Comprehensive analysis of imaging and pathological features in 20 cases of pulmonary mucosa-associated lymphoid tissue (MALT) lymphoma: a retrospective study

Introduction

Pulmonary mucosa-associated lymphoid tissue (MALT) lymphoma, a distinctive subtype of non-Hodgkin’s lymphoma (1), exemplifies primary extranodal lymphomas originating in the lung (2). Renowned for its indolent nature and infrequent occurrence, the clinical presentation of pulmonary MALT lymphoma is subtle (3), and its radiological manifestations are diverse, posing considerable diagnostic challenges (4). In contrast to more aggressive lymphomas, MALT lymphoma often lacks the hallmark symptoms of high-grade malignancies (5), making early detection elusive and potentially causing delays in therapeutic intervention.

Clinical manifestations of MALT lymphoma may vary but often include non-specific symptoms such as cough, chest pain, or shortness of breath (6,7). Systemic symptoms, such as fever and weight loss, are less common but can occur (8). The overall incidence of pulmonary MALT lymphoma is relatively low compared to other lymphomas (9,10). Risk factors for developing pulmonary MALT lymphoma may include a history of autoimmune diseases, chronic infections, or exposure to environmental factors that trigger chronic inflammation (11).

The treatment landscape for pulmonary MALT lymphoma primarily revolves around surgical resection, radiotherapy, and chemotherapy, with surgery being the preferred modality for localized disease (12,13). The indolent course of MALT lymphoma, coupled with its relative insensitivity to chemotherapy and radiotherapy, underscores the importance of accurate diagnosis and appropriate selection of treatment modality (14,15). Moreover, the prognosis of MALT lymphoma is generally favorable, with surgical interventions yielding better outcomes compared to cases where complete resection is not feasible (16).

The clinical significance of pulmonary MALT lymphoma transcends its rarity, delving into the domain of differential diagnosis (17). This is particularly critical when distinguishing it from prevalent pulmonary pathologies like adenocarcinomas, focal invasive mucinous adenocarcinoma of the lung, focal organizing pneumonia or infectious granulomas (18,19). The management and prognosis of these conditions vary significantly, underscoring the importance of accurate differentiation. The complexity of pulmonary MALT lymphoma is further complicated by its etiology, commonly associated with chronic inflammatory stimuli (20). This association is notable, especially in patients with autoimmune diseases or a history of chronic infections, adding layers of intricacy to the understanding of the disease (21,22).

Radiologically, pulmonary MALT lymphoma displays a spectrum of patterns on high-resolution computed tomography (HRCT), ranging from solitary or multiple nodules, areas of consolidation, to ground-glass opacities (23,24). These imaging features, although valuable, overlap significantly with those of other pulmonary conditions, thereby necessitating a more nuanced approach to interpretation (25,26). The role of imaging in MALT lymphoma extends to not only diagnosis but also to treatment planning and monitoring response to therapy. Pathologically, MALT lymphoma is characterized by the proliferation of marginal zone B-cells, which may manifest in a variety of cytological appearances (27). Immunohistochemistry plays a pivotal role in diagnosis, with markers such as CD20 and CD79a often showing positivity (28,29). The Ki67 proliferation index is another valuable tool, providing insights into the tumor’s growth dynamics (30). Ki67 indicates the level of cellular proliferation activity, representing the proliferation rate of MALT tumor cells. It reflects the degree of malignancy of the cells and is related to the prognosis of the patients. However, the lack of a histological grading system in MALT lymphoma contrasts with other lymphomas, where such grading significantly influences treatment decisions (31).

This study aimed to elucidate the imaging and pathological characteristics of pulmonary MALT lymphoma based on a comprehensive analysis of 20 cases from a thoracic specialty hospital. Our focus is to assist radiologists in understanding the disease’s unique imaging features from a pathological perspective, thereby improving differential diagnosis during initial chest imaging assessments. This understanding is critical in guiding further biopsy for definitive diagnosis and timely surgical intervention when feasible, or alternatively, opting for radiotherapy or chemotherapy. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1066/rc).

