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Lymphoma

MALT lymphoma in patients with autoimmune diseases: a comparative analysis of characteristics and clinical course

Abstract

MALT lymphoma, especially of extragastric origin, is thought to be associated with an underlying autoimmune disease (AD) in a significant proportion of patients. No systematic assessment of the clinical characteristics of MALT lymphoma arising in AD as opposed to patients without AD has been performed so far. Therefore, all patients diagnosed and treated for MALT lymphoma at our institution have prospectively undergone routine clinical and serological assessment for AD since 1997. In total, 158 patients were available for analysis, and 61 out of 158 patients (39%) were diagnosed with an underlying AD. Patients with AD were predominantly women and significantly younger at lymphoma diagnosis (56 versus 67 years, P=0.004), with a significantly higher rate of extragastric lymphomas (P=0.012). Furthermore, lymphomas in these patients showed a lower frequency of trisomy 3 (P=0.04) and a significantly lower response rate to Helicobacter pylori eradication therapy in the case of gastric lymphomas (P=0.03). All other parameters including estimated median time to relapse were comparable between both groups. Our data suggest that patients with AD develop MALT lymphoma significantly earlier in life. The clinical course, however, does not appear to be adversely influenced by the presence of AD, as neither rate of relapse nor times to relapse or survival are significantly different.

Introduction

Extranodal marginal zone B-cell lymphoma of the mucosa-associated lymphoid tissue (MALT lymphoma) is a distinct clinicopathological entity1, 2 comprising about 7% of all newly diagnosed non-Hodgkin's lymphomas.3 MALT lymphomas arise predominantly in lymphoid tissues acquired through chronic antigenic stimulation due to persistent inflammation/infection as illustrated by Helicobacter pylori (HP) in patients with gastric lymphoma.4, 5 Recently, it could be impressively demonstrated that this process can be reversed to a certain extent through removal of the causative stimulus, as exemplified by HP eradication therapy in early-stage gastric MALT lymphoma.5, 6 Molecular investigations have suggested that the MALT-lymphoma-specific t(11;18)(q21;q21), resulting in the API2/MALT1 fusion protein, is predictive of responsiveness to HP eradication, and thus marks the point of no return in the development of gastric MALT lymphoma.7, 8, 9, 10

While the majority of cases are diagnosed within the stomach, MALT lymphoma can be found throughout the body, and occurs in a multifocal fashion in a substantial proportion of patients.11 Beside HP, other infectious organisms, such as Campylobacter jejuni,12 Borellia burgdorferi13 or Chlamydia psittaci14 have also been implicated in the development of MALT lymphomas at various sites, suggesting that inflammation/infection might be the driving process in the development of MALT lymphoma, irrespective of the specific organism.

According to the literature, 30–40% of MALT lymphomas occur in an extragastric localization.15 As opposed to their gastric counterpart, these extra-gastric MALT lymphomas are thought to arise predominantly in patients with autoimmune diseases (AD). Especially the association of Sjogren's syndrome (SS) with MALT lymphoma of the salivary gland and of Hashimoto's thyroiditis (HT) with thyroid MALT lymphoma has been shown repeatedly.2 In general, these extragastric lymphomas seem to be independent of HP; therefore, HP eradication therapy is, despite various case reports,16, 17 regarded as an ineffective treatment strategy in such patients.18

As opposed to HP-associated gastric MALT lymphomas, the underlying stimulus for lymphoma development cannot be entirely removed in AD patients, as no causative therapy exists for AD. Thus, one could potentially expect an adverse effect of AD on the clinical course and the relapse rate in such patients. In addition, one might suspect that the complex immunologic interactions together with prolonged stimulation might lead to accumulation of pronounced genetic changes in MALT lymphomas arising in AD. These issues, however, have not been studied in detail, despite the high prevalence of AD in patients with MALT lymphomas.

In view of this, we have analysed patient characteristics, genetic aberrations and the clinical course of patients with MALT lymphoma diagnosed and treated at our institution with regard to the presence or absence of an underlying AD.

Patients and methods

Since the beginning of 1997, assessment of AD is being routinely performed in all patients diagnosed and treated for MALT lymphoma at our institution. We have evaluated the data from all patients administered between January 1997 and March 2006 with histologically verified MALT lymphoma1, 19 for the presence of AD.

