J Gastrointest Surg

DOI 10.1007/s11605-015-2862-8

ORIGINAL ARTICLE

Solid Pseudopapillary Neoplasms of the Pancreas:

a 19-Year Multicenter Experience in China
Pengfei Yu 1 & Xiangdong Cheng 2 & Yian Du 1 & Litao Yang 1 & Zhiyuan Xu 2 &
Wenjuan Yin 1 & Zhengxiang Zhong 3 & Xiaoguang Wang 3 & Hongbao Xu 4 &
Conggang Hu 5

Received: 6 February 2015 / Accepted: 12 May 2015

# 2015 The Society for Surgery of the Alimentary Tract

Abstract
Aim The aim of this study was to determine the clinicopathological features, surgical management, and prognosis of solid
pseudopapillary neoplasms (SPNs) of the pancreas.
Methods This study conducted a retrospective analysis of 97 patients who underwent surgery for a pathologically confirmed SPN
in five hospitals between January 1996 and December 2014.
Results The 97 cases included 93 female and 4 male patients, and the average age was 31.2 years. The tumor was
located in the body or tail (70.1 %), the head (20.6 %), and the neck (9.3 %). All patients underwent surgical
exploration, including distal pancreatectomy (63.9 %), pancreaticoduodenectomy (20.6 %) (partial portal vein or
superior mesenteric vein resection and artificial vascular graft reconstruction performed in 4.1 % of the patients),
central pancreatectomy (10.3 %), enucleation (5.2 %), and liver resection (1.0 %). 16.5 % of the patients had
malignant tumors. The positive rate of Ki-67 was 66.7 % in patients diagnosed with a malignant neoplasm and
was comparable to 8.4 % of the patients diagnosed to have a benign neoplasm (p<0.001). After a median follow-up
of 70.1 months, three patients had recurrence and one patient died of liver metastasis.
Conclusions SPN is a rare neoplasm with low malignant potential. Surgical resection is warranted even in the presence of local
invasion or metastases as patients demonstrate excellent long-term survival. Positive immunoreactivity for Ki-67 may predict the
malignant potential and poor outcome of SPNs.

Keywords Solid pseudopapillary neoplasms . Diagnosis . Introduction

Treatment . Prognosis
Solid pseudopapillary neoplasms (SPNs) are rare pancre-
atic tumors with a low potential for malignancy,
representing 1∼3 % of all pancreatic tumors and
,
10∼15 % of cystic tumors of the pancreas.1 2 A descrip-
tion of SPN was first published by Frantz in 1959.3 The
* Pengfei Yu
World Health Organization (WHO) classified these tu-
yupengfei23@163.com
mors as solid pseudopapillary tumors (SPTs) in 1996
and reclassified them as SPNs in 2010.4 SPN affects
1
Department of Abdominal Surgery, Zhejiang Cancer Hospital, 38# primarily young women during their reproductive phase
Guangji Road, Hangzhou 310022, China
and exhibits relatively indolent biological behavior with
2
Zhejiang Province Hospital of Traditional Chinese Medicine, a favorable prognosis; however, local recurrence or me-
Hangzhou, China
tastasis can occur after surgery.5 Many reports have
3
The Second Affiliated Hospital of Jiaxing Medical College, been published in recent years, but most of these stud-
Jiaxing, China
ies are single-center reports or small case series. Limited
4
Huzhou Center Hospital, Huzhou, China data are available on the pathogenesis, malignant poten-
5
Jinhua Guangfu Hospital, Jinhua, China tial, and optimal surgical strategy for SPN. So, we
 J Gastrointest Surg

