Annals of Oncology Advance Access originally published online on October 27, 2006
Annals of Oncology 2007 18(2):346-350; doi:10.1093/annonc/mdl388
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2006 European Society for Medical Oncology
hematologic malignancies |
Prevalence of HCV infection in nongastric marginal zone B-cell lymphoma of MALT
1 Division of Hematology
2 Division of Infectious and Tropical Diseases
3 Department of Pathology, IRCCS Policlinico San Matteo, University of Pavia, Pavia
4 Division of Hematology, Ospedali Riuniti, Bergamo
5 Division of Hematology, Niguarda Ca' Granda Hospital, Milano
6 Division of Hematology, University La Sapienza, Roma
7 Azienda Ospedaliera S. Andrea, University La Sapienza, Roma
8 Division of Hematology, Azienda Ospedaliera S. Giovanni Battista, Torino
9 Division of Hematology, Policlinico S. Maria alle Scotte, University of Siena
10 Department of Hematology, S. Bortolo Hospital, Vicenza
11 Department of Hematology, Catholic University Medical School, Roma
12 Division of Hematology, University of Udine, Udine, Italy
* Correspondence to: Dr L. Arcaini, Division of Hematology, Fondazione IRCCS Policlinico San Matteo, University of Pavia, Viale Golgi 19, 27100 Pavia, Italy. Tel: +39-0382-503595; Fax: +39-0382-502250; E-mail: luca.arcaini{at}unipv.it
 |
Abstract |
|---|
 Top Abstract introductionpatients and methodsresultsdiscussionReferences |
|---|
Background: Hepatitis C virus (HCV) infection is frequently associated with B-cell non-Hodgkin's lymphomas. We investigated the prevalence of HCV infection in nongastric marginal zone lymphomas of mucosa-associated lymphoid tissue (MALT) in order to define the relationship between the viral infection and the presenting features, treatment, and outcome.
Methods: We retrospectively studied 172 patients with a histological diagnosis of marginal zone B-cell lymphoma of MALT, except for stomach, and with available HCV serology, among a series of 208 patients.
Results: HCV infection was documented in 60 patients (35%). Most HCV-positive patients (97%) showed a single MALT organ involvement. HCV-positive patients showed a more frequent involvement of skin (35%), salivary glands (25%), and orbit (15%). The majority of stage IV HCV-positive patients (71%) had a single MALT site with bone marrow involvement. The overall response rate was similar in HCV-positive (93%) and HCV-negative patients (87%). Overall survival (OS) and event-free survival (EFS) did not differ according to HCV infection. In multivariate analysis, advanced disease (stage III–IV) was associated with a poorer OS (P = 0.0001), irrespective of HCV serostatus.
Conclusions: This study shows that nongastric marginal zone lymphomas are characterized by a high prevalence of HCV infection. Patients with involvement of a single MALT site have the highest prevalence of HCV. HCV-positive nongastric lymphomas of MALT show an indolent course similar to HCV-negative patients and seem an ideal target for exploiting the antilymphoma activity of antiviral treatments.
Key words: hepatitis C virus, infectious agents, MALT lymphoma, marginal zone
|
introduction |
|---|
|
TopAbstractintroductionpatients and methodsresultsdiscussionReferences |
|---|
Extranodal marginal zone B-cell lymphomas of mucosa-associated lymphoid tissue (MALT) are low-grade lymphomas and represent 8% of all non-Hodgkin's lymphomas (NHL) [1–3]. MALT lymphomas present frequently as indolent diseases, in middle and advanced age, with a female predominance [4–7]. In gastric MALT lymphoma, the Helicobacter pylori-related pathogenesis [8] and the efficacy of the antibiotic eradication are well known [9]. Other infectious agents are involved in the pathogenesis of specific MALT lymphomas: [10] Campylobacter jejuni for immunoproliferative small intestine disease [11], Borrelia burgdorferi for MALT lymphoma of the skin [12], and Chlamydia psittaci for MALT lymphoma of the orbit [13, 14]. MALT lymphomas may arise in a background of autoimmune disorders such as Hashimoto's thyroiditis for thyroid MALT lymphoma and Sjögren's syndrome for salivary glands MALT lymphoma [15].
