[Rare Tumors 2013; 5:e6][page 21]
Limited stage small cell carci-
Chunyan Peng, Shanshan Shen,
Affiliated Drum Tower Hospital of
noma of the gastrointestinal
Xiaoqi Zhang, Xiaoping Zou
Nanjing University Medical School, China
tumor. This study aims to analyze the clinical
characteristics and potential prognostic factors
for patients with limited stage small cell carci-
noma of the gastrointestinal tract. The records
of 27 patients with limited stage small cell car-
cinoma of the gastrointestinal tract, who all
received surgery with lymphadenectomy, were
retrieved and analyzed retrospectively. The
median age of patients was 60 years old (range
38-79). The primary locations of tumor were
the esophagus (74.1%) and stomach (14.8%).
The rate of preoperative accurate diagnosis
(16.7%) was low for small cell carcinoma of the
esophagus and stomach. 40.7% of all the
patients had regional lymph node metastases.
Five patients underwent surgery alone, and the
other 22 were treated with surgery + postoper-
ative chemotherapy. All patients had disease
progression or recurrence. The overall median
survival time was 10 months and the 1-year
survival rate was 37.0%. Patients who received
postoperative chemotherapy had a median sur-
vival time of 12 months, which was superior to
the 5-month survival of for those who only had
surgery (P<0.0001). TNM stage (P=0.02) and
postoperative chemotherapy (P<0.0001) were
considered as two prognostic factors in uni-
variate analysis. Postoperative chemotherapy
was a significant independent prognostic fac-
tor in multivariate analysis (P=0.01). The
prognosis for patients with limited stage small
cell carcinoma of the gastrointestinal tract
remains dismal, however, postoperative
chemotherapy may have the potential to
improve the outcome for these patients.
tract: a clinicopathologic and
Department of Gastroenterology, the
prognostic analysis of 27 cases
Small cell carcinoma of the gastrointestinal
tract is a rare and aggressive neuroendocrine
posed of small round or egg-shaped cells with
little cytoplasm. The most common site of SCC
is lung. In 1930, extrapulmonary SCC was first
Small cell carcinoma (SCC) is a rare aggres-
sive malignant neuroendocrine tumor com-
described by Duguid and Kennedy.1Since then,
cases of SCC have been reported in almost all
sites of the body, including the gastrointestinal
tract (GIT),2 head and neck,3urinary tract,4and
SCC of the GIT occurs infrequently.
Approximately 1000 cases have been reported
in the English literature with the estimated
prevalence of 0.1% to 1% of all gastrointestinal
tumors.6SCC can originate throughout the
GIT, with the esophagus frequently involved.
Early sporadic data have indicated that SCC
arising from different digestive locations has
similar biological behavior, including clinical
presentation and pattern of metastasis, which
suggests that SCC of the GIT could be regarded
and treated as one clinical entity.2Regrettably,
overall information about SCC of the GIT is
limited due to its rarity and the fact that most
reports focused on a particular location within
the GIT. Currently, its clinicopathological char-
acteristics and standard treatment are far from
being well established. Especially in the set-
ting of limited stage SCC of the GIT, early accu-
rate diagnosis is challenging and the role of
surgery is still controversial. Some reports sug-
gested that surgical resection of limited stage
SCC could result not only in a significant
locoregional control but also in long-term dis-
ease-free survival.7,8However, other data indi-
cated that patients treated with surgery alone
had rapid systemic recurrence.9,10
Therefore, this retrospective study was per-
formed to analyze the clinical characteristics
and potential prognostic factors for patients
with clinically limited stage SCC of the GIT.
