ORIGINAL ARTICLE

Solid-pseudopapillary neoplasms of the pancreas: clinicaland pathological features of 33 cases

Hongke Cai • Meiqi Zhou • Yue Hu •

Haifei He • Junqing Chen • Wei Tian •

Yongchuan Deng

Received: 28 September 2011 / Accepted: 15 December 2011 / Published online: 24 July 2012

� Springer 2012

Abstract

Purpose Solid-pseudopapillary neoplasms (SPNs) are

rare pancreatic tumors, with a low potential for malig-

nancy. The clinical and pathological features of 33 SPNs

were reviewed.

Methods This study conducted a retrospective analysis of

33 patients who underwent surgery for a pathologically

confirmed SPN from 2000 to 2011.

Results Thirty of the 33 patients (91 %) were female, and

the median age at diagnosis was 29.2 years (range 12–59).

The most common symptom was abdominal discomfort

with dull pain (58 %). Others included asymptomatic

lesions that were only detected incidentally during imaging

(21 %), a palpable abdominal mass (15 %) and indigestion

(6 %). All 33 patients underwent surgery with a curative

intent and 3 (9 %) underwent laparoscopic surgery. The

mean diameter of the tumors was 4.9 cm (range 2–15 cm),

and they occurred in the head (9, 27 %), neck (5, 15 %),

body or tail (19, 58 %) of the pancreas. One patient had

lymph node metastases, one patient had portal venous

invasion and 8 patients had perineural invasion. The patient

follow-up ranged from 4 to 118 months, and 32 patients

were alive and well without recurrence. One patient

relapsed 10 months after distal pancreatectomy with sple-

nectomy and underwent a second surgery via laparotomy.

Unfortunately, the patient died of multiple organ failure

12 days after the second surgery.

Conclusion SPNs are rare neoplasms with malignant

potential but excellent prognosis. Adequate surgical

resection, including laparoscopic surgery, may therefore be

performed safely and is associated with a long-term sur-

vival, even in invasive cases.

Keywords Solid-pseudopapillary neoplasms �Diagnosis � Treatment � Prognosis

Introduction

Solid-pseudopapillary neoplasms (SPNs) are rare pancre-

atic tumors with a low potential for malignancy, account-

ing for 0.17–2.7 % of all pancreatic tumors [1]. Dr. Frantz

[2] first described rhia tumor in 1959. The tumor has been

frequently identified as a papillary epithelial neoplasm,

solid and cystic tumor, solid and papillary tumor, papillary

cystic tumor, and solid and papillary epithelial neoplasm

because of its typical histological features including cystic,

solid, and pseudopapillary structures [3]. The World Health

Organization (WHO) classified these tumors as Solid-

pseudopapillary tumors (SPTs) in 1996 and reclassified

them as Solid-pseudopapillary neoplasms (SPNs) in 2010

[4]. SPNs are most prevalent in young females and are

thought to have a distinct indolent clinical course. Many

reports have been published in recent years, such as Li’s [5]

new argument for surgical procedures for SPNs or Mima’s

[6] case report and review of SPNs, but most of these

studies are single case reports or small case series

(Table 1). The aim of the present study was to examine

the clinical and pathological features, including the

immunohistochemical features, treatments and outcomes of

SPNs.

