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Latest revision as of 11:24, 26 May 2017

Summary

We report a case of pseudolymphoma of the liver in a 49-year-old woman without an underlying disease except for liver hemangioma. A 20-mm nodule was incidentally found in segment 2 of the liver by abdominal ultrasonography during a regular follow-up of the hepatic hemangioma. After a series of radiological examinations, a left lateral sectionectomy was performed because malignant hepatic tumor could not be excluded. The patient was discharged uneventfully 7 days after the operation. The pathology examination revealed a pseudolymphoma. No recurrence of the tumor was found 5½ years after the operation. To the best of our knowledge, only 46 cases of pseudolymphoma of the liver have been reported to date. A review of the literature showed that pseudolymphomas occur predominantly in females (89.4%), usually occur as a single tumor (80.4%), are no more than 20 mm in size (90.6%), and are frequently associated with either autoimmune disease or chronic liver disease. Because an accurate diagnosis is difficult to establish, vigilant follow-up is indicated, and surgical intervention is the choice of treatment once the suspiciousness of malignancy has been raised.

Keywords

computed tomography;liver;magnetic resonance imaging;pseudolymphoma;reactive lymphoid hyperplasia

1. Introduction

Pseudolymphoma (also referred to as reactive lymphoid hyperplasia or nodular lymphoid lesion) of the liver is a rare benign nonspecific lesion characterized by a marked proliferation of polyclonal lymphocytes forming follicles with an active germinal center.1 Even though the etiology and pathogenesis of pseudolymphomas are unknown, their association with chronic infection or inflammatory process suggests their correlation with immunological response.2 In addition, their association with malignancy has been reported. The preoperative diagnosis for pseudolymphoma is difficult because noninvasive radiologic imaging findings are usually equivocal. We describe a case of pseudolymphoma and review the literature to reveal the clinicopathological characteristics of this particular disease entity.

2. Case report

A 49-year-old woman who had a hepatic hemangioma noted since 1995 underwent an annual routine medical examination. The abdominal ultrasonography showed a hypoechoic lesion, about 20 × 16 × 14 mm in size, located in segment 2 of the liver in 2007. Laboratory tests revealed no elevation of hepatic enzymes (aspartate aminotransferase, 17 IU/L; alanine aminotransferase, 13 IU/L; alkaline phosphatase, 141 IU/L; gamma-glutamyltranspeptidase, 22 IU/L) and a normal lactate dehydrogenase level. Hepatitis B virus surface antigen and hepatitis C virus antibody were both negative. In addition, the levels of tumor markers including α-fetoprotein, carcinoembryonic antigen, and carbohydrate antigen 19-9 were all within the normal limits. The corresponding computed tomography (CT) scans revealed a relatively hypodense solid lesion with peripheral rim enhancement in arterial and portal venous phases (Fig. 1A and B). Magnetic resonance (MR) imaging showed hypointensity in axial T1-weighted images (Fig. 1C) and hyperintensity in axial T2-weighted images (Fig. 1D). Postgadolinium enhancement corresponded with the CT images. CT arterial portography demonstrated a perfusion defect in segment 2 of the liver. However, this small segment 2 tumor had no definite tumor stain on angiography study. A hypovascular tumor was impressed, and peripheral type cholangiocarcinoma, metastatic tumor, or sclerosed hemangioma should be differentiated. A left lateral sectionectomy was performed in March 2007. The patient had an uneventful postoperative course and was discharged on the 7th postoperative day.


Image findings of the lesion. (A) Abdominal computed tomography (CT) scans ...


Figure 1.

Image findings of the lesion. (A) Abdominal computed tomography (CT) scans showed a 20-mm-diameter, slightly hypodense mass with peripheral rim enhancement in arterial phase located in segment 2. (B) Early washout of the contrast medium with retained ring enhancement was seen in the portal phase. (C) Axial magnetic resonance (MR) imaging showed a hypointense nodule on segment 2 of the liver in the T1-weighted image, and (D) the lesion became hyperintense in the T2-weighted image. (E) Arterial portography with computed tomography demonstrated a perfusion defect in segment 2 of the liver. Angiography showed a hypervascular lesion on segment 6 of the liver (arrow). (F) However, the small tumor in segment 2 of the liver on previous CT and MR had no definite tumor stain.

