Annals of Oncology Advance Access originally published online on December 20, 2007
Annals of Oncology 2008 19(4):780-786; doi:10.1093/annonc/mdm529
hematologic malignancies |
Low-grade mucosa-associated lymphoid tissue lymphoma: a retrospective analysis of 97 patients by the Hellenic Cooperative Oncology Group (HeCOG)
1 Second Department of Internal Medicine, University General Hospital ‘Attikon’, University of Athens, Haidari
2 Department of Medical Oncology, ‘Papageorgiou’ Hospital, Aristotle University of Thessaloniki School of Medicine, Thessaloniki
3 Department of Pathology, Evangelismos Hospital, Athens
4 Department of Clinical Therapeutics, University of Athens, Athens
5 Department of Medical Oncology, Ioannina University, Ioannina
6 Department of Hematology, University Hospital, Alexandroupoli, Greece
* Correspondence to: Dr G. Papaxoinis, Second Department of Internal Medicine, Propaedeutic, University of Athens, Attikon Hospital, 1 Rimini street, 124 62 Haidari, Greece. Tel: +30-210-5831689; Fax: +30-210-5326454; E-mail: georgexoinis{at}yahoo.gr
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Abstract |
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Background: The aim was to examine characteristics and treatment results of patients with mucosa-associated lymphoid tissue (MALT) non-Hodgkin's lymphomas.
Patients and methods: Epidemiological and clinical features of 97 patients with MALT lymphoma from the Hellenic Cooperative Oncology Group registry were analysed retrospectively for their prognostic significance in progression-free survival (PFS) and overall survival (OS). Comparisons were made between patients with gastric and nongastric sites of primary lymphoma and between different therapeutic modalities.
Results: Sixty-five patients presented with gastric and 32 with nongastric lymphomas. The most frequent locations of nongastric lymphomas were the bowel, lung and parotid. Gastric lymphomas occurred more frequently in males and younger patients compared with nongastric lymphomas. Seventy-four per cent of patients had early (Ann Arbor stages I–II) and 26% had advanced (stages III–IV) disease. The median PFS for the entire population was 44 months. At 5 years, 47% of patients were progression free and the OS rate was 80%. The most reliable prognostic factor for PFS and OS was the Ann Arbor stage; 5-year PFS was 67% versus 13% and 5-year OS 91% versus 51% for patients with early versus advanced disease, respectively (P < 0.001). Of the patients treated with chemotherapy only, 87% achieved an objective response and 71% complete response. Surgery did not offer survival benefit compared with chemotherapy in localised gastric lymphoma.
Conclusion: MALT lymphomas represent a distinct disease entity with widespread extranodal origin, indolent clinical course and high chemosensitivity. Ann Arbor stage was the most reliable prognostic and predictive factor.
Key words: chemotherapy, extranodal, gastric, lymphoma, mucosa-associated lymphoid
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introduction |
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TopAbstractintroductionpatients and methodsresultsdiscussionReferences |
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Mucosa-associated lymphoid tissue (MALT) non-Hodgkin's lymphomas (NHLs) were first described in 1983 by Isaacson and Wright [1] and were first recognised as a distinct entity in the Revised European–American Lymphoma classification in 1994 [2]. They represent the third most common subtype (7%) of NHLs [3], while in our registry they are ranked second in incidence (10%) [4]. Histologically, MALT lymphomas are characterised by proliferation of neoplastic marginal cells that colonise reactive germinal centres, invade epithelial structures and form lymphoepithelial lesions. Their clinical course is indolent, with high response to therapeutic modalities, late relapses and long overall survival (OS). Although the stomach is the most common and most extensively studied site of involvement, MALT lymphomas can also emerge in many other locations throughout the body [5]. They also present relatively frequently as multifocal extranodal disease [6–11].
Only a few studies have been published in the literature in which MALT lymphomas, especially nongastric, were studied as a distinct entity irrespective of site of origin [6, 7, 10–13]. In order to assess the incidence, clinical characteristics and treatment results for nongastric in comparison with gastric lymphomas, we carried out a retrospective analysis of patients with low-grade MALT lymphoma from the Hellenic Cooperative Oncology Group (HeCOG) registry.
