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A role for surgery in primary pancreatic B-cell lymphoma: a case report

  • Theodore Liakakos1,
  • Evangelos P Misiakos1Email author,
  • Dimitrios Tsapralis1,
  • Irene Nikolaou2,
  • Gabriel Karatzas1 and
  • Anastasios Macheras1
Journal of Medical Case Reports20082:167

DOI: 10.1186/1752-1947-2-167

Received: 10 August 2007

Accepted: 19 May 2008

Published: 19 May 2008

Abstract

Introduction

Primary pancreatic lymphoma is a very rare but manageable malignant tumour which may be clinically confused as a pancreatic carcinoma. This case report demonstrates the value of surgical resection in the management of pancreatic lymphoma.

Case presentation

We report a case of a 65-year-old man who was admitted with obstructive jaundice, vague upper abdominal pain and weight loss. Ultrasonography and computed tomography showed a mass at the head of the pancreas which was compressing the bile duct. The patient underwent pancreaticoduodenectomy. Histopathologic and immunohistochemical assessment of the pancreatic lesion established the diagnosis of a diffuse, extranodal, high-grade B-cell non-Hodgkin's lymphoma. Several doses of chemotherapy were administered postoperatively and at present the disease remains in remission.

Conclusion

The favourable outcome for this patient and a thorough review of the literature underline the important role that operative resection may have in the management of at least the early stage of primary pancreatic lymphoma.

Introduction

Non-Hodgkin's lymphoma (NHL) most frequently arises from the lymphatic system, with the gastrointestinal (GI) tract representing the most commonly involved extranodal site, accounting for half of such cases. In Western series, GI lymphoma occurs principally in the stomach, followed by the small bowel and the colon [1]. Primary involvement of the pancreas in lymphoma is rare, representing a small fraction (less than 1 to 2%) of all pancreatic malignancies [2]. To distinguish primary pancreatic lymphoma (PPL) from secondary involvement of the pancreas by NHL, Behrns' diagnostic criteria include: a predominant pancreatic mass with gross involvement of only the peripancreatic lymph nodes; no hepatic or splenic involvement; no palpable superficial lymphadenopathy; no enlargement of the mediastinal lymph nodes on chest radiograph; and a normal leukocyte count [3].

Current standard management for PPL has relied mainly on the use of various chemotherapeutic protocols, such as the commonly used regimen of cyclophosphamide, doxorubicin, vincristine and dexamethazone (CHOP). The role of surgery in the management of pancreatic lymphoma has been limited to obtaining diagnostic tissue samples or to bypassing biliary obstruction [4]. More recently, less invasive techniques, such as image-guided percutaneous biopsy, have successfully provided a tissue diagnosis in more than 80% of patients [5].

Although initial results with chemotherapy were encouraging, recent studies with longer follow up of patients with NHL treated with standard chemotherapy with or without radiotherapy have demonstrated higher recurrence rates, particularly for patients with abdominal lymphomas [6]. Given the modest results of standard chemotherapy, the known benefits of surgical resection in the prognosis of other GI lymphomas [7], and recent improvements in clinical outcome after radical pancreatic surgery, the role of surgical resection in the treatment of pancreatic NHL is being reassessed [2].

Here we present the case of a patient initially managed as suffering from adenocarcinoma of the pancreas, who ultimately proved to have PPL. The combined treatment of radical surgical resection and chemotherapy resulted in a good clinical outcome.

Case presentation

A 65-year-old man with a 4-week history of mild epigastric pain radiating to the back (exacerbated after meals), progressive obstructive jaundice, anorexia and weight loss of 3 kg was admitted to our Department of Surgery in November 2005. There was no history of a change in bowel habit, melena, haematochezia, pancreatitis, liver or gallbladder disease. The patient had undergone open repair of an abdominal aortic aneurysm 5 years previously and he was a heavy smoker (40 pack-years) and had a high alcohol intake (300 ml/day).

Upon admission, the patient was icteric, afebrile and had normal vital signs. Physical examination revealed normal bowel sounds, deep jaundice and mild tenderness in the epigastrium and right upper quadrant, without evidence of peripheral lymphadenopathy, palpable mass or hepatosplenomegaly. The patient had an unremarkable haematological profile, but the liver function tests were abnormal: aspartate transaminase (AST) 253 IU/l, alanine transaminase (ALT) 393 IU/l, total bilirubin 7.9 mg/ml, direct bilirubin 6.41 mg/ml, alkaline phosphatase 236 U/l and gamma glutamyl transpeptidase (GGT) 462 U/l. Both serum carcinoembryonic antigen titre and serum carbohydrate antigen titre were normal.

