local resources and expertise do not allow CTC.
CTC has been proposed for postoperative surveillance because it combines contrast abdominopelvic CT, which is already part of standard post-CRC surveillance, with the ability to detect intraluminal lesions. Thus, CTC could be a one-step assessment for metachronous lesions, local recurrence, and distant metastases (107). In the largest cohort to date (108), 742 patients without clinical or laboratory evidence of recurrence underwent contrast-enhanced CTC after curative-intent CRC surgery. Six metachronous cancers and one anastomotic recurrence were found by CTC, with sensitivity of 100% for cancer and 81.8% for advanced neoplasia (using colonoscopy with pathologic confirmation as the reference standard). All intraluminal cancers were amenable to additional curative treatment; an additional 11 patients were found to have extracolonic recurrences. In patients who have undergone CRC resection, CTC requires expertise to differentiate normal postoperative findings (such as inflammatory changes at the anastomosis) from true re- currences (109). Also, using CTC for extraluminal surveillance requires use of intravenous contrast. Other issues are important to consider: CTC has relatively low sensitivity for the detection of flat and diminutive (<5 mm) colonic lesions (110), and sensitivity for nonadenomatous lesions (such as sessile serrated polyps), although not well-studied, is lower than for adenomas at comparable size thresholds (111, 112). Diminutive polyps have extremely low prevalence of advanced histology in average-risk patients; however, this might not apply to patients with CRC in whom even diminutive lesions could be clinically significant. There are no longitudinal studies examining the consequences of missing or nonreporting of diminutive flat lesions and nonadenomatous lesions in patients with CRC. In conclusion, although CTC has good diagnostic accuracy for cancer, the optimal timing of CTC in post-CRC resection surveillance and how it is best used in conjunction with other modalities remain undefined (109).
In patients with obstructive CRC precluding complete colonoscopy, we recommend CTC as the best alternative to exclude synchronous neoplasms. Double-contrast barium enema is an acceptable alternative if CTC is not available.
Strong recommendation, moderate-quality evidence
Older guaiac-based fecal occult blood tests are inferior to fecal immunochemical tests (FIT) for CRC screening (113). Limited data exist on the role of FIT for surveillance after CRC resection. One study (114) included 1736 patients with a personal or family history of colorectal neoplasia (24% had a personal history of CRC) who had undergone at least 2 colonoscopies and were offered an annual FIT. The diagnosis of CRC and advanced adenomas was made at a median of nearly 2 years earlier in patients with a positive FIT compared with those without testing, although it was unclear whether this applied to the subgroup of patients with personal history of CRC. The quality of the baseline examinations in this study was unknown; thus, it is possible that the interval cancers were lesions missed or incompletely resected, rather than metachronous lesions detected by FIT (115). Nevertheless, these data call for additional investigation to determine the role of FIT in postCRC resection surveillance.
Fecal DNA testing (116) has emerged as an option for CRC screening. Available data (117, 118) suggest that DNA abnormalities clear from stool after resection of colorectal neoplasms; however, the role of fecal DNA testing in surveillance programs after CRC resection is yet to be investigated.
There is insufficient evidence to recommend routine use of FIT or fecal DNA for surveillance after CRC resection.
The authors thank Kellie Kaneshiro, AMLS, AHIP (Research Informationist, Indiana University School of Medicine) for her expert help with the literature search. The views and opinions of authors expressed herein do not necessarily state or reflect those of the United States Government or the Department of Veterans Affairs.