Methods

Study design and participants

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and approved by the Ethics Committee of Nanjing Chest Hospital (No. 2023-KL035-01). Informed consent was waived for this retrospective study due to the exclusive use of de-identified patient data, which posed no potential harm or impact on patient care. All patients diagnosed with pulmonary MALT lymphoma by pathology in Nanjing Chest Hospital were retrospectively included from June 2017 to December 2023. Inclusion criteria were as follows: (I) the patients were diagnosed for pulmonary MALT lymphoma based on diagnostic criteria, including clinical, radiological, and histopathological assessments; (II) involvement of lung or/and bronchus, without hilar or mediastinal adenopathy or mass; (III) no evidence of extrathoracic lymphoma at before and at the time of primary diagnosis; (IV) no evidence of extrathoracic lymphoma within 3 months since onset; (V) no history of other pulmonary diseases before a diagnosis of pulmonary MALT lymphoma; (VI) completed data were available to retrieve from the hospital medical records system. Exclusion criteria were as follows: other causes of similar lung diseases, such as sarcoidosis, infectious processes, and other types of lymphomas. Finally, a total of 20 patients diagnosed with pulmonary MALT lymphoma were included in this study.

HRCT scanning

All patients underwent HRCT scans before histopathologic diagnosis. The technician sets specific parameters suitable for lung scanning, including the slice thickness, voltage, and current. Lung HRCT typically uses thinner slices (e.g., 1–2 mm) to achieve higher resolution images. HRCT imaging parameters were meticulously documented, comprising tumor dimensions, anatomical location, boundary delineation, density variations, and identification of any distinctive morphological features. Experienced radiologists independently reviewed the HRCT images, documenting tumor characteristics. HRCT imaging indicators were analyzed, including the morphology, size, clarity of boundaries, internal structure, and relation to the surrounding tissues of the tumor.

Pathologic assessment

Pathological assessments entailed a comprehensive evaluation of tumor histology, encompassing discernment of tumor cell phenotypes, determination of Ki67 proliferation index, and characterization of immunohistochemical profiles. Professional pathologists conducted pathological analysis, covering cytological features and immunohistochemical expression. Specific immunohistochemical markers were used to identify cell types characteristic of MALT lymphoma. Pulmonary MALT lymphoma shows infiltration by small lymphocytes, plasma cells, and marginal zone cells. Immunohistochemistry is essential, typically showing cells positive for CD20 and B-cell markers, and negative for CD5 and CD10, helping to distinguish it from other types of B-cell lymphomas.

Statistical analysis

Descriptive statistics were performed on the collected data. Appropriate statistical methods were used to assess the correlation between imaging and pathological features. All statistical analyses were conducted using SPSS software (version 26.0, IBM Corporation, Armonk, NY, USA). All data were tested for normal distribution by Shapiro-Wilk test. The measurement data that met the normal distribution were expressed as mean ± standard deviation. Categorical variables were presented as n (%).

Results

General characteristics

Baseline characteristics are shown in Table 1. This study involved 20 patients, with an average age of 63.19±7.06 years, ranging from 54 to 76 years. Regarding gender distribution, there were 11 male patients (55%) and 9 female patients (45%). The average duration of the disease was 409.81±635.58 days, ranging from 1 to more than 1,800 days. In terms of comorbidities, 8 patients (40%) had no additional underlying diseases. There were 4 patients (20%) with hypertension, 3 patients (15%) who consumed alcohol, 5 patients (25%) who smoked, 1 patient (5%) with diabetes, 1 patient (5%) with gastric ulcer, and 2 patient (10%) with heart disease.

Regarding clinical presentation of study disease, 6 patients (30%) were asymptomatic. Cough was observed in 7 patients (35%), chest pain in 4 patients (20 %), expectoration in 4 patients (20%), chest tightness in 2 patients (10%), fever in 2 patients (10%), wheezing in 1 patient (5%), and dyspnea in 1 patient (5%).

