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: Bernard.Burnand@inst.hospvd.ch