Hepatitis C virus (HCV) prevalence in patients with B-cell NHL is 
15%, with geographical variability, higher than in general population (1.5%) and in other hematologic malignancies (2.9%), suggesting a role of HCV in the etiology of B-cell NHL [16, 17]. HCV infection is frequently associated with marginal zone lymphoid neoplasms [18, 19] and these HCV-associated tumors may respond to antiviral therapy [20–22]. The pathogenetic role of HCV and the features of HCV infection in MALT lymphomas are not well established. In the IELSG series of nongastric MALT lymphomas (180 patients) [5], HCV serostatus was available in <50% of patients, while in the Lyon series (165 patients) data on HCV were not available [6]. In a recent Italian case–control study on HCV in B-cell NHL [23], among 25 MALT lymphomas only three were HCV positive. In a similar American case–control study [24], among 49 patients there were only two HCV-positive MALT lymphomas. On the contrary, a high prevalence (8/16, 50%) of HCV infection was reported in a small series of Italian patients affected by gastric and nongastric MALT lymphoma [25] and a French cross-sectional study found a high prevalence of HCV in MALT lymphoma patients (three HCV-positive patients with gastric MALT lymphomas among 17 patients with MALT lymphoma) [26].
We studied the prevalence of HCV infection in 172 patients with nongastric marginal zone lymphomas of MALT in order to define the relationship between the viral infection and the presenting features, treatment, and outcome.
|
patients and methods |
|---|
|
TopAbstractintroductionpatients and methodsresultsdiscussionReferences |
|---|
patients
We studied 208 cases of nongastric marginal zone B-cell lymphoma of MALT, diagnosed and treated from 1991 to 2004 (44 within 1995, 73 from 1996 to 2000, and 91 from 2001 to 2004), whose clinical and pathological data had been collected from lymphoma databases by the participating centers. Among this series, we retrospectively analyzed 172 patients for whom HCV serology was available. Among 36 patients lacking HCV serology, 13 (30%) were diagnosed within 1995, 13 (18%) from 1996 to 2000, and 10 (11%) from 2001 to 2004. In order to be included in the analysis, patients were required to have a confirmed histological diagnosis of MALT lymphoma, according to the World Health Organization/Revised European-American Lymphoma classification [27] and a complete staging including bone marrow examination. Patients had to present with their main disease manifestation in a nongastric extranodal site. We considered a site of disease as clinically dominant if relevant for the circumstances of the diagnosis (symptoms, signs, and radiological findings) and for the choice and target of the primary treatment [5]. We defined nodal involvement as locoregional and not locoregional (distant/diffuse). We divided patients, according to Ann Arbor stage, into two groups: localized disease (stage I–II) and advanced or disseminated disease (stage III–IV). The International Prognostic Index (IPI) was calculated according to the published criteria [28] and patients were classified into two groups: low/low-intermediate and high/high-intermediate. The study was conducted in accordance with institutional guidelines established for retrospective studies.
HCV infection
In all 172 patients, the presence of HCV antibodies was detected using an enzyme-linked immunosorbant assay, confirmed by a third-generation recombinant immunoblot assay. Reverse transcription-PCR was carried out in 34 cases (qualitative HCV-RNA); for 10 patients line probe assay genotyping was carried out.
statistical analysis
Numeric variables are summarized by their median and range. Categorical variables are described by counts and relative frequencies. Associations were tested via Fisher's exact test (for 2 x 2 tables) or using the 
2 approximation for larger tables. The Kaplan–Meier product-limit method was used to compute survival curves, and the log-rank test was adopted to carry out comparisons between different groups of patients.
