13. Appropriateness of Colonoscopy: Surveillance After Curative Resection of Colorectal Cancer 1
Transcription
13. Appropriateness of Colonoscopy: Surveillance After Curative Resection of Colorectal Cancer 1
■ 664 ■■■■■■■■■■■■■■■■■■■■■■■■■■ Special Topic ■■■■■■■■■■■■■■■■■■■■■■■■■■ ■ 13. Appropriateness of Colonoscopy: Surveillance After Curative Resection of Colorectal Cancer 1 M. Bochud *, B. Burnand *, F. Froehlich **, R. W. Dubois ***, J.-P. Vader *, J.-J. Gonvers ** * Institut Universitaire de Médecine Sociale et Préventive, Lausanne, Switzerland ** Policlinique Médicale Universitaire, Lausanne, Switzerland *** Protocare Sciences, Santa Monica, USA Introduction Almost all cancers of the colon and rectum are carcinomas that develop from the mucosal epithelium. Cancer of the colon and of the rectum are generally considered together under the heading of colorectal cancers. Most of these cancers are adenocarcinomas, and the development of carcinoma from an adenomatous polyp is considered to be the most common developmental feature of colorectal cancer. Patients with previous adenomatous polyps or colorectal cancer have an increased risk of developing a further cancer. In Europe, the annual age-standardized incidence (world population) of colorectal cancer is between 20 and 45 per 100 000 among males and between 15 and 30 per 100 000 among females [1]. Incidence rates increase in a regular fashion with age [1 – 3]. Surveillance monitors people with previously diagnosed colorectal disease: patients who have had polyps (described in a separate article in this issue of the Journal [4]), inflammatory bowel disease (described in a joint article in this issue of the Journal [5]) and colorectal cancer (described in this article) [6]. In November 1998, a multidisciplinary European expert panel convened in Lausanne, Switzerland, to discuss and develop criteria for the appropriate use of gastrointestinal endoscopy, a widely-used procedure, regarded as highly accurate and safe. The RAND appropriateness method was chosen for this purpose, because it allows the development of appropriateness criteria based on published evidence and supplemented by explicit expert opinion. A detailed description of the RAND appropriateness method, including the literature search process [7], and of the whole process, as well as the global results of the panel [8], are published as separate articles in this issue of the Journal. The literature review was based on a systematic search of Medline, Endoscopy 1999; 31 (8): 664 – 672 © Georg Thieme Verlag Stuttgart New York ISSN 0013-726X • Embase and the Cochrane Library conducted up to the end of 1997 and completed with some key articles published in 1998. Updating and revision of the literature review is currently ongoing. This article contains three parts; 1. the review of the literature that was used by the panelists to support their ratings of appropriateness of use of colonoscopic surveillance after curative intent resection of colorectal cancer; 2. an overview of the main panel results; 3. a summary of the published evidence and of the panel based appropriateness criteria. 1. Literature Review Occurrence of Colorectal Cancer Cancer registry-based studies in Finland and Italy have shown an increase in incidence between the 1970s and the 1990s [3, 9]. In the USA, from 1950 to 1984, cancer incidence increased in men and slightly decreased in women, the survival rates increased in both sexes [10]. The US SEER (Surveillance, Epidemiology, and End Results) data for the period 1973 to1992 show a decrease in recent years of the incidence and mortality rates of colorectal cancer [6]. Slight increases in survival have been observed, although these are not always consistent. The cumulative incidence of colorectal cancer in patients with a positive family history (first-degree relative) is higher than for patients with a negative history [11]. The cumulative incidence at age 50 years in patients with a negative history is reached by age 35 – 40 years in those with a positive history [11]. 1 The European Panel on Appropriateness of Gastrointestinal Endoscopy (EPAGE, Lausanne, Switzerland) 13. Appropriateness of Colonoscopy: Surveillance After Curative Resection of Colorectal Cancer Natural History and Symptoms The adenoma-carcinoma sequence has been described in the chapter on polyps [4]. It has been estimated from indirect evidence that it takes an average of 10 years for the transformation of an adenomatous polyp into an invasive cancer [6]. Etiology and Epidemiology The prevalence of adenomas appears to differ by age, gender, race and geographical location, but the relative influence of host versus external factors is not clear. Genetic and environmental factors very probably interact, and their interplay may vary throughout the large intestine [12]. Hereditary non-polyposis colorectal cancer (HNPCC) and familial adenomatous polyposis (FAP) show an autosomal dominant predisposition, and correspond to 4 – 7 %, and 1 % of all colorectal