Summary

Hepatobiliary involvement by malignant lymphoma is usually a secondary manifestation of systemic disease, whereas primary non-Hodgkins lymphoma of the extrahepatic biliary ducts is an extremely rare entity. We describe the case of a 57-year-old man who presented with an acute onset of obstructive jaundice and severe itching. Abdominal ultrasonography and computed tomography revealed intrahepatic and common hepatic ducts dilatation. Magnetic resonance cholangiopancreatography and endoscopic retrograde cholangiopancreatography showed a mid-common bile duct stricture. The patient was presumed to have cholangiocarcinoma of the common bile duct, and an en bloc resection of the tumor with Roux-en-Y hepaticojejunostomy and porta-hepatis lymph nodes dissection was performed. Histopathology and immunohistochemistry revealed a large B cell non-Hodgkins lymphoma. The patient received six cycles of combination chemotherapy using cyclophosphamide, vincristine, prednisone, and rituximab (CVP-R) protocol, and after a 5-year follow-up he is still in complete remission. We also reviewed the cases published from 1982 to 2012, highlighting the challenges in reaching a correct preoperative diagnosis and the treatment modalities used in each case.

Keywords

bile duct;non-Hodgkins lymphoma

1. Introduction

Non-Hodgkins lymphoma (NHL) accounts for 1–2% of all cases of malignant biliary obstruction.1 To our knowledge and after reviewing the literature since the first case was published by Nguyen2 in 1982, only 28 cases have been reported. Herein we present another case of primary NHL of the common bile duct. A literature review was conducted of the challenges in arriving at the diagnosis preoperatively and the debate around the optimal treatment modalities.

2. Case report

A 57-year-old man with no previous chronic medical illnesses presented with a 2-week history of severe itching all over his body, associated with general fatigue, malaise, and nausea, without vomiting or anorexia. He also reported having a yellowish discoloration of sclera, dark (tea color) urine, and a bulky foul-smelling stool. However, he denied any history of fever or chills, abdominal pain, previous episodes of similar symptoms, recent travels, or contact with sick people. He is not on any regular medications, and he denied recent ingestion of any drug. His surgical history and family history showed no significant finding. Moreover, he has a 40 pack-year smoking history but no history of alcohol consumption or illicit drug use.

On presentation his vital signs were within normal limits. The physical examination revealed deep scleral and skin jaundice with itching marks on his skin. There was no cervical lymphadenopathy and no stigmata of chronic liver disease. An abdominal examination revealed a soft and lax abdomen with mild tenderness over the epigastric and right upper quadrant areas, and active bowel sounds but no masses or hepatosplenomegaly.

His laboratory results showed hemoglobin, white cell count, and platelets of 15 g/dL, 7 × 103/mm3, and 162 × 103, respectively. His serum total bilirubin, direct bilirubin, alanine aminotransferase, aspartate aminotransferase, alkaline phosphatase, gamma glutamyl transpeptidase, lactate dehydrogenase, and amylase results were 18.3 mg/dL 16.1 mg/dL, 116 U/L, 66 U/L, 161 U/L, 658 U/L, 898 U/L, and 58 U/L, respectively. His blood carbohydrate antigen 19-9 level rose to more than 1200 U/mL, and carcinoembryonic antigen was within normal levels at 0.88 ng/mL. Hepatitis A, B, and C serology was negative.

Abdominal ultrasonography revealed dilated common hepatic and intrahepatic ducts. An endoscopic retrograde cholangiopancreatography (ERCP) was subsequently performed and showed a 3-cm mid-common bile duct stricture with significantly dilated intrahepatic and common hepatic biliary ducts. The rushing cytology of the common bile duct was suspicious for malignancy. A 9-cm, 10 F stent was inserted across this for drainage (Fig. 1A).


Imaging studies. (A) Endoscopic retrograde cholangiopancreatography showing the ...


Figure 1.

Imaging studies. (A) Endoscopic retrograde cholangiopancreatography showing the mid common bile duct stricture. (B) Computed tomography scan of the abdomen showing intrahepatic bile tract dilatation. (C) Magnetic resonance cholangiopancreatography showing the tapered stricture of the distal common bile duct.

The abdominal computed tomography (CT) scan revealed a mild intrahepatic biliary tree dilatation but was otherwise unremarkable (Fig. 1B).