Grossly, the lesion was a well-defined, nonencapsulated, yellowish-white, and firm mass measuring 20 × 15 × 15 mm, just beneath the capsule of the liver (Fig. 2) with a satellite lesion about 3 mm in size near the previous lesion. Hematoxylin–eosin-stained histological images showed that the tumor was composed of lymphoid hyperplasia with several enlarged, irregularly shaped, well-demarcated follicles with formation of germinal centers. The lymphocytes containing round nuclei with scant cytoplasm were mainly small in size and mature in appearance with scattered medium and large cells (Fig. 3A). Tangible body macrophages were discernible. Immunohistochemical stain revealed that the follicles were composed of CD20 (+), Bcl-2 (–) B cells (Fig. 3B and C), and the interfollicular area was composed of CD3 (+) small T cells (Fig. 3D). Reactive CD30 (+) immunoblasts were evenly distributed in the interfollicular region (Fig. 3E). The EBER (Epstein–Barr virus-encoded RNA) stain was negative (Fig. 3F). The whole picture favored a diagnosis of pseudolymphoma. In addition, the satellite nodule showed similar pictures. The patient received regular follow-up, and no recurrence was found during 5½ years of follow-up.


Pathological findings of the lesion. Gross pathologic specimen revealed a ...


Figure 2.

Pathological findings of the lesion. Gross pathologic specimen revealed a well-defined, nonencapsulated, yellowish-white, and soft hepatic tumor, located just beneath the capsule in segment 2 of the liver.


Histopathology of hepatic pseudolymphoma. Hematoxylin–eosin-stained histological ...


Figure 3.

Histopathology of hepatic pseudolymphoma. Hematoxylin–eosin-stained histological images showed that the mass was composed of hyperplastic lymphoid tissue with several enlarged, irregularly shaped, well-demarcated follicles with formation of germinal centers distributed evenly in the mass. (A) The lymphocytes containing round nuclei with scant cytoplasm are mainly small in size and mature in appearance with scattered medium and large cells, ×40. Immunohistochemical stain showed that the germinal centers were composed of B lymphocytes (B) positive to CD20 antibody, ×100, (C) but negative to Bcl-2 (–) antibody, ×100. (D) The interfollicular area was composed of small T lymphocytes positive to CD3 antibody, ×100. (E) Reactive immunoblasts positive to CD30 antibody were evenly distributed in the interfollicular region, ×100. (F) However, the Epstein–Barr virus-encoded RNA stain was negative, ×40.

3. Discussion

Pseudolymphoma was first described in the lung by Saltzstein in 19633 as a lymphocytic tumor associated with inflammation and with no evidence of systemic dissemination. Pseudolymphoma of the liver was first reported by Snover et al4 in 1981. This lymphoproliferative condition is also referred to as reactive lymphoid hyperplasia or nodular lymphoid lesion. Pseudolymphomas can be found in the gastrointestinal tract,5 orbit,6 and pancreas,7 but rarely in the liver. Based on a review of the PubMed database from 1981 to 2012 using the keywords “pseudolymphoma” and “lymphoid hyperplasia of the liver”, we found 64 lesions in 46 cases of pseudolymphoma (Table 1),1; 2; 4; 8; 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; 35; 36; 37; 38; 39; 40 ;  41 and most of the reports (37 reports, 80.4%) dealt with a single tumor. Interestingly, most of the cases (69.6%) were reported in Japan. However, whether this is attributable to racial/ethnic differences or lifestyle factors such as sashimi intake was not clear. When our case was included, the average age of the patients was 56.7 years (range = 15–85, median = 58) with female predominance (F/M = 42:5, 89.3%). The average size of the tumor was 15.1 ± 10.6 mm (range, 1–60), and most of the tumors (90.6%) were no more than 20 mm. Some of the patients presented with extrahepatic autoimmune disease [Sjögrens syndrome in 1 case; autoimmune thyroiditis in 3 cases; Takayashu aortitis with antiphospholipid syndrome in 1 case; calcinosis, Raynauds phenomenon, esophageal dysmotility, sclerodactyly, telangiectasia (CREST) syndrome in 1 case—representing a total of 12.8%]. Therefore, a relationship between pseudolymphoma of the liver and immunologic dysregulation was suggested.40 Many of the patients were found to have chronic liver disease (primary biliary cirrhosis in 6 cases, viral hepatitis in 5 cases, nonalcoholic steatohepatitis in 2 cases, representing a total of 35.1%). Pseudolymphomas have been reported to develop after interferon treatment for chronic hepatitis.26 These findings support the inflammatory nature of the lesion. More importantly, many of the patients had an accompanying malignancy [colon cancer in 4 cases, gastric cancer in 3 cases, triplicate carcinomas (gastric, cecal, and colon cancer) in 1 case, renal cell carcinoma in 3 cases, ovarian cancer in 1 case, and pancreatic cancer in 1 case, representing a total of 27.7%]. Therefore, immunoreaction again carcinoma cells might relate to the development of pseudolymphoma.32 Other associated diseases include diabetes mellitus, hypertension, and diverticulitis. Interestingly, decreasing size in pseudolymphoma had been reported.23 ;  40 This phenomenon might reflect the benign behavior of this particular tumor. To date, the pathophysiology of pseudolymphoma has not been understood.