The patient underwent ultrasonography of the liver, biliary tract and pancreas, which revealed a hypoechoic mass at the head of the pancreas. Further assessment of this finding with helical, contrast-enhanced abdominal computed tomography (CT) demonstrated the presence of a large, hypodense, non-homogeneous lesion at the head of the pancreas, with a maximal diameter of 5 cm, without dilatation of the main pancreatic duct (Figure 1). Limited lymphadenopathy was also detected in the peripancreatic and the para-aortic regions. The tumour was in contact with the superior mesenteric vein (SMV) without signs of infiltration or encasement of the vein or of the superior mesenteric artery (SMA). The patient also underwent upper GI endoscopy, which revealed mild gastritis in the gastric antrum without evidence of malignancy in the stomach or duodenum. A CT-guided fine needle aspiration (FNA) biopsy was not diagnostic, and the patient was scheduled for exploratory laparotomy.
https://static-content.springer.com/image/art%3A10.1186%2F1752-1947-2-167/MediaObjects/13256_2007_Article_354_Fig1_HTML.jpg
Figure 1

Contrast-enhanced helical CT scan. This scan demonstrates the heterogeneous enhancement of a large tumour of the head of the pancreas, in contact with the superior mesenteric vein (SMV), without signs of infiltration or encasement of the vein, or the superior mesenteric artery (SMA).

At surgery, a large mass at the pancreatic head was found, which could be easily separated from the contiguous vascular structures with blunt dissection. Interestingly, the tumour did not seem macroscopically to invade the surrounding viscera. A pancreaticoduodenectomy (Whipple procedure) was performed. Histologic evaluation of the surgical specimen revealed extensive involvement of the pancreas by a diffuse, extranodal, high grade, large cell, NHL (centroblastic lymphoma). A neoplastic population, consisting of large non-cleaved lymphoid cells with nucleoli, was seen to surround pancreatic ducts; no lymphoepithelial lesions were present (Figure 2). A few small reactive T lymphocytes CD3+ and CD45R0+ (Dako, Glosrtup, Denmark) were observed. Immunohistochemical assessment of the neoplastic cells revealed B lymphoid phenotypes CD20+ (Dako) (Figure 3) and CD10+ (Cell Marque Corporation, USA), and the cells were negative for CD3, CD45R0, CD30, CD15, ALK (anaplastic lymphoma kinase), EMA (epithelial membrane antigen) (Dako) and EBN-A2 (Epstein-Barr virus nuclear antigen 2) (Dako). Mitotic activity was very high (Ki67 (Dako) > 80%) (Fig. 4). The tumour was classified as stage IIE according to the Ann Arbor classification [8, 9]. The resection margins were free of disease. However, all adjacent lymph nodes in the gastric or peripancreatic region were infiltrated by the tumour.
https://static-content.springer.com/image/art%3A10.1186%2F1752-1947-2-167/MediaObjects/13256_2007_Article_354_Fig2_HTML.jpg
Figure 2

Neoplastic lymphoid population surrounding pancreatic duct with no evidence of lymphoepithelial lesions (H/E × 200).

https://static-content.springer.com/image/art%3A10.1186%2F1752-1947-2-167/MediaObjects/13256_2007_Article_354_Fig3_HTML.jpg
Figure 3

CD20 positivity of neoplastic lymphoid cells (CD20 × 200).

https://static-content.springer.com/image/art%3A10.1186%2F1752-1947-2-167/MediaObjects/13256_2007_Article_354_Fig4_HTML.jpg
Figure 4

High mitotic activity highlighted by Ki67 expression (Ki67 × 200).

In the immediate postoperative course, the patient had several episodes of bilious vomiting shortly after food intake, attributed to oedema of the gastrojejunostomy, which gradually resolved. He also developed a pancreatic fistula which completely resolved after 5 weeks without affecting the patient's nutritional status or electrolyte balance.

After surgery the patient underwent four chemotherapeutic sessions consisting of cyclophosphamide, novantrone, vincristine and prednisone, all administered at 3-week intervals. Twenty-one months after surgery the patient was alive and in a good clinical condition.

