Complications of pneumothorax in computed tomography-guided transthoracic needle biopsy and prognostic factors: study on patients with tumor-like lung lesions

Introduction

Lung cancer is among the leading causes of global cancer-related deaths (1). Lung cancer is on the rise in Vietnam; however, the majority of cases are detected in advanced stages, resulting in a significant fatality rate (2,3). Early detection and treatment of lung cancer are crucial as they dramatically decrease the associated mortality. However, in the context of the lungs, a lung tumor might present itself in many manifestations. Currently, there have been records of more than 80 different types of lung lesions. These include benign tumors, bronchial cancer, and metastatic cancer spreading from other parts of the body (4).

There are many methods of diagnosing tumor-like lesions, ranging from outdated methods such as sputum cell examination to invasive approaches such as biopsy via bronchoscopy or oesophageal endoscopy, transthoracic biopsy, or even surgical approach via mediastinoscopy and diagnostic thoracotomy (5). The selection of methods depends on the tumor’s location, size, and the medical equipment accessible at the local facilities. Bronchoscopy is typically a safe and preferred procedure, particularly for malignancies located in the central regions. Nevertheless, transthoracic biopsy is a feasible alternative for tumors located at a distance from the central areas or those that are not observable by bronchoscopy (6,7). Transthoracic biopsy, also known as transthoracic sampling or transthoracic needle biopsy, has always been considered a relatively safe approach and has high diagnostic capability (8). Transthoracic biopsies would provide a tissue sample of adequate size that is appropriate for pathological diagnosis. These larger tissue samples, as opposed to those acquired using bronchoscopy, would improve the accuracy and precision of the diagnosis (52–91%) (9,10).

However, this technique would still encounter some complications, such as pneumothorax (26%) and hemorrhage (10%) (11). Pneumothorax is widely reported as the most common complication of transthoracic biopsy. This complication previously is diagnosed using a chest X-ray, but chest CT will be used in some undetermined cases and serves as the gold standard to detect even a small amount of air in the pleural space. In one study, the average time it takes for a pleural drain to complete in 33 patients with pneumothorax from complications of transthoracic biopsy is 3.8 days (1–9 days across all patients) (12).

At the Department of Internal Medicine, Thu Duc City Hospital, bronchoscopy must be the first diagnostic technique performed if there is a possibility of lung tumors. In situations where patients are unable to receive a histopathological diagnosis because no tumor is visible or the biopsy results are negative, it may be considered necessary to perform a transthoracic lung tumor biopsy using a coaxial needle. This decision would be made after carefully evaluating the indications and consultation with experts in challenging cases.

Despite the procedures being initiated and carried out for the past five years, the rates of local problems still need to be discovered. This study attempts to determine the incidence of complications such as pneumothorax, hemoptysis, and air embolism and identify potential predictors of these complications. We present this article in accordance with the STARD reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-955/rc).

Methods

Study population

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Ethics Committee of Thu Duc City Hospital (No. 1455/QD-BV) and individual consent for this retrospective analysis was waived due to the retrospective nature of the study. We conducted a retrospective cohort study on 221 patients with tumor-like lung lesions admitted to the Department of Internal Medicine, Thu Duc City Hospital, Ho Chi Minh City, Vietnam, from January 1st, 2017, to December 30th, 2022. Thu Duc City Hospital is a suburban hospital with a capacity of 600 beds.

Inclusion criteria

• Patients who were diagnosed with tumor-like lung lesions and pleural tumors via computed tomography (CT) scan and were unable to be diagnosed with other histology methods like bronchoscopy, transbronchial aspiration, cell study of bronchial lavage fluid.
• Patients who underwent transthoracic biopsy and consent to the procedure.

Exclusion criteria

• Patients with coagulopathy, specifically patients with a platelet count less than 50 G/L or prothrombin rate less than 50%.
• The lesions had a high-risk possibility of angioma.
• The patient had emphysema or air bubble at the needle insertion site.
• The patients had uncontrolled coughing.
• The patients had undergone pneumonectomy in the opposite lung.
• The patients suffered from severe heart failure, arrhythmia, severe respiratory failure, hemodynamic instability, or assisted mechanical ventilation.
• The patients cannot cooperate with doctors.
• Patients with obstructive lung disease with a forced expiratory volume in 1 second (FEV1) less than 1 liter.
• Patients who cannot lie down.