Chest CT findings, patterns and features in patient

As shown in Table 2, the analysis of main pulmonary imaging changes in patients with MALT lymphoma revealed the following findings. Air bronchogram and bronchial dilation are the most common features. All 20 patients exhibited air bronchogram, with 14 of them showing associated bronchial dilation, accounting for 70% of cases. Among these, 8 cases (40%) displayed a beaded appearance of the dilated bronchial walls, and 6 cases (30%) presented with multiple air-filled cystic lesions, with the majority located around the dilated bronchi. Enhanced CT scans were performed on 10 patients, revealing vascular angiography sign in 7 cases, constituting 35%. Regarding the presence of pleural effusion, 17 cases (85%) showed none, while 3 cases (15%) presented with pleural effusion. All tumors were classified as low-grade. The average number of tumors per patient was 1.69±2.24, with a range from 1 to 10 tumors. The size of the tumors varied, averaging at 30.64±33.97 cm², with the smallest being 0.64 cm² and the largest 115.20 cm². In terms of tumor location, the left upper lobe was the most common site, observed in 13 patients (65%). Tumors in the right lower lobe were found in 7 patients (35%), while those in the left lower lobe and right upper lobe were each present in 3 patients (15%). The right middle lobe and left middle lobe each had tumors in 1 patient (5%). Regarding the border characteristics of these tumors, most (13 patients or 65%) had surrounding lung interstitial infiltration, while clear tumor boundaries were noted in 3 patients (15%).

Regarding calcification and necrosis, 9 cases (45%) showed no signs of either. Enhanced scans revealed non-enhancing circular or ribbon-shaped areas in 5 patients (25%), and calcified plaques were observed in 2 patients (10%). In the study of pulmonary MALT lymphoma, the relationship between the tumor and surrounding lung tissue reveals various radiological features. The round-glass opacity is the most common finding, with 13 out of 20 patients exhibiting more or less ground-glass opacity around the tumor (65%). In 6 patients (30%), there was a spiculated sign around the tumor. In 7 patients (35%), there was thickening of bronchovascular bundles and surrounding micronodules around the tumor, indicating varying degrees of infiltration in the peritumoral interstitium. In 3 cases (15%), infiltration of the surrounding lung interstitium was not apparent. In 2 cases, linear pleural traction was observed around the tumor periphery.

Histopathological classification and immunohistochemical findings

The immunohistochemical analysis of pulmonary MALT lymphoma in this study revealed the expression of various key immunomarkers as shown in Table 3. CD20, a B-cell marker, showed the highest positivity, being expressed in 12 patients (60%). Ckpan and CD3, markers associated with epithelial cells and T-cells respectively, were both positive in 11 patients (55%). Other markers such as Pax-5 and CD21, both linked to B-cell lineage, were positive in 6 patients (30%). Bcl-2 and CD79a, related to cell survival and B-cell antigen receptor complex respectively, showed positivity in 3 patients (15%).

Regarding the Ki67 positivity rate, which is indicative of cell proliferation, a range of values was observed. In 3 patients (15%), the Ki67 positivity rate was 5%, and another 3 patients (15%) did not undergo immunohistochemical analysis for this marker. Ki67 positivity rates of 30% and 10% were each found in 3 patients, while rates of 15%, 40%, and 20% were observed in 2 patients (10%), 1 patient (5%), and 1 patient (5%) respectively.

HRCT images and H&E-stained histologic findings in pulmonary MALT lymphoma

HRCT images (Figure 1) showed stromal infiltration around the tumor, which corresponds to the histological findings in Figure 2A, where tumor cells surrounded small blood vessels in a nodular pattern. The histological analysis in Figure 2B revealed that the tumor cells of MALT lymphoma grew diffusely as mononuclear lymphocytes. HRCT images (Figure 1A,1C) also showed bronchial dilatation, and the corresponding histology in Figure 2C demonstrated that the bronchial mucosa was largely intact, with tumor cells surrounding it. Additionally, in HRCT image (Figure 1C), bronchial dilatation with irregular, bead-like narrowing of the lumen was observed, which correlated with the histological findings in Figure 2D, where tumor cells were seen destroying part of the bronchial mucosa, forming lymphoepithelial lesions. The remaining bronchial mucosa was normal, and the lumen is irregularly dilated, with nearby blood vessels along the bronchi.

