IgG4-related disease and pleural effusion: a systematic review

Introduction

Immunoglobulin G4-related disease (IgG4-RD) is a fibroinflammatory entity associated with autoimmune pancreatitis that was first described in 2003. Evidence was later provided that this disease can affect multiple organs either synchronically or asynchronically (1). The nomenclature for IgG4-RD has evolved to also include single-organ diseases, previously regarded as unrelated diseases, with shared clinical, serological and histopathological features (2).

IgG4-RD is a histologically homogeneous entity, regardless of the affected organ. Distinctive findings include dense lymphoplasmacytic infiltration, storiform fibrosis, and obliterative phlebitis (3). Immunohistochemistry reveals elevated levels of IgG4+ plasma cells (>50/field) and an elevated IgG4+/IgG+ plasma cell ratio (>40%). Sixty percent of cases exhibited increased plasma levels of IgG4 (3). Whether IgG4 antibodies are pathogenic by themselves or just a marker or subproduct of the immune-mediated inflammatory process has not yet been elucidated. Several mechanisms may be involved in the development of the disease, which develops as a result of the upregulation of regulatory T-cells and Th2 cells in the tissues involved. This overexpression is distinctive of IgG4-RD and is substantially higher than in classic autoimmune conditions (2,4).

Only in 4% of cases, IgG4-RD involves the pleura and causes nodular or diffuse pleural fibrosis or pleural effusion (PE), which may be bilateral and massive (5). IgG4-RD may involve or not other organs (6,7). Having a low incidence, no large case series have been reported to discuss the characteristics of pleural fluid (PF) in IgG4-RD. Only a few narrative reviews provide some data (8,9). The objectives of this systematic review were to document the histological and biochemical characteristics of PF and pleural tissue, assess its clinical course, and determine the most effective treatments for the management of PE. We present this article in accordance with the PRISMA reporting checklist (10) (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2192/rc).

Methods

The review included all articles about IgG4-RD and PE published any time and in any format. Leading articles, reviews or letters to the editor not reporting new cases were excluded.

Data sources and database search strategy

Several public databases were searched by year of publication. Full-text articles had to be available in English, Spanish, French, Italian or Portuguese. The search period was set between January 1, 2011 and June 30, 2024. A literature search was performed of the following (online) electronic databases between July 1 and August 31, 2024: Medline (through PubMed interface), Embase, Scopus, Cochrane and Web of Science. Keywords were: (“Pleural effusion” (Mesh) AND “Immunoglobulin G4 related disease” (Mesh). Additional relevant articles were identified by manual inspection of reference lists from retrieved papers. All the studies that met the inclusion criteria were reviewed to identify potentially eligible studies. Titles and abstracts were screened and selected for full-text reading. Consensus was sought at every stage.

Data collection process

Data from the selected studies was extracted using a Microsoft Excel datasheet (Microsoft Excel 2016, Microsoft Corp, USA). The following information was collected: authors, year, number of cases reported; age and gender of patients; side and size of PE; appearance and characteristics of PF [transudate/exudate, differential nucleated RBC count and any biochemical measurement performed in PF; results of culture, cytology and pleural biopsy (where available); PE treatment; individual response to treatment, and complications]. Classification into transudate vs. exudate was performed based on the Light’s criteria (11).

Methodological quality of individual studies

As most of the articles reviewed were case reports, their quality in terms of type of study, internal and external validity, precision and heterogeneity was not assessed.

Results of interest

The results of interest were the demographic characteristics of patients; the biochemical and microbiological features of PE; the treatment administered and patient response; and final outcome (survival vs. mortality).

Statistical analysis

In the light of the broad heterogeneity and descriptive nature of the studies included, a simple statistical description (proportion, median and log rank) was provided for every result of interest.