conducted a retrospective review of SPNs in five med- Results

ical centers in order to further examine the clinical and
pathological features, surgical treatments, and outcomes Clinical Characteristics
of SPNs.
Three thousand four hundred sixty-two pancreatic neoplasms
were treated in these five institutions from January 1996 to
December 2014, and 113 patients were diagnosed as SPNs,
Methods
among which 97 cases were confirmed by pathology and rep-
resented 2.8 % of all pancreatic neoplasms. The 97 patients
This was a retrospective cohort study. Patients with SPN
included 93 females and 4 males, with a median age of
were identified from the hospital records in Zhejiang Can-
31.2 years (range 16∼57). The clinical presentation is unspe-
cer Hospital, Zhejiang Province Hospital of Traditional
cific, including abdominal pain (44.3 %), abdominal disten-
Chinese Medicine, The Second Affiliated Hospital of
sion (37.1 %), back pain (13.4 %), and vomiting (8.2 %).
Jiaxing Medical College, Huzhou Center Hospital, and
7.2 % of patients whose SPNs were found during routine
Jinhua Guangfu Hospital. Eligible patients underwent sur-
physical examinations were asymptomatic. Two patients were
gery for a pancreatic SPN between January 1996 and De-
referred to the hospital for the management of jaundice. No
cember 2014. Patients’ clinical presentation, radiological
patients had weight loss and a history of trauma or pancreati-
details, surgical data, pathological features, postoperative
tis, and the median duration of symptoms was 2.1 months
course, and long-term survival were collected and ana-
(range 5 days to 13 months). The tumors were 5.9 cm in
lyzed. Outpatient records combined with telephone inter-
diameter on average (range 1.5 to 14 cm) and were located
views were used for follow-up. Written informed consent
in the body and/or tail (70.1 %), the head (20.6 %), and the
was obtained from all the study participants. The study
neck (9.3 %). The clinical features of the 97 patients are listed
was approved by the ethics committee of the five
in Table 1.
hospitals.
Pathologically, SPN was defined as malignant if it
demonstrated extrapancreatic invasion, distant metasta-
Tumor Markers and Radiological Investigations
ses, lymph node involvement, pancreatic parenchymal
invasion, and perineural or vascular invasion. Surgical
Ninety of the 97 patients underwent tumor marker detection.
morbidity was defined as any complication at any time
CA-125 in five patients (5.5 %), CA-199 in three patients
and was classified according to a previous report.6 Pan-
(3.3 %), and CA-242 in two patients (2.2 %) had values great-
creatic fistula was defined in accordance with the rec-
er than the upper limits of the normal range.
ommendations of the International Study Group on Pan-
creatic Fistula.7
Histopathological slides from all patients were Table 1 Clinical features of 97 patients with SPNs
reviewed by a specialized pathologist. Immunohisto-
chemical stains for vimentin, α-1-antitrypsin, neuron- Clinical characteristics No. of patients (n=97)
specific enolase, synaptophysin, and chromogranin were
Age (years)
carried out when it was difficult to differentiate the
Mean (range) 31.2 (16∼57)
neoplasm from other pancreatic tumors.8 Clinicopatho-
Gender
logical characteristics were compared between patients
Female/male 93/4
with malignant neoplasms and those with benign
Symptoms (%)
lesions.
Abdominal pain 43 (44.3)
Abdominal distension 36 (37.1)
Statistical Analysis Back pain 13 (13.4)
Vomiting 8 (8.2)
Continuous data are presented as median (i.q.r.) unless Asymptomatic 7 (7.2)
indicated otherwise, with analysis using the independent Location (%)
t test or Mann-Whitney U test, as appropriate. Compari- Body and/or tail 68 (70.1)
sons of categorical data were performed using χ2 and Head 20 (20.6)
Fisher’s exact tests. All statistical analyses were per- Neck 9 (9.3)
formed with the SPSS 16.0 statistics software package Size (cm)
(SPSS Inc., Chicago, IL, USA). A p value <0.05 was Mean (range) 5.9 (1.5∼14)
considered to indicate statistical significance.
J Gastrointest Surg
Radiological investigations were performed before opera-
tion, including computed tomography (CT, 76.3 %), ultraso-
nography (US, 49.5 %), magnetic resonance imaging (MRI,
28.9 %), and 18F-fluorodeoxyglucose (FDG) positron emis-
sion tomography (PET, 4.1 %). Figure 1 shows the radiolog-
ical images of SPN. The mass was described on cross-
sectional imaging as heterogeneous (solid and cystic,
84.5 %), solid (12.4 %), and cystic (3.1 %). Calcifications
were present in 22.7 % of the patients, while hemorrhage
and/or necrosis was detected in 25.8 % of the patients. One
patient was found to have a single metastasis in the liver.
Inaccurate preoperative diagnoses were made for 33 % of
the patients, including pancreatic adenocarcinoma (13.4 %),
neuroendocrine tumor (9.2 %), cystadenoma (5.2 %), islet cell
tumor (3.1 %), and pancreatic cyst (2.1 %).
Surgical Management
All patients underwent surgical exploration. Sixty-two pa-
tients underwent distal pancreatectomy, including laparoscop-
ic distal pancreatectomy in 5 patients, 20 patients underwent
pancreaticoduodenectomy, and 4 of them had partial portal
vein or superior mesenteric vein resection and artificial vas-
cular graft reconstruction. Ten patients underwent central pan-
createctomy, and five patients underwent enucleation of SPN.
Fig. 1 a A CT scan showing a
low-density mass of the pancreas
head with calcification. b
Enhanced CT scan showing
slightly enhanced solid areas. c, d
MRI showing a well-demarcated
mass in the pancreas head, which
was close to the superior
mesenteric vein
One patient with liver metastasis underwent partial liver re-
section. The total operation time was 260±118 min, and the
intraoperative blood loss was 275±130 ml. Blood transfusion
was needed in nine patients during operation, each patient
received 2 U of blood.
Ninety-six patients had R0 resections, and there were no
surgical mortalities. Postsurgical complications occurred in 28
patients, including pancreatic fistula (n=18), infection (n=8),
delayed gastric emptying (n=4), and bleeding (n=1). Pancre-
atic fistulas were classified as grade A in eight patients, grade
B in seven patients, and grade C in three patients. Eight infec-
tion cases included five pneumonia, two wound infection, and
one intra-abdominal infection. Most of these patients were
conservatively managed with a successful outcome, but reop-
eration was necessary in one patient due to intra-abdominal
bleeding. The median postsurgical stay was 14.7 days (range 7
to 37 days) (Table 2).
Pathological Findings
Most tumors were characterized to have both cystic and solid
components with hemorrhagic areas. The neoplasms showed
typical pathological findings, that is, uniform cells with ovoid
nuclei and eosinophilic granules, arranged in sheets with
pseudopapillary architecture. Sixteen patients were diagnosed
 J Gastrointest Surg