Overall survival (OS) was calculated as the time between the date of diagnosis and the date of death or last follow-up for censored cases and event-free survival (EFS) as the time from the date of first line of therapy until date of event (treatment after an initial watch-and-wait policy, relapse or progression of disease, and death from any cause). Cox proportional hazards model was applied to carry out multivariate survival analysis.
|
results |
|---|
|
TopAbstractintroductionpatients and methodsresultsdiscussionReferences |
|---|
Most patients were older than 60 years (64%) and there was a female predominance (61%). The majority of patients (91%) showed a single MALT site involvement: skin in 49 (28%), salivary glands in 32 (19%), orbit in 25 (15%), Waldeyer's ring in 22 (13%), lung in 13 (8%), bowel in six (3%), breast in six (3%), and liver in three (2%). Ninety-four patients (55%) had localized disease (stage I–II) while 78 patients (45%) had advanced disease (stage III–IV). Bone marrow was involved in 54 patients (31%); 71 patients (41%) had nodal disease; and 18 patients (10%) showed mild splenomegaly. Fifty-nine patients had positive HCV serology: 23 were tested for HCV-RNA and 21 had viremia. Of the 113 serologically negative patients, 10 were tested for HCV-RNA and one showed viremia. Therefore, HCV infection was documented in 60 patients (35%). A total of 22 patients had viremia (22 of 24, 92%) and 12 of them had also a quantitative determination (>1 000 000 UI/ml in eight patients). In 12 patients, HCV genotype was studied: 2a/2c in 10 patients, 1a in one case, and 1b in one case. In five patients, liver biopsy was carried out, showing mild chronic hepatitis in two patients, moderate chronic hepatitis in two patients, and cirrhosis in one. Surface antigen of hepatitis B virus was positive in 11 of 155 tested patients (7%), two co-infected with HCV.
Prevalence of HCV was 47% in salivary glands, 43% in skin, and 36% in orbit lymphoma. In patients with multiple MALT sites, the HCV prevalence was 13%. Table 1 describes the primary MALT localizations according to HCV infection.
|
In the group of HCV-positive patients, 58 patients (97%) showed a single MALT organ involvement: skin in 21 (35%), salivary glands in 15 (25%), and orbit in 9 (15%). Among HCV-positive patients, 32 patients (53%) had localized disease, while 28 (47%) had advanced disease. Bone marrow involvement was present in 22 patients (37%) (in 10 patients <10%), 25 (42%) had nodal disease (13 locoregional), and a mild splenomegaly was present in 10 (17%). Among HCV-negative patients, 99 (88%) showed a single MALT organ involvement: skin in 28 (25%), salivary glands in 17 (15%), and orbit in 16 (14%). Sixty-two patients (55%) had localized disease, while 50 (45%) had advanced disease. Bone marrow involvement was present in 32 patients (29%), 46 (41%) had nodal disease (24 locoregional), and eight presented a mild splenomegaly (7%). Table 2 summarizes the clinical characteristics of HCV-positive and HCV-negative patients.
|
The clinical features associated to HCV positivity were as follows: female sex (P = 0.004), age >60 years (P = 0.007), mild splenomegaly (P = 0.04), and absence of leukemic disease (P = 0.01). In all, 87% of patients with Waldeyer's ring involvement were HCV negative (P = 0.01). The distribution of IPI categories was statistically different between HCV-positive and HCV-negative patients, in effect 73% HCV-negative patients ranked in low and low-intermediate IPI risk group while 51% HCV-positive patients ranked in intermediate-high and high IPI risk group (P = 0.01). Stage IV HCV-positive patients had a different pattern of dissemination compared with HCV-negative patients (P = 0.03): the majority of stage IV HCV-positive patients (72%) had a single MALT site with bone marrow involvement, while only HCV-negative patients had multiple MALT sites involvement.
