The American Journal of Surgery (2011) 202, 574 582

Clinical Surgery

Differences in clinicopathological characteristics of

colorectal cancer between younger and elderly patients:
an analysis of 322 patients from a single institution
Chia-Lin Chou, M.D.a,b, Shih-Ching Chang, M.D., Ph.D.a, Tzu-Chen Lin, M.D.a,
Wei-Shone Chen, M.D., Ph.D.a, Jeng-Kae Jiang, M.D., Ph.D.a,
Huann-Sheng Wang, M.D.a, Shung-Haur Yang, M.D., Ph.D.a, Wen-Yih Liang, M.D.c,
Jen-Kou Lin, M.D., Ph.D.a,*
a

Division of Colon and Rectal Surgery, Department of Surgery, Taipei Veterans General Hospital, National Yang-Ming
University, Taipei, Taiwan; bDivision of General Surgery, Department of Surgery, Chi-Mei Medical Center, Tainan, Taiwan;
and cDepartment of Pathology, Taipei Veterans General Hospital, National Yang-Ming University, Taipei, Taiwan
KEYWORDS:
Colorectal cancer;
Age;
Prognosis

Abstract
BACKGROUND: The prognosis of patients with colorectal cancer (CRC) of different onset ages is
controversial.
METHODS: Data were obtained from a prospective database at Taipei Veterans General Hospital.
There were 2,738 newly diagnosed patients with CRC from 2001 to 2006. Two extreme age groups,
younger (!40 years) and elderly ("80 years), were analyzed to compare clinicopathologic characteristics and prognosis after exclusion of specific cancer syndrome.
RESULTS: A total of 322 patients were enrolled in this prospective study. The younger group
consisted of 69 patients with mean age of 33.5 years, and the elderly group consisted of 253 patients
with mean age of 83.4 years. Younger patients had a higher incidence of mucinous cell type (14.5% vs
6.3%, P ! .05), poorly differentiated adenocarcinoma (26.1% vs 6.3%, P " .001), more advanced
disease (82.6% vs 41.9%, P " .001), poorer disease-free survival (67.2% vs 79.3%, P ! .048), and
cancer-specific survival (44.1% vs 73.1%, P " .001) than elderly patients.
CONCLUSIONS: In patients with CRC of younger onset, without relevant predisposing risk factors,
younger patients have more advanced stages of disease, more aggressive histopathologic characteristics, and poorer prognoses compared with older patients.
2011 Elsevier Inc. All rights reserved.

Colorectal cancer (CRC) is now the most common cancer in Taiwan. Despite advances in screening, diagnosis,
and treatment, as well as notable significant progress in
* Corresponding author. Tel.: 886-2-28757544; fax: 886-2-28757639.
E-mail address: jklin@vghtpe.gov.tw
Manuscript received March 31, 2010; revised manuscript October 6,
2010
0002-9610/$ - see front matter 2011 Elsevier Inc. All rights reserved.
doi:10.1016/j.amjsurg.2010.10.014

chemotherapeutic agents, CRC remains the third most common cause of cancer-related death in Taiwan.1 Although the
incidence of CRC increases with age, there has been an
increase in the proportion of patients diagnosed at younger
ages (20 40 years).2 The features and prognosis of CRC in
younger patients are still controversial and are not conclusive. Some studies have revealed a more advanced stage
of disease at the time of diagnosis,2 6 more aggressive

C.-L. Chou et al.

Colorectal cancer in extreme age

575
acteristics, disease stage, overall survival rate, disease-free
survival rate, and cancer-specific survival rate.

Statistical analysis

Figure 1 Diagram of the study flow. FAP ! familial adenomatous polyposis; HNPCC ! hereditary nonpolyposis CRC.

histopathologic characteristics,712 and poorer prognosis in

younger patients compared with older patients.1316 However, other studies have contradicted these findings.1722
The aim of this study was to compare the clinicopathologic
differences, disease-free survival, cancer-specific survival,
and overall survival between younger and elderly patients
with CRC treated at a large general hospital with a specialty
group for treating CRC.