Results

A total of 46 studies were reviewed, aggregately including 55 patients diagnosed with IgG4-related PE. These included 23 studies (12-34) that each reported between 1 and 4 cases. An additional 23 studies also contributed isolated cases (35-57). In total, 57 PF samples were analyzed. Figure 1 presents the flowchart of the study selection process. As many as 58.2% of cases (32/55) were diagnosed in Asia [Japan, n=19 (12,16,17,20,24-26,30,35-37,39,40,45-47,49,56,57); South Korea, n=8 (14,15,23,34,52); China, n=5 (22,29,50,54,55)]. In total, 25.5% (14/55) of cases were diagnosed in Europe [Spain, n=6 (19,33,38); Italy, n=3 (27,32,44)]. Interestingly, the United Kingdom (18), Belgium (28), Ireland (43), France (48) and Portugal (53) only reported a case. Finally, 9.1% of cases (5/55) were reported in Israel (31,41) and 7.3% (4/55) in USA (13,21,42,51). Two larger series were excluded, as individual data could not be extracted separately (58,59).

Figure 1 PRISMA flowchart of evidence synthesis. IgG4, immunoglobulin G4.

Demographic and clinical characteristics

The demographic, clinical and radiological characteristics of the 55 cases included in our review are shown in Table 1. Age-group distribution is shown in Figure 2. Median age was 66 years [range, 28–86 years; 85.5% of cases (47/55) were over 50 years old]. PE occurred more commonly in men than in women (74.5%; 41/55; ratio 2.9/1).

Figure 2 Age distribution of patients with IgG4-related disease and pleural effusion. IgG4, immunoglobulin G4.

Involvement of other organs was documented in 41 patients (74.5%). The lungs were involved in 30 cases (73.2%) [in 14 the involvement was only pulmonary (34,1%) (12,14,15,17,18,25,27,37,41,47,50,54,55); in 12 (29.3%) there were more organs affected (13,20,22-24,26,30,31,38,45,48,53); and in 4 (9.8%) no information was provided as to whether more organs were affected (32,36,40,51)]. In 6 patients (17.1%) involvement of organs other than the lung was documented (21,29,34,41,56). A case of trapped lung was documented (13). The pleura was the sole organ affected in only four patients (11.4%) (12,16,28,44) (Table 1).

Laterality of PE was available in 48 cases (87.3%). PE was unilateral in 29 cases (60.4%); 20 were right-sided (41.7%) (13,14,18,19,22,23,26,28,29,32,34,36,37,41-44,54-56), whereas 9 were left-sided (18.7%) (27,30,33,46,47,49-51,57). PE was bilateral in 19 cases (39.6%) (12,15-17,19-21,24,25,31,38-41,45,48,53). The size of the PE was documented in 38 cases (66.7%). PE size was <1/3 of the hemithorax in 11 cases (28.9%) (12-14,19,23,25,26,28,34,37,48); in 19 cases (50.0%) PE occupied one to two thirds of the hemithorax (17-19,29,30,36,39,40,44-47,49-51,54-57); and PE occupied more than two thirds of the hemithorax in 8 cases (21.1%) (15,16,22,24,27,32,38,43).

Pleural effusion

The color of the PE was documented in 19 cases (33.3%). PF was serous with different shades in 16 (84.2%) (17,18,23-25,27,36-38,40,44,45,51,54,56), and serohematic in three cases (15.8%) (29,32,43).

Cellular differentiation and the biochemical characteristics of PF (medians and ranges) were available in few cases (Table 2). Only 20.8% of PEs (5/24) had >5,000 cells/mm³. Neutrophil count percentage did not exceed 50% in any of the 16 PEs where this parameter was available. Mononucleated cell count was documented in 25 cases (45.45%) and was <50% in only one case (4%) (23). Finally, eosinophil count was >10% in 40.0% of the PEs where it was available (4/10) (21,23,33,54).