treatment and response
HCV infection did not condition the need for treatment: 89% of HCV-positive patients and 86% of HCV-negative patients underwent a first-line therapy. Fifty-nine percentage of HCV-positive and 53% of HCV-negative patients were treated with chemotherapy [P = ns (not significant)], 29% HCV-positive and 20% HCV-negative patients underwent radiotherapy (P = ns), while 12% HCV-positive and 27% HCV-negative patients received surgery (P = 0.04). Use of alkylators was similar between HCV-positive and HCV-negative patients (30% versus 29%, respectively); also, anthracyclines were similarly employed (33% versus 26%, respectively). The median time to treatment of patients initially followed with a watch-and-wait policy was 12 months, 9 months for HCV-negative, and 17 months for HCV-positive patients. The overall response rate (ORR) was similar in the two groups, counting for 70% complete remission (CR) and 23% partial remission (PR) (ORR 93%) in HCV-positive and 71% CR and 16% PR (ORR 87%) in HCV-negative patients. In HCV-positive group, the ORR was not conditioned by the type of treatment (P = ns): 91% of patients treated with chemotherapy, 92% of patients treated with radiotherapy, and 100% of patients treated with surgery obtained a CR or a PR. Also, in the HCV-negative group the ORR was not statistically different for each type of treatment (P = ns): 80% of patients treated with chemotherapy, 93% of patients treated with radiotherapy, and 96% of patients treated with surgery achieved a response.
outcome
OS and EFS did not differ according to HCV infection (Figures 1 and 2). Among HCV-positive patients, OS was not statistically different for IPI groups (low and low-intermediate versus high-intermediate and high risk) (P = ns); on the contrary, in the HCV-negative group, patients with low and low-intermediate IPI group had a better OS: 5-year OS was 94% [95% confidence interval (CI) 85–100] for HCV-negative patients belonging to low and low-intermediate risk groups and was 69% (95% CI 40–98) for those belonging to high-intermediate and high-risk groups (P = 0.004). The EFS was similar in HCV-positive and HCV-negative patients between low/low-intermediate and high/high-intermediate IPI groups. In the HCV-positive group, the type of the first-line treatment (chemotherapy, surgery, and radiotherapy) did not modify neither the OS nor the EFS, while it was related to a different 5-year EFS in HCV-negative patients: 60% (95% CI 32% to 88%) for radiotherapy, 33% (95% CI 7% to 59%) for surgery, and 29% (95% CI 11% to 46%) for chemotherapy (P = 0.02). The usage of anthracyclines did not modify either the OS or the EFS in both patients' groups.
|
|
In multivariate analysis, advanced disease (stage III–IV) was associated with a poorer OS (P = 0.0001) while HCV infection and the need for treatment were devoid of significance; therefore, the outcome in patients with like disease (similar localization and similar stage) and treated similarly was not influenced by HCV infection.
|
discussion |
|---|
|
TopAbstractintroductionpatients and methodsresultsdiscussionReferences |
|---|
The association between HCV infection and B-cell NHL has been demonstrated, especially in highly endemic geographical areas such as Italy, Japan, and southern parts of the United States; overall, the odds ratio of B-cell NHL for HCV infection ranges from 2 to 4 [29]. An Italian case–control study reported an odds ratio of 3.1 with a positive association for both indolent and aggressive B-cell NHL [23].
Lymphoplasmocytic, diffuse large-B-cell, and marginal zone lymphomas are the histotypes most frequently associated with HCV. In a recent study on 156 HCV-positive patients with diffuse large-B-cell lymphoma (DLBCL) from northern Italy, the prevalence of HCV positivity among patients with DLBCL was 16% [30]. Regarding lymphomas of marginal zone origin, it has been shown that splenic marginal zone B-cell lymphoma has a high prevalence of HCV infection [18], often in association with type II cryoglobulinemia [19]. In a recent Italian multicenter study on 309 patients with splenic marginal zone lymphoma, serologic testing for HCV was carried out in 255 patients (83%) and resulted positive in 49 patients (19%) [31]. Recently, a cross-sectional study conducted in Lyon suggested an association between HCV and gastric MALT lymphoma [26]. Studies specifically addressing the issue of HCV infection in nongastric marginal zone lymphomas of MALT are lacking, in particular, no case–control study has been conducted so far, given the rarity of these neoplasms, so that the few data available are obtained only from retrospective series. In the IELSG series of nongastric MALT lymphomas [5], HCV serostatus was available for 42% and it was positive in 24%, while in the Lyon series data on HCV were not reported [6].