Table 2 Surgical procedures and postoperative outcomes of 97 SPN

patients

No. of patients (n=97)

Operative procedure
Distal pancreatectomy (%) 62 (63.9)
Pancreaticoduodenectomy (%) 20 (20.6)
Central pancreatectomy (%) 10 (10.3)
Enucleation (%) 5 (5.2)
Liver resection (%) 1 (1.0)
Laparoscopic approach (%) 5 (5.2)
PV/SMV resection (%) 4 (4.1)
Operative time (min) 260±118
Blood loss (ml) 275±130
Postoperative complications (%) 28 (28.9)
Pancreatic fistula (%) 18 (18.6)
Grade A (%) 8 (8.2)
Grade B (%) 7 (7.2)
Grade C (%) 3 (3.1)
Infection (%) 8 (8.2)
Pneumonia (%) 5 (5.2)
Wound infection (%) 2 (2.1)
Intra-abdominal abscess (%) 1 (1.0)
Fig. 2 a Sheets and cords of cells arranged around fibrovascular septa
Delayed gastric emptying (%) 4 (4.1) and pseudopapillary structures are formed (H&E ×200). b Representative
Bleeding (%) 1 (1.0) micrographs of SPN exhibiting tumor invasion into the adjacent
Postoperative stay (days) 14.7 (7∼37) pancreatic parenchyma

