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Journal of Surgical Oncology 2010;101:396–400

Preoperative Carcinoembryonic Antigen Level as an Independent Prognostic

Factor in Potentially Curative Colon Cancer

JUNG WOOK HUH, MD, BYUNG RYUL OH, MD, HYEONG ROK KIM, MD, AND YOUNG JIN KIM, MD*
Department of Surgery, Chonnam National University Hwasun Hospital and Medical School, Gwangju, Korea

Objective: We evaluated the prognostic value of the preoperative serum carcinoembryonic antigen (CEA) level in patients with colon cancer.
Methods: We reviewed 474 patients who underwent potentially curative resection for nonmetastatic colon cancer. Patients were categorized into
two groups according to the preoperative serum CEA level: low CEA (<5 ng/ml) and high CEA (
5 ng/ml) groups.
Results: During the median 45-month follow-up period, the 5-year overall and disease-free survival rates for patients with a low CEA level were
81.7% and 82.4%, respectively, which were significantly higher than the rates for those with a high CEA level (69.9%; P ¼ 0.011 and 70.6%;
P ¼ 0.002, respectively). A multivariate analysis revealed that a preoperative serum CEA level was a significant independent prognostic factor for
both overall survival (P ¼ 0.021) and disease-free survival (P ¼ 0.026). Both the overall and disease-free survival rates in patients with stage II
tumors differed significantly between the low and high CEA groups, whereas the rates did not different between those with stage I and III tumors.
Conclusions: Preoperative serum CEA is a reliable predictor of recurrence and survival after curative surgery in patients with colon cancer,
particularly in those classified as having stage II disease.
J. Surg. Oncol. 2010;101:396–400. ß 2010 Wiley-Liss, Inc.

KEY WORDS: carcinoembryonic antigen; prognosis; colon cancer

INTRODUCTION
Carcinoembryonic antigen (CEA) is the most widely used and
readily available tumor marker for the management of colorectal
cancer. High preoperative serum CEA levels are associated with an
increased risk of recurrence and poor prognosis [1–8]. Moreover,
monitoring of the postoperative CEA level is commonly used in the
follow-up of colorectal cancer and perioperative serum CEA change is
a useful prognostic indicator for colorectal cancer [9–11].
Many studies have demonstrated the prognostic value of the
preoperative CEA level after surgical resection of colon and rectal
cancer, but whether the preoperative CEA level is an independent
prognostic variable in colon cancer has remained controversial [12–16].
Therefore, the aim of this study was to assess the prognostic value of
the preoperative serum CEA level in patients with colon cancer.
METHODS
In total, 554 patients who underwent potentially curative resection
for nonmetastatic colon cancer at our institution from January 1999 to
January 2008 were analyzed retrospectively. Curative resection was
defined as the absence of any gross residual tumor from the surgical
bed and a surgical resection margin that was pathologically negative
for tumor invasion. Patients with rectal cancer excluded so that a more
homogenous study population could be obtained. Eighty patients
were excluded from this study because preoperative serum CEA data
were not available. Thus, 474 patients who underwent curative
resection for nonmetastatic colon cancer were included in this
retrospective review of prospectively collected data.
Serum CEA levels were measured preoperatively with an Elecsys
CEA electrochemiluminescence assay on a Modular Analytics
E170 system (Roche Diagnostics GmbH, Tokyo, Japan) in which
the reference range was 5.0 ng/ml. Patients were categorized into
two groups according to their serum CEA concentrations: a low
CEA (<5 ng/ml) and a high CEA (
5 ng/ml) group. Postoperative
chemotherapy was considered for all patients with stage II and III
disease. The decision to administer postoperative chemotherapy was
made after assessing of the general health of the patients and with
their acceptance of the therapy. Of the 474 patients, 352 (74.2%)
received postoperative 5-fluorouracil-based chemotherapy. Patients
were followed at 3-month intervals for 2 years, at 6-month intervals for
the next 3 years, and annually thereafter. On a semiannual basis or
when a suspicion of recurrence existed, follow-up examinations
included a clinical history, physical examination, serum CEA
assay, chest X-ray or computed tomography, abdominopelvic-
computed tomography, colonoscopy, and positron emission tomogra-
phy scanning, if available. Recurrence was determined by clinical and
radiological examinations or by histological confirmation. The main
pattern of recurrence was recorded as the first site of detectable failure
during the follow-up period.
Statistical analyses were conducted using SPSS software (SPSS for
Windows, version 14.0; SPSS, Inc., Chicago, IL). Differences between
groups were tested with a Chi-square test. Survival rates were
calculated using the Kaplan–Meier method, and prognostic factors
and survival curves were compared using the log-rank test. Variables
with a statistical P-value <0.10 by univariate analysis were entered
into a Cox model multivariate analysis. A P-value 0.05 was deemed
to be statistically significant.
Grant sponsor: Chonnam National University Research Institute of Medical
Sciences.
*Correspondence to: Young Jin Kim, MD, Department of Surgery,
Chonnam National University Hwasun Hospital and Medical School, 160
Ilsimri, Hwasun-eup, Hwasun-gun, Jeonnam 519-809, Korea. Fax: þ82-61-
379-7661. E-mail: kimyjin@chonnam.ac.kr
Received 7 October 2009; Accepted 30 November 2009
DOI 10.1002/jso.21495
Published online 29 January 2010 in Wiley InterScience
(www.interscience.wiley.com).