Term definitions

• Tumor center-chest wall distance: the distance from the chest wall to the center of the tumor (at the section where the tumor is at largest size).
• Tumor-chest wall distance: the distance from the chest wall to the edge of the tumor (at the section where the tumor is at largest size).
• Tumor-skin distance: the distance from the tumor edge to the skin (at the section where the tumor is at the largest size).
• Criteria for malignant diagnosis: sufficient evidence from histopathology to confirm cancer.
• Diagnosis criteria for benign: (I) tuberculosis is confirmed through histology, which shows evidence of a positive response to tuberculosis treatment; (II) indications of benign progression: lesions spontaneously resolve with specific therapies that are not cancer-associated; and (III) evidence from the histology report following the surgical procedure.

Study procedure

All the patients were retrospectively collected as a convenience series. Patients who fulfilled the inclusion criteria and had no exclusion criteria underwent standard diagnostic procedures. In our institution, these criteria were based on the ATS guideline on transthoracic needle biopsy (13). All the patients had a first chest CT to facilitate tumor visualization and localization and determine the best route for bronchoscopy. All the measurements in the “Term definitions” section were done in this CT by radiologists. Bronchoscopy was the primary procedure for all patients. All patients with pulmonary tumor lesions on CT will be indicated for bronchoscopy. Bronchoscopic biopsy procedures include intrabronchial biopsy if tumors are seen, or blind transbronchial biopsy. After bronchoscopy, if no visible lesions that can be biopsied, no sample were collected, or the pathological results after biopsy are not consistent with the clinical presentation, we will conduct a consultation for the indication for transthoracic needle biopsy. The patients and their family received a detailed explanation of the transthoracic biopsy procedure, as well as the potential complications that may happen, such as pneumothorax, chest tube drainage if needed, hemorrhage, hemoptysis, and air embolism. Subsequently, the patients were requested to provide their signature on a written consent form, reaffirming their well-informed decision regarding the procedure. From this, we retrospectively review 221 patients in this study. CT scan was used to assist in performing all the biopsies and to determine post-op complications, such as pneumothorax, which was also confirmed by radiologists (detailed below).

CT-guided transthoracic needle biopsy procedure (14,15):

• All biopsies were performed by using our 32-slide conventional CT machine (Siemens, Erlangen, Germany). Operators (T.B.N. and T.N.A.T.) were both qualified for the procedures. To enable the shortest path for lung biopsy, patients were positioned either prone or supine, depending on the location of the lesion. CT images were acquired from the apex of the lungs to the diaphragm in order to identify the pulmonary lesion at the end of inspiration. The center of the lesion was determined at the CT landmark by placement of a radiopaque skin grid onto the patient’s skin. A second set of CT images were acquired, and the location of the puncture point was identified by measuring the distance between the skin surface and the pleura, the length of the needle path, and the minimum angle formed by the vertical line and the needle. Routine disinfection and draping was carried out after marking the body surface puncture site, with the puncture site positioned at the center. Subsequently, the chest wall was anesthetized layer by layer using 2% lidocaine. After local anesthesia, all biopsies were performed with an 18- or 20-gauge semi-automatic biopsy needle with coaxial (GSN1815/GSN2015, Geotek Medical, Ankara, Turkey; Figure 1). An initial puncture was done without piercing the pleura. After this, CT scans were acquired to locate the exact position of the biopsy needle tip, and biopsies were performed while trying to avoid piercing the ribs, bullae, blood vessels, and fissures. If the lesion was located along the extended path of the needle track, the biopsy procedure was continued; otherwise, the site of puncture point was changed. Prior to rapidly advancing the needle towards the identified lesion, the patient was instructed to hold the breath. Subsequently, a CT scan was done immediately to verify that the needle tip has successfully reached the intended lesion. Then, sampling using the aforementioned semi-automatic biopsy gun was performed. Because our institution were a sub-urban hospital, we did not have Rapid Onsite Evaluation (ROSE) available in our institution, so around 4 to 8 tissue cores were obtained during the biopsy to facilitate further histopathologic diagnosis, molecular and immunohistochemistry analyses. Specimens were immediately immersed in 10% formalin solution and were sent to the pathologist for examination. Routine CT scan was performed right after the procedure to promptly identify any possible complications, such as pneumothorax, hemothorax...

Figure 1 Semi-automatic biopsy needle with coaxial (GSN1815/GSN2015, Geotek Medical, Ankara, Turkey).