Materials and Methods
diagnosed histologically, who underwent
intended surgery with regional lymphadenec-
tomy in the Affiliated Drum Tower Hospital of
Nanjing University Medical School (Nanjing,
China) from March 2006 to August 2011. The
following data were collected for each patient:
demographic data, presenting symptoms,
methods of tumor diagnosis, staging proce-
dures, pathologic findings, types of treatment,
and survival time. Differential diagnoses were
made immuohistochemically by using antibod-
ies chromogranin A, synaptophysin, neuron-
specific enolase (NSE) and cluster differentia-
tion 56 (CD56). The histological and immuno-
chemical diagnosis of SCC was confirmed by
two independent pathologists. Staging work-up
included computed tomography (CT) scan of
the chest, abdomen and pelvis. Other modali-
ties included endoscopic ultrasound (EUS)
and magnetic resonance imaging. Tumors
were staged according to the 2002 American
We reviewed the records of 27 consecutive
patients with limited stage SCC of the GIT
Joint Committee on Cancer (AJCC) TNM stag-
ing system for each affected organ and
Veterans’ Administration Lung Study Group
(VALSG) criteria. The latter consists of two
staging categories: limited and extensive dis-
ease. Limited disease is defined as a tumor
confined to a localized anatomic region such
as any single organ (e.g. the esophagus, stom-
ach, colon, gallbladder, and pancreas), with or
without regional lymph node involvement.
Extensive disease is defined as a tumor spread
beyond any localized anatomic region. Survival
time was defined as the time from the date of
the end of treatment to death or the last follow-
up visit. All patients gave informed consents
prior to gastroscopy, surgery, or chemotherapy.
This study was approved by the Ethics
Committee of Drum Tower Hospital.
Statistical analysis was performed using
SPSS 11.5 software (SPSS Inc., Chicago, IL,
USA). The impact of clinical and pathologic
risk factors on survival was evaluated using
Kaplan-Meier life table analyses and log-rank
Rare Tumors 2013; volume 5:e6
Correspondence: Xiaoping Zou, Department of
Gastroenterology. The Affiliated Drum Tower
Hospital of Nanjing University Medical School,
321 Zhongshan Road, Nanjing, Jiangsu 210008,
China. Tel. +86.025.83304616.20601
Key words: carcinoma, small cell, gastrointestinal
tract, pathology, clinical.
Contributions: PCY designed the study, per-
formed the statistical analysis and wrote the
paper; SSS collected the data and conducted the
follow-up investigations; ZXQ was responsible for
the examinations on EUS and endoscopy of small
cell carcinoma of the gastrointestinal tract; ZXP
conceived of the study, and participated in its
design and helped to draft the manuscript. All
authors read and approved the final manuscript.
Conflict of interests: the authors declare no
potential conflict of interests.
Acknowledgements: we would like to thank Dr.
Jun Chen (Department of Pathology, the
Affiliated Drum Tower Hospital of Nanjing
University Medical School, China) for good
advice on pathology of small cell carcinoma.
Received for publication: 4 August 2012.
Revision received: 29 October 2012.
Accepted for publication: 10 December 2012.
This work is licensed under a Creative Commons
Attribution NonCommercial 3.0 License (CC BY-
©Copyright C. Peng et al., 2013
Licensee PAGEPress, Italy
Rare Tumors 2013; 5:e6
[page 22] [Rare Tumors 2013; 5:e6]
tests. The independent prognostic factors were
evaluated using Cox’s hazard regression
model. All tests were two-tailed and a P value
<0.05 was considered significant.
women) with limited stage SCC of the GIT
accounted for 0.2% of all patients with diges-
tive malignancies treated at our hospital dur-
ing the study period. The clinical characteris-
tics are summarized in Table 1. The median
age was 60 years (range 38-79). The common
symptoms were dysphagia (51.9%), loss of
appetite (40%) and jaundice (7.4%).
Paraneoplastic syndromes were not observed
in our series. The most common primary sites
were the esophagus (74.1%), followed by the
stomach (14.8%). The average tumor length
was 4.5 cm (range 0.2-14).
