Comparative diagnostic efficacy of ultrasound-guided, medical thoracoscopic, and blind pleural biopsy in tuberculous pleurisy

Introduction

Tuberculosis (TB) is a significant global public health issue. According to the World Health Organization’s Global Tuberculosis Report 2022, there were 10.6 million new cases of TB worldwide (1). In China and many developing countries, tuberculous pleurisy accounts for 6.5% to 8.7% of all TB cases (2). Tuberculous pleurisy is an inflammatory disease caused by direct infection with Mycobacterium tuberculosis (MTB) and/or type IV hypersensitivity of the pleura to tuberculosis components. It is characterized pathologically by increased permeability of pleural capillaries and fibrin exudation (3). Notably, the MTB culture of pleural fluid (PF) is positive in only about 30–50% of patients (4). Untreated cases can lead to pleural thickening, adhesions, and even encapsulation, ultimately resulting in severe ventilatory dysfunction and pulmonary impairment (5,6). The irreversible nature of this pathologic process highlights the clinical urgency for early and accurate diagnosis.

The current diagnostic gold standard relies on the acquisition of pathogenic evidence from PF or tissue. However, traditional testing techniques face significant challenges: the positive rate of acid-fast staining in PF is less than 10%, the sensitivity of liquid culture is only 30–50% (4), and the GeneXpert MTB/rifampicin (RIF) test, which reduces the diagnostic time to 2 hours, has a combined sensitivity of only 16.6% in PF (7). This diagnostic dilemma has prompted the use of invasive pleural biopsy (PB) techniques as an important complementary tool. Currently, three main biopsy modalities are used in clinical practice: blind pleural biopsy (BPB), ultrasound-guided pleural biopsy (USPB), and medical thoracoscopic pleural biopsy (MTPB), each with significant heterogeneity in their technical characteristics and clinical applications.

BPB, a traditional procedure, is conducted under the guidance of body surface anatomical landmarks using Cope or Abrams puncture needles. It offers the benefits of minimal equipment requirements and low cost. However, studies have indicated significant fluctuations in its diagnostic sensitivity, which may be attributed to operator experience dependence and the challenge of circumventing the heterogeneity of pleural lesion distribution (8,9). USPB facilitates targeted biopsies through real-time ultrasound imaging, accurately locating areas of pleural thickening and distinguishing intercostal blood vessels and their positions within specific rib spaces via color Doppler assessment. This technique aids the operator in selecting the safest location for subsequent pleural interventions, thereby minimizing the risk of vascular injury (10,11). Notably, USPB can be performed at the bedside, which is particularly valuable for hemodynamically unstable patients. However, the need for respiratory cooperation restricts its application in severely dyspneic populations. MTPB, as a visual diagnostic technique, allows for high-precision targeted biopsies through direct pleural cavity observation. Several studies have confirmed its diagnostic sensitivity of 93–100% for tuberculous pleurisy and the capability to synchronize pleurodesis (12-14). Nevertheless, some patients are too frail to endure MTPB, and certain studies have reported a higher incidence of postoperative complications compared to BPB and USPB (15,16).

While the effectiveness of individual techniques or pairs of techniques has been investigated in existing research, significant limitations persist in the comparative studies of three types of biopsy modalities. Firstly, most single-center retrospective studies have not effectively controlled for confounding factors such as the degree of pleural thickening and PF adenosine deaminase (ADA) (15,17,18). Secondly, these studies indicate a significant clinical bias in the selection of different biopsy modalities, with preferences such as MTPB being favored for complex pleural effusions (19). Additionally, there is a lack of a multidimensional efficacy evaluation system based on uniform diagnostic criteria. To address these methodological deficiencies, our study innovatively employed the PSM model to conduct the first-ever homogeneous comparison of three types of PB techniques by quantitatively balancing the baseline characteristics of patients. Through a systematic evaluation of diagnostic sensitivity, specificity, predictive value, and complications, our aim was to construct a PB pathway optimization scheme supported by evidence-based medicine, and to provide data that will aid in individualized decision-making across various clinical scenarios. We present this article in accordance with the STARD reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1033/rc).