Figure 1 High-resolution computed tomography images of typical cases. (A) consolidation was observed in the lower left lung lobe, accompanied by a ground-glass opacity around the tumor (yellow arrow 1), thickening of bronchovascular bundles (yellow arrow 2), and peripheral micronodules (yellow arrow 3). Within the lesion, signs of air bronchogram (yellow arrow 4) and small air bubbles (yellow arrow 5) were also identified; (B) consolidation was observed in the lower left lung lobe. Within the lesion, there was evidence of bronchial dilation (yellow arrow 1) and signs of air bubbles (yellow arrow 2). After contrast enhancement, vascular imaging signs were visible within the lesion (yellow arrow 3); (C) a mass shadow was present in the upper right lung lobe, with the focal mass with spiculated contours and surrounded by ground glass opacity (yellow arrow 1). Within the lesion, there were signs of air bronchogram (yellow arrow 2), bead-like bronchial dilatation (yellow arrow 3), and small air bubbles (yellow arrow 4).

Figure 2 H&E staining of pulmonary mucosa-associated lymphoid tissue lymphoma. (A) Tumor marginal cells surrounding blood vessels grow in a nodular pattern, with focal nodules merging with each other, as seen in low-power magnification with H&E staining (4×); (B) mononuclear lymphocytes in the center of the mass exhibit diffuse growth, with cells of moderate size, disrupting the alveolar structure, as observed in high-power magnification with H&E staining (40×); (C) the bronchial mucosa remains intact, with tumor cells wrapping around the periphery, and localized infiltration of a small number of tumor cells is visible in the mucosa (black arrow) (10×); (D) tumor cells destroy two-thirds of the bronchial mucosa, forming lymphoepithelial lesions, with remnants of mucosal epithelium observed locally (black arrow), accompanied by irregular bronchial dilation, as seen in low-power magnification with H&E staining (10×); (E) tumor cells disrupt the bronchial mucosa, with only a small number of residual epithelial cells visible (black arrow), accompanied by irregular bronchial dilation, as observed in low-power magnification with H&E staining (10×); (F) residual bronchial epithelial cells show positive staining for CKpan, EnVision two-step method, as seen in medium-power magnification with H&E staining (20×).

The presence of the “vacuum sign” on HRCT images (Figure 1A-1C) was associated with the histological findings in Figure 2E, where tumor cells had destroyed the bronchial mucosa, leaving only a small amount of epithelial remnants, while the distal airways showed dilated air spaces. Finally, histology in Figure 2F showed that the remaining bronchial mucosal epithelial cells in the tumor tissue express CKpan positively (CKpan stained the bronchial epithelial cells brown; areas of destroyed mucosa remained unstained, indicating the absence of epithelial cells. The brown-stained regions outlined the remaining bronchial lumen).

Discussion

This retrospective study on pulmonary MALT lymphoma provides a nuanced understanding of the disease through the correlation of HRCT imaging and pathological features. Our analysis of 20 cases reveals detailed insights into the characteristic patterns of this lymphoma subtype, emphasizing the importance of an integrated diagnostic approach. In pulmonary MALT lymphoma, changes in the bronchi, such as air bronchogram, bronchial dilation, and cystic lesions, are associated with the pathophysiology of the disease. Unlike bronchial dilation caused by other reasons, the characteristic feature of MALT lymphoma-related bronchial dilation is the beaded appearance of the dilated bronchi. In this group of 20 cases, all exhibited air bronchogram, with 17 cases showing associated bronchial dilation. Among these, 9 cases displayed bronchial dilation with a beaded appearance, and 8 cases had multiple cystic lesions, with most located around the dilated bronchi.

The primary reason for these bronchial changes is the unique growth pattern of tumor cells in MALT lymphoma. Most domestic literature suggests that these tumor cells proliferate along the pulmonary interstitium without disrupting the bronchi and blood vessels, which explains the visibility of air bronchogram. The surrounding connective tissue proliferation pulls on the bronchi, leading to bronchiectasis. However, the presence of proliferative connective tissue within the lesions and the reason it does not form regular columnar bronchiectasis but rather irregular bead-like patterns raise questions.