Data to determine whether the PE was a transudate or an exudate based on Light’s criteria were available in 37 cases (67.27%). In 20 of these cases, the PE was identified as an exudate (12,19,21-25,28-30,32,37,39-45). In an additional 15 cases, the PE was also reported as an exudate (46,47,49-52,54,56). A transudate was identified in two cases (34,57). Values for the PF/serum (PF/S) protein ratio, PF lactate dehydrogenase (LDH), and PF/S LDH ratio were suggestive of a transudate in 10.5% (2/19) (43,52); 38.2% (13/34) (12,24,25,30,37,40,45,49,51,52,54,56,57); and 11.1% (2/18) (45,52) of cases, respectively (Table 2). Values of adenosine deaminase (ADA) were ≥35 U/L in 66.7% of PEs. Values fell below this cut-off point in only nine cases (12,23-26,45,50,54,56,57). pH value was within the 7.35–7.45 range in only two PEs (41), whereas 38.5% (5/13) had values below the normal range (21,41,52) and 46.2% (6/13) had values above the normal range (12,34,45,52). Glucose values in PF were determined in 24 cases, being <60 mg/dL in only three cases (12.5%) (12,18,21). In two patients, PF was a chylothorax [triglycerides 215 mg/dL (17): right-sided, and 300 mg/dL (45): bilateral, respectively], which could explain the turbidity of the two samples.

PF microbiology and cytology results were documented in 34 and 27 cases, respectively. None of the samples grew pathogens and all cytological studies were negative for malignancy.

A pleural biopsy was performed in 45 cases (78.9%) (12,13,15-20,22-25,27-30,32,33,36-42). Additional cases were also reported with pleural biopsy (43-47,49-52,54-57). The biopsy was consistent with a diagnosis of IgG4-RD in all cases except two (19,41), resulting in a sensitivity of 95.6%.

Treatment of PE involved a chest drainage (6/45; 13.3%) (12,16,43,45), corticosteroids (51/55: 92.7%) or immunosuppressants following treatment with corticosteroids (8/54:14.8%) (21,25,33,38,41,45). Of the four patients who did not receive corticosteroids or immunosuppressants (12,30,33,43) therapy, two underwent a chest drain (12,43). The two cases of chylothorax also received octreotide therapy (17,45). Clinical course was satisfactory in 97.7% of the documented cases (43/44) after adjusting maintenance corticosteroid dose or adding immunosuppressant therapy (wherever necessary). Only a patient died of unknown causes (53).

Discussion

Most of the publications about PE and IgG4-RD were case reports or small case series (one to four cases). Hence, there is paucity of relevant data regarding the clinical signs and symptoms of the disease, the characteristics of PE, clinical course, and the most effective treatments available for the disease. Our systematic review was aimed at filling this gap of knowledge.

IgG4-RD affects three times as many men as women (60) and is more frequent in patients older than 50 years (61). The same findings were made in relation to cases of IgG4-related PE. Most patients were Asian (58.2%); the male/female ratio was 2.9/1; and 85.5% of patients were older than 50 years. IgG4-RD rarely affects only the pleura, which only occurred in 11.4% of cases (12,16,28,44).

PE is generally bilateral or right-sided (81.3%) and small/moderate in size (78.9%). PE is usually a paucicellular exudate, predominantly lymphocytic and protein-discordant. Total protein values in PF are generally higher than LDH values. This finding suggests that PF accumulates as a result of increased capillary permeability or lymphatic dysregulation, rather than to pleural space inflammation.

Determining the cause of PE secondary to IgG4-RD is challenging. In this systematic review, one of the cases had a 10-year history of unilateral PE (53). A review of undiagnosed PEs revealed that a third of these cases were caused by IgG4-RD, as they met the diagnostic criteria for the disease (62,63). Therefore, a thorough understanding of PF biochemistry in IgG4-RD may be useful for establishing PE etiology. In this context, pH and ADA values become relevant. Surprisingly, pH was within normal range in only two cases (15.4%), and a similar percentage of patients had PF acidosis or alkalosis. Discussing the methods used for sample processing is out of the scope of this review; however, for conclusive results to be obtained, it should be ensured that sample collection was performed in optimal conditions, as the pH of the PF is often not measured correctly, which may influence results (64). ADA values in PF were ≥35 U/L in 66.7% of cases, and >25 U/L in 5 cases (18.5%). The ADA enzyme plays a relevant role in T-lymphocyte proliferation and differentiation, having shown a good diagnostic yield for tuberculous pleuritis (65). The finding of elevated ADA values in the presence of a lymphocytic exudate requires a differential diagnosis with tuberculous pleuritis. ADA has two isoenzymes: ADA₁ and ADA₂. Whereas ADA₁ is found in all cells, ADA₂ is only present in monocytes/macrophages and increases when stimulated by living microorganisms inside these immune cells. Therefore, ADA₂ is elevated in tuberculous pleuritis (66). In contrast, IgG4-RD causes and elevation of ADA₁, although this data was only available in a case (52). Further studies are required to confirm this assumption. A negative PF and pleural tissue culture, along with histological findings in the latter will help differentiate these two entities. Whether the two reported cases of chylothorax (17,45) are related to the pathogenesis of the disease or to another cause is unclear and requires further examination. Two large series describe the clinicopathological characteristics of patients with IgG4 with associated pulmonary and pleural disease (21 cases) (58) and pulmonary disease (48 patients) (59). In the former, the pleura was involved in only 5 patients and no mention is made to the presence or not of pleural effusion (58). In the latter, the only data available was a lymphoplasmacytic pleural infiltration without pleural effusion in 9 patients (59).