PV portal vein, SMV superior mesenteric vein Follow-up and Survival

Follow-up included clinical examination, routine laboratory

with malignant SPN due to vascular invasion in seven
patients (portal vein or superior mesenteric vein in four
patients and splenic vein in three patients), pancreatic
parenchyma infiltration in six patients, lymph node in-
volvement in two patients, and metastatic character in
one patient (Fig. 2).
Immunohistochemical analysis was performed in selected
cases. Vimentin (Vim) was positive in 89 of 95 patients, α-1-
antitrypsin (AAT) was positive in 79 of 83 patients, neuron-
specific enolase (NSE) was positive in 75 of 87 patients, pro-
gesterone receptors (PRs) were positive in 73 of 89 patients,
and CD99 was positive in 53 of 61 patients. Estrogen recep-
tors (ERs), synaptophysin (Syn), cytokeratin (CK), and
chromogranin A (CgA) were expressed only focally in a few
tumors (Fig. 3).
Patients were divided into two groups based on the
standard of aggressiveness of SPNs (malignant group vs.
benign group). The clinicopathological details as predic-
tive factors to evaluate malignant SPNs are shown in
Table 3. The positive rate of Ki-67 was 66.7 % (10/15)
in patients diagnosed with a malignant neoplasm and was
comparable to 8.4 % (6/71) of the patients diagnosed to
have a benign neoplasm (p<0.001).
tests, abdominal US, and CT/MRI every 3 to 6 months. Me-
dian follow-up was 70.2 (3.5–221.5)months. Three patients in
the malignant group had recurrence. The patient who had
undergone partial resection of the liver developed liver metas-
tases 5 months after operation. She received S-1 and was alive
with liver metastasis for 25 months.
Discussion
SPNs are a rare neoplasm with a low malignant potential,
usually affecting young women in their second or third decade
of life.8 The pathogenesis of the tumor is unknown, although
its tendency to affect young women has suggested that sex
hormones may be involved in the origin of SPT.9 However,
no differences in immunohistochemical stains for sex hor-
mone receptor proteins or in clinicopathological characteris-
tics had been found attributable to gender alone.10 The risk
factor assessment showed that more than 50 % of SPN pa-
tients were infected with hepatitis B virus,11 and in our study,
76.3 % of female patients had taken contraceptive drugs for a
long time. This suggests that an investigation is needed to
determine whether hepatitis B virus infection or contraceptive
J Gastrointest Surg

Fig. 3 a Immunohistochemical
staining for vimentin (original
magnification ×400). b
Immunohistochemical staining
for α-1-antitrypsin (original
magnification ×400). c
Immunohistochemical staining
for neuron-specific enolase
(original magnification ×400). d
Immunohistochemical staining
for CD99 (original magnification
×400). e Immunohistochemical
staining for Ki-67 (original
magnification ×400)

drugs may be involved in the pathogenesis of SPNs, since
these factors are still unclear.
As patients lack distinctive symptoms, the majority of these
tumors are diagnosed during complementary abdominal im-
aging techniques such as US, CT, and MRI.12 On US or CT,
the lesion is usually large and its internal structure goes from
having cystic thick wall or with an inner irregular margin to a
predominantly solid mass with some cystic component.13,14
On dynamic contrast-enhanced CT, the tumor enhanced less
than the adjacent normal pancreas.15 MRI is better than CT in
differentiating the cystic or solid component inside the tumor
and providing information about resectability.16 The use of
fine-needle aspiration cytology (FNAC) either percutaneously
or EUS guided can help distinguish SPNs from other pancre-
atic tumors.17 However, seeding of the needle tract by
neoplastic cells and complications, such as bleeding, pancre-
atic fistula, and biliary fistula during the procedure, also had
been reported.18 PET may not add additional information for
diagnosis.19 The accuracy of preoperative diagnosis in this
study was 67.0 % even in the absence of FNAC. The results
show that abdominal images combined with age and gender
are sufficient for making a diagnosis of SPN, and FNAC
should be performed when the radiological diagnosis was
not clear enough.
Surgery is the only curative treatment for SPN.20 Surgical
approach depends on the location, size, as well as the nature of
the neoplasms. The feasibility of organ-preserving or laparo-
scopic surgery for SPNs has been reported,21,22 as also con-
firmed in the current cases. Routine lymphadenectomy is not
recommended in recent studies, due to the rare incidence of
 J Gastrointest Surg

