Efficacy and safety of pleurodesis for lung cancer patients with interstitial lung disease
Highlight box
Key findings
• Pleurodesis using talc or minocycline might be the treatment option against malignant pleural effusion (MPE) secondary to lung cancer with interstitial lung disease (ILD).
What is known and what is new?
• The efficacy rate of pleurodesis with talc and minocycline is about 70%. Acute respiratory distress syndrome (ARDS) after pleurodesis with talc is a concern. The partially expanded lung before pleurodesis is known as the predictor of pleurodesis failure. The efficacy and safety of pleurodesis against MPE complicated with ILD have not been elucidated.
• In this study, excluding the cases of partially expanded lung, the efficacy rate of pleurodesis against MPE complicated with ILD was comparable to that of previous reports. Presenting ground glass opacity and consolidation treated with systemic prednisolone within 6 months before pleurodesis might be the risk factor for developing ARDS.
What is the implication, and what should change now?
• Pleurodesis against MPE might be the therapeutic option for patients complicated with ILD. However, two cases of ARDS were observed in the patients administered systemic prednisolone against ILD within 6 months before pleurodesis. The clinicians should carefully consider the indication for pleurodesis.
Introduction
Approximately 40% of malignant pleural effusion (MPE) cases are associated with lung cancer and cause various symptoms, including dyspnea, cough, and chest pain (1-3). These symptoms impair quality of life and performance status (PS); thus, physicians must manage MPE to alleviate symptoms and prevent re-accumulation of pleural effusion Sterilized graded talc is widely used as a sclerosant for pleurodesis, with a 30-day efficacy rate >70% (4-6). A meta-analysis revealed that talc has a higher efficacy than other agents (e.g., bleomycin and doxycycline), and is linked to a lower incidence of fever and procedure-related pain (2). Talc is effective and safe compared with other sclerosants; however, the development of acute respiratory distress syndrome (ARDS) as a result of talc use is a concern (7).
Interstitial lung disease (ILD) is a common comorbidity of lung cancer (8). The prevalence of lung cancer in patients with idiopathic pulmonary fibrosis (IPF) is approximately 14% (9). In addition, patients often develop treatment-related pneumonitis, and approximately 10–20% of ILD cases are complicated with lung cancer (10,11). Maintaining PS and preventing iatrogenic acute exacerbation of ILD has been the focus of clinical treatment of lung cancer patients with ILD. Previous research suggested that the presence of ILD is a risk factor for developing ARDS (12). However, to the best of our knowledge, no study has evaluated the efficacy and safety of pleurodesis exclusively in lung cancer patients with ILD. The objective of the present study was to investigate the efficacy and safety of pleurodesis in this population. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1541/rc).
Methods
Patients and evaluation of the efficacy of pleurodesis
This was a single-center retrospective study including lung cancer patients with ILD who developed MPE. The patients received treatment at Nippon Medical School Hospital (Tokyo, Japan) between January 2010 and December 2022. In our facility, talc and minocycline were mainly selected for the treatment of those patients. Patients who underwent pleurodesis were assigned to the sclerosant groups. The diagnosis of ILD was reached based on the medical record and radiological images. We reviewed the latest chest computed tomography (CT) images before pleural effusion accumulation and the clinical history of each patient. We also referred to previous studies on ILD complicated with lung cancer, and categorized patients into two patterns based on chest CT features (13-15). According to the American Thoracic Society/European Respiratory Society/Japanese Respiratory Society/Latin American Thoracic Society clinical practice guideline for IPF, the usual interstitial pneumonia (UIP) and probable UIP patterns on chest CT exhibited a similar clinical course (16). We categorized the patients into those who presented UIP or probable UIP patterns, and those who did not. We also categorized ILDs into idiopathic interstitial pneumonia (IIP), connective tissue disease-associated interstitial lung disease (CTD-ILD), and drug-induced interstitial lung disease (DIILD) or radiation-induced lung injury (RILI) based on the medical history (17,18).