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patients and methods |
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patient selection
In the present study, we reviewed 97 patients with MALT lymphoma diagnosed, treated and followed from December 1989 until December 2006 in five major referral medical institutes in Greece: Second Department of Internal Medicine, Athens University, ‘Attikon’ Hospital, Haidari; Department of Medical Oncology, ‘Papageorgiou’ Hospital, Aristotle University of Thessaloniki, Thessaloniki; Department of Medical Oncology, Ioannina University, Ioannina; Department of Clinical Therapeutics, University of Athens, Athens and University Hospital, Alexandroupoli. Patient data used in the study were derived from the HeCOG registry. Diagnoses were made according to the World Health Organization classification of NHLs [14]. All the original histological slides were reviewed by an expert haematopathologist (DR).
staging procedures, treatment modalities and response assessment
Details concerning the history and physical examination, complete blood count, biochemistry serum tests [including lactate dehydrogenase (LDH)], serum protein electrophoresis and immunoglobulins, chest X-rays, computed tomography of the neck, chest, abdomen and pelvis, magnetic resonance imaging scan, bone scan and gastrointestinal (GI) endoscopy (if needed) were used to interpret the epidemiological, clinical and laboratory features of patients with MALT lymphoma. They were staged according to the Ann Arbor classification, modified by Musshoff in the case of GI lymphoma [15]. When a tumour resection was carried out, surgical and histopathology reports were used for classification. We also recorded the therapeutic regimens in these patients. Three therapeutic modalities were used: surgery, radiotherapy and chemotherapy. Chemotherapy was classified as anthracycline-based or nonanthracycline (other) chemotherapy. Response was assessed according to the standardised criteria reported in the international workshop for NHL [16].
statistical methods
The basic characteristics of patients with MALT lymphoma of gastric and nongastric origin were compared according to the Fisher's exact test (for 2 x 2 tables) and the chi-square test for larger tables. The Fisher's exact test was also used to compare the response rate (RR) of patients treated with anthracycline-based versus other chemotherapy regimens in order to examine their efficacy. Survival estimations were made for all patients. Progression-free survival (PFS) was determined as the time from the start of treatment to the date of disease progression or death from any cause. OS was considered as the time from the date of first biopsy to the date of death from any cause. Univariate and multivariate analyses according to a Cox proportional hazards model were used to determine independent prognostic factors for survival. PFS and OS were compared between patients treated with anthracycline-based and other chemotherapy regimens and between patients with localised gastric lymphoma (stage I) treated only with primary chemotherapy and those treated with complete surgical resection with or without adjuvant chemotherapy. The Kaplan–Meier method [17] was used for survival estimations and the log-rank test for survival comparisons. All comparisons were two tailed and a P value of 0.05 or less was considered statistically significant.
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results |
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patient demographic, clinical and laboratory characteristics
The demographic, clinical and laboratory findings of patients are presented in Table 1. Among 97 patients with MALT lymphoma, 65 had the primary site located in the stomach and 32 in other sites. There were 53 males and 44 females [male/female (M/F) ratio = 1.2]. Male predominance was obvious in the gastric group (M/F ratio = 1.6), whereas in the nongastric group the disease was more frequent in females (M/F ratio = 0.7); however, the M/F ratio did not differ significantly between the two groups (P = 0.082). Patients with nongastric lymphoma were marginally but significantly older than patients with gastric lymphoma (P = 0.042). The majority of patients from both groups had an Ann Arbor stage I disease. Patients with nongastric lymphomas tended to have more advanced disease, but this difference was not statistically significant (P = 0.153). Approximately one-third of the patients presented with B symptoms and only a small minority had bone marrow infiltration, increased serum LDH or paraprotein. Among patients with known LDH values, significantly more patients with stage III or IV disease had increased LDH values than those with stage I or II disease (30.4% versus 10.4%, P = 0.022, data not shown). Only 30% of patients presented with lymph node disease and 12% with involvement of two or more extranodal sites (other than bone marrow). These figures were higher in patients with nongastric compared with gastric lymphomas, but the difference was not significant. The most frequent sites of origin of nongastric MALT lymphomas were the bowel (11%), lungs (6%) and parotids (4%). Lymphomas occurred less frequently in other sites: thyroid (2%), eyes (2%), tonsils (2%), rhinopharynx (1%), liver (1%), breast (1%), skin (1%), soft tissue (1%) and central nervous system (1%).
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treatment and response to chemotherapy
In total, 91 patients were treated with surgery, chemotherapy, radiotherapy or any combination thereof. The majority of patients (57% with gastric and 78% with nongastric lymphoma) were treated only with chemotherapy. Surgery alone was carried out on 17% of patients with gastric and 3% with nongastric lymphoma, while chemotherapy and surgery were carried out in 15% and 10% of gastric and nongastric lymphoma patients, respectively. Radiotherapy was applied in nine patients: four patients received only radiotherapy (two gastric, one breast and one parotid); two received chemotherapy and radiotherapy (one gastric and one ocular); two were treated with surgery and radiotherapy (one gastric, one thyroid) and one patient with gastric lymphoma received triple therapy.