Methods
Between 2001 and 2006, there were 2,738 newly diagnosed cases of histopathologically confirmed colorectal adenocarcinoma at Taipei Veterans General Hospital. Of
1,409 patients undergoing microsatellite instability (MSI)
tests, 99 were identified as having high-frequency MSI.
Patients with family histories of CRC, evidence of hereditary nonpolyposis CRC as determined from MSI tests and
deoxyribonucleic acid sequencing data, familial adenomatous polyposis, or inflammatory bowel disease were excluded. Two extreme age groups, defined as those aged !40
years and those aged "80 years, were included in this
prospective study (Fig. 1). All clinical and pathologic data
were recorded prospectively. The recorded data included
age at diagnosis, gender, location of tumor, presenting clinical features, histologic type, tumor differentiation, presence
of synchronous tumor, stage, presence of metastasis at initial diagnosis, and time of recurrence. The tumor, node,
metastasis (TNM) staging system23 was used for tumor
staging and reviewed by a gastrointestinal histopathologist
(W.-Y.L.). Postoperatively, all patients were followed up at
3-month intervals for the first 2 years, 6-month intervals
from years 3 to 5, and annually thereafter. The end of
follow-up was December 31, 2009. The 2 extreme age
groups were compared with regard to gender, tumor char-

All data were recorded using a standard data form and

analyzed using SPSS version 15.0 (SPSS, Inc., Chicago,
IL). Quantitative values were compared using t tests for
independent groups. For categorical data, #2 or Fishers
exact tests were applied. Overall survival and diseasefree survival were measured from the time of diagnosis of
CRC until death from any cause or disease recurrence.
Survival curves were constructed using the Kaplan-Meier
method, and differences in survival were compared using
the log-rank test. Statistical significance was considered
as P " .05.

Results
Patients and clinical data
A total of 322 patients with sporadic colorectal adenocarcinoma were enrolled. Sixty-nine patients were diagnosed at !40 years of age (mean age, 33.5 # 4.5 years;
range, 22 40 years), and 253 patients were diagnosed at
"80 years of age (mean age, 83.4 # 2.9 years; range,
80 95 years) (Table 1). The elderly group was predominantly male (202 men [79.8%] vs 51 women [20.2%], P "
.001). Although there was no statistical difference in tumor
sites between the 2 age groups, the most common sites for
cancer occurrence were the sigmoid colon and the rectum in
both groups (52.3% in younger patients vs 61.2% in elderly
patients, P ! .221). The most common symptom in both
groups was rectal bleeding (28.7% in younger patients and
26.3% in elderly patients, P ! .179). Younger patients with
CRC were more likely to have abdominal pain than elderly
patients (25.0% and 13.3%, respectively, P " .001). The
proportion of patients who required emergency surgery
was similar in both age groups: 16.6% in the elderly
group and 15.9% in the younger group (P ! 1.000). The
surgical mortality rate showed a trend to be higher in the
elderly group (4.7%) than in the younger group (0%),
although the difference was not statistically significant
(P ! .065).

Tumor characteristics
The pathologic differences between the 2 groups are
summarized in Table 2. Synchronous cancers were found in
1.4% of patients in the younger group and 3.2% of those in
the elderly group (P ! .444). Compared with later onset
CRC, earlier onset CRC was more likely to be mucinous or
signet-ring cell type (14.5% vs 6.3%, P ! .05) or poorly
differentiated adenocarcinoma (26.1% vs 6.3%, P " .001)

576
Table 1

The American Journal of Surgery, Vol 202, No 5, November 2011

Characteristics of 322 patients in the 2 age groups
Age !40 y
(n ! 69)

Factor

Category

Age (y)