Biopsy samples were evaluated according to the criteria established by Isaacson1 and adopted in the recent WHO classification for MALT lymphoma.20 All histologies were (re-) assessed by two reference hematopathologists at our institution (AC, LM). In all patients, immunologic phenotyping was done on paraffin sections for demonstration of light-chain restriction and for the phenotype CD20+CD5−CD10−cyclinD1−, which is consistent, in context with the microscopic appearance, with extranodal marginal zone B-cell lymphoma of MALT. All patients underwent extensive staging before initiation of therapy, consisting of ophthalmologic and otorhinolaryngologic examination, gastroscopy with multiple biopsies, endosonography of the upper GI tract, enteroclysis, colonoscopy, computed tomography of thorax and abdomen and bone marrow biopsy, as previously suggested.11 Staging was performed according to the Ann Arbor staging system as modified by Mushoff and Radaskiewicz.21, 22

Clinical information evaluated included age of the patient, first diagnosis, site and extent of the lymphoma, HP status, response to HP eradication therapy, occurrence of and time to relapse, presence of monoclonal immunoglobulins as assessed by serum electrophoresis, quantitative measurements of IgG, IgM and IgA and immunofixation, and survival. Routine assessment of AD included detailed patients' history, physical examination and the serological evaluation of rheumatoid factor, anti-nuclear antibodies, anti-RO antibodies and anti-LA antibodies, thyroid antibodies along with assessment of T3, T4 and thyroid ultrasound in case of parameters suggestive of HT. Only patients in whom these data were available (158 out of 219) were included in this analysis.

Paraffin-embedded biopsy samples were tested for MALT-lymphoma-specific genetic aberrations including t(11;18)(q21;q21), t(14;18)(q32;q21) involving IGH and MALT1, t(1;14)(p22;q32), t(3;14)(q14;q32) involving FOXP1 and IGH and trisomies 3 and 18. T(11;18)(q21;q21) involving API2 and MALT1 was assessed by reverse transcriptase–polymerase chain reaction, t(14;18)(q32;q21) involving IGH and MALT1, t(1;14)(p22;q32) involving BCL10 and IGH, t(3;14)(q14;q32) involving FOXP1 and IGH and trisomies 3 and 18 were investigated by fluorescence in situ hybridization, as previously published.23 These genetic studies were carried out on representative biopsies where a diagnosis of MALT lymphoma had been established by histopathology if enough material was available.

The statistical analyses were done with the SPSS 14.0 (SPSS Inc.) program. Binary outcome variables were tested for significant differences with the Fisher's exact test. A P-value below 0.05 was considered statistical significant. The survival analyses were done with the Kaplan–Meier method and the different curves were tested for significance with the log-rank test. Continuous non-parametric variables were compared with the Mann–Whitney U-test.

Results

In total, 158 patients with a median age of 63 years (inter-quartile-range (IQR), 50–74) and a median follow-up time of 47 (IQR, 25–72) months were evaluable for analysis (see Table 1). In these patients, sufficient clinical and serological assessment of AD had been performed. In total, 61 out of these 158 cases (39%) suffered from concurrent AD: SS (n=43; 71%), HT (n=8; 13%), rheumatoid arthritis (n=2; 3%), systemic lupus erythematosus (n=2; 3%) and miscellaneous (n=6; 10%). Among these patients with AD, 48 were women (79%) and 13 men (21%), as opposed to 43 women (44%) and 54 men (56%) without AD (P=0.001). In addition, 13 patients had variously elevated serologic autoimmune parameters without a clinical correlate. Patients with AD were diagnosed with MALT lymphoma at a significantly younger age, that is 56 years (IQR, 48–69) as opposed to 67 years (IQR, 54–76) in patients without AD (P=0.004).

Table 1 Results

The majority of patients (98/158, 62%) in our series had extragastric MALT lymphoma, with the rate of extragastric MALT lymphoma being significantly higher in patients with AD (46/61 versus 52/97; P=0.012). Among the 61 patients with AD, 16 suffered from gastric lymphoma, while 27 had lymphoma of the salivary glands, 11 of the ocular adnexa, 6 of the thyroid and one of the breasts. For detailed characteristics, see Table 2.

Table 2 Characteristics of patients with AD

The overall rate of multifocal disease was 42% (66/158) and was evenly (P=0.069) distributed between the two patient groups.

The histological feature of plasmacytic differentiation (PD) defined by the presence of sheets of light-chain-restricted plasma cells was found in 30% of the patients and was not different between both cohorts (P=0.336). Information on the presence of monoclonal gammopathy/paraprotein was available in 86 patients, with 36 of them showing monoclonal immunoglobulin production (42%), without a significant difference between patients with and without AD (P=0.19). As opposed to a previous series,24 no correlation between the presence of monoclonal gammopathy and PD was found in this cohort of patients (P=0.18).