Methods

Study design

The study design comprised patients with tuberculous pleurisy, treated from January 2014 to April 2024 at Chongqing University Fuling Hospital. Tuberculous pleurisy was initially suspected in patients with the following PF characteristics (20): observed on chest radiography/computed tomography; high in ADA, lymphocyte-rich, straw-colored, and no malignant cells. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Ethics Committee of Chongqing University Fuling Hospital (No. 2022CQSFLZXYYEC-09). As this was a retrospective study, written consent was not feasible at the time of initial data collection. However, all patients were contacted during the follow-up period, and verbal informed consent was explicitly obtained from each of them.

Study population

The term “tuberculous pleurisy” was used to search for data in the Lianzhong electronic medical record database, including the patients’ progress at outpatient follow-ups. Further data regarding patients’ current status was collected via telephone interview. The records of 510 patients were initially reviewed.

For inclusion in this study, patients were older than 18 years, had undergone biopsy via USPB, BPB, or MTPB, and had received standard anti-tuberculosis therapy. Patients with any of the following were excluded: PF due to heart failure, cirrhosis, hypoproteinemia, pleural tumors, or other causes; experimental anti-tuberculosis treatment without PB; follow-up less than 12 months; lost to follow-up; or lack of laboratory data. Finally, 333 patients were enrolled, and the patients were categorized by the method of biopsy, USPB, BPB, or MTPB, with 97, 84, and 152 patients, respectively (Figure 1).

Figure 1 Flowchart of the patient inclusion and exclusion. BPB, blind pleural biopsy; MTPB, medical thoracoscopic pleural biopsy; USPB, ultrasound-guided blind pleural biopsy.

Biopsy protocol

USPB: patients positioned laterally/sitting. Thickened pleural areas identified via ultrasound. Sterile 18G Tru-Cut needle (Bard-Magnum, Covington, GA, USA) inserted under real-time guidance; 2–4 specimens collected. MTPB: lateral position with sedation. 15mm incision made, trocar inserted. Olympus-290 scope visualized lesions (Olympus, Tokyo, Japan); biopsies taken using MTN biopsy forceps (Micro-Tech, Nanjing, China). Closed drainage tube placed post-procedure. BPB: seated position with 18G Abrams’s needle (Weigao, Weihai, China). Vertical insertion at ultrasonic-marked site. Specimens collected at 3/6/9 o’clock positions. All methods followed standard disinfection, local anesthesia (2% lidocaine), and specimen fixation protocols.

Data collection

Patient demographic and baseline data were retrieved from electronic medical record system, including gender, age, body mass index (BMI), tuberculosis history, serum albumin, erythrocyte sedimentation rate (ESR), tuberculosis antibody (TB-Ab), pleural thickness, PF/serum carcinoembryonic antigen (CEA), PF white blood cell (WBC), PF lymphocytes, PF lactate dehydrogenase (LDH), PF ADA, pleural/serum protein ratio, PF with septations, ultrasound depth of PF, and comorbidities. Comorbidities included pneumoconiosis, diabetes mellitus (DM), hypertension, coronary heart disease (CHD), hepatitis B virus (HBV), tumor, human immunodeficiency virus (HIV) infection, and connective tissue disorder (CTD). Data concerning post-procedural complications were collected, including reflex vagotonia, pain, subcutaneous emphysema, subcutaneous hematoma, pneumothorax, air embolism, hemothorax, and wound infection. Reflex vagotonia consisted of a series of adverse reactions such as dizziness, chest tightness, pallor, sweating, and even fainting during the puncture. We routinely used pain questionnaires, combined with patient progress records and analgesic medication use. For subcutaneous emphysema, we used a combination of physical examination and chest imaging. Detailed checks and reviews were conducted by two people throughout the data collection process.

Case definition for tuberculous pleuritis

All tissue specimens were placed on filter paper, fixed with 10% formaldehyde, and sent for histopathological examination. The diagnostic criteria for tuberculous pleurisy were the presence of tuberculous granulomas (with or without caseation) or a positive acid-fast bacilli (AFB) test after excluding other granulomatous diseases (21). For patients without typical tuberculous pathologic changes, tuberculous pleurisy might also be considered based on patient history, clinical presentation, chest radiography, PF ADA, thoracentesis findings after ruling out malignancy and other pleural diseases, and effective anti-tuberculosis treatment.