cancers, respectively [13] while the risk of malignancy is 100 % [14]. The age distribution of colorectal cancer shows a predominance in patients > 50 years with less than 10 % of patients being younger than 50 [15]. A European cancer registry study [16] analyzing 68, 283 colorectal cancer cases found mean ages at diagnosis ranging from 65 to 71.5 years. In a retrospective study [17] of 1,112 patients operated on for colorectal cancer between 1961 and 1980, the authors described a steady increase with secular time in right-sided colonic cancer and a reduction in the overall incidence of rectal and rectosigmoidal carcinoma. This shift in predominance of location to the right colon is confirmed in a population-based cancer register study in the USA [12]. Some authors argue that aging of the population per se may be an important feature in the changing distribution of colorectal cancer [15]. A more frequent incidence of colorectal cancer in the right colon in women and in older patients has been frequently but not always observed [15, 16, 18 – 20]. Endoscopy 1999; 31 665 Inflammatory bowel disease accounts for less than 1 % of all colorectal cancer cases (see corresponding chapter) together with Peutz-Jeghers syndrome and familial juvenile polyposis, in which the colorectal cancer risk is elevated but not to such a great extent as in HNPCC and FAP [6]. Finally, patients with previous adenomatous polyps or colorectal cancer have an increased risk of developing a further cancer. Symptoms Several retrospective studies have examined the proportion of patients with colorectal cancer who had abdominal symptoms and signs prior to diagnosis: general symptoms (general weakness, diarrhea, constipation, weight loss), abdominal pain, change in bowel habits, bleeding, obstruction were commonly, however variously found [22 – 24]. In elderly patients with colorectal cancer, 18 % had abdominal pain, 40 % general symptoms and 38 % blood in the stools. A population-based retrospective study [25] analyzed symptoms at outset and their evolution over time (1940 – 1989): the proportion of symptomatic patients did not significantly differ, but the proportion of patients presenting with an obstruction decreased (from 30 % to 6 %) as well as the proportion of those with a rectal or abdominal mass and abdominal pain. Symptoms of overt bleeding and obstruction are more common with rectosigmoid cancers, weakness and abdominal mass occur more frequently in proximal cancers [6]. However, abdominal pain, constipation, change in stools and diarrhea were not associated with colorectal cancer in a prospective study [26] of 1,223 consecutive colonoscopies. To summarize, symptoms and signs are non-specific indicators of colorectal cancer because they are also frequent in people with other diseases [6]. Risk Factors Histology About 75 % of new cases of colorectal cancer occur in people with no known predisposing factors for the disease, who are considered to be at average risk [6]. The remaining cases occur in patients with a higher-than-average risk. Apart from patients with a genetic predisposition, patients with a family history of colorectal cancer, but without any currently-known genetic susceptibility, account for most of those at high risk (15 – 20 %) [6]. A large American prospective study [11] (combining results from the Nurses Health Study and the Health Professionals Follow-up Study) found an age-adjusted relative risk of colorectal cancer for both sexes of 1.72 (CI95: 1.34 – 2.19) in patients with a positive family history of colorectal cancer (first-degree relatives), with a higher risk among younger people (< 45). Another prospective study [14] and a large casecontrolled study in Utah reported similar results [21]. Young people (< 40) most often present with adenocarcinomas (87 %) mainly of intestinal type and rarely of mucinous (10 %) or other histological types [19]. Mucinous adenocarcinoma are rarer in older patients and occur more frequently in the right colon. Colon-Cancer Survival The Eurocare study [16] carried out a survival analysis on 68 ,283 colon cancer cases diagnosed from 1978 to 1985 in 21 populations in ten European countries. Significant intercountry colon cancer survival differences exist, which cannot be explained either by methodological or by demographic differences. For patients aged 60 to 69 years, the mean European 5-year cumulative relative survival rate was 40 %. However, an improvement in prognosis corresponding to a 4 % reduction in the risk of death per year 666 Endoscopy 1999; 31 M. Bochud et al. was observed in all countries. Age at diagnosis was inversely related to prognosis. A German multicentric observational study [27] in 1,121 patients with invasive rectum cancers found a 5-year survival rate of 55 % for patients without postoperative residual tumours, and 7 % for those with residual tumours. The 5year survival rate for people without distant metastases was 56 % and 8.7 % for those with metastases. Diagnostic Procedures Colonoscopy represents the best