Pathologically, tumor cell infiltration into the mucosa of the small bronchi leads to lymphoepithelial lesions. On the same pathological slide, only dilated blood vessels are seen, with no accompanying bronchi. Since bronchi and blood vessels typically run together, it is speculated that the bronchi are invaded by the tumor. Immunohistochemistry reveals CKpan positive expression in the remaining bronchial mucosal epithelial cells within the tumor tissue. Bronchoscopy has revealed uneven mucosal surfaces in the segmental or lobar bronchi, with narrowed or occluded lumens in a few cases. Some believe that bronchiectasis is caused by proximal narrowing and subsequent distal expansion of the bronchi. To explain these bronchial changes (air bronchogram, bronchiectasis, air cysts) in pulmonary MALT lymphoma, one must consider the pathological changes observed where the bronchi are invaded by the tumor. The study’s findings, combined with the latest literature, suggest that the irregular bronchial wall expansion and the bead-like appearance could be due to the specific invasion and growth patterns of tumor cells in the bronchial structures, resulting in distortion and deformation of the bronchial architecture (32).

The characteristic of the tumor-lung interface in pulmonary MALT lymphoma is the absence of a capsule around the tumor, with a transition zone from the tumor body to normal lung tissue. Pathologically, tumor cells infiltrate the interstitium around the tumor, leading to a series of imaging changes, such as peritumoral ground-glass opacity, thickening of bronchovascular bundles with surrounding micronodules, and spiculated contours (33). Our pathology data indicate that mononuclear lymphocytes proliferate around bronchovascular walls and septa, forming discrete nodules that merge at the periphery of the tumor. Among the 20 cases, 4 cases (20%) showed no obvious interstitial infiltration, while 16 cases (80%) exhibited peritumoral interstitial infiltration. Among these, 7 cases had extensive infiltration around the tumor, manifested as peritumoral ground-glass opacities, thickening of bronchovascular bundles, and surrounding micronodules, while 6 patients had less peritumoral interstitial infiltration, showing peritumoral ground-glass opacity and spiculated contours. The peritumoral interstitial infiltration is highly characteristic. Lesions with more air bronchogram and bronchial dilation tend to have more surrounding interstitial infiltration, while those with fewer air bronchogram and bronchial dilation have less peritumoral interstitial infiltration (34). Larger lesions exhibit more interstitial infiltration, while smaller lesions have less interstitial infiltration. Tumor cells infiltrate the mucosa of the fine bronchi and the alveolar epithelium, forming lymphoepithelial lesions. Peritumoral mononuclear-like lymphocytes surround the bronchi, blood vessel walls, and interlobular septa, proliferating in a nodular pattern and merging with one another (35).

It is an indolent lymphoma with slow progression and relatively favorable prognosis. For isolated lesions, surgical resection is the preferred treatment; for multiple lesions, when MALT is suspected on imaging, timely lung biopsy is recommended, and after confirmation, hematological oncology-directed chemotherapy is initiated. Among our 14 surgical cases, 12 were completely resected, all being isolated lesions undergoing lobectomy. In our cohort, 5 patients received lung biopsy for pathological confirmation, with 4 having multiple lesions and 1 having a solitary lesion (surgery was recommended, but the patient opted for hematological oncology-directed chemotherapy). Our study, limited by its retrospective design and small sample size, underscores the necessity for future research employing larger patient cohorts and prospective methods. Longitudinal studies are crucial for providing comprehensive treatment outcomes and insights into long-term survival, further enriching our understanding of pulmonary MALT lymphoma.

Conclusions

In conclusion, the findings from our study significantly contribute to the existing knowledge of pulmonary MALT lymphoma, underscoring the crucial role of combining radiological and pathological assessments for accurate diagnosis. This integrated approach not only aids in guiding clinical decisions but also has the potential to improve patient outcomes significantly. Our study emphasizes the need for ongoing research in this area, to refine diagnostic criteria, and to develop more targeted and effective therapeutic strategies for patients with this lymphoma subtype.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1066/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1066/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1066/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1066/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and approved by the Ethics Committee of Nanjing Chest Hospital (No. 2023-KL035-01). Informed consent was waived for this retrospective study due to the exclusive use of de-identified patient data, which posed no potential harm or impact on patient care.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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