Discussion

PPL is a very rare neoplasm that may be confused with adenocarcinoma, the most common neoplasm of the pancreas. An extensive review of the international literature has revealed a total of 162 adult patients with biopsy-proven NHL primarily involving the pancreas (Table 1) [2, 3, 1017]. The clinical manifestation of PPL is non-specific and differentiation from pancreatic adenocarcinoma on a clinical basis is difficult. Only in cases where a patient presents with abdominal pain and a palpable mass without jaundice is the clinical suspicion of pancreatic lymphoma, over adenocarcinoma, enhanced.
Table 1

Literature review of primary pancreatic lymphoma: patients' characteristics, pathologic types, treatment and outcome

First author

Year

Number (n)

Pathology

Operation

Chemotherapy

Radiotherapy

Outcome

Response

Feather

1951

1

DLBCL

Total Pancreatectomy

None

None

16 months – NED

CR

Acherman

1976

3

DLBCL

None

CHOP

Yes

12 months – NED

CR

Boddie

1980

2

DLBCL

     

Freed

1983

1

NR

Distal Pancreatectomy

None

None

12 months – NED

CR

Teefy

1986

2

DLBCL (1) FLCL (1)

None

Yes

Yes

12 months – Death

PR

Hart

1987

14

Histiocytic (9) Poorly diff lymphocytic (2) Well diff lymphocytic (1) T-cell (1) Undifferentiated(1)

Distal Pancreatectomy (1)

CHOP (14)

1 of 14

NR (1 with resection) Death (7) at 3 to 108 months)

NR

Webb

1988

9

DLBCL (6) Follicular mixed (2) Small cleaved (1)

Distal Pancreatectomy (1)

MACOP-B (8) CAMEL (1)

None

95 months-NED (1) 21 months-NED (8)

CR

Mansour

1989

12

NR

Distal Pancreatectomy(1)

CHOP (11)

5 of 9

Death (5) in 2 to 11 months, Recurrence (2) in 3 and 48 months

PR

Cappell

1989

1

DLBCL

     

Tuchek

1993

7

NR

None

CHOP (1) CVP (1) CAMEL (1)

NR

Death (4) Alive (3) at 60, 72, 96 months

CR

Borrowdale

1994

1

NR

Whipple

Yes

None

Death in 12 months

CR

Behrns

1994

12

DLBCL (7) Small cleaved (2) Mixed (3)

Whipple (1) Bypass (4)

CHOP (4)

4 of 12

Death in 38 months at most

PR

Fidias

1995

3

DLBCL

None

CHOP

None

Death (1) Recurrence (1) NED in 36 months(1)

CR (2) PR (1)

Tanaka

1996

1

DLBCL (1)

Whipple

CHOP

NR

NED in 36 months

CR

Ezzat

1996

5

DLBCL (5)

Whipple (1)

CHOP (4) CHOP-Ble (1)

NR

NED in 21 to 84 months (4)

PR

Rumstadt

1997

2

DLBCL (2)

Whipple (2)

CHOP (1)

None

NED in 29 months

CR

Bouvet

1997

11

DLBCL (10) Mixed follicular (1)

Whipple (1) Distal Pancreaticoduo-denectomy (2)

CHOP-Bleo

7of 11

Death (3) Recurrence (2) NED (6)

CR

James

1997

2

DLBCL (1)

None

CHOP (1) PACEBO + CHOP (1)

1 of 2

NED in 24 months

PR

Koniaris

2000

8

DLBCL (7) Nixed follicular (1)

Whipple (3)

CHOP (6) MACOP-B

None

Death (2) NED (3, resection)

CR

Islam

2001

1

DLBCL

Bypass, biopsy

CHOP

None

NED in 18 months

CR

Nishimura

2001

19

DLBCL (15) T-cell (4)

Pancreatectomy(10)

CHOP (5) Mitomycin Tegafur (1) Unspecified chemo (1)

NR

1-year actuarial survival B-cell: 51.9% T-cell: 0%

PR

Boni

2002

1

DLBCL (1)

Laparoscopy-biopsy

Chemo (1)

None

NED in 9 months

CR

Hauksson

2002

1

DLBCL

PTC stenting biopsy

Chemo

NR

NR

NR

Volmar

2004

14

DLBCL (6) follicular (4) Suggestive of lymphoma (3) B lymphoma (1)