diagnostic procedure and has been shown to be superior to rigid sigmoidoscopy plus double contrast barium enema (DCBE) when colonic disease is suspected [28]. Colonoscopy has been shown, in a retrospective study in general clinical practice, to more effectively detect colorectal cancer, especially at an early stage, (sensitivity 97.3 %) than DCBE (sensibility 87 %) [29]. In a large non-randomised controlled trial [30], including 21,000 patients aged 40 years and older, mainly asymptomatic, DCBE missed 25 % of the lesions found at colonoscopy. Therapeutic Endoscopy Early invasive colorectal cancer can be treated locally either by endoscopic or local excision: the reported incidence of lymph node metastases in such cases ranges from 0 to 15.4 %. Kikuchi detected no colorectal cancer-related deaths after a 5-year follow-up [39]. Patients with pedunculated or subpedunculated polyps that can be easily excised by endoscopic polypectomy are at low risk of lymph node metastases. Tumour localisation in the rectum is associated with more lymph node metastases [39]. Patients with submucosal carcinoma invasion should undergo bowel resection [39]. Rationale for Surveillance After Surgical Resection The two main goals of colorectal cancer follow-up are first to detect a recurrence and second to detect new primary cancers, that is metachronous tumours [36, 40]. A prospective study [41] in 321 patients with excision of colonic neoplasms found polyps in 12.5 %, benign strictures in 7.1 %, ulceration in 3.2 % and a carcinoma recurrence in 3.6 % within a period of two years after surgery. Rates of Metachronous Cancers and Cancer Recurrences Several other studies indicated better diagnostic performance by colonoscopy [31, 32]. However, insufficient procedural competence and experience on the part of the endoscopist may decrease test performance [6]. Miss rates are low for adenomas > 1 cm but there are significant miss rates for adenomas < 1 cm [33]. In several retrospective [22, 42] and prospective studies [18, 43, 44], one meta-analysis of follow-up studies of patients operated on curatively [45] and one RCT [37], recurrences occured in approximately one-third of patients (24 – 39 % in follow-up studies) and metachronous cancers were found in 1 – 5 % of patients. Treatment, Surveillance and Prevention Surgery is the primary treatment modality for most colorectal cancers. Special subgroups of patients can benefit from adjuvant chemotherapy or radiotherapy. Nearly twothirds of patients are treated curatively [18, 34], but 26 – 50 % of these will experience a recurrence [35 – 37]. Patients in whom cancer is diagnosed at an early stage have a better survival rate than those with advanced cancers [38] (Table 1). Table 1 Survival rates of patients with colorectal cancer according to Duke’s stage Study Mandel 1993 [39] N Duke's Stage 46 551 5-yr survival (%) A B C D Average 94.3 84.4 56.6 2.4 70.0 Although local recurrences appear to occur frequently, in 47 % of cases, after an average follow-up period of four years [37], intraluminal recurrences are relatively uncommon (6 – 14 %) [43, 46] and metastases are frequent (53 – 54 %) [37, 43]. When Do Recurrences Occur? Most recurrences occur within two years of initial surgery [23, 34, 35, 47, 48]. Few recurrences (1 – 12 %) occur after five years [37, 49, 23, 46]. In a prospective study, the mean time to detection of recurrence ranged from 18 to 27 months [50], from 4 to 156 months in a large but much less recent prospective study [18]. A median time to recurrence of 16.7 months has also been observed [46]. It appears that left-sided primary tumours recur somewhat more often (3 – 9 %) than right sided ones [23, 47, 48, 50], and those more frequently in the rectum [46, 50]. Recurrences According to Primary Tumour Stage A more advanced stage of the primary tumour is associated with a higher recurrence rate [47, 48] (Table 2). Endoscopy 1999; 31 667 13. Appropriateness of Colonoscopy: Surveillance After Curative Resection of Colorectal Cancer Table 2 Recurrences of colorectal cancer according to primary tumour stage Study Pub. date Design N No. (%) of recurrences in Duke’s A No. (%) of No. (%) of No. (%) of No. (%) of Comments recurrences recurrences recurrences recurrences in Duke’s B1 in Duke’s B2 in Duke’s C1 in Duke’s C2 Adloff et al. [48] 1989 cohort 322 (follow-up program) 1/15 (7 %) 5/55 (9 %) 29/146 (20 %) 4/9 (44 %) 53/97 (55 %) Adolff et al. [48] 1989 cohort 587 (no follow-up) 4/66 (6 %) 11/71 (15 %) 98/286 (34 %) 7/15 (47 %) 96/149 (64 %) Mäkelä et al. [55] 1995 RCT 106 10/28 (18 %) 18/48 (37 %) 15/30 (50 %) Kjeldsen et al. [50] Ovaska et al. [36] 1997 RCT 597 (13 %) (20 %) (48 %) 1989 cohort 402 15/1 13 (13 %) 58/212 (27 %) 47/77 (61 %) Symptoms of Recurrent Disease Symptoms of recurrence are abdominal or perineal pain, change in bowel habits, rectal and vaginal bleeding, anorexia and weight loss, cough or bone pain. About one half of recurrent cancers diagnosed are associated with symptoms [18, 23, 51] . Efficacy of Diagnostic