Out of the 60 patients with gastric lymphoma, 49 (80%) were associated with HP infection. The incidence of HP infection was not significantly different between patients with (14/16 patients, 87%) or without AD (35/44, 80%; P=0.481). Relapse rate (P=0.312) and time to relapse (P=0.376) in patients with gastric lymphoma were also comparable between both groups. HP eradication therapy, however, was significantly less effective in the treatment of gastric MALT lymphoma in patients with AD (P=0.031), with only one out of 14 patients with AD (7%) responding to antibiotic therapy as opposed to 12 out of 31 (39%).

Genetic analyses could be carried out in a total of 99 patients in whom sufficient material was left and revealed the presence of trisomy 3 in 25% (25/99), trisomy 18 in 9% (9/99), t(11;18) in 26% (26/99), t(14;18) involving IGH/MALT1 in 10% (10/99), and t(3;14) in 2% (2/99) of the patients. T(1;14) was not detected in any of the patients (0/99). Trisomy 3 was inversely associated with the presence of AD (P=0.043), whereas there was no significant correlation with any other genetic aberration investigated (trisomy 18: P=0.703; t(11;18): P=0.077; t(14;18): P=548; t(3;14): P=not applicable, t(1;14): P=not applicable).

After a median follow-up time of 47 (IQR, 25–72) months, the overall relapse rate as well as the estimated median time to relapse was not significantly different (P=0.354) between both groups (Figure 1). In addition, a subgroup analysis revealed no influence of AD on relapse, both in gastric (P=0.471) and in extragastric MALT lymphoma (P=0.623). The latter, however, were at significantly higher risk of relapse as opposed to gastric MALT lymphomas (P=0.004) (Figure 2), which is in keeping with other series in the literature.25 On the other hand, no significant influence of genetic aberrations or the presence of a monoclonal gammopathy/paraprotein (P=0.99) on time to relapse was detected. There was, however, again a trend towards a longer time to relapse in patients with t(11;18)(q21;q21) in our patients (P=0.13).

Figure 1
figure1

Time to relapse and autoimmune disease.

Figure 2
figure2

Time to relapse and extra-gastric disease.

After the median follow-up period of 47 (IQR, 25–72) months, 75% of the patients are alive and the median survival time has not been reached (Figure 3).

Figure 3
figure3

Overall survival time.

Discussion

This is the first study to evaluate systematically the clinical characteristics, genetic abnormalities as well as the clinical course of MALT lymphoma in patients with AD as compared to patients without AD, staged and treated at our institution. Apart from a small series suggesting a lower response of gastric MALT lymphomas to HP eradication therapy in patients with AD,26 the issue of a potential influence of AD on the course of MALT lymphoma has not been studied in detail. The initial finding that AD is an adverse factor for response to HP eradication has suggested that HP might probably be a bystander phenomenon in the development of gastric MALT lymphoma in such patients. The potential influence of AD on the long-term outcome of patients with MALT lymphoma, however, has not been studied.

The observation that AD predisposes patients to the development of MALT lymphoma is indeed underscored by our finding that AD patients were significantly younger at diagnosis of MALT lymphoma than patients without AD (56 versus 67 years, P=0.004). Furthermore, our data clearly support the hypothesis that autoimmune conditions indeed cause MALT lymphoma since the proportion of AD was far higher than would be seen in the general population.27, 28 Not surprisingly, a female predominance of lymphoma patients with AD (79 versus 21%, P=0.001) was seen in our series, as has generally been suggested for autoimmune conditions. Also in keeping with previous observations is the finding that the majority of patients with AD suffered from extragastric MALT lymphoma, with lymphoma of the parotid and the ocular adnexa constituting the most common localization (Table 2). Interestingly, none of our patients with AD suffered from lymphoma of the lung, which is generally one of the most common localizations of MALT lymphoma, suggesting that the as yet undetected cause of MALT in the lung might be infectious rather than autoimmune.

Surprisingly, our data do not suggest a detrimental effect of underlying AD on the clinical course of MALT lymphoma. While the rate of extra-gastric MALT lymphoma was higher in AD-patients, and these lymphomas per se have a higher rate of relapse as compared to gastric MALT lymphomas,25 no significant influence of AD on relapse rate and estimated median time to relapse was found.