Magnetic resonance cholangiopancreatography showed a marked tapered stricture at the distal common bile duct with mild to moderate dilatation of biliary tree proximally, and a normal pancreatic duct (Fig. 1C).

Based on the above presentation and investigations, a presumptive diagnosis of cholangiocarcinoma was made, and extrahepatic biliary tract excision, a Roux-en-Y hepaticojejunostomy, and porta-hepatis lymph nodes excision were performed.

A histopathologic examination of the common bile duct revealed a large B cell-type NHL with tumor-free surgical resection margins (Fig. 2), and the porta-hepatis lymph nodes showed a reactive nonspecific hyperplasia. Immunohistochemical staining was positive for CD3, CD5, CD20, CD45, BCL2, and Ki67, and negative for CD15 and CD30 (Fig. 3).


Histopathology of the common bile duct showing proliferating lymphocytes of ...


Figure 2.

Histopathology of the common bile duct showing proliferating lymphocytes of medium to large size, in a background of eosinophils, neutrophils, and reactive T cell lymphocytes. Many mitotic figures and apoptotic bodies are seen.


Immunohistochemistry showing (A) positive CD20, a marker of B cell lymphoma; (B) ...


Figure 3.

Immunohistochemistry showing (A) positive CD20, a marker of B cell lymphoma; (B) positive Ki67 in 80% of the slide reflecting a high grade; (C) negative CD15, a marker of Hodgkins lymphoma; (D) negative CD30, a marker of Hodgkins lymphoma.

The patient was referred to the oncology clinic, where a positron emission tomography showed no evidence of malignant lesions. He received six cycles of chemotherapy using the CVP-R (cyclophosphamide, vincristine, prednisone, and rituximab) protocol. One-year follow-up chest, abdomen, and pelvis CT and whole-body positron emission tomography scans revealed no evidence of malignancy. He received six maintenance courses of rituximab (anti-CD20) and remains in complete remission 5 years from the time of diagnosis with a normal whole-body CT scan.

3. Discussion

Diffuse large B cell lymphoma (DLBCL) is the most common lymphoid neoplasm and the most common histologic subtype of NHL, accounting for approximately 25% of all cases.3 It has an overall incidence rate of 3–7 cases per 100,000 persons per year. The incidence also increases with age (median age 64 years), and the disease appears to be slightly more predominant in men (55% of cases) and Caucasian Americans.4 DLBCL typically presents with rapid nodal enlargement in the neck or abdomen, and systemic “B” symptoms are observed in 30% of patients.5 The extranodal extramedullary disease occurs in up to 40% of the cases, and the gastrointestinal tract is the most common site of involvement. In such cases, the presenting symptoms are abdominal pain, loss of appetite, weight loss, vomiting, and night sweats.6

Among all patients with malignant biliary obstruction, NHL accounts for 1–2% of all cases. Their presentation with obstructive jaundice is mostly secondary to compression of the extrahepatic bile ducts by periportal, perihepatic, or peripancreatic lymphadenopathy, associated tumor lysis, or direct hepatic involvement.1

It is extremely rare for NHL to arise primarily from the extrahepatic bile ducts. As shown below in (Table 1),2; 7; 9; 10; 11; 12; 13; 14; 15; 16; 17; 18; 19; 20; 21; 22; 23; 24; 25; 26; 27; 28; 29; 30; 31; 32; 33 ;  34 a literature review of the period between 1982 and 2012 revealed only 28 cases, with an acute onset of obstructive jaundice being the presenting symptom in most. Of note is that only one case presented with a picture of acute pancreatitis.