Statistical analysis

PSM analysis with a multivariable logistic regression model was performed for matching the following factors: gender, age, BMI, tuberculosis history, serum albumin, ESR, TB-Ab, pleural thickness, PF/serum CEA, PF WBC, PF lymphocytes, PF LDH, PF ADA, pleural/serum protein ratio, PF with septations, ultrasound depth of PF, and comorbidities. Matched pairs of patients between the USPB and BPB, USPB and MTPB, and MTPB and BPB groups were derived using a 1:1 greedy nearest neighbor matching within a propensity score of 0.02. In the USPB and BPB, USPB and MTPB, and MTPB and BPB groups, there were 60, 77, and 78 matched patient pairs, respectively.

Categorical variables were shown as percentages, and continuous variables as mean ± standard deviation (SD). The distributions of variables were assessed with the Kolmogorov-Smirnov test. Chi-squared or McNemar tests were used to compare categorical variables. Continuous variables were compared by paired Student’s t-test or Mann-Whitney U test. SPSS version 26 for Windows (SPSS, Chicago, IL, USA) was applied for data analyses. P<0.05 was considered statistically significant.

Results

Baseline characteristics before and after PSM

As shown in Table 1, prior to PSM, significant differences were observed between the USPB and BPB groups in baseline characteristics, including ESR, TB-Ab, pleural thickness, PF ADA, PF separation, and PF LDH. After PSM, all variables were balanced between the two groups (60 matched pairs), with no statistically significant differences (all P>0.05).

As shown in Table 2, before PSM, the USPB and MTPB groups exhibited significant disparities in age, serum albumin, PF ADA, PF LDH, PF/serum protein ratio, and HBV prevalence. Following the PSM (77 matched pairs), these differences were eliminated (all P>0.05), confirming successful covariate balancing.

As shown in Table 3, pre-PSM analysis revealed significant differences between BPB and MTPB groups in age, ESR, TB-Ab, pleural thickness, HBV, and diabetes prevalence. After PSM (78 matched pairs), all baseline variables were balanced, with no statistically significant differences (all P>0.05).

PSM effectively balanced baseline characteristics across all pairwise comparisons (standardized differences <10%), and eliminated confounding factors such as age, comorbidities, and laboratory markers. This methodological rigor ensured a reliable foundation for subsequent analyses of diagnostic performance and complications.

Diagnostic performance based on pathological manifestations and complications after PSM

As indicated in Tables 4,5, following PSM, the USPB demonstrated a sensitivity of 80.0% (24 true positives, 6 false negatives) compared to 50.0% (15 true positives, 15 false negatives) for the BPB (P=0.01). Both techniques exhibited identical specificity at 80.0% (24 true negatives, 6 false positives for USPB; 24 true negatives, 6 false positives for BPB). The PPV was higher for the USPB compared to the BPB (80.0% vs. 71.4%, P=0.48). Similarly, the NPV was also higher for the USPB compared to the BPB (80.0% vs. 61.5%, P=0.10). However, neither PPV nor NPV achieved statistical significance. Additionally, complication rates were comparable between USPB and BPB. Pain (16.7% vs. 20.0%, P=0.67) and subcutaneous hematoma (8.3% vs. 10.0%, P=0.76) were the most common adverse events. No significant differences were observed in other complications.

As shown in Tables 4,6, the MTPB exhibited superior sensitivity of 90.0% (45 true positives, 5 false negatives) compared to 70% for USPB (P=0.01). Specificity was equivalent between the two methods (81.5%, 22 true negatives, 5 false positives). The PPV was higher for the MTPB compared to the USPB (90.0% vs. 87.5%, P=0.70), while the NPV was significantly higher for MTPB compared to the USPB (81.5% vs. 59.5%, P=0.06). Similarly, neither PPV nor NPV achieved statistical significance. At the same time, MTPB had marginally higher rates of pneumothorax (3.9% vs. 2.6%, P=0.65) and reflex vagotonia (5.2% vs. 3.9%, P=0.70), though these differences were not statistically significant.