H. Cai � M. Zhou � Y. Hu � H. He � J. Chen � W. Tian �Y. Deng (&)

Department of Surgical Oncology, Second Affiliated Hospital,

Zhejiang University College of Medicine, No. 88 Jiefang Road,

Zhejiang, People’s Republic of China

e-mail: dengyc001@126.com

123

Surg Today (2013) 43:148–154

DOI 10.1007/s00595-012-0260-3

Patients and methods

The detailed clinicopathological, treatment and outcome

data of all patients with a diagnosis of SPN who underwent

surgical treatment from January 2000 to March 2011 were

obtained from Second Affiliated Hospital Zhejiang Uni-

versity College of Medicine, a leading comprehensive

teaching hospital in Hangzhou, China. A total of 33 cases

were identified. All available pathology reports and slides

that supported the diagnosis of SPN were reviewed. The

clinical data including sex, age, presentation, risk factors,

preoperative imaging, type of surgical procedure, operative

time, postoperative complications, recurrence, and death

were retrospectively collected. Pancreatic fistulas were

defined according to the concept of International Study

Group on Pancreatic Fistula [7]. The infectious complica-

tions included wound infection, pneumonia, urinary tract

infection, intra-abdominal infections and abdominal

abscess. Independent pathological assessments were also

made of tumor location, size, the resection margin status,

pattern of growth, lymphovascular space invasion, peri-

neural invasion, cellular atypia. Twenty-five specimens

were assessed by immunohistochemical staining to confirm

the diagnosis. Although the criteria for the aggressiveness

of SPNs are not well established, many scholars still con-

sider that there are factors associated with greater malig-

nant potential, such as tumors greater than 13 cm,

metastasis at the first operation, inadequate resection,

invasive growth into the surrounding pancreatic tissue,

vascular or perineural invasion, significant nuclear pleo-

morphism, and a focal sarcomatoid carcinoma component

[8–11]. Long-term survival data and follow-up information

were collected using the patients’ medical records and

personal interviews conducted by telephone. The median

follow-up period was 45 months (range 4–118). The study

protocol was approved by the Institutional Review Board.

Fisher’s exact test and the t test were used for categorical

and continuous data, respectively. Statistical analyses were

performed using the SPSS 15.0 statistics software package

(SPSS Inc., Chicago, IL, USA). A P value \0.05 was

considered to indicate statistical significance.

Results

The 33 patients included 30 females and 3 males, with a

median age of 29.2 years (range 12–59). The most com-

mon symptom was abdominal discomfort with a dull pain

(19, 58 %), others include asymptomatic lesions that were

only detected incidentally during imaging (7, 21 %), a

palpable abdominal mass (5, 15 %) and indigestion

(2, 6 %). None of the patients has jaundice and history of

pancreatic neoplasm or pancreatitis in the cohort. Risk

factors such as Hepatitis B or C infection (4, 12 %), cig-

arette smoking (4, 12 %), alcohol (3, 9 %), diabetes (1,

3 %), abdominal trauma (1, 3 %), pancreatitis (1, 3 %)

were evaluated before the diagnosis of SPN. Twenty-nine

of the 33 patients underwent tumor marker detection.

CA125 in 3 patients (10 %), CA199 in 1 patient (3 %) and

b-HCG in 1 patient (3 %) had values greater than the upper

limits of the normal range. All 33 patients underwent

ultrasonography (US) and computed tomography (CT),

furthermore 2 underwent magnetic resonance imaging

(MRI) and 1 underwent magnetic resonance cholangio-

pancreatography (MRCP). The characteristic imaging

findings included a well-demarcated mass with both solid

and cystic components (31, 94 %; Fig. 1), only a solid

component (2, 6 %), peripheral irregular enhancement (30,

91 %), calcification (9, 27 %), dilated pancreatic duct

(5, 15 %), and portal vein invasion (1, 3 %). None of the

patients was found to have hepatic and lymph nodes

metastases on imaging. MRI can help to identify intratu-

moral hemorrhage. One patient underwent preoperative

percutaneous fine-needle aspiration biopsy and another one

underwent endoscopic US-guided fine-needle aspiration

biopsy, which correctly diagnosed as SPN. All 33 patients

underwent surgery with a curative intent, including distal

pancreatectomy with splenectomy (11, 33 %), enucleation

Table 1 New findings associated with SPNs (10 years, impact factor [5.0)

First Author Years Journal Cases Specific view

Tanaka [17] 2001 Cancer Research 18 b-catenin mutations and Wnt signaling in tumorigenesis.

Yeh [35] 2002 Gut 10 PR is expressed in SPN; however, TFF1, EGF and EGFR are not.

Antonio [41] 2005 Lancet Oncology 1 Gemcitabine provides effective chemotherapy.

Nirag [33] 2008 Cancer 24 Large, clear cytoplasmic vacuoles are useful for diagnosis.

Jani [22] 2008 Endoscopy 28 EUS-FNA was useful in preoperative diagnosis.

Charitini [38] 2009 Cancer 28 CD10 is not reliable in the differential diagnosis.

PR progesterone receptor, TFF1 trefoil factor 1, EGF epidermal growth factor, EGFR epidermal growth factor receptor, EUS-FNA endoscopic

ultrasound-guided fine-needle aspiration

Surg Today (2013) 43:148–154 149

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of the tumor (8, 24 %) including laparoscopic enucleation

(3, 9 %), pancreaticoduodenectomy (6, 18 %), central

pancreatectomy (4, 12 %), pancreatectomy without sple-

nectomy (3, 9 %), pancreaticoduodenectomy with partial

portal vein resection and artificial vascular graft recon-

struction (1, 3 %). The median operative time, estimated

blood loss, and intraoperative transfusion requirements

were 294 min (range 185–615), 225 mL (range 50–2000),

and 0.6 U (range 0–10), respectively. All of the patients

underwent R0 resection. However, 9 (27 %) of the 33

patients developed postoperative complications, including

pancreatic fistula (4, 12 %), infection (4, 12 %), chylous

leak (2, 6 %), bleeding (1, 3 %). The pancreatic fistulas

included 2 patients with grade A, 1 grade B, and 1 grade C.