Table 3 Predictive factors of malignant SPNs In our study, 16 patients were diagnosed with malignant
Clinicopathologic factors Malignant (n=16) Benign (n=81) p value SPN due to vascular invasion, pancreatic parenchyma infiltra-
tion, lymph node involvement, or liver metastasis. Some stud-
Mean age (years) 34.4 (19–57) 29.3 (16–53) 0.56a ies have shown a correlation between tumor size >5 cm, tumor
Sex ratio (F:M) 15:1 78:3 0.64b necrosis, male sex, and SPNs with malignant potential.10,28,29
Symptoms However, several univariate analyses indicated that the clini-
Present 15 75 cal factors, including sex, age, tumor size, tumor location,
Absent 1 6 0.87b increased tumor markers, and tumor characteristics, were not
Tumor location intensively related to the malignant potential of SPNs.30,31
Body and/or tail 13 55 These results were consistent with those in our study. Besides,
Head 3 17 0.34b we found that the positive rate of Ki-67 was 66.7 % in patients
Neck 0 9 diagnosed with a malignant neoplasm and was comparable to
Tumor size (cm) 8.4 % of the patients diagnosed to have a benign neoplasm
<5 4 35 (p<0.001). Our findings indicate that positive status for Ki-67
>5 12 46 0.17b may correlate with the malignancy and poor outcome of
Tumor markers SPNs. However, the accumulation of large-scale clinical data
Increased 3 7 is still necessary to support this view.
Normal 13 74 0.22b An SPN is composed of small, uniform tumor cells with
Calcification round nuclei and eosinophilic cytoplasm. The tumor is char-
Present 5 17 acterized by a combination of solid components consisting of
Absent 11 64 0.37b pseudopapillae with fibrovascular stalks and cystic compo-
Hemorrhage/necrosis nents with variable degeneration and hemorrhage.32 The typ-
Present 3 22
ical immunohistochemistry of SPNs includes positive staining
Absent 13 59 0.48b
for Vim, AAT, α-1-antichymotrypsin (AACT), and NSE,33,34
Tumor feature
but the unique immunohistochemical features with expression
of PR and CD10 were not consistent.8,35 According to recent-
Solid and cystic 12 70
ly published data, a particular dot-like intracytoplasmic ex-
Solid 4 8 0.20b
pression of CD99 appears to be highly unique for SPN,36,37
Cystic 0 3
and this distinctive staining pattern was present in 86.9 % of
Ki-67 (positive rate) 66.7 % (10/15) 8.4 % (6/71) <0.001b
our cases. Thus, CD99 accompanied by other useful markers
a
Mann-Whitney U test would help establish the diagnosis of SPNs.
b
Fisher’s exact test The prognosis of SPNs is good, even with invasion as well
as metastases or local recurrence. More than 95 % of patients
with SPN limited to the pancreas are cured by complete sur-
lymph node metastasis.23 However, complete, aggressive sur- gical excision,38 and long-term survival was also observed in
gical resection should be performed for these neoplasms even patients with malignant SPNs.39 The overall 5-year survival
in the presence of invasion into adjacent organs and distant was estimated to be 95 % in a review of 718 patients reported
metastases based on the prolonged survival after complete in the English literature.40 Due to the favorable prognosis and
surgical resection.24,25 Cheng and colleagues reported that excellent long-term survival, predictive factors of survival are
en bloc synchronous portal vein-superior mesenteric vein or difficult to identify. Therefore, all SPN patients need long-
adjacent organ resection should be carried out to achieve a term follow-up, which is as important as the evaluation of
complete resection.26 In our study, most patients who had benign and malignant tumors.
pancreatic parenchyma infiltration or vascular invasion with
R0 resection did not develop local recurrence or distant
metastasis.
The role of chemotherapy or chemoradiotherapy for the Conclusion
treatment of SPN is unclear, and some investigators have re-
ported successful treatment using gemcitabine or paclitaxel SPNs are an infrequent tumor with low malignant potential;
therapy.21,27 One patient who underwent aggressive surgery however, surgical resection is warranted even in the presence
for liver metastases in this series developed recurrence of local invasion or metastases as patients demonstrate excel-
5 months later. S-1 was administered, and she was alive lent long-term survival. The proliferative index assessed by
25 months after treatment, thus suggesting that S-1 may be a immunohistochemical staining for Ki-67 may predict the ma-
useful treatment for malignant SPN. lignant potential and poor outcome of SPNs. Further studies
J Gastrointest Surg
should aim at acquiring more understanding of SPNs and
establishing guidelines for diagnosis and treatment.
Acknowledgments We express our appreciation to Dr. Thomas Aloia
(Surgical Oncology, MD Anderson) who has offered many valuable com-
ments and suggestions. This study is supported by the Department of
Health of Zhejiang Province (2013KYB043).
Conflict of Interest No benefits in any form have been received or will
be received from a commercial party related directly or indirectly to the
subject of this article.
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