As shown in Tables 4,7, MTPB (34 true positives, 6 false negatives) outperformed BPB (16 true positives, 24 false negatives) in sensitivity (85.0% vs. 40.0%, P<0.001). Specificity was similar between the groups (BPB: 78.9%, 30 true negatives, 8 false positives; MTPB: 78.9%, 30 true negatives, 8 false positives). MTPB also demonstrated a significantly higher NPV compared to BPB (83.3% vs. 55.6%, P=0.006), while the PPV showed no statistical difference (81.0% vs. 66.7%, P>0.99). In the process, BPB showed a slightly higher incidence of wound infection (3.8% vs. 2.6%, P=0.66) and hemothorax (2.6% vs. 1.3%, P=0.56), but no statistically significant disparities were noted.

The data presented above indicated that post-PSM pathological analysis confirmed MTPB as the method with the highest diagnostic sensitivity and NPV for tuberculous pleurisy, which made it the most reliable for minimizing false-negative outcomes. USPB offered moderate diagnostic accuracy, whereas BPB, despite being less invasive, carried a significantly higher risk of missed diagnoses, thus requiring careful clinical application. More importantly, the complication rates among the three methods are similar, with no significant differences in major adverse events.

Discussion

In this study, the diagnostic efficacy and safety of BPB, USPB, and MTPB in tuberculous pleurisy were systematically compared for the first time using PSM modeling. The results indicated that MTPB had significantly better sensitivity and NPV than USPB and BPB, whereas the sensitivity of USPB and BPB was in descending order. The specificity and PPV were not statistically different among the three methods, and neither were the complication rates.

The high diagnostic sensitivity of MTPB was inseparable from its operational visualization mode. By directly visualizing the pleural cavity and targeting lesion tissue, MTPB overcame sampling bias caused by the heterogeneity of pleural lesion distribution, significantly reducing sampling error. This advantage was validated in several studies: for instance, a prospective study by Sobhy et al. demonstrated that the sensitivity of MTPB for tuberculous pleurisy was as high as 94%, significantly better than USPB (77.78%, P<0.05). The difference was mainly attributed to MTPB’s ability to accurately identify focal lesions (15). Similarly, Behera et al. found that the sensitivity of MTPB was significantly higher than BPB (86.2% vs. 62.1%, P=0.003) in a cohort study of patients with complex pleural effusions, aligning with the results of this study (18). This sensitivity advantage is reflected not only in diagnostic efficacy but may also be related to the synergistic effect of its therapeutic function. MTPB can be synchronized with pleurodesis for effective separation of adhesions and drainage of encapsulated effusions, leading to improved visualization and an increased biopsy detection rate. For example, Ledwani et al. reported that MTPB combined with pleurodesis increased the diagnostic yield of complex pleural effusions while reducing the need for subsequent thoracic drainage (19). Therefore, MTPB is not only a highly sensitive diagnostic tool but also an integrated diagnostic and therapeutic protocol applicable to cases with extensive pleural thickening or fibrosis.

USPB, partially visualized through real-time imaging, has a diagnostic sensitivity lower than MTPB but significantly higher than BPB. It is reasonable to infer that this advantage primarily comes from the ultrasound-guided precise localization of pleural thickening areas and the technological capability of color Doppler imaging to bypass intercostal vessels, thereby reducing the risk of complications such as vascular injury (10,11). Nonetheless, there is a debate among existing studies on whether pleural thickening affects the diagnostic sensitivity of USPB. For instance, Zhang et al. found that the sensitivity of USPB was significantly higher when pleural thickness was ≥3 mm (85.2% vs. 61%, P=0.001), indicating that anatomical features might influence sampling efficacy (22). However, Zhou et al. suggested in a prospective randomized controlled trial that the difference in sensitivity between USPB and MTPB was not related to pleural thickness but depended more on the operator’s ability to target the lesion area (23). In this study, after balancing the baseline characteristics of the patients through PSM, there was no statistically significant difference in pleural thickness between the groups (P>0.05), and the results of the sensitivity comparison between USPB and MTPB did not show an independent effect of pleural thickness. This finding aligns with Zhou et al.’s suggestion. However, it should be noted that while the PSM model is effective in controlling confounding factors, it may limit the detection of subtle differences due to reduced sample size. Therefore, the association between pleural thickness and diagnostic sensitivity requires further validation through multicenter large-sample studies in the future, particularly subgroup analyses with different thickening thresholds (e.g., <3 vs. ≥3 mm).