Four infection cases included one wound infection, one

pneumonia, one urinary tract infection, and one intra-

abdominal infection and abdominal abscess. Most of these

patients were conservatively managed with a successful

outcome, but reoperation was necessary in one patient due

to a pancreatic fistula and abdominal abscess. Adjuvant

chemotherapy or radiotherapy was not given to any of the

patients. Long-term follow-up data (median 45 months,

range 4–118 months) showed 32 patients lived with dis-

ease-free survival and 1 (1, 3 %) experienced local recur-

rence 10 months after distal pancreatectomy with

splenectomy and underwent a second surgery via laparot-

omy. Unfortunately, the patient died of multiple organ

failure 12 days after the second surgery (perioperative

mortality 3 %).

Nineteen of the 33 tumors (58 %) were located in the

pancreatic body and tail, 9 (27 %) in the head, and 5

(15 %) in the neck. The mean diameter of the tumors was

4.9 cm (range 2–15 cm). Tumors greater than 10 cm in

diameter were found in 4 (12 %) patients, between 5 and

10 cm in 14 (42 %) patients, and less than 5 cm in 15

(46 %) patients. All 33 patients had tumor-free resection

margins. Most tumors were characterized to have both

cystic and solid components with hemorrhagic areas

(Fig. 2). Two tumors were entirely solid, but no entirely

cystic tumors were observed, which was consistent with the

preoperative imaging detection. There were fibrous cap-

sules around the tumors (29, 88 %) and the lesions were

sometimes accompanied by calcification (10, 30 %). The

tumor contained small and uniform tumor cells with round

nuclei with both solid and cystic growth patterns (Fig. 3a,

b). The typical features included a pseudopapillary pattern

with fibrovascular stalks. Other common histological

findings included foam cells and cholesterol crystals. Fur-

ther microscopic examination showed perineural invasion

(13, 39 %), local invasion of the peripancreatic tissue (11,

33 %), capsule invasion (3, 9 %), portal vein invasion with

tumor thrombus (1, 3 %), and lymph node metastases (1,

3 %). Nuclear atypia was found in 3 (9 %) tumors. One

tumor showed a solid-pseudopapillary neoplasm combined

with acinar cell carcinoma of pancreas. Hyaline globules

were not noted in the pathological descriptions, possibly

due to limited experience. The immunohistochemical fea-

tures of the tumors were characterized in 27 patients

(Table 2). Nuclear b-catenin labeling was detected in 12

patients; the positive rate was 12/12 (100 %). In addition,

a1-antitrypsin was detected in 26/26 (100 %), vimentin in

26/27 (96 %), synaptophysin in 24/25 (96 %), neuron-

specific enolase in 23/24 (96 %), progesterone receptor in

14/15 (93 %), CD10 was 8/9 (89 %), pancytokeratin in

7/13 (54 %), estrogen receptor in 0/7 (0 %), and chro-

maffin granule protein A in 0/17 (0 %).

The sex ratio of SPNs between females and males was

30:3 (10:1) and the age distribution was prone to 25–45.

There was no significant difference (P [ 0.5) in the clinical

symptoms between different age groups (every decade was

divided into a group). SPN in the head of the pancreas was

larger than those located in the other parts of the pancreas

Fig. 1 A CT scan shows a well-demarcated mass with both solid and

cystic components

Fig. 2 Both cystic and solid components with intratumoral

hemorrhage

150 Surg Today (2013) 43:148–154

123

(P \ 0.01). The age of patients with tumors in different

locations, however, showed no dramatic statistical signifi-

cance (P [ 0.5). All patients were divided into two groups

based on the standard of aggressiveness of SPNs (low-risk

group vs. high-risk group). The clinicopathological details

as predictive factors to evaluate high-risk SPNs are shown

in Table 3. A statistical analysis showed that there were no

significant differences (P [ 0.5) between two groups in the

prognosis. In addition, the prognosis between female and

male did not show a significant difference (P [ 0.5). There

was also no statistical difference between postoperative

complications and the prognosis between laparoscopic

surgery and ordinary surgery (P [ 0.1). The small sample

size may have biased the statistical analysis, and data from

a larger number of patients are thus required to support the

conclusion.