According to the TNM classifications, 10
cases were stage I, 10 cases were stage II, and
7 cases were stage III. Of the 27 patients,
40.7% (11/27) postoperatively had lymph node
metastasis and 63.0% (17/27) had lymphatic
Twenty-seven patients (18 men and 9
stomach) underwent gastroscopic examina-
tions and were biopsied. Among 20 esophagus
SCC, 50% were located in the lower third of the
esophagus, 40% were in the middle, and only
10% were in the upper third. In terms of endo-
scopic appearance, 15 were classified as ulcer-
ative type, 3 were mushroom type, and 2 were
submucosal protruded type (Figure 1A).
Interestingly, in one of the submucosal SCCs
of the esophagus, a patch-like erosion was
observed at 24-28 cm (6:00-7:00 position)
before staining, and a large irregular
unstained area was present near the tumor
after Lugol’s iodine staining (Figure 1B and
C). Three patients (2 esophagus, 1 stomach)
preoperatively underwent endoscopic ultra-
sound (EUS) examinations that exhibited
homogeneous hypoechoic or isoechoic masses
with regular borders originating from submu-
cosal layer or muscularis propria, which were
initially mistaken as granular cell tumors
(Figure 1D) or stromal tumors. Only 4 (16.7%)
biopsy specimens yielded a positive diagnosis
for SCC, 8 (33.3%) were misclassified as
undifferentiated adenocarcinoma, 5 (20.8%)
were interpreted as squamous carcinoma, 4
(16.7%) were displayed as epithelial tumors,
and 3 (12.5%) were considered as reactive or
Primary SCCs of the lung were excluded in
all the patients based on the CT scans of the
chest. Twenty-four patients (20 esophagus, 4
nonneoplastic. The remaining 3 cases (1 pan-
creas, 1 colon, and 1 gallbladder), all of whom
received contrast-enhanced CT for diagnosis,
were not biopsied preoperatively. In the case of
SCC in pancreas, CT displayed a large, hetero-
geneous, and marked enhancing mass at the
pancreatic head (Figure 2A and B).
Histology and immunohistochemistry
five cases (92.6%) had pure SCC, 1 (3.7%)
case of gallbladder had mixed type glandular
adenocarcinoma differentiation (Figure 3A),
Histology in SCC of the GIT was similar to
classical SCC: spindle-shaped cells with scanty
cytoplasm and hyperchromatic nuclei. Twenty-
Figure 1. Endoscopic views of the small cell carcinoma of esophagus. A) A submucosal
elevated lesion (1.5x1.5 cm) covered with normal esophageal mucosa at 25 cm in esoph-
agus; B) a patch-like erosion is observed at 24-28 cm (6:00-7:00 position) in esophagus
before staining; C) a large irregular unstained area at 24-28 cm in esophagus after Lugol’s
iodine staining; D) a homogeneous, isoechoic mass (1.0x1.1 cm2) with a regular border
originating from submucosal layer in esophagus, which is diagnosed as a granular cell
tumor by EUS.
Figure 2. Small cell carcinoma of the pancreas in a 56-year-old man. A) Computed
tomography (CT) scanning demonstrates a 5.0x3.8 cm mass at the head of the pancreas,
with atrophic pancreatic parenchyma and main pancreatic duct dilation. B) Contrast-
enhanced CT scanning shows a marked, heterogeneous enhancement in both peripheral
and central portion of the tumor at 30s after administration of contrast medium.
[Rare Tumors 2013; 5:e6][page 23]
and 1 (3.7%) case of esophagus had mixed
type glandular squamous differentiation.
All surgical specimens were immunohisto-
chemically stained for epithelial and neuroen-
docrine markers. Of all cases, 20 (74.1%) were
synaptophysin positive (Figure 3B), 14
(51.9%) were chromogranin A positive, 12
(44.4%) were CD56 positive, and 10 (37.0%)
were NSE positive.