ß 2010 Wiley-Liss, Inc.

 10969098, 2010, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jso.21495 by INASP/HINARI - INDONESIA, Wiley Online Library on [08/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Preoperative CEA in Colon Cancer 397
TABLE I. Patients Characteristics (n ¼ 474) TABLE II. Correlation Between Preoperative Serum CEA Level and
Clinicopathologic Variables (n ¼ 474)
Number of patients (%)
Lowa CEA High CEA
Median age, years (range) 64 (23–92) (n ¼ 317) (n ¼ 157) P
Gender
Male 286 (60.3) Age, years
Female 188 (39.7) <65 166 (52.4) 81 (51.6) 0.874
Tumor location
65 151 (47.6) 76 (48.4)
Ascending colon 156 (32.9) Gender
Transverse colon 73 (15.4) Male 188 (59.3) 98 (62.4) 0.514
Descending colon 28 (5.9) Female 129 (40.7) 59 (37.6)
Sigmoid colon 217 (45.8) Smoking
TNM stage No 287 (90.5) 137 (87.3) 0.275
I 47 (9.9) Yes 30 (9.5) 20 (12.7)
II 236 (49.8) Location
III 191 (40.3) Right colon 151 (47.6) 78 (49.7) 0.675
Operative method Left colon 166 (52.4) 79 (50.3)
Open 350 (73.8) Tumor diameter, cm
Laparoscopic 124 (26.2) <5.0 161 (50.8) 56 (35.7) 0.002

5.0 156 (49.2) 101 (64.3)
Differentiation
Well þ moderate 277 (87.4) 129 (82.2) 0.127
RESULTS Poor þ mucinous 40 (12.6) 28 (17.8)
T category
Clinical and pathological characteristics of the 474 patients are T1 þ T2 52 (16.4) 7 (4.5) <0.001
summarized in Table I. This analysis included 286 (60.3%) men with a T3 þ T4 265 (83.6) 150 (95.5)
median age of 64 years (range, 20–92). Using the 6th UICC TNM N category
staging system, 47, 236, and 191 patients had stage I–III cancers, Negative 203 (64.0) 80 (51.0) 0.006
respectively. When we set the serum CEA cutoff value of at 5 ng/ml, an Positive 114 (36.0) 77 (49.0)
Vascular or neural invasion
elevated preoperative CEA level was observed in 157 (33.1%)
Negative 228 (71.9) 100 (63.7) 0.068
patients. Serum CEA level was significantly associated with tumor Positive 89 (28.1) 57 (36.3)
size, T category, N category, number of lymph nodes retrieved, and No. of lymph nodes retrieved
operative method; however, no association was observed between the <12 111 (35.0) 40 (25.5) 0.036
serum CEA level and age, gender, smoking, tumor location, tumor
12 206 (65.0) 117 (74.5)
differentiation, or lymphatic or neural invasion (Table II). Operative method
With a median follow-up period of 45 months (range, 1–127), the Open 224 (70.7) 126 (80.3) 0.025
5-year overall and disease-free survival rates of this cohort were 77.6% Laparoscopic 93 (29.3) 31 (19.7)
and 78.4%, respectively. Overall survival curves among the two CEA CEA, carcinoembryonic antigen.
groups differed significantly the 5-year overall survival rates of patients a
Cutoff, 5 ng/ml.
with low CEA and high CEA were 81.7% and 69.9%, respectively
(P ¼ 0.011). Furthermore, the disease-free survival curves among the
groups differed significantly the 5-year disease-free survival rates of
patients with low CEA and high CEA were 82.4% and 70.6%, DISCUSSION
respectively (P ¼ 0.002).
In the univariate analysis, factors associated with poorer overall Since its first description and characterization by Gold and
survival were age, tumor location, T category, N category, number Freedman in 1965 [17], CEA has remained the most widely
of lymph nodes retrieved, vascular or neural invasion, and preoperative investigated tumor marker. CEA is an intracellular protein normally
serum CEA level; moreover, factors associated with poorer disease- found in low concentrations in the embryonic and fetal gut and normal
free survival were T category, N category, vascular or neural adult human cells. It may also be elevated under several malignant and
invasion, and preoperative serum CEA level (Table III). A multivariate benign gastrointestinal tract conditions [18]. CEA is overexpressed
analysis revealed that T category, number of lymph nodes retrieved, primarily by adenocarcinomas including colon, rectum, breast, and
vascular or neural invasion, and preoperative serum CEA level were lung and more than 90% of primary colorectal carcinomas produce
independent prognostic factors for overall survival. Additionally, CEA [19]. In colon cancer, CEA modulates intercellular adhesion and
T category, vascular or neural invasion, and preoperative serum CEA functions as a promoter of cellular aggregation [20,21], suggesting that
level were independent prognostic factors for disease-free survival CEA has an important role as a facilitator of tumor invasion and
(Table IV). metastasis. Nakamura et al. [22] reported that seven clinicopatholo-
When the low and high CEA groups were subdivided according to gical variables, including undifferentiated tumors, deep tumor inva-
TNM stage, both the 5-year overall and disease-free survival rates sion, lymphatic and venous invasion, node metastasis, liver metastasis,
differed between the two groups only in patients with stage II colon and advanced stages were significantly greater for patients with a
cancer. For stage II cancer, the low CEA group had significantly higher positive CEA (>5 ng/ml) than for patients with a negative CEA
5-year overall and disease-free survival rates than the high CEA group (<5 ng/ml). We found that the serum CEA level was significantly
(P ¼ 0.011 and P ¼ 0.048, respectively; Fig. 1A,B). However, for stage associated with tumor size, T category, N category, number of lymph
III tumors, the 5-year overall and disease-free survival did not differ nodes retrieved, and operative method, but no association was detected
significantly between the low and high CEA groups (P ¼ 0.610 and between the serum CEA level and tumor differentiation or lymphatic or
P ¼ 0.178, respectively; Fig. 2A,B); moreover, the 5-year overall and neural invasion.
disease-free survival rates did not differ between the two groups in CEA is the most widely accepted and frequently used tumor marker
patients with stage I colon cancer (data not shown). in the field of colorectal cancer, and the measurement method is