Summary of Recommendations
We recommend that patients with CRC undergo high-quality perioperative clearing with colonoscopy. The procedure should be performed preoperatively or within a 3- to 6-month interval after surgery in the case of obstructive CRC. The goals of perioperative clearing colonoscopy are detection of synchronous cancer and detection and complete resection of precancerous polyps. We recommend that patients who have undergone curative resection of either colon or rectal cancer receive their first surveillance colonoscopy 1 year after surgery (or 1 year after the clearing perioperative colonoscopy). Additional surveillance recommendations apply to patients with rectal cancer (see “Additional Considerations in Surveillance of Rectal Cancer”). We recommend that, after the 1-year colonoscopy, the interval to the next colonoscopy should be 3 years (i.e., 4 years after surgery or perioperative colonoscopy), and then 5 years (i.e., 9 years after surgery or perioperative colonoscopy). Subsequent colonoscopies should occur at 5-year intervals, until the benefit of continued surveillance is outweighed by diminishing life expectancy. If neoplastic polyps are detected, the intervals between colonoscopies should be in accordance with the published guidelines for polyp surveillance intervals. These intervals do not apply to patients with Lynch syndrome. Patients with localized rectal cancer who have undergone surgery without total mesorectal excision, those who have undergone transanal local excision (transanal excision or transanal endoscopic microsurgery) or endoscopic submucosal dissection, and those with locally advanced rectal cancer who did not receive neoadjuvant chemoradiation and then surgery using total mesorectal excision techniques are at increased risk for local recurrence. In these situations, we suggest local surveillance with flexible sigmoidoscopy or EUS every 3–6 months for the first 2–3 years after surgery. These surveillance measures are in addition to recommended colonoscopic surveillance for metachronous neoplasia. In patients with obstructive CRC precluding complete colonoscopy, we recommend CTC as the best alternative to exclude synchronous neoplasms. Double-contrast barium enema is an acceptable alternative if CTC is not available. There is insufficient evidence to recommend the routine use of FIT or fecal DNA for surveillance after CRC resection.
1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015;65:5–29.
2. Meyerhardt JA, Mayer RJ. Follow-up strategies after curative resection of colorectal cancer. Semin Oncol 2003;30:349–360.
3. Pfister DG, Benson AB 3rd, Somerfield MR. Clinical practice. Surveillance strategies after curative treatment of colorectal cancer. N Engl J Med 2004;350:2375–2382.
4. Kjeldsen BJ, Kronborg O, Fenger C et al
. The pattern of recurrent colorectal cancer in a prospective randomised study and the characteristics of diagnostic tests. Int J Colorectal Dis 1997;12:329–334.
5. Rex DK, Kahi CJ, Levin B et al
. Guidelines for colonoscopy surveillance after cancer resection: a consensus update by the American Cancer Society and the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2006;130:1865–1871.
6. Edge SB, Byrd DR, Compton CC et al
. eds. AJCC Cancer Staging Manual 7th ed. Springer: New York. 2010.
7. Rex DK, Schoenfeld PS, Cohen J et al
. Quality indicators for colonoscopy. Gastrointest Endosc 2015;81:31–53.
8. Rex DK, Schoenfeld PS, Cohen J et al
. Quality indicators for colonoscopy. Am J Gastroenterol 2015;110:72–90.
9. Guyatt GH, Oxman AD, Vist GE et al
. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008;336:924–926.
10. Fisher DA, Jeffreys A, Grambow SC et al
. Mortality and follow-up colonoscopy after colorectal cancer. Am J Gastroenterol 2003;98:901–906.
11. Ramsey SD, Howlader N, Etzioni R et al
. Surveillance endoscopy does not improve survival for patients with local and regional stage colorectal cancer. Cancer 2007;109:2222–2228.
12. Rulyak SJ, Lieberman DA, Wagner EH et al
. Outcome of follow-up colon examination among a population-based cohort of colorectal cancer patients. Clin Gastroenterol Hepatol 2007;5:470–476 quiz 477.
13. Tjandra JJ, Chan MK. Follow-up after curative resection of colorectal cancer: a meta-analysis. Dis Colon Rectum 2007;50:1783–1799.
14. Pita-Fernandez S, Alhayek-Ai M, Gonzalez-Martin C et al
. Intensive follow-up strategies improve outcomes in nonmetastatic colorectal cancer patients after curative surgery: a systematic review and meta-analysis. Ann Oncol 2015;26:644–656.
15. Black WC, Haggstrom DA, Welch HG. All-cause mortality in randomized trials of cancer screening. J Natl Cancer Inst 2002;94:167–173.
16. Haggstrom DA, Imperiale TF. Surveillance approaches among colorectal cancer survivors after curative-intent. Minerva Gastroenterol Dietol 2009;55:483–500.
17. Kjeldsen BJ, Kronborg O, Fenger C et al
. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg 1997;84:666–669.
18. Makela JT, Laitinen SO, Kairaluoma MI. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg 1995;130:1062–1067.
19. Ohlsson B, Breland U, Ekberg H et al
. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis Colon Rectum 1995;38:619–626.
20. Pietra N, Sarli L, Costi R et al
. Role of follow-up in management of local recurrences of colorectal cancer: a prospective, randomized study. Dis Colon Rectum 1998;41:1127–1133.
21. Rodriguez-Moranta F, Salo J, Arcusa A et al
. Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial. J Clin Oncol 2006;24:386–393.