Statistical analysis

The data is imported and processed using the STATA 14.0 software, with descriptive statistics for the patients’ baseline characteristics. The chi-squared test was used to determine related factors of pneumothorax complications, with statistical significance P<0.05.

We evaluate the prognosis threshold of pneumothorax complications via the measurement of tumors in patients and distances relative to tumors with the help of the ROC model with sensitivity and specificity as variables. The ROC model got the corresponding coordinates on the horizontal axis as the rate of false positives in the test, the vertical axis as the test sensitivity, and the area under the ROC curve (AUROC curve). The more the curve deviates upward and leftward, the more diagnostically relevant the test result is (16). We would collect the variables with AUROC ≥0.7 and use the sensitivity and specificity coefficient to determine the threshold of pneumothorax complication prediction.

Results

Participants characteristics and complication rate of transthoracic biopsy

Between January 1st, 2017 and December 30th, 2022, a total of 221 patients with lung tumors were indicated for transthoracic biopsy at Thu Duc City Hospital in Vietnam.

Demographic characteristics of the patients included 140 males (63.4%) and 81 females (36.6%) with a mean age of 59.7±11.9 years. The first-attempt sample collection rate is 95%, and 11 patients needed a second attempt at sample collecting (Table 1).

All 221 patients underwent a biopsy with the guidance of a CT scan; the shortest range is right at the chest wall, the longest distance from the chest wall is 63.2 mm, and the average distance recorded is 37.2 mm. Besides that, the average needle insertion range recorded is 57.4±8.8 mm, with the shortest range being 30 mm and the longest being 92.7 mm. The smallest tumor size is 10 mm³, and the biggest recorded is up to 325 mm³ (Table 2).

The study results showed no reported cases of air embolism and revealed that 44 out of 221 patients developed hemoptysis, representing a prevalence of 19.9%. The majority of the cases of hemoptysis resolved spontaneously within 24 hours. Out of 221 patients, 12 (5.4%) developed both hemoptysis and pneumothorax. However, all of these complicated cases gradually resolved on their own after the patients received supplemental oxygen. Out of the total of 221 patients, 61 individuals (27.6%) were detected to have pneumothorax. Among these cases, 4 patients required chest tube drainage (Table 3).

Prognosis factors of CT-guided transthoracic needle biopsy’s complication

The results show the relationship between the distances and complications of pneumothorax. Remarkably, of the 99 patients with chest wall to tumor edge distance equal to or more than 20 mm, the rate of pneumothorax is 51.5%. Meanwhile, in the less-than 20 mm group, that rate is only 8.2% with P<0.001. Similarly, regarding the skin to tumor distance, of the 93 patients in the more-than-40 mm group, the rate of pneumothorax is 54.8%; in the less-than-40 mm group, that rate is only 7.8% with P<0.001.

We also found a correlation between the tumor sizes and the pneumothorax complications, specifically, if patients had tumors with a diameter less than 2 cm, they are proning to post-biopsy pneumothorax, with P=0.04 (Table 4).

The results of multivariate logistic regression analysis in Table 5 showed that the most important prognostic factor of pneumothorax was the skin-tumor edge distance (95% CI Coef: 0.127–0.289; P<0.001). Another factor that was significant in the multivariate model was tumor size (P=0.04). These factors were further analyzed by the Area under the ROC curve to determine a specific cutoff in predicting complications (Table 5).

Figure 2 represents the ROC for chest wall-tumor edge distance, the area under the curve is 0.8414, which reaffirms the reliability of these figures in prognosis for pneumothorax complications.

Figure 2 AUROC curve of chest wall-tumor edge distance in prognosis for pneumothorax complications. ROC, receiver operating characteristic; AUROC, area under the receiver operating characteristic.

Analytical clearance for the cutoff threshold shows that if the chest wall-tumor edge distance exceeds 23 mm, it would have the highest accuracy, 78.18%, and sensitivity and specificity at 72.13% and 80.50%, respectively. Therefore, a distance ≥23 mm is considered the risk threshold for pneumothorax complications (Table 6).

Figure 3 represents the data of ROC for skin-tumor edge distance, the area under the curve is 0.8396 which reaffirms the reliability of these figures in pneumothorax complications prognosis.

Figure 3 AUROC curve of skin-tumor edge distance in prognosis for pneumothorax complications. ROC, receiver operating characteristic; AUROC, area under the receiver operating characteristic.