Discussion

The incidence of SPNs among all pancreatic tumors in the

current series was 1.7 %, which is consistent with previous

reports that describe such incidence ranges from 0.17 to

2.7 % [1]. The number of cases has increased significantly

over the past three decades; however, Nguyen [12] indi-

cated that the apparent increasing number of SPNs reported

in the current literature is potentially related to a ‘‘publi-

cation bias’’ or ‘‘diagnostic bias’’. Another study confirmed

that SPNs are more common in female subjects of African–

American and Asian descent [3]. The current study sug-

gests that SPNs usually occur in patients between 25 and

45 years of age, and the median age at diagnosis is

29.2 years. The clinical presentation of SPNs is usually

nonspecific. Previous studies have reported that about

70–90 % of patients presented with symptoms [13, 14].

The current review found that 79 % had symptoms

including abdominal discomfort with a dull pain, a

Fig. 3 a, b H&E staining shows small and uniform tumor cells with round nuclei with both solid and cystic growth patterns

Table 2 Immunohistochemical features of SPNs

Antigen Total

number

Positive

(%)

Negative

(%)

Nuclear b-catenin 12 12 (100) 0 (0)

a1-antitrypsin 26 26 (100) 0 (0)

Vimentin 27 26 (96) 1 (4)

Synaptophysin 25 24 (96) 1 (4)

Neuron-specific enolase 24 23 (96) 1 (4)

Progesterone receptor 15 14 (93) 1 (7)

CD10 9 8 (89) 1 (11)

Pancytokeratin 13 7 (54) 6 (46)

Estrogen receptor 7 0 (0) 7 (100)

Chromaffin granule protein A 15 0 (0) 15 (100)

Table 3 Clinicopathological details as predictive factors to evaluate

high-risk SPNs

Clinicopathological

factors

High-risk group

(n = 17)

Low-risk group

(n = 16)

p value

Gender 1.000

Female 15 15

Male 2 1

Median age (years) 30.0 (19–59) 26.8 (12–42) 0.436

Presentation 0.225

Present 15 11

Absent 2 5

Tumor size (cm) 5.8 (2–15) 4.0 (2–12) 0.091

Tumor location 0.491

Head/neck 6 8

Body/tail 11 8

Calcification 0.708

Present 6 4

Absent 11 12

Tumor nature 0.485

Solid 2 0

Mixed 15 16

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palpable abdominal mass, and indigestion. In addition, a

statistical analysis showed no significant difference in the

clinical presentations in different age groups. The preop-

erative risk factor assessment showed that 12 % of SPN

patients were infected with hepatitis B or C virus, and

12 % were smokers. This suggests that an investigation is

needed to determine whether hepatitis B/C virus infection

or smoking may be involved in the pathogenesis of SPNs,

since these factors are still unclear.

The origin of SPN is uncertain, some of the studies have

suggested that they arise from pluripotent stem cells of the

pancreas [3, 15]. Tang [16] indicated that a mutation of

b-catenin and loss of membrane E-cadherin leads to dis-

ruption of adhesion junctions and eventual disorganized

growth that forms the characteristic pseudopapillary pat-

tern of SPN. Yukichi [17] and Sikora [18] suggested that

the Wnt pathway may be the most important pathways in

the occurrence of SPNs, since b-catenin and E-cadherin are

important molecules in the Wnt signaling pathway.

Interestingly, one tumor in the current study showed a

solid-pseudopapillary neoplasm combined with acinar cell

carcinoma of the pancreas, which raises the question of

whether these two neoplasms share similar gene mutations

or signaling pathways. However, these tumors may have

simply occurred by chance. Further studies are in progress

to confirm whether there is correlation between the two

tumors.

CT is the most frequently used method for diagnosing

SPN, and shows the presence of a heterogeneously

enhanced solid and cystic mass [19]. However, the imaging

may vary greatly depending on the distribution of solid and

cystic components and the hemorrhagic changes. Intratu-

moral calcifications and septa are characteristic features of

SPN. However, the proportion of calcification in this study

is only 9 %. MRI was better than CT in detecting the cystic

or solid components of the tumor in Yu’s study [20]. ERCP

shows displacement of nearby structures or near normal

images of the pancreatic duct [11]. PET may not add

additional information for diagnosis [21]. A fine-needle

aspiration biopsy could be used to increase the accuracy of

the preoperative diagnosis [22]. However, a review article

showed that only 7 % were diagnosed by FNA and punc-

ture-related complications have been frequently reported

[1]. Therefore, a radiologic diagnosis is recommended

when surgery is planned.