Treatment and prognosis
racoscopy or gastroscopy. Among all the
patients undergoing operations, five were
treated with surgery alone and the other 22
were treated with surgery + postoperative
chemotherapy. Of the 5 patients undergoing
surgery alone, three declined further treat-
ment, and the other two were not candidates
for chemotherapy because of poor perform-
ance status. Among those who received
chemotherapy, twelve cases received etoposide
combined with cisplatin (EP), and the other 10
cases received a combined regimen of
cyclophosphamide + doxorubicin + cisplatin
All of the 27 patients underwent radical sur-
gery and in 2 cases (1 esophagus and 1 stom-
ach) local resection was first performed by tho-
(CAP). All 27 patients died and none was lost to
follow-up. The median survival was 10 months.
The 6- and 12-month survival rates for the
whole group were 70.4% and 37.0%,respective-
ly (Figure 4A). In view of different primary
sites, the median survival time for patients
with SCC of the esophagus was 12 months fol-
lowed by that of SCC of the stomach (median
survival time, 11 months). There was no statis-
tically significant difference in survival time
among patients with SCC of these different
locations (P=0.30). With regard to different
Table 1. Clinical characteristics of patients
with small cell carcinoma of the gastroin-
testinal tract (N=27).
Characteristic No. in group
(% of entire group)
Lymph node involvement
Lymphatic vessel invasion
Surgery + chemotherapy
Table 2. Univariate analysis of survival on clinical and pathologic factors.
Variables Median survival
Survival rate (%)
Tumor length (cm)
Lymph node involvement
Lymphatic vessel invasion
Surgery + chemotherapy
Figure 3. Mixed small cell adenocarcinoma of the gallbladder. A) Haematoxylin &Eosin
stained sections shows small, round cells with scanty cytoplasm, granular nuclear chro-
matin and inconspicuous nucleoli (left), which is combined with components of adeno-
carcinoma (right) (Magnification x100); B) immunohistochemical staining for synapto-
physin, which is positive in the small cell carcinoma area and negative in the adenocarci-
[page 24][Rare Tumors 2013; 5:e6]
therapeutic options, the median survival time
for patients who received surgery alone was
5.0 months, with a 6-month survival rate of 0%.
For patients undergoing surgery + postopera-
tive chemotherapy, the median survival time
was 12 months, with a 6-month survival rate of
86.4% and a 12-month survival rate of 50%
(Figure 4B). Furthermore, there was a statisti-
cally significant difference in survival between
surgery alone versus surgery + postoperative
chemotherapy (P<0.0001). Also, there was no
significant difference in the median survivals
for the cases with EP and with CAP (12 vs 11
months, P=0.26). Univariate analyses revealed
that TNM stage and postoperative chemother-
apy correlated with the outcome of patients
(Table 2). Multivariate analysis indicated that
postoperative chemotherapy was a significant
independent prognostic factor for overall sur-
vival [Hazard ratio, 0.43; 95% CI (0.004-0.49);
P=0.01] (Table 3), which suggested that the
patients who underwent postoperative
chemotherapy had a better prognosis. In addi-
tion, all the patients had disease progression
despite multimodal therapy during the follow-
up, including 7 local recurrences and 20 dis-
tant metastasis. The most frequent sites of
metastasis were as follows: lymph node (45%),
liver (40%), lung (10%), and bone (5%).
pathogenesis is remaining largely unknown.
Ho et al. suggested that SCC might be of endo-
dermal origin derived from a pluripotent stem
cell, which might have differentiated into
mucin or keratin producing cells.11This sug-
gestion is supported by the findings of Chen
and Matsui.12,13Similarly, our study also indi-
cates that SCC of the esophagus and gallblad-
der are admixed with other histologic types of
carcinoma such as adenocarcinoma or squa-
mous cell carcinoma. Moreover, in one case
with SCC of the esophagus, Lugol’s iodine
staining exhibited a clearly unstained area
near the tumor, and biopsies revealed moder-
ate dysplasia. Maitra et al. have described that
dysplastic epithelium was present in gallblad-
der SCC.14 Burke et al. found that overlying
adenomas were present in 45% of SCC of the
large intestine.15In addition, a few genetic and
molecular alternations have been recorded,
including the identification of high prolifera-
tive activity, prevalence of p53 overexpression,
Rb loss, telomerase activation and k-ras muta-
tions.14,16-18However, these genetic and molec-
ular data are only derived from SCC of the
esophagus. To date, it is unclear whether such
factors play a role in the pathogenesis of SCC
of the GIT, but further investigations into their
SCC of the GIT is a kind of rare and highly
aggressive malignancy; however, the exact
functions is warranted.