Tools to Detect Recurrences Clinical examination has a sensitivity of about 58 – 73 % and a specificity of about 100 % for detection of recurrent cancers [50]. Most blood tests have a low sensitivity and few controlled studies are available to support their use [51]. Increased CEA levels are found in only 25 % of patients with early cancer and in 75 % with advanced cancer. Twenty percent of colorectal cancers do not impact on CEA level. The reported sensitivity of CEA in detecting colorectal cancer recurrence ranges from 58 % to 89 %, and the specificity from 75 % to 98 % [35]. Although numerous studies have examined the possible benefit of CEA in detecting recurrences, no comparative study has demonstrated its usefulness in reducing mortality [35, 51]. Ultrasonography is useful for detecting liver metastases with an estimated sensitivity and specificity of 92 – 94 % and 99 – 100 %, respectively [50]. Thoracic imaging is generally recommended each year for detection of lung metastases [51]. people were included in a regular followup program on a volunteer basis people who refused to have regular follow-up and consulted when symptoms appeared patients of both groups had rather intensive follow-up follow-up 18 – 60 months Double-contrast barium enema is less sensitive for detection of early neoplasia than colonoscopy [32]. The specificity of colonoscopy to detect an intraluminal recurrence is close to 100 % (CI95: 97 – 100) and the sensibility 57 % (CI95: 34 – 78) [50]. However, because most local recurrences are extraluminal, it has been considered that colonoscopy alone is of limited usefulness in the detection of recurrences [43, 51]. Impact of Different Surveillance Programmes on Patient Outcome The rationale for early diagnosis of recurrence is that it could improve the curative resection rate of colorectal cancer [37]. It would thus seem reasonable to think that this could improve the long-term prognosis of patients; however, the evidence currently available in favour of an intensive follow-up programme vs. a less intensive one is weak. A meta-analysis [45] including seven cohort studies (N = 3,283), found no significant difference if all study results were combined. However, a 9 % better 5-year survival rate in patients with intensive follow-up after colorectal cancer surgery was found if only the studies including CEA testing were pooled. In this meta-analysis, the cumulative recurrence rate of patients undergoing intensive follow-up was approximately 16 % at one year, 25 % at two years, 30 % at three years, 34 % at four years and 37 % at five years. These results should be viewed with caution as no randomized controlled trial was available at that time and because the heterogeneity of the follow-up protocols. 668 Endoscopy 1999; 31 Table 3 M. Bochud et al. Randomized controlled trials of various surveillance follow-up programmes after colorectal cancer surgery Study Publication date and place N Sexes (M/F) Age Groups compared Mäkelä 1995 [56] 1995, Finland 106 52/54 63/69 (± 15) conventional intensive vs. intensified follow-up follow-up did not improve 5 year survival of reresectability Ohlsson 1995 [55] 1995, Sweden 107 51/56 65 (40 – 83) intense vs. no follow-up Kjeldsen 1997 [38] 1997, Denmark 597 326/271 <76 intense vs. virtually no follow-up (5, 10 and 15 yr) Northover (unpublisehd) Schoemaker 1998 [57] 1996, UK 1998, Australia 213 207/1 18 69/67 intensive vs. standard follow-up 325 The crucial role of CEA was indeed not supported by many other studies [52, 53]. A recent, thorough and systematic review [35] has identified three published randomized controlled trials [37, 54, 55] and one unpublished study comparing different postoperative surveillance programmes (Table 3). No evidence of an improved survival rate with an intensified follow-up could be demonstrated. Two randomized trials [37, 56] have been published since Richard’s review. In their study, Schoemaker et al. [56] failed to show any benefit from an Main result Definition of intense follow-up history, status, FOBT, blood tests, chest x-ray and CEA every 3 mo for 2 yr and then every 6 mo for 3 yr, liver US every 6 mo, yearly CT history, status, intensive FOBT, blood follow-up tests, chest did not x-ray and CEA improve every 3 mo for survival 2 yr and then every 6 mo for 3 yr, pelvis CT at 3, 6, 12, 18 and 24 mo (those with abdominoperineal resection) no improve- medical history ment in and examinaoverall tion, digital survival or rectal exam, in cancergyn exam, related FOBT, chest, survival x-ray, Hb, ERS, liver enzymes at 6, 12, 18, 24, 30, 48, 60, 120, 150, 180 mo Endoscopic controls in intense follow-up Comment colonoscopy at 3 mo and then yearly the main difference between the 2 groups is liver US and CT rigid sigmoid- lack of oscopy every power to 3 mo for 2 yr detect a difference in and then mortality every 6 mo for 3 yr, colonoscopy at 3, 15, 30 and 60 mo; endoscopic control (colo or sigmo) of the anastomosis at 9, 21 and 42 mo colonoscopy patients in at 6, 12, 18, the