To assess the re-accumulation of pleural effusion, we compared the chest radiograph captured at 1 month after pleurodesis with that captured following chest drain tube removal. Based on a previous phase 2 study which evaluated the efficacy of sterilized graded talc in Japan, effective and ineffective cases were defined by a rate of pleural effusion re-accumulation <10% and ≥10%, respectively, in the hemithorax after chest drain tube removal (19). Cases in which the drain tube could not be removed, a reduction in pleural effusion was not observed, or repeated thoracentesis was required within a month were defined as failures. The safety evaluation was performed using the Common Terminology Criteria for Adverse Events version 5.0 criteria (20). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee of Nippon Medical School Hospital (approval number: B-2022-536) and individual consent for this retrospective analysis was waived.
Procedure of pleurodesis
For the treatment, a solution of 1% lidocaine (10 mL) with 0.9% sterilized saline (20 mL) was instilled into the chest cavity through the drain tube before administering the sclerosant. Subsequently, a solution of sterilized graded talc (4 g) (Unitalc®; Noblepharma, Tokyo, Japan), which corresponds to Steritalc® (Novatech, La Ciotat, France), or minocycline (200 mg) (Nichi-Iko, Toyama, Japan) with 0.9% sterilized saline (50 mL) was instilled. The drain tube was clamped for 2 hours. Rotation of the body and thoracic suction in patients were performed at the discretion of the physician.
Statistical analysis
The Mann-Whitney U test, Fisher’s exact test, and Student’s t-test were used to analyze the categorical variables in each group. We determined the efficacy rate, and pleural progression-free survival (PPFS). PPFS was estimated with the Kaplan-Meier method. The odds ratio was calculated through logistic regression analysis to identify factors responsible for failure of pleurodesis. Data analysis was performed with the IBM SPSS Statistics program (version 28.0.1.0; IBM, Armonk, NY, USA).
Results
Patient characteristics and pleurodesis agents
Of those, 26 patients underwent pleurodesis. Fourteen and 12 patients received talc and minocycline. Three patients in the minocycline group received a double dose. In each group, no additional other sclerosants, including OK-432 (picibanil), were used after the initial pleurodesis. The median follow-up duration was 3.4 months (range, 0.2–73.1 months). The characteristics of patients who underwent pleurodesis with talc and minocycline are shown in Table 1. The median age and the proportions of females, and never smokers were significantly higher in the talc group versus the minocycline group. Notably, DIILD and RILI were more frequent in the talc group compared with the minocycline group (71.4% vs. 8.3%, P=0.002, respectively). In contrast, IIP was more frequent in the minocycline group (14.3% vs. 83.3%, P=0.001, respectively). In addition, more cases of UIP or probable UIP pattern were observed in the minocycline group (7.1% vs. 41.7%, P=0.07, respectively). One patient in the minocycline group received pirfenidone; nintedanib was not administered to any of the patients in either group. The proportion of poor PS, use of immunosuppressants, and lung expansion before pleurodesis did not differ significantly between the two groups. There were also no significantly differences in C-reactive protein (CRP), lactate dehydrogenase (LDH) and Krebs von den Lungen-6 (KL-6) values between groups.