Median (range)
!25
2630
3135
3640

Gender
Site

Presenting clinical features at diagnosis

Rectal bleeding
Abdominal pain
Change in bowel habits
Weight loss
Constipation
Diarrhea
Nausea or vomiting
Tenesmus
Bloating
Other
Surgery
Emergent
Elective
Operative methods
Radical resection
Segmental resection
Bypass/stoma only
Postoperative chemotherapy
Stage 2
Stage 3
Stage 4
Surgical mortality

34.3
2
16
18
33

82.6
195
47
11

8084
8589
"90

33 (47.8%)
36 (52.2%)

202 (79.8%)
51 (20.2%)

Right colon
Left colon
Rectosigmoid

22 (31.8%)
11 (15.9%)
36 (52.3%)

80 (30.4%)
22 (8.4%)
161 (61.2%)

31
27
10
8
6
4
2
5
11
4

(28.7%)
(25.0%)
(9.3%)
(7.4%)
(5.6%)
(3.7%)
(1.9%)
(4.6%)
(10.2%)
(3.7%)

89
45
38
11
34
20
8
6
41
46

11 (15.9%)
58 (84.1%)
60
6
3
49/59
2/2
23/28
24/29
0

(8093)
(77.1%)
(18.6%)
(4.3%)

Male
Female

and to exhibit perineural invasion (13.0% vs 4.0%, P !

.018). Comparison of younger and elderly patients revealed
that younger patients exhibited a high incidence of adTable 2

(2240)
(2.9%)
(23.2%)
(26.1%)
(47.8%)

Age "80 y
(n ! 253)

".001
.221

(26.3%)
(13.3%)
(11.2%)
(3.3%)
(10.1%)
(5.9%)
(2.4%)
(1.8%)
(12.1%)
(13.6%)

.179
".001
1.000
.048
.394
.586
.911
.109
1.000
.012
1.000

42 (16.6%)
211 (83.4%)

(87.0%)
(8.7%)
(4.3%)
(83.1%)
(100%)
(82.1%)
(82.8%)
(0%)

224
24
5
48/111
5/5
29/72
14/34
12

(88.5%)
(9.5%)
(2.0%)
(43.2%)
(100%)
(40.3%)
(41.2%)
(4.7%)

.718
.841
.493
".001

.065

vanced stage (82.6% vs 41.9% for younger and elderly

patients, respectively, P " .001) and presence of metastasis
at initial diagnosis (42.0% vs 13.4%, P " .001). There was

Pathologic features

Feature
Synchronous tumor
Histology type
Adenocarcinoma
Mucinous/signet-ring cell
Differentiation
Well/moderate
Poor/undifferentiated
Tumor-infiltrating lymphocytes
Lymphovascular invasion
Perineural invasion
Average sampling lymph nodes
TNM stage
I
II
III
IV

Age !40 y
(n ! 69)

Age "80 y
(n ! 253)

1 (1.4%)

8 (3.2%)

59 (85.5%)
10 (14.5%)

237 (93.7%)
16 (6.3%)

51 (73.9%)
18 (26.1%)
11 (15.9%)
21 (30.4%)
9 (13.0%)
22.00 # 12.27

237 (93.7%)
16 (6.3%)
42 (16.6%)
52 (20.6%)
11 (4.3%)
16.60 # 8.35

6
6
28
29

(8.7%)
(8.7%)
(40.6%)
(42.0%)

53
94
72
34

(20.9%)
(37.2%)
(28.5%)
(13.4%)

P
.444
.05
".001
1.000
.115
.018
".001
".001

C.-L. Chou et al.

Table 3

Colorectal cancer in extreme age

577

Recurrence and survival

Median follow-up (mo)

Lost to follow-up
Recurrence (local and/or distant)
5-y overall survival rate
5-y disease-free survival rate
5-y cancer-specific survival rate

Age !40 y
(n ! 69)

Age "80 y
(n ! 253)

30.6

37.9

3 (4.3%)
15/43 (34.9%)
44.1%
67.2%
44.1%

no statistical difference in the presence of tumor-infiltrating

lymphocytes (15.9% vs 16.6%, P ! 1.000) or lymphovascular invasion (30.4% vs 20.6%, P ! .115) between
younger and elderly patients, respectively.