intensive 24, 30, 48, follow-up 60, 120, group had 150, 180 mo earlier diagnosis of recurrence and more frequent new surgery with curative intent; no CEA used unpublished study no signifhistory and yearly yearly coloicant differ- clinical exami- colonoscopy noscopy ence in nation, liver CT; failed to desurvival be- colonoscopy, tect any tween the chest x-rays, asymptom2 groups at simple screening atic local 5 years yearly recurrences follow-up intensive follow-up on survival rate and of colonoscopy to detect early recurrences. A Danish study [37] found no improvement of survival rate with intensive follow-up but did, however, report an earlier diagnosis (9 months) and a greater “resectability” of recurrence. Richard et al. [35] further identified five published cohort studies [34, 44, 49, 57, 58] comparing follow-up with no follow-up (four of which were included in Bruinvels metaanalysis). The only study [44] to show a significant reduction in the 5-year mortality rate had significant methodo- 13. Appropriateness of Colonoscopy: Surveillance After Curative Resection of Colorectal Cancer logical weaknesses. In addition, because they were written in foreign languages, Richard et al excluded two cohort studies [48, 59] which indicated favourable results of follow-up compared to no follow-up. One of the cohort studies [44] suggests that highly compliant patients (42 % of patients) have a significantly better survival rate at five years (80 % vs. 59 %, P < 0.002) than non-compliant patients (27 %) and partially compliant patients (32 %). This latter group had the worst outcome, non-compliant patients were older, but the groups compared had similar tumour stages. The specific role of endoscopic surveillance cannot, however, be estimated from these studies, because no study compared groups with and without endoscopy, and the follow-up programmes always included several other tests in addition. From a separate analysis of the characteristics of diagnostic tests in their randomised controlled study [50], Kjeldsen et al. indicated that clinical examination, digital rectal examination, proctoscopy, colonoscopy and chest Xray would be the most useful tests to be included in a follow-up programme. The other diagnostic tests were found to have too low a sensitivity to be useful (blood hemoglobin, FOBT, double-contrast barium enema, liver enzymes). Actually, there are trends moving towards the simplification of surveillance programs. In a clinical update published by the ASGE, Rex emphasised that the primary purpose of surveillance colonoscopy after surgical resection of a colon cancer is to detect metachronous adenomas and not recurrent cancer [60]. If clearing colonoscopy has not been performed preoperatively, it should be done 2 – 3 months postoperatively [60]. Surveillance colonoscopy should then be performed at 3 – 5 year intervals or according to associated polyp findings, similarly to post-polypectomy surveillance: 3 years on average, 5 years after removal of a single tubular adenoma, shorter intervals when numerous adenomas or large sessile adenomas have been removed [60]. Endoscopy 1999; 31 669 Table 4 Definition of terms for screening for colorectal cancer after curative intent resection of a colorectal cancer Adenomas’ features and the associated risk for colorectal cancer. Findings at the previous or index colonoscopy High risk Any of the following: – villous or tubulo-villous histology – size ≥ 1 cm – multiple adenomas – large sessile adenomas – high grade dysplasia Low risk All of the following: – single adenoma – size < 1 cm – tubular histology or non-neoplastic polyp Clinical Variables The clinical variables used for surveillance after curative intent resection of colorectal cancer are shown in Table 5. A series of 3 indications examined the appropriateness of colonoscopy in presence of rising CEA levels in patients with successful colon cancer resection. Table 5 Surveillance following curative intent resection of colorectal cancer (15 items) Variables Number of categories Categories Diagnosis of colonoscopy performed since resection 4 Interval since last colonoscopy 3 Interval since resection 3 2. Panel Results Evaluation done 3 Considering the above review of relevant literature, the panel evaluated 15 specific theoretical patient scenarios related to the use of colonoscopy for surveillance after curative intent resection of colorectal cancer, using an explicit two round modified Delphi panel expert method (RAND appropriateness method) which is described in a joint publication [7]. – no colonoscopy since resection – no polyp or sign of colorectal cancer – low risk polyp – high risk polyp – 1 – < 3 years ago – 3 – < 5 years ago – ≥ 5 years ago – 1 – < 3 years – 3 – < 5 years – ≥ 5 years ago – no abdominal US or CT – abdominal US or CT done, negative – abdominal US or CT done, positive General Panel Results Definition of Terms All terms and definitions were reviewed and approved by the panelists; they are listed in Table 4. Patients with a history of familial adenomatous polyposis (FAP) or a history of non polyposis hereditary colorectal cancer (NPHCC) were excluded. In addition, only patients with a “clean” colon at the index or previous colonoscopy were considered. Surveillance following curative intent resection of colorectal cancer was assessed in 15 clinical scenarios. Four scenarios were rated as inappropriate, 1 as uncertain and 10 as appropriate. Agreement between panelists was obtained in 10/15 scenarios. 