Table 1. Reported cases in the literature (including our case).
Case Author(s) Age Sex Tumor number Tumor size (mm) Preoperative diagnosis Treatment Associated disease
1 Snover et al4 15 F 1 N/A Cirrhosis N/A Primary immunodeficiency
2 Tanabe et al9 30 F 1 15 Unknown Resection Acute enteritis
3 Jiménez et al10 34 F 1 27 Not reported Resection Nil
4 Willenbrock et al11 36 F 1 18 N/A N/A Focal nodular hyperplasia of the liver, hemangioma
5 Endou et al8 38 F 1 18 N/A N/A Pancytopenia
6 Zen et al40 40 M 1 20 N/A Resection Chronic hepatitis B
7 Ohtsu et al12 42 F 3 14, 15, and smaller HCC Resection Hepatitis B
8 Lin13 44 F 1 15 Metastatic tumor Resection Colon cancer
9 Park et al14 46 F 1 10 Metastatic tumor Resection Renal cell carcinoma, Hepatitis B
10 Nagano et al15 47 F 1 17 HCC Resection Autoimmune thyroiditis
11 Fukuo et al34 47 F 2 5, 15 HCC or inflammatory pseudotumor Resection Primary biliary cirrhosis
12 Okubo et al16 49 F 1 20 Suspected HCC Resection Sjogrens syndrome
13 Mori et al17 49 F 1 18 N/A N/A Hepatitis B
14 Shiozawa et al18 51 F 1 20 N/A N/A Nil
15 Sharifi et al1 52 F 1 4 Primary biliary cirrhosis Transplantation Primary biliary cirrhosis
16 Machida et al21 53 F 3 10, 12 and 15 HCC Resection Autoimmune thyroiditis
17 Sharifi et al1 56 F 1 15 Primary biliary cirrhosis Transplantation Primary biliary cirrhosis CREST syndrome
18 Sharifi et al1 56 M 1 7 Not reported Resection Diverticulitis
19 Hayashi et al37 56 F 1 15 Metastatic tumor or HCC TAE, resection Nonalcoholic fatty liver disease
20 Fujinaga et al19 58 F 1 15 N/A N/A Hypertension
21 Nichijima et al20 58 F 1 12 N/A N/A Hypertension, diabetes mellitus
22 Yoshikawa et al41 58 F 1 8 Metastatic tumor Resection Gastric cancer
23 Domínguez-Pérez et al35 58 F 1 10 Malignancy, premalignancy Resection Primary biliary cirrhosis
24 Marchetti et al38 58 F 1 12 Metastatic tumor Resection Ovarian cancer
25 Isobe et al22 59 F 1 9 Malignant tumor Resection Diabetes mellitus
26 Domínguez-Pérez et al35 59 F 1 20 HCC Transplantation Advanced liver cirrhosis
27 Osame et al39 60 F Multiple 5, 5, 6, 6, 7, 8, 10, 10, 35, 60, and several tiny ones Metastatic tumor Resection Renal cell carcinoma
28 Yoshikawa et al41 61 F 1 NA Metastatic tumor Resection GIST
29 Yoshikawa et al41 62 F 1 4 Metastatic tumor Resection Pancreatic cancer
30 Ota et al23 63 F 1 16 Reactive lymphoid hyperplasia Observation Nil
31 Okada et al24 63 F 2 4, 13 HCC Resection Primary biliary cirrhosis, primary aldosteronism
32 Zen et al40 63 F 2 5, 9 Reactive lymphoid hyperplasia Resection Primary biliary cirrhosis Autoimmune thyroiditis Adrenocortical adenoma
33 Takahashi et al2 64 F 1 10 HCC Resection Colon cancer
34 Zen et al40 64 F 2 10, 35 N/A Biopsy Takayasu aortitis Antiphospholipid syndrome
35 Katayanagi et al25 ;  40 66 F 1 15 Suspected lymphoma Resection Diabetes mellitus Nonalcoholic steatohepatitis
36 Tanizawa et al26 67 F 1 20 HCC Resection Nil
37 Matsumoto et al27 67 F 1 12 Reactive lymphoid hyperplasia Ethanol injection Hypertension
38 Kobayashi et al36 68 F 1 10 Pseudotumor or metastatic tumor Resection Colon cancer
39 Pantanowitz et al28 69 F 1 17 Metastatic tumor Resection Renal cell carcinoma
40 Okuhama et al29 70 M 1 40 HCC Resection Nil
41 Maehara et al30 72 F 1 15 MALT lymphoma Resection Nil
42 Kim et al31 72 M 1 17 HCC Resection Gastric cancer, hepatitis C
43 Sato et al32 75 F 2 14, 20 Metastatic tumor Resection Gastric cancer, cecal cancer, colon cancer
44 Takahashi et al2 77 F 1 15 Metastatic tumor Resection Colon cancer
45 Zen et al40 81 M 1 55 N/A Biopsy Cholecystolithiasis
46 Grouls33 85 F 2 8, 14 N/A Autopsy Gastric cancer
47 Our case 49 F 2 20, 3 Malignant tumor Resection Hepatic hemangioma

CREST = calcinosis, Raynauds phenomenon, esophageal dysmotility, sclerodactyly, telangiectasia; GIST = gastrointestinal stromal tumor; HCC = hepatocellular carcinoma; MALT = mucosa associated lymphoid tissue; N/A = not available; TAE = transarterial embolization.