SPNs are prone to involve the body and tail of the

pancreas. The current study found that 58 % tumors were

located in the region. There are nine reported cases of

extrapancreatic SPNs, primarily located in the ovary

(3 cases) [23], omentum (2 cases) [24, 25], peritoneum,

[26] liver [27], mesocolon [28], retroperitoneum [29].

SPNs in the head of the pancreas were larger than those

located in the other parts of pancreas in the present study,

which contrasted with the findings in Salvia’s report [30],

but were consistent with the findings of Nguyen’ [12].

There was no significant difference in the age of patients

with tumors in different locations, in contrast to all the

previous reports.

The gross appearance characteristics show both cystic

and solid components with hemorrhagic areas, fibrous

capsules and sometimes calcification. The solid portions of

the tumor are composed of uniform and polygonal epi-

thelioid cells with well-vascularized stroma and a disco-

hesive arrangement [31]. Hyaline globules [32] or large,

clear cytoplasmic vacuoles [33] should help identify SPNs

in the differential diagnosis; however, these could not be

assessed in the current series due to a lack of data and

limited experience. Other characteristics, including an

insidious pattern of invasion and nuclear grooves may

helpful in diagnosis [32]. This study found the presence of

calcification and the tumor nature itself to not be predictive

factors for high-risk SPNs, in contrast to Ho’s recent study

[34]. The typical immunohistochemistry of SPNs includes

positive staining for b-catenin, vimentin, progesterone

receptor, CD56, neuron-specific enolase, CD10, and more

recently, negative membranous E-cadherin, positive cyclin

D1, and positive FLI1 [35, 36]. However, the presence of

CD10 is inconsistent in recent studies [37, 38]. The sen-

sitivity of CD10 was 89 % in the current study.

Surgical resection is the treatment of choice for SPNs

even with metastasis or local recurrence. Distal pancrea-

tectomy with/without splenectomy is the most common

surgical procedure because the tumor is frequently located

in the body and tail of the pancreas. Routine lymphade-

nectomy is not recommended, due to the rare incidence of

lymph node metastasis. However, there are many studies

that indicate a relationship between lymph node positivity

and recurrence [39, 40]. Minimally invasive surgery is

increasingly emphasized in the treatment of the SPNs. A

minimized resection and the standard resection both have

excellent curative effects on long-term follow-up [5].

Miyazaki [29] performed a Laparoendoscopic Single site

Surgery for a 7-cm retroperitoneal SPN. Laparoscopic

enucleations were performed in 3 of the current patients,

and the statistical analysis of postoperative complications

and the prognosis showed no difference between laparo-

scopic surgery and ordinary surgery. However, the benefits

of minimally invasive surgery are obvious, including less

trauma, a shorter surgical time and hospital stay, and less

influence on the quality of life. Minimally invasive surgery

may become the standard surgical treatment of SPNs in the

future. However, the accumulation of large-scale clinical

data is still necessary to support this view.

The overall 5-year survival rate of SPNs is about 95 %

[1]. Although the malignant potential of SPN is low,

approximately 10–15 % of patients develop metastatic

152 Surg Today (2013) 43:148–154

123

disease, most often involving the liver or peritoneum [15].

Aggressive behavior can be unpredictable, and many

scholars have proposed a number of different criteria

[8–11]. However, the statistical analysis in the current

study showed that aggressive behavior may not be related

to gender and prognosis. Therefore, all SPN patients need

long-term follow-up, which is more important than the

evaluation of benign and malignant tumors. Rare cases are

difficult to remove or present with metastasis, which may

benefit from chemotherapy [41] and radiotherapy, but clear

role for these therapies has been demonstrated [42]. An in-

depth study of molecular pathways may reveal specific

molecular targets to provide important adjuncts in the

treatment of SPNs.

In conclusion, SPNs are rare neoplasms that most

commonly occur in young females with a malignant

potential, but an excellent prognosis. Adequate surgical

resection, including laparoscopic surgery, may be per-

formed safely and is associated with a long-term survival,

even in invasive cases. The role of adjuvant therapy

remains to be studied.

Conflict of interest Y. Deng and other co-authors have no conflict

of interest to declare.

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