670 Endoscopy 1999; 31 Specific Clinical Panel Results The main results are worded as an overall statement representing several clinical scenarios in Table 6. In some cases, the same scenario may apply to more than one statement. Detailed appropriateness and necessity criteria are available in a computerized form accessible via Internet (http:// www.epage.ch). Table 6 Description of appropriateness of indications for colonoscopy for surveillance after curative intent resection of colorectal cancer Clinical situation In individuals who received no colonoscopy since curative intent resection of colorectal cancer, indication for colonoscopy is appropriate after 5 years of follow-up (possibly appropriate after 1 year of follow-up) In individuals who received at least one colonoscopy since curative intent resection of colorectal cancer, indication for colonoscopy is appropriate – after 1 year of follow-up if last surveillance colonoscopy showed high risk adenomas – after 3 years of follow-up if last surveillance colonoscopy showed low risk adenomas – after 5 years of follow-up if last surveillance colonoscopy showed no adenomas and no cancer inappropriate – before 3 years of follow-up if last surveillance colonoscopy showed no or low risk adenomas and no cancer In individuals with rising CEA levels, indication for colonoscopy is appropriate in presence of a negative abdominal imaging (US*, CT1) * US: ultrasonography, 1 CT: computed tomography Description of Necessity Three out of the fifteen scenarios were judged necessary (20 %). Essentially, if no colonoscopy has been performed since curative intent resection of a colorectal cancer, it has been considered necessary to perform a colonoscopy after 5 years of follow-up. If a follow-up colonoscopy has already been performed, a subsequent colonoscopy is necessary after 3 years if high risk adenomas were found at the surveillance colonoscopy. In presence of rising CEA levels, in no situation was colonoscopy considered necessary. 3. Conclusions Although colonoscopy has been considered to be an essential diagnostic tool in a surveillance programme after curative intent resection of a colorectal cancer [48], the available evidence from RCTs and systematic reviews does not indicate a major improvement of survival rate with an intensive follow-up including colonoscopy. A small improvement in survival (20 % or less) cannot be definitely excluded. Colonoscopy has been considered as possibly useful to detect metachronous cancers, and it has been suggested M. Bochud et al. that a schedule similar to post-polypectomy surveillance should be used [6, 60]. Despite this relatively poor scientific evidence, surveillance colonoscopy was often considered appropriate by the multidisciplinary panel at some point after curative intent resection of a colorectal cancer. Subsequent follow-up colonoscopies were essentially considered appropriate, and sometimes also necessary, according to the level of risk of developing a new cancer (e.g. sooner in presence of high risk adenomas). Acknowledgement The authors gratefully acknowledge the selfless commitment and invaluable contribution of the expert panel members, who made this project possible: Marcello Anti (IT), Peter Bytzer (DK), Mark Cottrill (UK), Michael Fried (CH), Roar Johnsen (NO), Gerd Kanzler (DE), François Lacaine (FR), Cornelis Lamers (NL), Roger J. Leicester (UK), Mattijs E. Numans (NL), Javier P. Piqueras (ES), Jean-François Rey (FR), Giacomo Sturniolo (IT), Robert P. Walt (UK). This work was supported by the EU BIOMED II Programme (BMH4-CT96-1202), the Swiss National Science Foundation (32.40522.94) and the Swiss Federal Office of Education and Science (95.0306-2). References 1 Parkin DM, Whelan SL, Ferlay J, Raymond L, Young J. International Agency for Research on Cancer. WHO and International Association of cancer registries (eds). Cancer incidence in five continents. Lyon: VII. IARC Scientific Publications 1997; 143 2 Cooper GS, Yuan Z, Landefeld CS, Johanson JF, Rimm AA. A national population-based study of incidence of colorectal cancer and age. Implications for screening in older Americans. Cancer 1995; 75: 775 – 781 3 Capocaccia R, De Angelis R, Frova L, Gatta G, Sant M, Micheli A, Berrino F, Conti E, Gafa L, Roncucci L, et al. Estimation and projections of colorectal cancer trends in Italy. Int J Epidemiol 1997; 26: 924 – 932 4 Bochud M, Burnand B, Froehlich F, Dubois RW, Vader JP, Gonvers JJ. Appropriateness of colonoscopy: Surveillance after polypectomy. Endoscopy 1999; 31: 654 – 663 5 Froehlich F, Larequi-Lauber T, Gonvers JJ, Dubois RW, Burnand B, Vader JP. Appropriateness of colonoscopy: Inflammatory bowel disease. Endoscopy 1999; 31: 647 – 653 6 Winawer SJ, Fletcher RH, Miller L, Godlee F, Stolar MH, Mulrow CD, Woolf SH, Glick SN, Ganiats TG, Bond JH, et al. Colorectal cancer screening – clinical guidelines and rationale (1997; 112: 594). Gastroenterology. 