Journal of Surgical Oncology


398 Huh et al.
Fig. 1. Survival curves of patients with stage II colon cancer
according to the preoperative serum carcinoembryonic antigen
(CEA) level. A: Overall survival. B: Disease-free survival. [Color
figure can be viewed in the online issue, available at www.interscience.
wiley.com.]
standardized and readily available. The majority of studies evaluating
preoperative CEA levels reveal it to be an independent prognostic
factor after surgical resection for colorectal cancer [1–8,10], although
some contradictory studies reported that the CEA level is a predictor
for survival [12–16]. We concur with this and confirmed a preoperative
elevation in serum CEA as an independent prognostic factor for both
5-year overall and disease-free survival in this analysis. Patients with
high CEA levels may have as yet undetected occult metastases at
the time of the operation. Lloyd et al. [23] reported that, of stage I and
II patients, 32.8% tested positive for disseminated tumor cells after
Journal of Surgical Oncology
10969098, 2010, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jso.21495 by INASP/HINARI - INDONESIA, Wiley Online Library on [08/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Fig. 2. Survival curves of patients with stage III colon cancer
according to the preoperative serum carcinoembryonic antigen (CEA)
level. A: Overall survival. B: Disease-free survival. [Color figure can
be viewed in the online issue, available at www.interscience.
wiley.com.]
surgery, and patients who were marker-positive for disseminated
cells in postresection lavage samples showed a significantly poorer
prognosis. These reports suggested that residual tumor cells might be
present even though curative resection was performed.
Not all studies have found that the preoperative serum CEA level
predicts outcome in stage II and III colorectal cancer. Wanebo et al. [7]
suggested that a preoperative CEA >5 ng/ml predicts a significant
increase in recurrence rate for Dukes’ B patients, whereas for Dukes’ C
patients, the increased recurrence rate was even more pronounced with
a cutoff point of 10 ng/ml. Goslin et al. [12] and Lewi et al. [24] showed
 10969098, 2010, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/jso.21495 by INASP/HINARI - INDONESIA, Wiley Online Library on [08/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Preoperative CEA in Colon Cancer 399
TABLE III. Univariate Analyses of Factors for 5-Year Overall Survival that higher preoperative CEA levels are associated with poorer
(OS) and Disease-Free Survival (DFS) prognosis only in Dukes’ C disease, and not Dukes’ B disease. In
5-year 5-year
contrast, after reviewing 563 colorectal cancer patients, Staab et al.
No. OS (%) P DFS (%) P [25] reached a different conclusion. They reported that the differences
between survival curves based on preoperative CEA ranges of <5 and
Age, years >5 ng/ml are significant for patients with TNM stage II tumors
<65 247 79.8 0.058 79.7 0.742 (P < 0.02) but not for patients with lymph node metastases (P ¼ 0.1).