22. Schoemaker D, Black R, Giles L et al
. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology 1998;114:7–14.
23. Secco GB, Fardelli R, Gianquinto D et al
. Efficacy and cost of risk-adapted follow-up in patients after colorectal cancer surgery: a prospective, randomized and controlled trial. Eur J Surg Oncol 2002;28:418–423.
24. Wattchow DA, Weller DP, Esterman A et al
. General practice vs surgical-based follow-up for patients with colon cancer: randomised controlled trial. Br J Cancer 2006;94:1116–1121.
25. Primrose JN, Perera R, Gray A et al
. Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial. JAMA 2014;311:263–270.
26. Wang T, Cui Y, Huang WS et al
. The role of postoperative colonoscopic surveillance after radical surgery for colorectal cancer: a prospective, randomized clinical study. Gastrointest Endosc 2009;69:609–615.
27. Grossmann EM, Johnson FE, Virgo KS et al
. Follow-up of colorectal cancer patients after resection with curative intent-the GILDA trial. Surg Oncol 2004;13:119–124.
28. Baca B, Beart RW Jr, Etzioni DA. Surveillance after colorectal cancer resection: a systematic review. Dis Colon Rectum 2011;54:1036–1048.
29. Castells A. Postoperative surveillance in nonmetastatic colorectal cancer patients: yes, but. Ann Oncol 2015;26:615–617.
30. Rose J, Augestad KM, Cooper GS. Colorectal cancer surveillance: what's new and what's next. World J Gastroenterol 2014;20:1887–1897.
31. Young PE, Womeldorph CM, Johnson EK et al
. Early detection of colorectal cancer recurrence in patients undergoing surgery with curative intent: current status and challenges. J Cancer 2014;5:262–271.
32. Assessment of frequency of surveillance after curative resection in patients with stage II and III colorectal cancer. Available at http://www.clinicaltrials.gov/ct2/show/NCT00225641?term=colofol&rank=1
Accessed October 2, 2015.
33. Lepage C, Phelip JM, Cany L et al
. Effect of 5 years of imaging and CEA follow-up to detect recurrence of colorectal cancer: the FFCD PRODIGE 13 randomised phase III trial. Digest Liver Disease 2015;47:529–531.
34. Figueredo A, Rumble RB, Maroun J et al
. Follow-up of patients with curatively resected colorectal cancer: a practice guideline. BMC Cancer 2003;3:26.
35. Jeffery M, Hickey BE, Hider PN. Follow-up strategies for patients treated for non-metastatic colorectal cancer. Cochrane Database Syst Rev 2007 CD002200.
36. Renehan AG, Egger M, Saunders MP et al
. Impact on survival of intensive follow up after curative resection for colorectal cancer: systematic review and meta-analysis of randomised trials. BMJ 2002;324:813.
37. Allen JI. Where the dragon truly sleeps. Gastrointest Endosc 2009;69:616–619.
38. Singh A, Kuo YF, Goodwin JS. Many patients who undergo surgery for colorectal cancer receive surveillance colonoscopies earlier than recommended by guidelines. Clin Gastroenterol Hepatol 2013;11:65–72 e1.
39. Barillari P, Ramacciato G, Manetti G et al
. Surveillance of colorectal cancer: effectiveness of early detection of intraluminal recurrences on prognosis and survival of patients treated for cure. Dis Colon Rectum 1996;39:388–393.
40. Barrier A, Houry S, Huguier M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis 1998;13:93–98.
41. Granqvist S, Karlsson T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg 1992;158:307–312.
42. Hassan C, Gaglia P, Zullo A et al
. Endoscopic follow-up after colorectal cancer resection: an Italian multicentre study. Dig Liver Dis 2006;38:45–50.
43. Juhl G, Larson GM, Mullins R et al
. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg 1990;14:255–260 discussion 260-261.
44. Obrand DI, Gordon PH. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum 1997;40:15–24.
45. Togashi K, Konishi F, Ozawa A et al
. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum 2000;43:S47–S53.
46. Lee SY, Kim BC, Han KS et al
. Incidence and risk factors of metachronous colorectal neoplasm after curative resection of colorectal cancer in Korean patients. J Dig Dis 2014;15:367–376.
47. Le Clercq CM, Winkens B, Bakker CM et al
. Metachronous colorectal cancers result from missed lesions and non-compliance with surveillance. Gastrointest Endosc 2015;82:325–333 e2.