Recurrence and survival

Median follow-up in all patients was 36.4 months (range,
.2104.6 months; 30.6 months in the younger group and
37.9 months in the elderly group; Table 3). Twenty-three
patients (7.1%) were lost to follow-up: 3 in the younger
group (4.3%) and 20 (7.9%) in the older group (P ! .451).
In total, 15 patients (34.9%) in the younger group and 44 in
the elderly group (19.9%) developed either local or distant
recurrence (P ! .05). The younger group had respective

Figure 2

20 (7.9%)
44/221 (19.9%)
51.0%
79.3%
73.1%

P
.924
.451
.05
.247
.048
".001

1-year, 3-year, and 5-year overall survival rates of 67.6%,

49.8%, and 44.1%, whereas the respective rates were
82.6%, 61.7%, and 51.0% in the elderly group (Fig. 2).
There was no significant statistical difference of 5-year
overall survival between the 2 groups (44.1% in younger
patients vs 51.0% in elderly patients, P ! .247). As shown
in Figures 3 and 4, 5-year disease-free survival and cancerspecific survival in the younger group (67.2% and 44.1%,
respectively) were significantly lower (P " .001) than in the
elderly group (79.3% and 73.1%, respectively). Using univariate and multivariate Cox proportional-hazards regression analyses of disease-free survival and cancer-specific
survival, TNM staging (P " .001) and emergency surgery
(P " .05) were found to be the independent prognostic
factors (Tables 4 and 5).

Kaplan-Meier estimates of overall survival for extreme-aged patients with CRC.

578

The American Journal of Surgery, Vol 202, No 5, November 2011

Figure 3

Kaplan-Meier estimates of disease-free survival for extreme-aged patients with CRC.

Comments
CRC is perceived as a disease of older persons, but as
many as 7% of patients who develop CRC are "40 years of
age at the time of diagnosis.2,24 This has been a subject of
interest in the medical literature, and many investigators
have published their observations concerning CRC of earlier onset.322 Most of the studies that have examined the
clinical and pathologic features of younger patients with
CRC did not distinguish those with known family histories
or predisposing risk factors, such as inflammatory bowel
disease (ulcerative colitis, Crohns disease, or regional enteritis), familial adenomatous polyposis, and hereditary nonpolyposis CRC syndrome, from those without these factors.
CRC affects these predisposing factors at a younger age. A
family history of CRC is associated with an increased risk
for the disease, especially among younger individuals.25 We
aimed to characterize clinical and pathologic features between these 2 unique populations, with age being the sole
differing characteristic after the exclusion of patients with
CRC with specific predisposing factors.
Most previous studies have found no significant difference of CRC in gender distribution, regardless of age. However, a male predominance was noted in our elderly group.
This was an existing bias, because about half the patients in
our hospital were veterans.

In our series, younger patients with CRC were characterized by a tendency for mucinous or signet-ring cell type
(14.5%), poorly differentiated adenocarcinoma (26.1%), advanced stage (82.6%), and presence of metastasis at initial
diagnosis (42.0%). These findings are similar to those of
previous Western studies.212 Moreover, a prior comparison
of characteristics of colon cancer in patients aged 20 to 40
and 60 to 80 years reported more mucinous and signet cell
tumors and higher percentages of poorly differentiated and
anaplastic tumors in the younger group compared with the
older group.19 Defective deoxyribonucleic acid mismatch
repair gene leads to hereditary CRC associated with Lynch
syndrome. Such patients exhibit different clinicopathologic
features, such as MSI histology or predominant rightsided tumors, and have a better prognosis.26 29 Importantly,
even with the present exclusion of patients with Lynch
syndrome from our study, there were still statistically significantly higher percentages of mucinous or signet-ring cell
type, poorly differentiated tumor, and poor prognosis in the
group with CRC of younger age onset.
We found that a majority of younger patients were diagnosed with advanced disease at the time of presentation
(82.6%) relative to elderly patients (41.9%) (P " .001). Up
to 42% of younger patients had metastases at initial diagnosis. These findings are consistent with other reports in the
literature.1316 A recent large population analysis revealed

C.-L. Chou et al.