Table 1. Literature review of primary NHL of the biliary ducts between 1982 and 2012.2; 7; 9; 10; 11; 12; 13; 14; 15; 16; 17; 18; 19; 20; 21; 22; 23; 24; 25; 26; 27; 28; 29; 30; 31; 32; 33 ;  34
Case Author Age (y)/sex Preliminary diagnosis Histopathologic diagnosis Treatment modality Outcome
1 Nguyen2 59/male Sclerosing cholangitis Lymphohistiocytic lymphoma, diffuse type Surgery Chemotherapy Died after 8 mo
2 Takehara et al11 60/male Non-Hodgkins lymphoma of the extrahepatic duct Surgery Chemotherapy Unknown
3 Kaplan et al12 42/male Cholangitis High-grade non-Hodgkins lymphoma Surgery: Cholecystectomy, segmental resection of the CBD, and hepaticoduodenostomy Chemotherapy using cyclophosphamide, vincristine, etoposide, methotrexate, and cytosine arabinoside Died after 10 mo
4 Tartar and Balfe13 48/male Bile duct wall lymphoma Surgery Chemotherapy Alive after 14 mo
5 Tzanakakis et al14 70/male Mixed small and large cell non-Hodgkins lymphoma Surgery Chemotherapy Died after 4 mo
6 Kosuge et al15 68/female B cell lymphoma of the CBD Surgery Chemotherapy Radiotherapy Died after 16 mo
7 Brouland et al16 34/female GB carcinoma vs. sclerosing cholangitis T cell-rich B cell lymphoma (centroblastic type) of the CBD Surgery Chemotherapy using MACOP-B Alive after 48 mo
8 Machado et al17 43/female Bile duct lymphoma Surgery Radiotherapy Alive after 6 mo
9 Chiu et al18 25/female Malignant lymphoma of the bile duct Surgery Died after 12 mo
10 Andre et al19 44/female Klatskin tumor Non-Hodgkins lymphoma of the extrahepatic duct Surgery Chemotherapy Alive after 48 mo
11 Maymind et al20 39/female Diffuse large B cell lymphoma of the CBD Surgery Chemotherapy using six courses of CHOP protocol Radiotherapy Alive after 13 mo
12 Podbielski et al21 66/male Klatskin tumor vs. sclerosing cholangitis Large B cell non-Hodgkins lymphoma Surgery: En bloc resection of the tumor Unknown
13 Oda et al22 58/male Non-Hodgkins lymphoma of the extrahepatic duct Surgery Died after 32 d
14 Corbinais et al23 29/male High-grade T cell non-Hodgkins lymphoma of the CBD Chemotherapy using COP plus CHOP protocol Alive after 12 mo
15 Eliason and Grosso24 41/male Klatskin tumor Diffuse large B cell lymphoma of the extrahepatic ducts Surgery: CBD excision, Roux-en-Y hepaticojejunostomy, and cholecystectomy Unknown
16 Gravel et al25 4/male Sclerosing cholangitis, histiocytosis X or lymphoma Lymphoblastic lymphoma of the pre-B type of the biliary ducts Surgery: Exploratory laparotomy, incisional biopsy of the GB, and then cholecystectomy Chemotherapy using methotrexate, vincristine, doxorubicin, and prednisone Alive after 18 mo
17 Kang et al26 73/female Pancreatic vs. cholangiocarcinoma Low-grade B cell lymphoma of MALT type Surgery: Whipples operation Alive after 23 mo
18 Ferluga et al27 3/female Klatskin tumor Grade II follicular lymphoma of the GB, cystic duct and CBD Surgery: Resection of GB and CBD followed by hepaticojejunostomy Alive after 36 mo
19 Suzuki et al28 71/female Bile duct carcinoma MALT lymphoma of the CBD Surgery: Pylorus-preserving pancreaticoduodenectomy Unknown
20 Joo et al9 21/female Bile duct cholangiocarcinoma Diffuse large B cell malignant non-Hodgkins lymphoma Surgery Chemotherapy using CHOP protocol Radiotherapy using 3060 cGy external irradiation Alive after 17 mo
21 Sugawara et al29 33/male Hepatic hilar cholangiocarcinoma Follicular lymphoma of the extrahepatic duct Surgery: Extrahepatic duct resection with right and left hepaticojejunostomy Alive after 12 mo
22 Shito et al30 71/male Klatskin tumor MALT lymphoma of the main hepatic duct junction Surgery: Left hepatic and caudate lobectomy, bile duct resection and LN dissection Chemotherapy using three courses of CHOP protocol Alive after 45 mo
23 Dote et al10 63/male Pancreatic head carcinoma or cholangiocarcinoma of the CBD Diffuse large B cell non-Hodgkins lymphoma of the CBD Surgery: Subtotal stomach-preserving pancreaticoduodenectomy Chemotherapy using three courses of R-CHOP protocol Alive after 8 mo
24 Christophides et al31 53/female Infiltrative cholangiocarcinoma vs. hepatocellular carcinoma High-grade follicular lymphoma (grade 3A) of the extrahepatic ducts Surgery: Extended right hepatectomy and Roux-en-Y hepaticojejunostomy Chemotherapy using CHOP-R protocol Alive after 48 mo
25 Kang et al32 60/male Klatskin tumor Diffuse large B cell non-Hodgkins lymphoma of the CHD Surgery: CHD excision, Roux-en-Y hepaticojejunostomy and LN dissection Chemotherapy: Adjuvant chemotherapy was scheduled Unknown
26 Yoon et al7 62/male Cholangiocarcinoma of the bile duct Marginal zone B cell lymphoma of the MALT type Surgery: Right hemihepatectomy, bile duct resection and LN resection Unknown
27 Luigiano et al33 30/male Acute pancreatitis Malignant large B cell-type lymphoma of the CBD Surgery: Resection of the CBD Chemotherapy using CHOP-R protocol Alive after 6 mo
28 Khozeimeh et al34 32/male Klatskin tumor Follicular lymphoma of the bile duct Surgery: En bloc resection of the bile duct and GB and Roux-en-Y hepaticojejunostomy Chemotherapy using four courses of rituximab (anti-CD20) and galiximab (anti-CD80) Alive after 72 mo
29 This study 57/male Cholangiocarcinoma of the CBD High-grade large B cell non-Hodgkins lymphoma of the CBD Surgery: CBD resection, Roux-en-Y hepaticojejunostomy and LN dissection Chemotherapy using six courses of CVP-R protocol Alive after 41 mo