Based on previously reported cases, in terms of preoperative imaging findings, most of the lesions are depicted as hypoechoic lesions on ultrasound with or without well-defined margins27 and having a low density on plain CT but variable density in contrast CT.2 ;  41 MR imaging showed nonspecific signal intensity and angiography did not show tumor stain.41 In our patient, there were no risk factors for hepatocellular carcinoma, and the liver was not cirrhotic and the α-fetoprotein level was normal. The corresponding CT and MR images showed a solitary tumor in segment 2 of the liver with peripheral enhancement. The metastatic tumor or cholangiocarcinoma should be suspected first. Common benign tumors such as hemangiomas or focal nodular hyperplasias were not likely. Because the malignancy could not be excluded, the preoperative biopsy was an essential tool to establish a final diagnosis.2 However, for fear of needle implantation of malignant tumor cells, the patient decided to receive a left lateral sectionectomy without a biopsy. Our study, consistent with literature reports, shows that it is difficult to preoperatively distinguish pseudolymphomas from malignant tumors and metastases on the basis of radiological findings.2 ;  41 In fact, accurate preoperative diagnosis proved difficult and was achieved in only three patients,23; 27 ;  40 whereas the most frequent diagnosis before operation was malignancy (80.0%) including hepatocellular carcinoma in 12 cases, metastatic tumor in 12 cases, and malignant tumor in four cases (3 of uncertain nature and 1 of lymphoma).

Histologically, pseudolymphomas consist of hyperplastic lymphoid follicles, lymphocytes, and other inflammatory cells, and an accurate diagnosis of pseudolymphoma relies on immunohistochemical analysis. Usually, immunohistochemical staining showed positive for CD3, CD4, CD8 (T markers), and CD20 and CD79a (B cell markers), which indicated the polyclonality of the tumor. However, staining for Bcl-2, IgG4, ALK, and SMA was negative.41 Furthermore, CD3-positive cells were mainly localized in the parafollicular area and CD20 immunostaining was positive for B follicles, whereas Bcl-2 staining was negative, indicating the pseudolymphomas reactive and nonneoplastic nature.38 In accordance with these findings, in our case, the immunohistochemical stain showed that the follicles were composed of CD20 (+), Bcl-2 (–) B cells, and the interfollicular area was composed of CD3 (+) small T cells. Moreover, reactive CD30 (+) immunoblasts were evenly distributed in the interfollicular region, and the EBER stain was negative.

Even though their precise etiology and pathogenesis remain unknown, pseudolymphomas have a much better prognosis than malignant lymphomas. Treatment methods for the 40 patients were recorded: resection in 32 cases (80.0%), liver transplantation in three cases, biopsy in two cases, ethanol injection in one case, autopsy in one case, and observation in one case. Ten of the 47 cases have multiple tumors (21.3%) and only one case had more than three tumors.39 Furthermore, our case was the second case associated with hepatic hemangioma,11 and the patient survived well 5½ years after the operation without tumor recurrence.

In conclusion, pseudolymphoma of the liver should be considered in the differential diagnosis of small hepatic tumors (≤ 20 mm), especially when a single hypovascular tumor is found in a female patient and the patient has no risk factors of hepatocellular carcinoma. Because it is difficult to preoperatively distinguish pseudolymphomas from malignant tumors and metastases on the basis of radiological findings, vigilant follow-up of patients is essential and surgical intervention is the choice of treatment once the suspiciousness of malignancy has been raised.

Acknowledgments

We thank Professor Kengo Yoshimitsu, Chairman of the Department of Radiology, and Dr Akinobu Osame, Faculty of Medicine, Fukuoka University, for providing unpublished data in their work. In addition, the authors thank Ms Eunice J. Yuan for secretarial assistance. Authors' contributions: conception and design of study, KLL, RHY; acquisition of data, CTY, RHY; analysis and/or interpretation of data, KLL, MCL, RHY; drafting the manuscript, CTY; revising the manuscript critically for important intellectual content, KLL, MCL, RHY; approval of the version of the manuscript to be published (the names of all authors must be listed), CTY, KLL, MCL, RHY.

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