1997; 112: 1060 – 1063 7 Vader JP, Burnand B, Froehlich F, Dubois RW, Bochud M, Gonvers JJ. The European Panel on Appropriateness of Gastrointestinal Endoscopy (EPAGE): Project and methods. Endoscopy 1999; 31: 672 – 678 8 Vader JP, Froehlich F, Dubois RW, Beglinger C, Wietlisbach V, Pittet V, Ebel N, Gonvers JJ, Burnand B. The European Panel on the Appropriateness of Gastrointestinal Endoscopy (EPAGE): Conclusions and WWW site. Endoscopy 1999; 31: 678 – 694 13. Appropriateness of Colonoscopy: Surveillance After Curative Resection of Colorectal Cancer 9 Kemppainen M, Raiha I, Sourander L. A marked increase in the incidence of colorectal cancer over two decades in SouthWest Finland. Journal of Clinical Epidemiology 1997; 50: 147 – 151 10 Chu KC, Tarone RE, Chow WH, Hankey BF, Ries LA. Temporal patterns in colorectal cancer incidence, survival, and mortality from 1950 through 1990. Journal of the National Cancer Institute 1994; 86: 997 – 1006 11 Fuchs CS, Giovannucci EL, Colditz GA, Hunter DJ, Speizer EE, Willett WC. A prospective study of family history and the risk of colorectal cancer. N Engl J Med 1994; 33: 1669 – 1674 12 Devesa SS, Chow WH. Variation in colorectal cancer incidence in the United States by subsite of origin. Cancer 1993; 71: 3819 – 3826 13 Dunlop MG. Science, medicine, and the future – colorectal cancer. BMJ 1997; 314: 1882 – 1885 14 Orrom WJ, Brzezinski WS, Wiens EW. Heredity and colorectal cancer. A prospective, community-based, endoscopic study. Dis Colon Rectum 1990; 33: 490 – 493 15 Fleshner P, Slater G, Aufses AHJ. Age and sex distribution of patients with colorectal cancer (see comments). Dis Colon Rectum 1989; 32: 107 – 111 16 Sant M, Capocaccia R, Verdecchia A, Gatta G, Micheli A, Mariotto A, Hakulinen T, Berrino F. Comparisons of colon-cancer survival among European countries: The Eurocare Study. Int J Cancer 1995; 63: 43 – 48 17 Greene FL. Distribution of colorectal neoplasms. A left to right shift of polyps and cancer. Am Surg 1983; 49: 62 – 65 18 Tornqvist A, Ekelund G, Leandoer L. Early diagnosis of metachronous colorectal carcinoma. Aust N Z J Surg 1981; 51: 442 – 445 19 Griffin PM, Liff JM, Greenberg RS, Clark WS. Adenocarcinomas of the colon and rectum in persons under 40 years old. A population-based study. Gastroenterology 1991; 100: 1033 – 1040 20 Alley PG, McNee RK. Age and sex differences in right colon cancer. Dis Colon Rectum 1986; 29: 227 – 229 21 Slattery ML, Kerber RA. Family history of cancer and colon cancer risk: the Utah Population Database (published erratum appears in J Natl Cancer Inst Dec 7, 1994: 86: 1802). J Natl Cancer Inst 1994; 86: 1618 – 1626 22 Kemppainen M, Raiha I, Rajala T, Sourander L. Characteristics of colorectal cancer in elderly patients. Gerontology 1993; 39: 222 – 227 23 Lautenbach E, Forde KA, Neugut AI. Benefits of colonoscopic surveillance after curative resection of colorectal cancer. Annals of Surgery 1994; 220: 206 – 211 24 Raftery TL, Samson N. Carcinoma of the colon: a clinical correlation between presenting symptoms and survival. American Surgeon 1980; 46: 600 – 606 25 Beard CM, Spencer RJ, Weiland LH, O’Fallon WM, Melton LJ. Trends in colorectal cancer over a half century in Rochester, Minnesota, 1940 to 1989. Ann Epidemol 1995; 5: 210 – 214 26 Chak A, Post AB, Cooper GS. Clinical variables associated with colorectal cancer on colonoscopy: a prediction model. Am J Gastroenterol 1996; 91: 2483 – 2488 27 Hermanek P, Wiebelt H, Staimmer D, Riedl S. Prognostic factors of rectum carcinoma – experience of the German Multicentre Study SGCRC. German Study Group Colo-Rectal Carcinoma. Tumori 1995; 81: 60 – 64 28 Lindsay DC, Freeman JG, Cobden I, Record CO. Should colonoscopy be the first investigation for colonic disease? British Medical Journal Clinical Research Ed 1988; 1988: 167 – 169 29 Endoscopy 1999; 31 671 Rex DK, Rahmani EY, Haseman JH, Lemmel GT, Kaster S, Buckley JS. Relative sensitivity of colonoscopy and barium enema for detection of colorectal cancer in clinical practice (see comments). Gastroenterology 1997; 112: 17 – 23 30 Winawer SJ, Flehinger BJ, Schottenfeld D, Miller DG. Screening for colorectal cancer with fecal occult blood testing and sigmoidoscopy. Journal of the National Cancer Institute 1993; 85: 1311 – 1318 31 Steine S, Stordahl A, Lunde OC, Loken K, Laerum E. Doublecontrast barium enema versus colonoscopy in the diagnosis of neoplastic disorders: aspects of decision-making in general practice. Family Practice 1993; 10: 288 – 291 32 Thorson AG, Christensen MA, Davis SJ. The role of colonoscopy in the assessment of patients with colorectal cancer. Dis Colon Rectum 1986; 29: 306 – 311 33 Rex DK, Cutler