Forty-two per cent of patients with gastric and 63% of patients with nongastric lymphoma received anthracycline-based regimens, which included the combination of cyclophosphamide, vincristine and prednisone with adriamycin, epirubicin or mitoxantrone (CHOP, CEOP and CNOP). Nonanthracycline-based regimens were received by 31% of patients with gastric and 25% of patients with nongastric lymphoma. These regimens included the combination of fludarabine and mitoxantrone, cyclophosphamide, vincristine and prednisone or chlorambucil and prednisone. Rituximab was administered to 22% of patients with gastric and 31% of patients with nongastric lymphoma.
The RR was 87% in the 55 eligible patients treated with chemotherapy only (Table 2). Complete response (CR) was achieved in 71%, partial response in 16%, stable disease in 6% and progressive disease in 7% of patients treated with chemotherapy alone. Chemotherapy was highly effective irrespective of primary site, Ann Arbor stage and type of chemotherapy (Table 2). The RR did not differ significantly between groups, whereas the CR rate was significantly higher in patients with early compared with advanced stage of disease.
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survival analysis
The median time of follow-up was 47.2 months (range 0.5–128 months). The median time to progression of the entire population was 44 months, whereas the median OS was not reached yet. Five-year PFS was 47% and 5-year OS 80% (Figure 1). OS and PFS were significantly better (P < 0.001) in patients with early (stage I, II) disease than in patients with advanced (stage III, IV) disease (Figure 2). Among patients treated with chemotherapy only, there was no statistically significant difference in PFS and OS between those who received anthracycline-based or other chemotherapy (Figure 3).
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As the role of surgery in the treatment of patients with localised gastric MALT lymphoma remains controversial, PFS and OS were compared between patients with stage I gastric lymphomas treated with surgery and subsequent adjuvant chemotherapy and those treated with chemotherapy alone. There was no statistically significant difference between the groups, although the number of patients was not sufficient to draw meaningful conclusions (Figure 4).
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The prognostic significance of various factors was examined by univariate analysis (Table 3). Among these, advanced stage, two or more extranodal sites of disease, lymph node disease, bone marrow infiltration, B symptoms and anaemia (Haemoglobin <12 g/l) were found to adversely affect PFS and OS, and increased serum LDH and a gastric site of primary disease adversely affected OS. Upon multivariate analysis, advanced stage retained its prognostic significance for both PFS and OS, and the presence of increased serum LDH, gastric primary disease, more than one extranodal sites and B symptoms were significant only for OS (Table 4).
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discussion |
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TopAbstractintroductionpatients and methodsresultsdiscussionReferences |
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This study compared the characteristics of patients with gastric and nongastric MALT NHLs. The results from this study are mostly in agreement with previously reported data. The most frequent sites of nongastric lymphomas in this study were the bowel, the lung and the parotid. Despite the low number of patients in our study, this observation is in agreement with other studies reporting the salivary glands, the orbit, the lung, the intestine and the skin as the most common nongastric lymphoma sites [6, 11–13].
In our study, gastric lymphomas predominated in males (M/F ratio 1.6), whereas nongastric lymphomas were more common in females (M/F ratio 0.7). Similarly, two other studies have shown higher rates of gastric lymphomas in males (M/F ratio 1.7–2.0) [18, 19], in contrast to other studies in which nongastric lymphomas tended to be more frequent in females (M/F ratio 0.6–0.87) [6, 11, 13].
The low frequency of B symptoms, increased serum LDH and bone marrow infiltration observed in our study and described by others are consistent with the indolent nature of MALT lymphomas [6, 7, 11–13]. In contrast, the slight difference in mean age found in our study is not confirmed by the literature [12].
We observed that advanced stage (Ann Arbor III–IV) disease occurred more frequently in patients with nongastric lymphomas (34% versus 21% in those with gastric lymphomas). Earlier studies found similar rates of advanced stage disease in patients with nongastric lymphomas (27%–37%) [6, 7, 12, 13], whereas in more recent studies, an even higher rate of disseminated disease was observed (44%–46%) [10, 11]. This may be due to the more extensive examinations and more stringent classification procedures used in this group of patients. In addition, a relatively high proportion of our patients did not undergo bone marrow biopsy, which could have led to a shift to early stages. Although more thorough examination may lead to more precise staging, the necessity of extensive invasive methods needs to be confirmed. For example, one study showed that the presence of multiple mucosal sites of involvement did not seem to adversely impact survival, suggesting that multiple endoscopies would not provide survival advantage [12]. Another study showed that among patients with disseminated disease, those with bone marrow or nodal involvement had the poorest survival [11].