Colorectal cancer in extreme age

Figure 4

579

Kaplan-Meier estimates of cancer-specific survival for extreme-aged patients with CRC.

that persons aged "50 years presented with disease that

was, in comparison with older patients, less localized and
more distant.30 The observations of more advanced stage
and higher rate of metastasis in the younger age group
are not understood. They may reflect a more aggressive
nature of tumors in younger patients or delayed diagnosis.
The clinical features at presentation in our cohort, showing
that the common presenting symptom of younger patients
was rectal bleeding and abdominal pain, were similar to
those found in other published series.24 Younger patients

are generally considered in better physical condition, with

fewer medical morbidities and reduced possibility of CRC,
compared with elderly patients. Younger patients presenting
with bleeding on defecation or other mild nonspecific discomfort may be more likely to ignore or tolerate these
symptoms, seeking medical attention only upon the development of more serious symptoms. This may explain the
present finding that younger patients had a higher proportion of abdominal pain at initial presentation than elderly
patients (P " .001). Moreover, even when a younger patient

Table 4 Significant predictive factors for disease-free survival in a Cox proportional-hazards analysis of 322 extreme-aged
patients with CRC
Prognostic factor

Univariate HR
(95% CI)

Multivariate HR
(95% CI)

Stage
Age (!40 vs "80 y)
Gender
Mucinous/signet-ring cell
Poor/undifferentiated differentiation
Lymphovascular invasion
Perineural invasion
Emergent operation
Postoperative chemotherapy

3.763
1.887
.563
1.436
2.327
3.483
3.949
2.449
4.612

".001
.052
.058
.489
.039
".001
.004
.009
".001

2.520
.910
.753
.764
.949
2.164
.981
2.518
2.221

".001
.817
.415
.626
.905
.029
.972
.013
.035

CI ! confidence interval; HR ! hazard ratio.

(2.3765.958)
(.9953.578)
(.3101.020)
(.5154.004)
(1.0425.198)
(1.8806.451)
(1.55610.021)
(1.2464.813)
(2.5958.195)

(1.4584.355)
(.4092.026)
(.3801.490)
(.2582.257)
(.4002.250)
(1.0824.328)
(.3492.759)
(1.2205.197)
(1.0594.660)

580

The American Journal of Surgery, Vol 202, No 5, November 2011

Table 5 Significant predictive factors for cancer-specific survival in a Cox proportional-hazards analysis of 322 extreme-aged
patients with CRC
Prognostic factor

Univariate HR (95% CI)

Multivariate HR (95% CI)

Stage
Age (!40 vs "80 y)
Gender
Mucinous/signet-ring cell
Poor/undifferentiated differentiation
Lymphovascular invasion
Perineural invasion
Emergent operation
Postoperative chemotherapy

7.949
2.718
.551
2.143
.873
3.975
3.392
2.852
4.433

".001
".001
.006
.489
.660
".001
".001
".001
".001

8.471
.859
.613
.884
2.919
1.107
1.017
2.219
.944

".001
.581
.052
.884
".001
.675
.963
.007
.832

(5.55911.367)
(1.7844.139)
(.361.842)
(1.1903.861)
(.4751.602)
(2.6096.056)
(1.8386.257)
(1.8054.505)
(2.8916.799)

(5.50713.030)
(.5021.472)
(.3741.004)
(.4541.721)
(1.7734.805)
(.6881.783)
(.4932.099)
(1.2433.962)
(.5551.606)

CI ! confidence interval; HR ! hazard ratio.