No

Yes

NR

Death (3) Alive (11) in a mean 11.8- month followup

2 PR 11 CR

Nayer

200410

8

DLBCL (4) High-grade B-cell (1) Low grade B (2) Suspicious (1)

None

Chemo (4) Chemo and auto SCT (2) Nr (2)

3 of 8

6 alive at 2 to 6 months

PR

Pezzilli

2004

1

T-cell lymphoma

None

Chemo (1)

None

Death (1)

NR

Arcari

2005

5

DLBCL (3) Lymphoplasmacytic (2)

Pancreatectomy (2)

CVP/CHOP(3) CHOP(1) CVP(1)

2 of 5

Death (3) Alive 2, (1, resection)

PR

Grimison

2005

4

DLBCL (3) Follicular (1)

None

CHOP(2) Rituximab-CHOP(1) CVP(1)

4

Death 132 months Alive 3 at 15, 25, 64 months

PR

Ji

2005

1

DLBCL (1)

Whipple (1)

NR

NR

NR

NR

Savopoulos

2005

1

ALCL (1)

Biopsy

None

None

Died 2nd postoperative day

-

Kang

2006

1

Non-Hodgkin's lymphoma

Biopsy

NR

NR

NR

NR

Lin

2006

6

DLBCL (6)

Whipple (2) Pancreatectomy (1) Biliary decompression (1)

Chemo (6)

γ-radiotherapy (1)

Death (3) at 2, 37, 49 months NED in 21 months (1)

PR

Battula

2006

1

DLBCL (1)

Whipple (1)

CHOP (1)

NR

NR

NR

Liakakos

2007

1

DLBCL (1)

Whipple (1)

Cyclophosphamide Novantrone Vincristine Prednisone

No

Alive (2 years)

PR

DLBCL, diffuse large B-cell lymphoma; FLCL, follicular large cell lymphoma; CHOP, cyclophosphamide, doxorubicin, vincristine, prednisolone; PACEBO, prednisolone, hydroxydaunorubicine, cyclophosphamide, etoposide, bleomycin, vincristine; CAMEL, cyclophosphamide, adriamycin, vincristine, prednisone; CVP, cyclophosphamide, vincristine, prednisone; SCT, stem cell transplantation; NED, no evidence of disease; NR, not reported; CR, complete response; PR, partial response

There are some biochemical markers which, in conjunction with suspicious clinical manifestations, may help focus the physician's attention on the possibility of a pancreatic lymphoma. More specifically, lactate dehydrogenase (LDH) and β2 microglobulin are considered to be tumour markers in lymphoproliferative disorders and have an important positive prognostic value. Serum carbohydrate antigen 19-9 (CA 19-9) level in patients with PPL is usually not elevated. This is in contrast with pancreatic adenocarcinoma, in which almost 80% of cases have a high CA19-9 level [11].

Pancreatic lymphoma, like most extralymphatic lymphomas, is predominantly of intermediate or high-grade histology, with diffuse large B-cell lymphoma being the predominant type [12]. Less than 20% of reported cases demonstrate low-grade histology. The majority of pancreatic lymphomas reported to date in the literature have been classified as of B-cell type, but several cases of T-cell lymphomas have also been described [13].

CT is the most common imaging technique used in the detection and characterization of PPL. On CT, two different morphologic patterns of pancreatic involvement are seen; one is a localized, well-circumscribed tumour with diffuse enlargement infiltrating most of the pancreatic gland. This pattern may mimic the imaging findings of acute pancreatitis with gland enlargement and irregular infiltration of the peripancreatic fat [14]. The well-circumscribed tumoural form can be easily misinterpreted as a ductal adenocarcinoma, especially in patients with dilatation or encasement of the pancreatic and common bile ducts [15]. In contrast, the combination of a bulky, localized tumour in the pancreatic head without significant dilatation of the main pancreatic duct, as seen in our case, strengthens a diagnosis of pancreatic lymphoma over adenocarcinoma. Furthermore, if enlarged lymph nodes are encountered below the level of the renal veins, in association with a large pancreatic tumour, virtual exclusion of adenocarcinoma is possible [14].