Compared to the other two assays, the sensitivity of BPB was significantly lower, falling below the previously reported range of 68–80% (24,25). This phenomenon was considered to be related to operator’s experience, needle type, and sample size differences (26). Additionally, this study observed that BPB had the lowest NPV, ranging from 55.6–61.5%, indicating a high level of uncertainty in its negative results. This uncertainty may be associated with the localized distribution of pleural lesions or insufficient sampling depth. Consequently, in clinical practice, it is recommended to combine negative BPB results with ADA testing in PF, GeneXpert MTB molecular diagnostics, or serum γ-interferon release assay (IGRA) to enhance overall diagnostic accuracy. For instance, Du et al. suggested that Xpert analysis of PB specimens could provide an accurate diagnosis of pleural tuberculosis in patients with negative AFB smears, with a sensitivity of up to 85.5% (27). This strategy is particularly applicable in scenarios where MTB culture is not accessible.

Previous studies have indicated that major complications of MTPB encompass subcutaneous emphysema, hemorrhage, medical pneumothorax, and respiratory failure (28,29), while pneumothorax and hemothorax are predominantly associated with BPB (30). However, this study found no statistically significant difference in the overall complication rates among the MTPB, USPB, and BPB groups (P>0.05), with pain (15.4–20.0%) and subcutaneous hematoma (6.4–10.0%) being the most frequently reported adverse events. Notably, the incidence of pneumothorax in MTPB (3.8–5.1%) was marginally higher than that in USPB (2.6–5.0%) and BPB (3.3–5.1%), but the difference was not statistically significant (P>0.5). This could be due to the necessity of creating an artificial pneumothorax to enhance the field of view during MTPB (31). The complication profile in this study differed slightly from previous reports (e.g., respiratory failure was not observed), and this variance may be attributed to several factors: firstly, operator’s experience is crucial in complication prevention, and standardization of the procedure by experienced operators could decrease the risk of vascular injury and pneumothorax (32); secondly, the relatively small sample size of the present study (60–78 cases post PSM) could influence the detection rate of rare complications (e.g., respiratory failure); additionally, the heterogeneity of the included patients (e.g., differences in comorbidities, pain tolerance) could also result in biased outcomes. For instance, Ma et al. (33) identified chronic obstructive pulmonary disease as an independent risk factor for post-thoracoscopic pneumothorax through a retrospective analysis [odds ratio (OR) =9.023, P=0.003], and the lower prevalence of such patients in our study might have obscured this association. Future multicenter, large-scale studies are required to further validate the independent effects of different techniques on complication risk and to develop a risk stratification model based on patient characteristics.

Admittedly, this study employed a single-center retrospective design, and while PSM was used to balance baseline characteristics, uncontrolled confounders, such as differences in operator experience, may still exist. Furthermore, the small sample size, ranging from 60 to 78 paired samples post-PSM, could have impacted the statistical validity. Future research should involve multicenter prospective studies to further validate these findings. Additionally, future prospective studies could systematically incorporate these variables (e.g., PF ADA, WBC, lymphocytes, LDH, and ultrasound characteristics) to develop predictive models. Finally, the exploration of combining novel molecular testing techniques, like macro-genome sequencing, with biopsy techniques could enhance diagnostic efficiency.

Conclusions

In summary, our findings suggested that MTPB could be the diagnostic tool of choice for patients with a high suspicion of tuberculous pleurisy; USPB could serve as an alternative when conditions are limited; and BPB remains a viable option in areas with limited access to advanced techniques like thoracoscopy or ultrasound. The safety profiles of the three methods are comparable, and clinical selection should consider equipment conditions, operator experience, and individualized patient needs.

Acknowledgments

We sincerely appreciate Med Jaden Inc. for editing the English language quality and style of this manuscript.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1033/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1033/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1033/prf

Funding: This work was supported by the Chongqing 2023 Public Health Key Specialty (Discipline) Construction Project.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-1033/coif). All authors report that this work was supported by the Chongqing 2023 Public Health Key Specialty (Discipline) Construction Project. The authors have no other 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 and its subsequent amendments. The study was approved by the Ethics Committee of Chongqing University Fuling Hospital (No. 2022CQSFLZXYYEC-09). As this was a retrospective study, written consent was not feasible at the time of initial data collection. However, all patients were contacted during the follow-up period, and verbal informed consent was explicitly obtained from each of them.

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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