In our series, we have used the time to relapse as a surrogate marker for the clinical course due to the indolent nature of MALT lymphoma, which rarely results in lymphoma-associated deaths. Thus, overall survival would neither be feasible nor accurate in the description of the clinical course of MALT lymphoma. In fact, at a median follow-up time of 47 months (IQR: 25–72 months), median survival has not been reached in our patients, which is in keeping with other studies evaluating the clinical behaviour of MALT lymphoma (Figure 3).29, 30, 31 The absence of an adverse influence of AD on the clinical course in our series nevertheless is somewhat surprising. As opposed to infectious agents such as HP, which may potentially be eliminated using antibiotic treatment, there is no causative therapy for the AD encountered in our patients. Thus, one might hypothesize that the continuous persistence of the inflammatory drive initially leading to the development of MALT lymphoma should also accelerate relapses as compared to patients in whom this drive could be eliminated. Contrary to this rationale, however, our series suggests that this is apparently not the case, at least at a median follow-up of 47 months. In view of this, it appears reasonable to treat and follow patients with AD and MALT lymphoma in a similar way as patients without an AD.

In our series, the overall rate of HP infection in patients with gastric lymphoma was 80% and was similar irrespective of the presence or absence of AD (87 vs 80%; P=0.481). In addition, the clinical course of patients with gastric MALT lymphoma with AD appeared not to be different as reflected by a similar relapse rate (P=0.312) as well as time to relapse (P=0.376). There was, however, a significant difference in terms of response to HP eradication between the two groups, as only 1/14 patients with AD as opposed to 12/31 without AD showed response of the lymphoma after antibiotic therapy (P=0.031). As all our patients had undergone extensive staging according to our standard protocol,25 one can assume with reasonable certainty that all these patients indeed had primary gastric lymphoma and did not suffer from secondary spread to the stomach, which could explain non-response to HP eradication. In addition, the fact that HP-eradication is significantly less effective in patients with AD is consistent with previous findings from a small pilot study reported at our institution.26 This interesting finding could possibly be explained by the fact that gastric lymphoma development in AD patients is accelerated by the presence of two different stimuli. In addition, the refractoriness to HP-eradication in AD might suggest that HP is indeed a bystander phenomenon not related to lymphoma development in a substantial proportion of patients. The finding that the rate of t(11;18)(q21;q21) was not different between the two groups of patients (P=0.46) despite the diverging response rate is indeed suggestive of AD as an independent risk factor.

In general, patients without AD had a higher rate of trisomy 3, 34 versus 16% (P=0.0043) and a higher rate of t(11;18), 34 versus 18%, though the latter was not statistically significant (P=0.077). This is also somewhat surprising because one could hypothesize that the chronic inflammation with continuous DNA damages may trigger the lymphoma to develop more genetic aberrations. In addition, the translocation t(11;18)(q21;q21) seemed to be associated, though statistically not significant, with a favourable outcome as suggested in a previous study.25 This observation also suggests that genetic abnormalities are not necessarily associated with a more aggressive disease. In case of t(11;18)(q21;q21), this genetic event appears to result in a genomic stabilization of the disease, as t(11;18)(q21;q21) is always the exclusive translocation detected32 as again also seen in our present series. The occurrence of trisomy 18, t(14;18) involving IGH/MALT1 and t(3;14) involving FOXP1 and IGH were similar between both groups, whereas t(1;14) involving BCL10 and IGH was not found in any of the patients.

AD, however, were significantly associated with younger patients' age at lymphoma diagnosis and the presence of extra-gastric lymphomas. Both observations appear reasonable, as younger patients are more likely to suffer from AD, which predisposes them, on the other hand, to the development of extra-gastric lymphomas. Interestingly, extra-gastric lymphomas had per se a significantly higher relapse rate compared to their gastric counterparts (Figure 2). This finding, which was also reported in previous studies,25, 29 however, apparently is not related to the presence of AD, and for the time being remains elusive.

The typical indolent course of MALT lymphoma was once again reflected in the low mortality rate of 19% in our study after a median follow-up time of 45.5 (IQR, 25–72) months. However, again a pronounced relapse rate of 36%, especially in extra-gastric MALT lymphoma, was seen even after long periods of complete remissions, which warrants lifelong follow-up as suggested in a smaller previous study.25

In conclusion, these data demonstrate that the presence of an AD has no significant influence on the long-term clinical course of MALT lymphoma. Therefore, it appears to be reasonable to manage and follow patients with MALT lymphoma and AD in a similar way as patients without an underlying autoimmune condition and not subject them to more rigorous follow-up procedures. Judging from our data, however, patients with gastric MALT lymphoma and AD might not be optimal candidates for HP eradication as sole treatment.

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Acknowledgements

This project was supported by the FWF (P19346-B12).

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Wöhrer, S., Troch, M., Streubel, B. et al. MALT lymphoma in patients with autoimmune diseases: a comparative analysis of characteristics and clinical course. Leukemia 21, 1812–1818 (2007). https://doi.org/10.1038/sj.leu.2404782

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Keywords

  • MALT lymphoma
  • autoimmune disease
  • prognosis

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