seeks medical help, CRC may not be initially suspected in

the absence of associated risk factors of colorectal disease.
Less aggressive screening and surveillance among younger
people may lead to a higher percentage of advanced-stage
tumors at presentation. Lower symptom tolerance in elderly
patient populations may explain why these patients were
more likely to present with more nonspecific symptoms than

Figure 5

younger patients (P ! .012). OConnell et al24 found that

delays are a result of patient-related factors such as lack of
access, ignoring symptoms, and patient denial, as well as
physician-related factors such as misdiagnosis. One study
that specifically examined physician-related factors in late
diagnosis found that "50% of patients had physician-related delays in diagnosis.31

Kaplan-Meier Estimates of TNM-specific survival for extreme-aged patients with CRC.

C.-L. Chou et al.

Colorectal cancer in extreme age

A number of studies have investigated the outcomes of

colorectal disease in younger patients. Studies that compared stage-to-stage survival of younger versus older patients with CRC found that younger patients with Duke A or
B tumors appear to have better survival than older patients
with similar-stage disease.3,21,32,33 Perhaps this is secondary
to better tolerance of surgery and adjuvant therapy by the
younger patients. By contrast, younger patients diagnosed
with Duke C or D lesions do the same or worse than older
patients with similar-stage disease. This may be related in
part to the more aggressive pathology and nature of the
disease in younger patients. These factors result in a lower
overall 5-year survival rate for younger patients with colorectal carcinoma, because more younger patients present
with later-stage disease.24 Our study demonstrated that the
overall survival rate of the younger group decreased dramatically in the first 3 years. A significant proportion of
initial metastasis at diagnosis and rapid progression of advanced disease resulted in a marked decrease of the overall
survival of the younger group in the first 3 years. The
process of aging, underlying morbidities, and progression of
CRC resulted in slowly decreasing survival plot of the
elderly patients. Finally, the survival plots of the 2 study
groups became very similar after the third year, and there
was no difference in the overall survival rate between the 2
groups (P ! .247).
We observed that younger patients had significantly poor
disease-free survival and cancer-specific survival. Cancer
stage and emergency surgery were independent prognostic
factors in the multivariate analysis of disease-free survival
and cancer-specific survival. This means that poor diseasefree survival and cancer-specific survival in younger patients were correlated with advanced nature and late presentation symptoms of the disease. In an attempt to further
evaluate whether this different prognosis is due to more
advanced stage at presentation, we constructed TNM-specific survival curves for the 2 cohorts of patients. We combined stages I and II as the early stage and stages III and IV
as the advanced stage. The TNM-specific survival curves
are shown in Figure 5. Different prognosis between the 2
cohorts of patients was due to a more advanced stage at
presentation (P " .001).
Previous studies have reported variable outcomes, with
some studies showing no differences and others showing
that younger patients do better or worse than older patients.
The major discrepancies in findings between these reports
might originate from selection biases for retrospective studies. As results from a tertiary canter, selection bias could not
be avoided, and this was a limitation of this study. Lack of
routine MSI testing for all patients in our institution was
another limitation to confirm that all patients with Lynch
syndrome were excluded from this study.
We suggest that patients and physicians should pay attention to CRC-related symptoms such as rectal bleeding or
abdominal pain, even in younger patients without obvious
CRC risk factors. Most tumors were located in the sigmoid

581
colon and rectum, which can easily be reached with flexible
sigmoidoscopy. Our study also demonstrated a more advanced stage of disease, more aggressive histopathologic
characteristics, and poorer prognosis in younger patients
compared with older patients. The uncommon occurrence of
CRC in young adults with no predisposing genetic risk
factors requires a high index of suspicion when examining
people aged !40 years with symptoms of abdominal pain
and hematochezia.

Conclusions
CRC in younger patients is associated with more advanced disease, more aggressive histopathologic characteristics, and poorer disease-free survival and cancer-specific
survival than in older patients. Our findings should promote
increased awareness and aggressive pursuit of symptoms in
younger patients who are not thought to be at high risk for
cancer, with the possibility that these symptoms may represent an underlying colorectal malignancy.

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