Table 1
| Characteristics | Talc group (n=14) | Minocycline group (n=12) | P value |
|---|---|---|---|
| Age (years) | 72.0 [45–84] | 66.0 [51–77] | 0.04 |
| >75 years | 6 (42.9) | 1 (8.3) | 0.06 |
| Sex | |||
| Male | 9 (64.3) | 12 (100.0) | |
| Female | 5 (35.7) | 0 | 0.04 |
| Smoking | |||
| Ever | 9 (64.3) | 12 (100.0) | |
| Never | 5 (35.7) | 0 | 0.04 |
| PS | |||
| 0–1 | 10 (71.4) | 6 (50.0) | |
| >2 | 4 (28.6) | 6 (50.0) | 0.42 |
| Histology | |||
| LUAD | 10 (71.4) | 6 (50.0) | |
| LUSC | 2 (14.3) | 4 (33.3) | |
| SCLC | 1 (7.1) | 2 (16.7) | |
| Other | 1 (7.1) | 0 | 0.41 |
| ILD | |||
| IIP | 2 (14.3) | 10 (83.3) | 0.001 |
| CTD-ILD | 2 (14.3) | 1 (8.3) | >0.99 |
| DIILD or RILI | 10 (71.4) | 1 (8.3) | 0.002 |
| CT scan patterns | |||
| UIP or probable UIP | 1 (7.1) | 5 (41.7) | 0.07 |
| Presenting GGO and consolidation treated with prednisolone | |||
| Within 6 months before pleurodesis | 3 (21.4) | 2 (16.7) | >0.99 |
| Use of immunosuppressants during pleurodesis | |||
| Prednisolone | 2 (14.3) | 3 (25.0) | 0.64 |
| Other | 2 (14.3) | 1 (8.3) | >0.99 |
| Antifibrotic agent | |||
| Pirfenidone | 0 | 1 (8.3) | 0.46 |
| Lung expansion before pleurodesis | |||
| Partially expanded | 5 (35.7) | 5 (41.7) | >0.99 |
| LDH (U/L) | 204 [137–1,219] | 208 [122–412] | 0.63 |
| CRP (mg/dL) | 2.25 [0.07–11.79] | 4.25 [0.76–12.6] | 0.35 |
| KL-6 (U/mL) | 553 [239–2,903] | 570 [280–3,515] | 0.53 |
| No KL-6 data available | 2 (14.3) | 1 (8.3) | |
Data are presented as median [range] or n (%). PS, performance status; LUAD, lung adenocarcinoma; LUSC, lung squamous cell carcinoma; SCLC, small cell lung cancer; ILD, interstitial lung disease; IIP, idiopathic interstitial pneumonia; CTD-ILD, connective tissue disease-associated interstitial lung disease; DIILD, drug-induced interstitial lung disease; RILI, radiation-induced lung injury; CT, computed tomography; UIP, usual interstitial pneumonia; GGO, ground glass opacity; LDH, lactate dehydrogenase; CRP, C-reactive protein; KL-6, Krebs von den Lungen-6.
Efficacy of each pleurodesis agent
The efficacy rate (Table 2) in one month was 64.3% for the talc group and 50.0% for the minocycline group. The odds ratio (Table 3) showed that the presence of a partially expanded lung before pleurodesis was an independent predictive factor for failure of pleurodesis [odds ratio: 7.00, 95% confidence interval (CI): 1.20–40.83, P=0.04]. UIP or probable UIP pattern on chest CT and using prednisolone were not statistically significant factors. Thus, we performed an analysis after excluding patients who did have partially expanded lungs before pleurodesis. The efficacy rate was 7 out of 9 (77.8%) and 5 out of 7 (71.4%) in the talc and minocycline. In the talc group, 9 out of 14 patients were available for follow-up at 3 months, and 6 (42.9%) of these patients showed no pleural effusion exacerbations. In the minocycline group, 5 out of 12 patients were available for follow-up at 3 months, and 2 (16.7%) of these patients showed no pleural effusion exacerbations. PPFS (Figure S1) was 64 days for the talc group and 22 days for the minocycline group.
Table 2
| Effectiveness | Talc group (n=14) | Minocycline group (n=12) | P value |
|---|---|---|---|
| Effectiveness of pleurodesis for all patients | 9 (64.3) | 6 (50.0) | 0.69 |
| Effectiveness of pleurodesis after the exclusion of patients with partially expanding lung | 7/9 (77.8) | 5/7 (71.4) | >0.99 |
Data are presented as n (%).
Table 3
| Variables | Univariate analysis | ||
|---|---|---|---|
| Odds ratio | 95% CI | P value | |
| Age >75 years | 2.29 | 0.39–13.33 | 0.41 |
| Male | 1.13 | 0.15–8.21 | >0.99 |
| Smoking history | 1.13 | 0.15–8.21 | >0.99 |
| PS >2 | 3.30 | 0.64–17.16 | 0.23 |
| IIP | 1.80 | 0.37–8.62 | 0.69 |
| CTD-ILD | 0.65 | 0.051–8.23 | >0.99 |
| DIILD or RILI | 0.65 | 0.13–3.21 | 0.70 |
| UIP or probable UIP pattern | 3.00 | 0.48–18.93 | 0.20 |
| Using prednisolone during pleurodesis | 8.00 | 0.75–85.73 | 0.13 |
| Talc pleurodesis | 0.56 | 0.12–2.68 | 0.69 |
| Partially expanded lung | 7.00 | 1.20–40.83 | 0.04 |
PS, performance status; IIP, idiopathic interstitial pneumonia; CTD-ILD, connective tissue disease-associated interstitial lung disease; DIILD, drug-induced interstitial lung disease; RILI, radiation-induced lung injury; UIP, usual interstitial pneumonia.