48. Samadder NJ, Curtin K, Wong J et al
. Epidemiology and familial risk of synchronous and metachronous colorectal cancer: a population-based study in Utah. Clin Gastroenterol Hepatol 2014;12:2078–2084 e1-2.
49. Tate JJ, Rawlinson J, Royle GT et al
. Pre-operative or postoperative colonic examination for synchronous lesions in colorectal cancer. Br J Surg 1988;75:1016–1018.
50. Milsom JW, Shukla P. Should intraoperative colonoscopy play a role in the surveillance for colorectal cancer? Dis Colon Rectum 2011;54:504–506.
51. Corley DA, Jensen CD, Marks AR et al
. Adenoma detection rate and risk of colorectal cancer and death. N Engl J Med 2014;370:1298–1306.
52. Kaminski MF, Regula J, Kraszewska E et al
. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med 2010;362:1795–1803.
53. Pohl H, Srivastava A, Bensen SP et al
. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology 2013;144:74–80 e1.
54. Kahi CJ, Anderson JC, Rex DK. Screening and surveillance for colorectal cancer: state of the art. Gastrointest Endosc 2013;77:335–350.
55. Chen F, Stuart M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum 1994;37:568–572.
56. Balleste B, Bessa X, Pinol V et al
. Detection of metachronous neoplasms in colorectal cancer patients: identification of risk factors. Dis Colon Rectum 2007;50:971–980.
57. Kawai K, Sunami E, Tsuno NH et al
. Polyp surveillance after surgery for colorectal cancer. Int J Colorectal Dis 2012;27:1087–1093.
58. Rajaratnam SG, Dennett ER. Development of metachronous neoplasms after colorectal cancer resection: absence of synchronous neoplasms predicts a lower risk. N Z Med J 2009;122:61–66.
59. Borda A, Martinez-Penuela JM, Borda F et al
. Drawing up an individual risk index for development of metachronous neoplastic lesions in resected colorectal cancer. Rev Esp Enferm Dig 2012;104:291–297.
60. Green RJ, Metlay JP, Propert K et al
. Surveillance for second primary colorectal cancer after adjuvant chemotherapy: an analysis of Intergroup 0089. Ann Intern Med 2002;136:261–269.
61. Moon CM, Cheon JH, Choi EH et al
. Advanced synchronous adenoma but not simple adenoma predicts the future development of metachronous neoplasia in patients with resected colorectal cancer. J Clin Gastro- enterol 2010;44:495–501.
62. Carballal S, Rodriguez-Alcalde D, Moreira L et al
. Colorectal cancer risk factors in patients with serrated polyposis syndrome: a large multicentre study. Gut 2015 Aug 11. pii: gutjnl-2015-309647 http://dx.doi.org/10.1136/gutjnl-2015-309647
[Epub ahead of print].
63. Lieberman DA, Rex DK, Winawer SJ et al
. Guidelines for colonoscopy surveillance after screening and poly- pectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2012;143:844–857.
64. Rex DK, Ahnen DJ, Baron JA et al
. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012;107:1315–1329 quiz 1314, 1330.
65. Das A, Chak A, Cooper GS. Temporal trend in relative risk of second primary colorectal cancer. Am J Gastroenterol 2006;101:1342–1347.
66. Mulder SA, Kranse R, Damhuis RA et al
. The incidence and risk factors of metachronous colorectal cancer: an indication for follow-up. Dis Colon Rectum 2012;55:522–531.
67. Bouvier AM, Latournerie M, Jooste V et al
. The lifelong risk of metachronous colorectal cancer justifies long-term colonoscopic follow-up. Eur J Cancer 2008;44:522–527.
68. Eckardt VF, Stamm H, Kanzler G et al
. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy 1994;26:523–527.
69. Freeman HJ. Natural history and long-term outcomes of patients treated for early stage colorectal cancer. Can J Gastroenterol 2013;27:409–413.
70. Khoury DA, Opelka FG, Beck DE et al
. Colon surveillance after colorectal cancer surgery. Dis Colon Rectum 1996;39:252–256.
71. Lan YT, Lin JK, Li AF et al
. Metachronous colorectal cancer: necessity of post-operative colonoscopic surveillance. Int J Colorectal Dis 2005;20:121–125.
72. Luchtefeld MA, Ross DS, Zander JD et al
. Late development of metachronous colorectal cancer. Dis Colon Rectum 1987;30:180–184.
73. Mathew J, Saklani AK, Borghol M. Surveillance colonoscopy in patients with colorectal cancer: how often should we be doing it? Surgeon 2006;4:3–5 62.