Survival data from our series are consistent with other studies and confirm the indolent nature of MALT lymphomas. The time to progression in our series was 44 months (3.7 years), whereas previous studies reported a longer median time to progression (5.6–7 years) [6, 7, 11–13, 19, 20]. A possible reason for this discrepancy could be the heterogeneity of treatments used in the 17-year period of our study.
There are currently no generally accepted prognostic factors for MALT lymphomas. In our analysis, the Ann Arbor stage was the most reliable prognostic factor for both PFS and OS, consistent with the findings of several other studies [8, 13, 18, 19]. In contrast, other investigators did not observe any correlation between the disease stage and survival, but identified other prognostic factors, such as β2 microglobulin, anaemia, hypoalbuminemia, lymph node or bone marrow involvement and poor performance status [7, 11, 12]. In these series, the prevalence of disseminated disease was higher than in the former studies. A possible explanation for this disagreement could be that the use of extensive testing may have shifted some patients with occult distant disease to the advanced disease subset. These patients would likely have similar prognosis to those with localised disease, as indicated above [12]. Findings from Raderer et al. [10] also support these speculations. After subjecting their patients to a thorough investigation, they reported a relatively high rate of advanced disease (46%), but observed similar outcomes between those with localised and disseminated diseases. Nevertheless, although the relationship between disease dissemination, Ann Arbor classification and outcomes may be unclear, the awareness of the disease spread is important for the decision of local versus systemic treatment. Therefore, although our data indicate that advanced disease stage is predictive of adverse outcomes, these results should be interpreted with caution. Studies identifying other prognostic markers are needed.
High serum LDH levels have been shown to adversely impact OS in MALT lymphomas only in univariate analysis of prognostic factors [11, 12, 18]. We found that this is also true by multivariate analysis. In addition, we did not observe any association of serum LDH levels with the stage of disease (data not shown), which has also been shown by Thieblemont et al. [7]. However, Considering the limitations of applying Cox models to the small number of events and low death rate (80%, 5-year survival) observed in our study, the results of the multivariate analysis of prognostic factors for OS should be interpreted with caution.
This study examined one of the largest series of patients with MALT lymphoma treated with chemotherapy only. The RR observed in this subset was 87% and the CR was 71%. These results are comparable with those reported in the literature. Thieblemont et al. [7] showed a 63% CR rate in 70 patients treated with chemotherapy only, while Arcaini et al. [11] found a higher CR rate (73%) in their analysis of 94 patients. We also show that disease stage is predictive for response to chemotherapy, as described by Arcaini et al. [11].
Our patients received various commonly used chemotherapy regimens. Anthracycline-based treatments or rituximab did not offer any survival advantages in this study. As rituximab therapy was started only recently, the follow-up, however, may have been too short to reveal any benefit. Other retrospective studies also observed no difference in efficacy between specific regimens [11, 13], and several prospective phase II trials reported similar results [21–24]. Randomised trials are therefore needed to identify the best chemotherapy regimen and the specific subsets of patients who will benefit from this regimen.
The role of surgery in localised gastric MALT lymphoma has been better evaluated. Although initial reports favoured the use of surgery [25–28], later studies showed that its use in combination with chemotherapy is not more effective than the conservative treatment [19, 29–31]. Currently, surgery only plays a role in cases of emergency and not in an elective treatment approach. The relatively high proportion of our patients who were subjected to surgery belonged mainly to the early period, when surgery was regarded as an appropriate therapeutic method. We did not observe any benefit of surgery in stage I gastric lymphoma patients, consistent with the current treatment practice. This is further supported by the results of a prospective randomised study in patients with marginal-zone B-cell lymphoma of the stomach which favoured the use of chemotherapy over surgery or radiotherapy in terms of event-free survival, but not OS [32].
In conclusion, our study showed that low-grade MALT lymphomas constitute a distinct disease entity that can originate from various locations throughout the body. Their clinical course was indolent with late relapses and long survival [33]. The patients with advanced disease, however, had significantly worse prognoses. Considering the substantial chemosensitivity of MALT lymphomas, prospective randomised clinical trials investigating predictive markers of responsiveness are needed.
Received for publication April 26, 2007. Revision received September 26, 2007. Accepted for publication October 18, 2007.
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