Demographically, the clinical features of our
patients with limited stage SCC of the GIT are
similar to those of patients with carcinomas in
the corresponding affected organ of the GIT.
Similar to the findings of Brenner et al,2most
of our patients were men with the median age
of 60 years. The most common primary loca-
tion of limited stage SCC of the GIT is the
esophagus. Of note, several reports have
addressed that SCC of the GIT rarely secretes
various ectopic hormones such as vasoactive
intestinal peptide, gastrin, calcitonin, adreno-
corticotropic hormone and antidiuretic hor-
mone,19-23which can result in paraneoplastic
syndromes and even dominate clinical presen-
tation. Our series did not exhibit clinical signs
of paraneoplastic syndromes, so we did not
assess these hormone levels. In clinical prac-
tice, it is nevertheless necessary to evaluate
paraneoplastic syndromes in the patients
especially when there is a clinical suspicion of
SCC of the GIT.
Grossly, most endoscopic and radiological
features of limited stage SCC of the GIT are
identical to those of other carcinomas of the
corresponding sites. Our study reveals that two
esophageal SCCs and one gastric SCC were
submucosal tumors. Further EUS examina-
tions found homogeneous hypoechoic or isoe-
choic solid masses with clear margins arising
from the submucosal layer or muscularis pro-
pria. These masses were misclassified as gran-
ular cell tumors or stromal tumors by EUS.
This phenomenon might be caused by rapid
proliferation of the tumor into the submucosal
layer. In our case of SCC of the pancreas, the
mass was heterogeneously enhanced by con-
trast enhanced CT, as reported by Ichikawa et
al.24and Namieno T et al.25Generally, the ade-
nocarcinomas of the pancreas are hypovascu-
lar, and neuroendocrine tumors are hypervas-
cular by contrast-enhanced CT, which suggests
that contrast-enhanced CT is useful for the dif-
ferential diagnosis of SCC of the pancreas.
However, the diagnosis should be made care-
fully by contrast enhanced CT for large SCC of
the pancreas with necrosis, which may present
as a heterogeneously low-density mass on con-
trast-enhanced CT scanning. In addition,
radio-labeled somatostatin analogue scanning
is also used to detect metastatic diseases and
Table 3. Multivariate analysis of survival on clinical and pathologic factors.
Variables Hazard ratio (95% CI)P
Tumor length (≥4.5 cm)
Lymph node involvement
Lymphatic vessel invasion
CI, confidence interval.
Figure 4. Kaplan-Meier curve of overall survival for the patients. A) Survival curve of
patients with small cell carcinoma of the gastrointestinal tract with limited stage; B) sur-
vival curves for the patients with and without chemotherapy (Solid line: surgery +
chemotherapy; dashed line: surgery; P<0.0001)
[Rare Tumors 2013; 5:e6][page 25]
evaluate the stage of SCC of the GIT,26but its
routine use in SCC of the GIT remains contro-
The diagnosis of SCC of the GIT primarily
depends on histopathology, but it is extremely
difficult to confirm the diagnosis preoperative-
ly based on the biopsy. In our study, 83.3%
cases were diagnosed as undifferentiated ade-
nocarcinoma, squamous carcinoma or other
types. The following reasons may account for
the misdiagnosis based on the biopsy: first,
biopsy specimen is difficult to be obtained
because of the proliferations of tumor cells
mainly in the submucosal layer; second, histo-
logical heterogeneity is common; third, micro-
scopic features usually resemble other malig-
nancies such as malignant lymphoma or undif-
ferentiated carcinoma; and finally, SCC in
biopsy material always becomes distorted and
obscures the diagnosis.27,28Consequently,
more tissues and multipoint biopsies should
be performed to establish a correct diagnosis.