In the present series, HCV infection was documented in 35%. Although our cases are prevalent and not analyzed in a case–control study, this finding appears to be of biological and clinical relevance because it sheds new light on the association between HCV infection and a specific type of B-cell NHL. Anyway, due to the retrospective nature of our study, data should be interpreted cautiously, also considering the well-known high seroprevalence of HCV infection in our country. In fact, Italy is a hyper-endemic area where the prevalence of HCV is estimated at about 4% and increases with age, following a North–South gradient [32]. Nonetheless, 88% of patients belonging to our series come from Hematology Units from northern Italy, which has a relatively low HCV seroprevalence (1.6%) [32].
This study also shows that, among nongastric marginal zone lymphomas, those with HCV infection are characterized by a preferential involvement of a single MALT site, and in particular the percentage of HCV-positive patients seems to be particularly high in lymphomas of salivary glands (47%), skin (43%), and orbit (36%). These data, while underlying the link between HCV infection and salivary glands lymphoma [5, 15], reveal a possible relationship between HCV and two other MALT presentations of lymphoma: orbit and skin. A small series of orbit lymphomas with prevalent lymphoplasmocytic histology and cryoglobulinemia was reported in 1985, but HCV infection was unknown at that time [33]. Recently, Ferreri et al. [34] found HCV seropositivity in 13% of ocular adnexa lymphoma of MALT-type with a more aggressive behavior. On the basis of these data, some well-defined forms with a single and peculiar MALT localization seem the typical presentation of HCV-related MALT lymphomas.
The findings of this study carry some clinical and therapeutic implications: in HCV-related MALT lymphoma, the role of the antiviral treatment (after or instead of antilymphoma treatment), aimed to eradicate the underlying viral trigger, is an attractive therapeutical option. The report of four cases of extranodal MALT lymphomas receiving antiviral treatment with three of them obtaining a response of lymphoma favors this therapeutic option [21, 22]. The possibility of exploiting the antilymphoma activity of the antiviral treatment in HCV-positive nongastric marginal zone B-cell lymphoma of MALT should be investigated in a prospective study.
In conclusion, this study illustrates that nongastric MALT lymphomas are characterized by a high prevalence of HCV infection. Patients with involvement of a single MALT site, especially orbit, skin, and salivary glands, have the highest prevalence of HCV infection. HCV-related nongastric lymphomas of MALT show an indolent behavior, overlapping with HCV-negative cases, and seem the ideal target for exploiting the antilymphoma activity of the antiviral treatment.
Received for publication April 23, 2006. Revision received September 12, 2006. Accepted for publication September 13, 2006.
|
References |
|---|
|
TopAbstractintroductionpatients and methodsresultsdiscussionReferences |
|---|
1. The Non-Hodgkin's Lymphoma Classification Project. (1997) A clinical evaluation of the International Lymphoma Study Group. Classification of non-Hodgkin's lymphoma. Blood 89:3909–3918.
2. Cavalli F, Isaacson PG, Gascoyne RD, Zucca E. (2001) MALT lymphomas. Hematology (Am Soc Hematol Educ Program) 241:258.
3. Thieblemont C. (2005) Clinical presentation and management of marginal zone lymphomas. Hematology (Am Soc Hematol Educ Program) 307–313.