Safety of each pleurodesis agent
Analysis of adverse events (Table 4) showed that the incidence of fever and pain did not differ between the talc and minocycline groups (fever: 21.4% vs. 8.3% P=0.60, pain: 42.9% vs. 33.3% P=0.70). One case of grade 5 ARDS was observed in each group within 7 days after pleurodesis. The comparison of patient characteristics between those who developed ARDS and those who did not is provided in Table S1. All patients who had developed ARDS had a history of systemic prednisolone therapy within the 6 months before pleurodesis. The individual patient data who developed ARDS were described in Table S2.
Table 4
| Adverse events | Talc group (n=14) |
Minocycline group (n=12) | P value |
|---|---|---|---|
| Fever | 3 (21.4) | 1 (8.3) | 0.60 |
| Pain | 6 (42.9) | 4 (33.3) | 0.70 |
| ARDS | 1 (7.1) | 1 (8.3) | >0.99 |
Data are presented as n (%). ARDS, acute respiratory distress syndrome.
Discussion
In this retrospective study, we analyzed the efficacy and safety of pleurodesis in MPE patients secondary to lung cancer with ILD. This is the first investigation to evaluate pleurodesis in this patient population. In our facility, talc and minocycline are the main sclerosants used for pleurodesis among MPE secondary to lung cancer patients with ILD. Talc was used in patients with DIILD and RILI, while minocycline was mainly used in patients with IIPs. Importantly, the presence of a partially expanded lung before pleurodesis was a predictor of failure. The efficacy rate of the patients presented fully expanded lung complicated with ILD was comparable to that of previous reports. Our study suggests that pleurodesis using talc or minocycline is the treatment option against MPE in patients with ILD.
The present study shows that the overall success rate of pleurodesis using talc and minocycline was lower than that reported in previous analyses. Previous studies reported that the 30-day efficacy rate of talc was 71–90% (4,6,19,21). Moreover, it has been reported that the efficacy rate of tetracycline derivatives is approximately 70–90% (22-24). Thus far, only a few studies have evaluated pleurodesis with minocycline, and the latest study reported an efficacy rate of 69% (25). However, after excluding patients who had partially expanded lungs, the efficacy rates in the talc and minocycline groups were 77.8% and 71.4%. These efficacy rates were comparable to those of the previous reports.
Univariate analysis showed that the presence of partially expanded lungs before pleurodesis was a predictor of pleurodesis failure (odds ratio: 7.00, 95% CI: 1.20–40.83, P=0.04). Previous research studies have reported similar findings (26,27). The using systemic glucocorticoids interferes with the inflammatory response, which induces pleural adhesion and leads to pleurodesis failure (27-29). However, the calculated odds ratio of using systemic prednisolone was not significantly high (odds ratio: 8.00, 95% CI: 0.75–85.73, P=0.13), possibly due to the small sample size and the varying doses of prednisolone used. In addition, UIP or probable UIP pattern on CT was not a significant factor for pleurodesis failure.