CS, Lemmel GT, Rahmani EY, Clark DW, Helper DJ, Lehman GA, Mark DG. Colonoscopic miss rates in adenomas determined by back-to-back colonoscopies (see comments). Gastroenterology 1997; 112: 24 – 28 34 Ekman CA, Gustavson J, Henning A. Value of a follow-up study of recurrent carcinoma of the colon and rectum. Surg Gynecol Obstet 1977; 145: 895 – 897 35 Richard CS, McLeod RS. Follow-up of patients after resection for colorectal cancer: a position paper of the canadian society of surgical oncology and the canadian society of colon and rectal surgeons. Canadian Journal of Surgery 1997; 40: 90 – 100 36 Ovaska JT, Jarvinen HJ, Mecklin JP. The value of a follow-up programme after radical surgery for colorectal carcinoma. Scan J Gastroenterol 1989; 24: 416 – 422 37 Kjeldsen BJ, Kronborg O, Fenger C, Jorgensen OD. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br J Surg 1997; 84: 666 – 669 38 Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, Ederer F. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota colon cancer control study. N Engl J Med 1993; 328: 1365 – 1371 39 Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, Uchida Y. Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum 1995; 38: 1286 – 1295 40 Vernava AM3, Longo WE, Virgo KS, Coplin MA, Wade TP, Johnson FE. Current follow-up strategies after resection of colon cancer. Results of a survey of members of the American society of colon and rectal surgeons. Dis Colon Rectum 1994; 37: 573 – 583 41 Weinstock LB, Shatz BA. Endoscopic abnormalities of the anastomosis following resection of colonic neoplasm. Gastrointest Endosc 1994; 40: 558 – 561 42 Luchtefeld MA, Ross DS, Zander JD, Folse JR. Late development of metachronous colorectal cancer. Dis Colon Rectum 1987; 30: 180 – 184 43 Barkin JS, Cohen ME, Flaxman M, Lindblad AS, Mayer RJ, Kalser MH, Steinberg SM. Value of routine follow-up endoscopy program for the detection of recurrent colorectal carcinoma. Am J Gastroenterol 1988; 83: 1355 – 1360 44 Eckardt VF, Stamm H, Kanzler G, Bernhard G. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy 1994; 26: 523 – 527 45 Bruinvels DJ, Stiggelbout AM, Kievit J, van Houwelingen HC, Habbema JD, van de Velde CJ. Follow-up of patients with colorectal cancer. A meta-analysis. Annals of Surgery 1994; 219: 174 – 182 672 Endoscopy 1999; 31 46 Galandiuk S, Wieand HS, Moertel CG, Cha SS, Fitzgibbons RJJ, Pemberton JH, Wolff BG. Patterns of recurrence after curative resection of carcinoma of the colon and rectum. Surg Gynecol Obstet 1992; 174: 27 – 32 47 Barillari P, Ramacciato G, Manetti G, Bovino A, Sammartino P, Stipa V. 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 48 Adloff M, Arnaud JP, Ollier JC, Schloegel M. Can the prognosis of patients treated surgically in cancer of the rectum or colon be improved by follow-up? Prospective study of 909 patients. Chirurgie 1989; 115: 228 – 236 49 Tornqvist A, Ekelund G, Leandoer L. The value of intensive follow-up after curative resection for colorectal carcinoma. Br J Surg 1982; 69: 725 – 728 50 Kjeldsen BJ, Kronborg O, Fenger C, Jorgensen OD. The pattern of recurrent colorectal cancer in a prospective randomised study and the characteristics of diagnostic tests (in Process Citation). Int J Colorectal Dis 1997; 12: 329 – 334 51 Kronborg O. Optimal follow-up in colorectal cancer patients: what tests and how often? Semin Surg Oncol 1994; 10: 217 – 224 52 Moertel CG, Fleming TR, Macdonald JS, Haller DG, Laurie JA, Tangen C. An evaluation of the carcinoembryonic antigen (CEA) test for monitoring patients with resected colon cancer. JAMA 1993; 270: 943 – 947 53 Minton JP, Hoehn JL, Gerber DM, Horsley JS, Connolly DP, Salwan F, Fletcher WS, Cruz ABJ, Gatchell FG, Oviedo M. Results of a 400-patient carcinoembryonic antigen second-look colorectal cancer study. Cancer 1985; 55: 1284 – 1290 54 Ohlsson B, Breland U, Ekberg H, Graffner H, Tranberg KG. Follow-up after curative surgery for colorectal carinoma. Randomized comparison with no follow-up. Dis Colon Rectum 1995; 38: 619 – 626 55 Makela JT, Laitinen SO, Kairaluoma MI. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Archives of Surgery 1995; 130: 1062 – 1067 56 Schoemaker D, Black R, Giles L, Toouli J. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology 1998; 114: 7 – 14 57 Ovaska J, Jarvinen H, Kujari H, Perttila I, Mecklin JP. Followup of patients operated on for colorectal carcinoma. American Journal of Surgery 1990; 159: 593 – 596 58 Pugliese V, Aste H, Saccomanno S, Bruzzi P, Bonelli L, Santi L. Outcome of follow-up programs in patients previously resected for colorectal cancer. Tumori 1984; 70: 203 – 208 59 Mentges B, Stahlschmidt M, Bruckner R. Effectiveness of after-care in colonic cancer. Langenbecks Arch Chir 1987; 370: 223 – 234 60 Rex DK. Surveillance colonoscopy after resection of colorectal polyps and cancer. ASGE Clinical Update 1998; 6: 1 – 4 M. Bochud et al. Corresponding Author Dr. Bernard Burnand IUMSP Bugnon 17 CH-1005 Lausanne Switzerland Fax: + 41-21-3144954 E-mail: [email protected]