4. Thieblemont C, Berger F, Dumontet C, et al. (2000) Mucosa-associated lymphoid tissue lymphoma is a disseminated disease in one third of 158 patients analyzed. Blood 95:802–806.
5. Zucca E, Conconi A, Pedrinis E, et al. (2003) Non-gastric marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue. Blood 101:2489–2495.
6. Thieblemont C, de la Fouchardiere A, Coiffier B. (2003) Non-gastric mucosa-associated lymphoid tissue lymphomas. Clin Lymphoma 3:212–224.[Web of Science][Medline]
7. Zinzani PL, Magagnoli M, Galieni P, et al. (1999) Nongastrointestinal low-grade mucosa-associated lymphoid tissue lymphoma: analysis of 75 patients. J Clin Oncol 17:1254–1258.
8. Farinha P and Gascoyne RD. (2005) Helicobacter pylori and MALT lymphoma. Gastroenterology 128:1579–1605.[CrossRef][Web of Science][Medline]
9. Zucca E, Bretoni F, Roggero E, Cavalli F. (2000) The gastric marginal zone B-cell lymphoma of MALT type. Blood 96:410–419.
10. Suarez F, Lortholary O, Hermine O, Lecuit M. (2006) Infection-associated lymphomas derived from marginal-zone B-cells: a model of antigen-driven lymphoproliferations. Blood 107:3034–3044.
11. Lecuit M, Abachin E, Martin A, et al. (2004) Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med 350:239–248.
12. Roggero E, Zucca E, Mainetti C, et al. (2000) Eradication of Borrelia burgdorferi infection in primary marginal zone B-cell lymphoma of the skin. Hum Pathol 31:263–268.[CrossRef][Web of Science][Medline]
13. Ferreri AJ, Guidoboni M, Ponzoni M, et al. (2004) Evidence for an association between Chlamydia psittaci and ocular adnexal lymphomas. J Natl Cancer Inst 96:586–594.
14. Ferreri AJ, Ponzoni M, Guidoboni M, et al. (2005) Regression of ocular adnexal lymphoma after Chlamydia psittaci-eradicating antibiotic therapy. J Clin Oncol 23:5067–5073.
15. Ambrosetti A, Zanotti R, Pattaro C, et al. (2004) Most cases of primary salivary mucosa-associated lymphoid tissue lymphoma are associated either with Sjoegren syndrome or hepatitis C virus infection. Br J Haematol 126:43–49.[CrossRef][Web of Science][Medline]
16. Gisbert JP, Garcia-Buey L, Pajares JM, et al. (2003) Prevalence of hepatitis C virus infection in B-cell non-Hodgkin's lymphoma: systematic review and meta-analysis. Gastroenterology 125:1723–1732.[CrossRef][Web of Science][Medline]
17. Gisbert JP, Garcia-Buey L, Arranz R, et al. (2004) The prevalence of hepatitis C virus infection in patients with non-Hodgkin's lymphoma. Eur J Gastroenterol Hepatol 16:135–138.[CrossRef][Web of Science][Medline]
18. Arcaini L, Paulli M, Boveri E, et al. (2004) Splenic and nodal marginal zone lymphomas are indolent disorders at high hepatitis C virus seroprevalence with distinct presenting features but similar morphologic and phenotypic profiles. Cancer 100:107–115.[CrossRef][Web of Science][Medline]
19. Saadoun D, Suarez F, Lefrere F, et al. (2005) Splenic lymphoma with villous lymphocytes, associated with type II cryoglobulinemia and HCV infection: a new entity? Blood 105:74–76.[Medline]
20. Hermine O, Lefrere F, Bronowicki JP, et al. (2002) Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med 347:89–94.
21. Kelaidi C, Rollot F, Park S, et al. (2004) Response to antiviral treatment in hepatitis C virus-associated marginal zone lymphomas. Leukemia 18:1711–1716.[CrossRef][Web of Science][Medline]
22. Vallisa D, Bernuzzi P, Arcaini L, et al. (2005) Role of anti-hepatitis C virus (HCV) treatment in HCV-related, low-grade, B-cell, non-Hodgkin's lymphoma: a multicenter Italian experience. J Clin Oncol 23:468–473.