Contrast-enhanced CT also offers certain criteria to define the resectability of pancreatic tumours: the absence of extrapancreatic disease; preservation of the fat plane between the tumour and the confluence of superior mesenteric and portal vein (SMPV); and absence of tumour involving or encasing the SMA, coeliac or hepatic arteries [15]. Therefore, one may rely on the CT findings without the need for additional imaging studies in order to evaluate the resectability of a pancreatic head tumour.

Although certain serum abnormalities and CT changes are suggestive of lymphoma, tissue examination is essential for diagnosis. Patients presenting with advanced disease may be diagnosed by peripheral lymph node FNA, core or open biopsy [2, 16]. However, there are cases in which the performance of explorative laparotomy becomes mandatory due to the inability of the aforementioned diagnostic modalities to differentiate between pancreatic adenocarcinoma and some other types of pancreatic malignancy [4, 11].

At present, the standard protocols for management of pancreatic lymphomas include a number of chemotherapy regimens [10]. The most commonly used regimen is the first-generation therapy CHOP [2], but a range of second- and third-generation regimens are also used. Expected outcomes for all NHL treatments, based on multi-institutional studies using CHOP or an equivalent chemotherapy, with or without radiotherapy, regardless of location, are a complete response rate of approximately 50%, and a partial response rate of approximately 30%. Overall, a 3-year disease-free survival rate of 46% has been reported after such therapies [6].

The observed moderate long-term survival rates for pancreatic NHL with chemotherapy and radiotherapy alone, and the improvements in morbidity and mortality associated with pancreatic surgery, call for a re-evaluation of therapeutic strategies for NHL of the pancreas [17]. A retrospective analysis and a comparison of 15 surgically treated patients with PPL (treated between 1951 and 2000 in several centres) with non-operatively treated stage I or II pancreatic NHL patients (encountered over a similar period) by Koniaris et al. [2] demonstrated markedly improved complete remission and cure rates in the surgically treated group. Detailed comparison between the surgically treated and non-surgically treated groups reveals that age, histologic subtypes and male to female ratio were similar in the two groups. Tumour size was clearly larger in the non-operated group and in many cases patients treated conservatively had unresectable disease. However, the successfully resected group represented a dramatic complete response rate of 100% and long-term survival rate of 94%. These data suggest that for surgically resectable stage I or II pancreatic NHL, resection should be an option in the multimodal therapeutic regimen [11]. To the potential role of surgery in the treatment of pancreatic NHL should be added its well-established place in the management of lymphoma involving other GI organ systems, such as gastric and small bowel lymphomas [7].

Conclusion

When a patient with a pancreatic mass is encountered, preoperative contrast-enhanced CT or magnetic resonance imaging should be obtained. Only in cases in which the resectability of a pancreatic head mass is regarded as impossible, according to the above criteria, should the performance of a definite tissue diagnosis be contemplated. This is achieved with the aid of percutaneous FNA and flow cytometry analysis. If a mass located in the head of the pancreas is regarded as potentially resectable, we advocate explorative laparotomy of the patient. If the intraoperative findings confirm the feasibility of resection of the tumour, pancreaticoduodenectomy is advocated, provided that the surgery is performed by surgeons well-practised with the nuances required for safe pancreatic resection, especially in the case of PPLs, which also respond well to treatment with chemotherapy and radiotherapy alone.

Consent

Written informed consent was obtained from the patient for publication of this case report and accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Abbreviations

ALT: 

alanine transaminase

AST: 

aspartate transaminase

CA 19-9: 

carbohydrate antigen 19-9

CHOP: 

cyclophosphamide, doxorubicin, vincristine and dexamethazone

CT: 

computed tomography

EBN-A2: 

Epstein-Barr virus nuclear antigen 2

EMA: 

epithelial membrane antigen

FNA: 

fine needle aspiration

GGT: 

Gamma glutamyl transpeptidase

GI: 

gastrointestinal

LDH: 

lactate dehydrogenase

NHL: 

non-Hodgkin's lymphomas

PPL: 

primary pancreatic lymphoma

SMA: 

superior mesenteric artery

SMPV: 

superior mesenteric and portal vein

SMV: 

superior mesenteric vein.

Declarations

Authors’ Affiliations

(1)
Third Department of Surgery, University of Athens School of Medicine, Attikon University Hospital
(2)
Department of Pathology, University of Athens School of Medicine, Attikon University Hospital

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© Liakakos et al; licensee BioMed Central Ltd. 2008

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.