74. Patchett SE, Mulcahy HE, O'Donoghue DP. Colonoscopic surveillance after curative resection for colorectal cancer. Br J Surg 1993;80:1330–1332.
75. Skaife P, Seow-Choen F, Eu KW et al
. A novel indicator for surveillance colonoscopy following colorectal cancer resection. Colorectal Dis 2003;5:45–48.
76. Stigliano V, Fracasso P, Grassi A et al
. Endoscopic follow-up in resected colorectal cancer patients. J Exp Clin Cancer Res 2000;19:145–148.
77. Battersby NJ, Coupland A, Bouliotis G et al
. Metachronous colorectal cancer: a competing risks analysis with consideration for a stratified approach to surveillance colonoscopy. J Surg Oncol 2014;109:445–450.
78. Couch DG, Bullen N, Ward-Booth SE et al
. What interval between colorectal cancer resection and first surveillance colonoscopy? An audit of practice and yield. Colorectal disease: the official journal of the Association of Coloproctology of Great Britain and Ireland 2013;15:317–322.
79. McFarland RJ, Becciolini C, Lallemand RC. The value of colonoscopic surveillance following a diagnosis of colorectal cancer or adenomatous polyp. Eur J Surg Oncol 1991;17:514–518.
80. Castells A, Bessa X, Daniels M et al
. Value of postoperative surveillance after radical surgery for colorectal cancer: results of a cohort study. Dis Colon Rectum 1998;41:714–723 discussion 23-24.
81. Liu L, Lemmens VE, De Hingh IH et al
. Second primary cancers in subsites of colon and rectum in patients with previous colorectal cancer. Dis Colon Rectum 2013;56:158–168.
82. Limburg PJ, Ahlquist DA. Second primary colorectal cancer: the consequence of management failure at several potential levels. Ann Intern Med 2002;136:335–337.
83. Giardiello FM, Allen JI, Axilbund JE et al
. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol 2014;109:1159–1179.
84. Chen TA, Horng JT, Lin WC. Metachronous colorectal cancer in Taiwan: analyzing 20 years of data from Taiwan Cancer Registry. Int J Clin Oncol 2013;18:267–272.
85. Hassan C, Pickhardt PJ, Zullo A et al
. Cost-effectiveness of early colonoscopy surveillance after cancer resection. Dig Liver Disease 2009;41:881–885.
86. Lieberman DA, Weiss DG, Harford WV et al
. Five-year colon surveillance after screening colonoscopy. Gastroenterology 2007;133:1077–1085.
87. Cone MM, Beck DE, Hicks TE et al
. Timing of colonoscopy after resection for colorectal cancer: are we looking too soon? Dis Colon Rectum 2013;56:1233–1236.
88. Giardiello FM, Allen JI, Axilbund JE et al
. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2014;147:502–526.
89. Platell C, Salama P, Barwood N et al
. Performing a colonoscopy 12 months after surgery for colorectal neoplasia. ANZ J Surg 2005;75:282–285.
90. Kapiteijn E, Marijnen CA, Nagtegaal ID et al
. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 2001;345:638–646.
91. Mellgren A, Sirivongs P, Rothenberger DA et al
. Is local excision adequate therapy for early rectal cancer? Dis Colon Rectum 2000;43:1064–1071 discussion 1071-1074.
92. Paty PB, Nash GM, Baron P et al
. Long-term results of local excision for rectal cancer. Ann Surg 2002;236:522–529 discussion 529-530.
93. You YN, Baxter NN, Stewart A et al
. Is the increasing rate of local excision for stage I rectal cancer in the United States justified? A nationwide cohort study from the National Cancer Database. Ann Surg 2007;245:726–733.
94. Garcia-Aguilar J, Mellgren A, Sirivongs P et al
. Local excision of rectal cancer without adjuvant therapy: a word of caution. Ann Surg 2000;231:345–351.
95. Sajid MS, Farag S, Leung P et al
. Systematic review and meta-analysis of published trials comparing the effectiveness of transanal endoscopic microsurgery and radical resection in the management of early rectal cancer. Colorectal Dis 2014;16:2–14.
96. Chang AJ, Nahas CS, Araujo SE et al
. Early rectal cancer: local excision or radical surgery? J Surg Educ 2008;65:67–72.
97. Kawaguti FS, Nahas CS, Marques CF et al
. Endoscopic submucosal dissection versus transanal endoscopic microsurgery for the treatment of early rectal cancer. Surg Endosc 2014;28:1173–1179.