23. Mele A, Pulsoni A, Bianco E, et al. (2003) Hepatitis C virus and B-cell non-Hodgkin lymphomas: an Italian multicenter case-control study. Blood 102:996–999.
24. Engels EA, Chatterjee N, Cerhan JR, et al. (2004) Hepatitis C virus infection and non-Hodgkin lymphoma: results of the NCI-SEER multi-center case-control study. Int J Cancer 111:76–80.[CrossRef][Web of Science][Medline]
25. Luppi M, Longo G, Ferrari MG, et al. (1996) Additional neoplasms and HCV infection in low-grade lymphoma of MALT type. Br J Haematol 94:373–375.[CrossRef][Web of Science][Medline]
26. Seve P, Renaudier P, Sasco AJ, et al. (2004) Hepatitis C virus infection and B-cell non-Hodgkin's lymphoma: a cross-sectional study in Lyon, France. Eur J Gastroenterol Hepatol 16:1361–1365.[CrossRef][Web of Science][Medline]
27. Harris NL, Jaffe ES, Diebold J, et al. (2000) The World Health Organization classification of neoplasms of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting—Airlie House, Virginia, November, 1997. Hematol J 1:53–66.[Medline]
28. Shipp M, Harrington D, Anderson J. (1993) A predictive model for aggressive non-Hodgkin's lymphoma. The International Non-Hodgkin's Lymphoma Prognostic Factors Project. N Engl J Med 329:987–994.
29. Negri E, Little D, Boiocchi M, et al. (2004) B-cell non-Hodgkin's lymphoma and hepatitis C virus infection: a systematic review. Int J Cancer 111:1–8.[CrossRef][Web of Science][Medline]
30. Visco C, Arcaini L, Brusamolino E, et al. (2006) Distinctive natural history in hepatitis C virus positive diffuse large B-cell lymphoma: analysis of 156 patients from northern Italy. Ann Oncol 17:1434–1440.
31. Arcaini L, Lazzarino M, Colombo N, et al. (2006) Splenic marginal zone lymphoma: a prognostic model for clinical use. Blood 107:4643–4649.
32. Ansaldi F, Bruzzone B, Salmaso S, et al. (2005) Different seroprevalence and molecular epidemiology patterns of hepatitis C virus infection in Italy. J Med Virol 76:327–332.[CrossRef][Web of Science][Medline]
33. Lazzarino M, Morra E, Rosso R, et al. (1985) Clinicopathologic and immunologic characteristics of non-Hodgkin's lymphomas presenting in the orbit. A report of eight cases. Cancer 55:1907–1912.[CrossRef][Web of Science][Medline]
34. Ferreri AJ, Viale E, Guidoboni M, et al. (2006) Clinical implications of hepatitis C virus infection in MALT-type lymphoma of the ocular adnexa. Ann Oncol 17:769–772.
CiteULike 
Connotea 
Del.icio.us What's this?
Related articles in Ann Oncol:
- in this issue
Ann Oncol 2007 18: 209.[Extract] [Full Text]
This article has been cited by other articles:
|
|
 |
|
  M. Paulli, L. Arcaini, M. Lucioni, E. Boveri, D. Capello, F. Passamonti, M. Merli, S. Rattotti, D. Rossi, R. Riboni, et al. Subcutaneous 'lipoma-like' B-cell lymphoma associated with HCV infection: a new presentation of primary extranodal marginal zone B-cell lymphoma of MALT Ann. Onc., October 25, 2009; (2009) mdp454v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Kahl and D. Yang Marginal Zone Lymphomas: Management of Nodal, Splenic, and MALT NHL Hematology, January 1, 2008; 2008(1): 359 - 364. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||