65 227 75.0 76.7 This finding is in accord with our results, which showed that both
Gender overall and disease-free survival rates differed significantly between
Male 286 77.5 0.707 77.0 0.453
low and high CEA groups only in patients with stages II colon cancer.
Female 188 77.9 80.7
Smoking In patients with stage I tumors, these results might have been caused by
No 424 76.7 0.227 77.6 0.235 extremely excellent postoperative overall and disease-free survival:
Yes 50 87.0 85.2 only two patients died and no patients developed recurrence during the
Location 45-month follow-up period. Additionally, to find the meaningful cutoff
Right colon 229 81.0 0.062 80.8 0.119 point for serum CEA in stage III colon cancer, we stratified serum CEA
Left colon 245 74.2 76.3 levels by comparing the survival curves of patients below and above
Tumor diameter, cm each serum CEA level, starting at 1 ng/ml and increasing by increments
<5.0 217 80.9 0.454 81.3 0.102 of 1–30 ng/ml; however, no differences in survival rates were found

5.0 257 75.1 76.0
between the groups (data not shown). Only the T and N categories
Differentiation
Well þ moderate 406 78.1 0.684 79.6 0.136 translated into an independent predictor for survival in patients with
Poor þ mucinous 68 75.2 70.8 stage III colon cancer, and encouraging results were found for 5-year
T category overall and disease-free survival rates of 72.1% and 69.5%,
T1 þ T2 59 91.0 0.015 97.8 <0.001 respectively, in stage III disease (data not shown). Taken together,
T3 þ T4 415 76.1 75.8 this may suggest a stage-specific prognostic role for serum CEA levels.
N category These contradictory findings in various studies may have occurred
Negative 283 81.5 0.013 85.3 <0.001 because of different CEA cutoff values and differences in sample size,
Positive 191 72.1 69.5 pathologic staging, and follow-up duration.
Vascular or neural invasion
This study has the limitations of any retrospective study and is
Negative 328 81.8 <0.001 86.1 <0.001
Positive 146 68.5 60.6 subject to various biases. Furthermore, the cutoff value for CEA
No. of lymph nodes retrieved elevation is still set arbitrarily in many studies, leading to an
<12 151 68.1 0.002 74.4 0.169 insufficient determination of the prognostic function of serum CEA

12 323 82.3 80.2 levels [1,3,4,6,26]. Further large-scale studies are necessary to
Operative method determine a specific valid cutoff point for serum CEA level to achieve
Open 350 76.1 0.104 77.5 0.408 prognostic stratification. In conclusion, our study suggests that the
Laparoscopic 124 85.5 82.0 preoperative serum CEA level is a reliable predictor of recurrence and
Preoperative CEA survival after curative surgery in patients with colon cancer,
Lowa 317 81.7 0.011 82.4 0.002
particularly in those classified as having stage II disease.
High 157 69.9 70.6

CEA, carcinoembryonic antigen.

a
Cutoff, 5 ng/ml.
TABLE IV. Multivariate Analyses of Factors for 5-Year Overall Survival
(OS) and Disease-Free Survival (DFS)
Hazards ratio (CI) P Colon Rectum 1999;42:921–929.
OS
Age (
65 years vs. <65 years) 1.490 (0.983–2.257) 0.060
Location (left vs. right) 1.239 (0.796–1.927) 0.342
T category (T3 þ T4 vs. T1 þ T2) 3.430 (1.069–11.010) 0.038
N category (positive vs. negative) 1.241 (0.808–1.907) 0.325
Retrieved nodes (<12 vs.
12) 2.081 (1.341–3.231) 0.001
Vascular or neural invasion 1.858 (1.213–2.845) 0.004
(positive vs. negative)
Preoperative CEA (higha vs. low) 1.634 (1.077–2.478) 0.021
DFS
T category (T3 þ T4 vs. T1 þ T2) 8.862 (1.229–63.912) 0.030
N category (positive vs. negative) 1.500 (0.965–2.331) 0.072
Vascular or neural invasion (positive 2.816 (1.821–4.355) <0.001
vs. negative)
Preoperative CEA (higha vs. low) 1.608 (1.057–2.445) 0.026
CEA, carcinoembryonic antigen.
a
Cutoff, 5 ng/ml.
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