CBD = common bile duct; CHD = common hepatic duct; CHOP = cyclophosphamide, hydroxydaunorubicin, oncovin and prednisone; COP = cyclophosphamide, oncovin and prednisone; CVP-R = cyclophosphamide, vincristine, prednisone, and rituximab; GB = gallbladder; LN = lymph node; MACOP-B = methotrexate, adriamycin, cyclophosphamide, oncovin, prednisone, and bleomycin.

In all cases reviewed, including the one reported above, the clinical presentation, the laboratory investigations, and the results of CT and cholangiography were more consistent with sclerosing cholangitis, Klatskin tumor (cholangiocarcinoma at the hepatic duct bifurcation), or pancreatic carcinoma.

It is very difficult to diagnose primary lymphoma of the extrahepatic bile ducts on the basis of CT scan, magnetic resonance imaging, and cholangiography results. However, Yoon et al7 suggested that despite the paucity of published cases, radiologists should raise the possibility of primary biliary tree lymphoma when cholangiography shows smooth, mild luminal narrowing of the extrahepatic ducts without mucosal irregularities, in spite of the diffuse thickening of the ductal wall on CT/magnetic resonance images.

It is crucial to differentiate primary NHL of the bile ducts from other causes of obstructive jaundice, as the treatment approach and prognosis are fundamentally different. There have been recent reports of success with endoscopic ultrasound-guided fine-needle aspiration biopsy (EUS-FNAB) in reaching a definitive tissue diagnosis, thus avoiding the surgical interventions that were performed in almost all of the reported cases for lymphomas mistakenly thought to be chemotherapy- or radiotherapy-resistant malignancies.8

In our case, the patients clinical presentation, high level of carbohydrate antigen 19-9, a mid-common bile duct stricture on ERCP, brush cytology suspicious for malignant cells, and a dilated common bile duct on CT scan were consistent with cholangiocarcinoma of the bile duct. It was only upon surgical resection of the tumor and histopathologic as well as immunohistochemical examination of the specimens that a definitive diagnosis of high-grade B cell-type NHL of the common bile duct was made.

DLBCL is an aggressive form of lymphoma, and its primary extranodal involvement of the common bile duct is an extremely rare disease. There is therefore unfortunately no consensus on the best treatment modality to be used. Joo et al9 and Dote et al10 suggest that surgery is important for establishing the diagnosis and removing the lymphoma, and that subsequent chemotherapy and/or radiotherapy after the initial surgery might be effective.

Our case revealed that surgical resection of the tumor for definitive tissue diagnosis followed by a combination of chemotherapy using six cycles of CVP-R, maintain the patient in a complete remission for more than 5 years. However, further follow-up and more studies are required to further elucidate the most appropriate treatment modality.

In conclusion, although primary NHL of the biliary ducts is an extremely rare disease, it should be considered in the differential diagnosis of malignant obstructive jaundice. A tissue biopsy by either EUS-FNAB or surgical intervention showing a characteristic histopathologic and immunohistochemical findings is the gold standard for definitive diagnosis. The best treatment modality is still to be identified, although surgical resection of the tumor followed by chemotherapy and/or radiotherapy is considered an effective option.

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