Moreover, electron-microscopical, immunohis-
tochemical and molecular findings are useful
for the differential diagnosis. Similar to previ-
ous reports,18,29our results showed that most of
operative specimens were positive for synapto-
physin and chromogranin A. However, for the
diagnosis of SCC of the GIT, it is unnecessary
to make immunohistochemical assessment of
because of the paucity of SCC of the GIT, it is
better to exclude the primary SCC of the lung
first when establishing the diagnosis of SCC of
SCC of the GIT has a very poor prognosis
with a high metastatic potential. The literature
reports that the median survival ranges from 6
to 12 months, and the 1-year survival rate
varies from 30% to 50% for all stages of SCC of
the GIT.2,6Not surprisingly, patients with limit-
ed stage have a more favorable outcome than
those with extensive stage SCC of the GIT.
Brenner et al. found that the patients of limit-
ed stage had a better survival, with a median
survival of 21.9 months and a 1-year survival
rate of 72% as compared with those with
extensive stage, who had a median survival of
5.8 months and a 1-year survival rate of 29% .2
Lv et al. reported a median survival of 14.0
months and a 1-year survival rate of 62.1% for
limited stage in a series of esophageal SCC.10
In our study, the overall median survival and 1-
year survival rate were 10 months and 37.0%,
respectively. Compared with previous results,
the patients in our series had a poorer progno-
sis due to the small sample size, a higher
regional lymph node metastasis (40.7%), and
lymphatic invasion (63.0%). In addition,
Brenner et al. demonstrated that performance
status, weight loss and the extent of disease
were independent prognostic factors for all
stages of SCC of the GIT.2Casas et al. consid-
ered tumor size and additional chemotherapy
as independent prognostic factors in
esophageal SCC with limited stage.31Chen et
suggested that both surgery and
chemotherapy strongly correlated with survival
in esophageal SCC with limited stage.12Our
multivariate analysis found that postoperative
chemotherapy significantly improved the out-
come of patients with limited stage SCC of the
GIT. Unfortunately, similar to other data,2,10,29
all patients in our group had disease progres-
sion or recurrence despite multimodal therapy.
Consequently, it is of the utmost importance to
perform a study of appropriate regimens for
SCC of the GIT with limited stage.
Chemotherapy is now recognized as the cor-
nerstone of treatment for SCC of the GIT
because micrometastases are frequently pres-
ent and the rate of recurrence is high,10,12,32
even in the setting of limited disease. In our
series, postoperative chemotherapy signifi-
cantly improved survival in patients with limit-
ed stage. However, current chemotherapeutic
agents for SCC fail to eliminate tumor cells of
adeno or squamous phenotype completely.2,33
Surgery therefore has a potential role in limit-
ed stage, given the high prevalence of mixed
tumor histology. Yet, the exact role of surgical
treatment remains controversial in limited
stage. The most important explanation for this
controversy is that the survival superiority
found for different treatments may reflect a
selection bias of more aggressive therapies for
more suitable patients who are in better condi-
tions before treatment. Our study could not
respond to the question about the role of the
surgery in limited stage, although surgical
resection was frequently the first choice in our
series. Therefore, without randomized con-
trolled trials of treatment, it will remain diffi-
cult to draw conclusions about the most effec-
tive treatment. In practice, limited stage SCC
of the GIT should be regarded as a systemic
disease and treated by multimodal approaches.
nosis. Our retrospective study shows a survival
advantage favoring postoperative chemothera-
py for limited stage SCC of the GIT. More
prospective studies on a larger scale should be
conducted to further illuminate the pathogen-
esis of limited stage SCC of the GIT and define
the optimal therapeutic regimen.
In conclusion, SCC of the GIT is a relatively
rare and aggressive tumor with a dismal prog-
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