Histological findings (dense lymphoplasmacytic infiltrates, storiform-type fibrosis and obliterative phlebitis) are not pathognomonic of this entity, as some vasculitis can mimic its characteristics (67-69). Notably, a pleural tissue biopsy will not only be useful to establish a differential diagnosis with tuberculosis, but also to exclude a neoplasm (70). This explains that a pleural biopsy was available in a high proportion of cases (78.9%). Dis-Lopez et al. reported another case of pleural involvement (pulmonary nodules) and pleural histological findings suggestive of IgG4-RD. However, this case was not included in our review since secondary PE was not documented (53). Findings were unspecific in only two cases (19,41). It is worth noting that, in one case, biopsy was performed after one-month corticosteroid therapy (19).

Corticosteroids were most frequently included in the treatment (92.7%). This therapy is recommended for asymptomatic patients, as it induces remission and slows down progression into fibrosis and organ dysfunction (71). However, a standard dose and duration of treatment have not yet been established and are variable. Prednisone or prednisolone are usually used at a maximum dose of 1 mg/kg/day and can be maintained for up to 20 months. Immunosuppressants such as glucocorticoid-sparing agents were used in a small proportion of cases (14.8%) after glucocorticoid therapy had failed or side effects had occurred due to sustained use of glucocorticoids. However, there is no consensus about the most effective immunosuppressant therapy. Treatment choice may include mycophenolate mofetil (21), azathioprine (25,33,41), methotrexate (33) and rituximab (38,45) at variable doses.

Treatment response can be assessed using a responder index (72). However, in the case reports reviewed, improvement was assessed based on the general clinical status of the patient, previous radiological abnormalities, and a reduction in serum IgG4 concentrations. There was high variability in the duration of response monitoring. In some cases, disease improved even when untreated (30,33). Clinical course was benign in 97.7% of cases, and a patient with a 10-year history of PE and cardiac dysfunction died of unknown causes (53).

This review has some limitations. Firstly, the papers reviewed are case reports rather than large case series or comparative studies. This means that the quality of the literature reviewed limits the internal validity, external validity and precision of our conclusions. Additionally, PE secondary to IgG4-RD is approached from different perspectives. While some authors place the focus on the clinical manifestations of the disease, others assess PF biochemistry, the treatments administered and patient response to treatment. Due to the heterogeneity of the evidence provided in the articles, some fail to provide useful information for this review. This may hinder the correct assessment of some characteristics or the evaluation of the efficacy of response to a particular treatment.

Conclusions

The data obtained suggest that patients with IgG4-related PE are usually men older than 50 years with more organs involved, with a small/moderate right-sided or bilateral PE. PF is a lymphocytic exudate without a specific pattern, except for an elevated ADA concentration. Pleural biopsy can be useful for establishing diagnosis. PE generally responds to treatment with corticosteroids combined or not with immunosuppressants. Further prospective studies are needed to gather comprehensive information about the disease, including its physiopathological mechanisms. A better understanding of the disease would facilitate early diagnosis and a more appropriate management, which would prevent irreversible damage to the organs involved.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2192/rc

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2192/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-2024-2192/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.

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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