98. Park SU, Min YW, Shin JU et al
. Endoscopic submucosal dissection or transanal endoscopic microsurgery for nonpolypoid rectal high grade dysplasia and submucosa-invading rectal cancer. Endoscopy 2012;44:1031–1036.
99. Repici A, Hassan C, De Paula Pessoa D et al
. Efficacy and safety of endoscopic submucosal dissection for colorectal neoplasia: a systematic review. Endoscopy 2012;44:137–150.
100. Gleeson FC, Larson DW, Dozois EJ et al
. Local recurrence detection following transanal excision facilitated by EUS-FNA. Hepatogastroenterology 2012;59:1102–1107.
101. Morken JJ, Baxter NN, Madoff RD et al
. Endorectal ultrasound-directed biopsy: a useful technique to detect local recurrence of rectal cancer. Int J Colorectal Dis 2006;21:258–264.
102. Levin B, Lieberman DA, McFarland B et al
. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 2008;134:1570–1595.
103. Park SH, Lee JH, Lee SS et al
. CT colonography for detection and characterisation of synchronous proximal colonic lesions in patients with stenosing colorectal cancer. Gut 2012;61:1716–1722.
104. Rockey DC, Paulson E, Niedzwiecki D et al
. Analysis of air contrast barium enema, computed tomographic colonography, and colonoscopy: prospective comparison. Lancet 2005;365:305–311.
105. Sosna J, Sella T, Sy O et al
. Critical analysis of the performance of double-contrast barium enema for detecting colorectal polyps >or=6 mm in the era of CT colonography. AJR Am J Roentgenol 2008;190:374–385.
106. Halligan S, Wooldrage K, Dadswell E et al
. Computed tomographic colonography versus barium enema for diagnosis of colorectal cancer or large polyps in symptomatic patients (SIGGAR): a multicentre randomised trial. Lancet 2013;381:1185–1193.
107. Almond LM, Snelling S, Badiani S et al
. CT colonog- raphy after colorectal cancer resection: a one-stop assessment of metachronous mucosal lesions, local recurrence, and distant metastases. Radiology 2011;260:302–303.
108. Kim HJ, Park SH, Pickhardt PJ et al
. CT colonography for combined colonic and extracolonic surveillance after curative resection of colorectal cancer. Radiology 2010;257:697–704.
109. Hong N, Park SH. CT colonography in the diagnosis and management of colorectal cancer: emphasis on pre- and post-surgical evaluation. World J Gastroenterol 2014;20:2014–2022.
110. Pickhardt PJ. Missed lesions at CT colonography: lessons learned. Abdom Imaging 2013;38:82–97.
111. Park SH, Kim SY, Lee SS et al
. Sensitivity of CT colonography for nonpolypoid colorectal lesions interpreted by human readers and with computer-aided detection. AJR Am J Roentgenol 2009;193:70–78.
112. Pickhardt PJ, Choi JR, Hwang I et al
. Nonadenomatous polyps at CT colonography: prevalence, size distribution, and detection rates. Radiology 2004;232:784–790.
113. Levin B, Lieberman DA, McFarland B et al
. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. CA Cancer J Clin 2008;58:130–160.
114. Lane JM, Chow E, Young GP et al
. Interval fecal immunochemical testing in a colonoscopic surveillance program speeds detection of colorectal neoplasia. Gastroenterology 2010;139:1918–1926.
115. Lieberman D, Imperiale TF. Interval fecal immunochemical testing in colonoscopic surveillance program. Gastroenterology 2011;140:1359–1360 author reply 1360-1361.
116. Imperiale TF, Ransohoff DF, Itzkowitz SH et al
. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med 2014;370:1287–1297.
117. Kisiel JB, Yab TC, Taylor WR et al
. Stool methylated DNA markers decrease following colorectal cancer resection-implications for surveillance. Dig Dis Sci 2014;59:1764–1767.
118. Syngal S, Stoffel E, Chung D et al
. Detection of stool DNA mutations before and after treatment of colorectal neoplasia. Cancer 2006;106:277–283.
119. Kahi CJ, Haggstrom DA. Colonoscopy after Colorectal Cancer Resection. In:. Colonoscopy: Principles and Practice Second Edition eds Waye JD, Rex DK, Williams CB, Wiley-Blackwell: Oxford. UK. 2009. http://dx.doi.org/10.1002/9781444316902.ch55