No difference was observed between the two groups in the frequency of fever and pain. These adverse events were relatively mild and improved within a few days. In our study, we observed ARDS after pleurodesis with talc and minocycline. The mechanism underlying the occurrence of acute respiratory failure, especially the development of ARDS, is not elucidated. However, these complications may be associated with the migration of sclerosants to the systemic circulation and intense inflammation in the pleural space (30). Tetracycline and large-particle talc, namely Unitalc® (Nobelpharma), were used into this study for pleurodesis. Large-particle talc causes less systemic inflammatory response and hypoxemia compared with small-particle-size talc (31,32). Previous large studies using graded talc or minocycline did not report the incidence of ARDS (21,25,33). However, a retrospective study reported several cases of ARDS after pleurodesis with talc, suggesting that interstitial lung abnormalities detected through chest CT were risk factors for ARDS (12). Whereas pleurodesis using minocycline was considered safe, and our study was the first report linking pleurodesis with minocycline to ARDS (34,35). The cases in our study developed ARDS were characterized by presenting ground glass opacity and consolidation within 6 months before pleurodesis, and required systemic prednisolone therapy. Notably, UIP or probable UIP patterns were not observed in these cases. It is considered that unstable clinical conditions such as recent onset ILD presenting ground glass opacities and consolidation required systemic prednisolone to treat might have related to the development of ARDS. The predictive factors responsible for ARDS have not been elucidated. Therefore, further investigations are warranted.
Our study had several limitations. Firstly, this was a single-center retrospective study; thus, there is inevitable bias in the selection of the sclerosant by the attending physician. Secondly, our investigation adopted the evaluation method used in a phase II study conducted in Japan (19). Of note, the methods employed to evaluate the effectiveness of pleurodesis varied between studies. Thus, an exact comparison of the present findings with those of previous studies was difficult. Thirdly, several biases were contained in our study. The retrospective review of medical records and imaging contributed to bias in the diagnosis of ILD. The attending physician decision and the patient’s background biased the sclerosant selection. Fourth, sample sizes of both groups are small. These limited the interpretability of data with regard to the efficacy and safety of pleurodesis in this setting.
In summary, we performed the first retrospective study analyzing pleurodesis using talc or minocycline for lung cancer patients with ILD. The data revealed that the presence of a partially expanded lung before pleurodesis was an independent factor for the failure of pleurodesis. The present study suggests that pleurodesis against MPE secondary to lung cancer complicated with ILD, can be one of the effective treatment options. However, the cases with the novel presenting ground glass opacity and consolidation that required systemic prednisolone therapy within 6 months before pleurodesis might be associated with the development of ARDS. Clinicians should carefully consider the indication of pleurodesis in patients at risk of complications.
Conclusions
The pleurodesis using talc or minocycline in patients with MPE secondary to lung cancer and various types of ILD is considered to be an effective treatment option. However, two cases of ARDS were observed; thus, clinicians should carefully consider the indication for pleurodesis. The prospective studies are required to delineate this further.
Acknowledgments
None.
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1541/rc
Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1541/dss
Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1541/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-24-1541/coif). Akihiko Miyanaga received these horaria from AstraZeneca, Nippon Kayaku, Merck, Kyowa Kirin, and Pfizer. T.T. has received honoraria from AstraZeneca and Chugai Pharmaceutical. Masaru Matsumoto has received honoraria from Astra Zeneca, Chugai Pharmaceutical, Taiho Pharmaceutical, and Ono Pharmaceutical. Kazuo Kasahara has received honoraria from MSD, AstraZeneca, Chugai Pharmaceutical, Bristol-Myers Squib, Taiho Pharmaceutical, Pfizer, Eli Lilly, and Boehringer Ingelheim, and has received consulting fees from Chugai Pharmaceutical, Taiho Pharmaceutical, Eli Lilly, AstraZeneca, and has patents with Boehringer Ingelheim serves on boards for AstraZeneca and Eli Lilly. M.S. had grants or contracts: Taiho Pharmaceutica, Chugai Pharmaceutical, Eli Lilly, Nippon Kayaku, and Kyowa Hakko Kirin, as well as honoraria from AstraZeneca, MSD K.K, Chugai Pharmaceutical, Taiho Pharmaceutical, Eli Lilly, Ono Pharmaceutical, Bristol-Myers Squibb, Nippon Boehringer Ingelheim, Pfizer, Novartis, Takeda Pharmaceutical, Kyowa Hakko Kirin, Nippon Kayaku, Daiichi-Sankyo Company, Merck Biopharma, and Amgen Inc. The other 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). The study was approved by the Ethics Committee of Nippon Medical School Hospital (approval number: B-2022-536) and individual consent for this retrospective analysis was waived.
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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