Analytical clearance for the cutoff threshold shows that if the skin-tumor edge distance is greater than 42 mm, it would have the highest accuracy, at 76.47% and sensitivity and specificity at 78.69% and 75.63% respectively. Therefore, a distance ≥42 mm is considered the risk threshold for pneumothorax complications (Table 7).

Figure 4 represents the data of ROC for skin-chest wall distance; the area under the curve is 0.5011, which shows the low reliability of this prognosis, and it didn’t meet the prognosis standard.

Figure 4 AUROC curve of skin-chest wall distance in prognosis for pneumothorax complications. ROC, receiver operating characteristic; AUROC, area under the receiver operating characteristic.

Figure 5 represents the data of ROC for skin-tumor center distance; the area under the curve is 0.6782, which shows the low reliability of this prognosis, and it didn’t meet the prognosis standard (<0.7).

Figure 5 AUROC curve of skin-tumor center distance in prognosis for pneumothorax complications. ROC, receiver operating characteristic; AUROC, area under the receiver operating characteristic.

Figure 6 represents the data of ROC for chest wall-tumor center distance; the area under the curve is 0.6721, which shows the low reliability of this prognosis, and it didn’t meet the prognosis standard (<0.7).

Figure 6 AUROC curve of wall-tumor center distance in prognosis for pneumothorax complications. ROC, receiver operating characteristic; AUROC, area under the receiver operating characteristic.

Figure 7 represents the data of ROC for tumor size; the area under the curve is 0.3087, which shows the low reliability of this prognosis, and it didn’t meet the prognosis standard (<0.7).

Figure 7 AUROC curve of tumor size distance in prognosis for pneumothorax complications. ROC, receiver operating characteristic; AUROC, area under the receiver operating characteristic.

Discussion

Participants characteristics

The average age of the individuals involved in the study is 59.7 years, within the range observed in previous transthoracic biopsy studies. The male percentage was double that of the female, with statistics of 63.4% and 36.6% respectively. This phenomenon is probably due to the fact that the prevalence of smoking among men is scientifically shown to be higher than that among women, and numerous studies have clearly shown that smoking is one of the primary factors responsible for lung cancers (17).

In our study, 11 participants underwent a second try at collecting samples. The successful first-time sample collection rate is 95%, with 210 out of 221 cases resulting in successful collection. Overall, our sample collection success rate is 100%, higher than the figures found by Harrison [81 out of 89 cases (91%)] (10). Our study’s remarkably high success rate can be attributed to the utilization of CT assistance in virtually all cases, even those involving tumors adjacent to the chest wall, and the excellent collaboration between patients and doctors. Utilizing CT-guided biopsy could significantly enhance the success rate and prevent the need for a second effort. Unsuccessful biopsies can be caused by factors such as patient movement, inability to hold their breath, or poor cooperation due to cognitive loss or senility in older patients (18).

Complication rate of transthoracic biopsy

The incidence of pneumothorax in our study was 27.6%, with the corresponding number being 61 patients, and only 4 (1.9%) necessitated chest drainage. This proportion is lower than the figures shown in a meta-analysis, in which the rates for pneumothorax and chest drainage are 38.8% and 5.7%, respectively (19). Furthermore, our study indicates that patients’ characteristics, such as gender and age, do not pose a risk factor for a higher rate of complications during a biopsy, aligning with the findings of Bozbaş et al. (20) and Tongbai et al. (21). However, Wiener et al. observed that individuals aged 60 to 70 years appear to have a higher likelihood of biopsy complications, contrasting with those above 80 years (22). We did document a correlation between the tumor size and the pneumothorax rate; specifically, the smaller the tumor diameter, the higher the risk of pneumothorax. This finding aligns with Wu et al., who speculates that small lesion size also plays a role in the development of pneumothorax (23).

Approximately 20% of the overall population experiences complications related to hemoptysis, with the majority of cases being mild and self-limited. Previous studies have documented the correlation between pleura-tumor distance and the rate of hemoptysis following a biopsy (24,25). Our research indicates that a small proportion of cases, precisely 22.75%, had a pleura-tumor distance above 2.5 cm. Our investigation did not document any instances of air embolism. Encountering this problem is highly uncommon. Based on medical literature, the incidence of air embolism is approximately 0.2–1% (18,26).

Prognosis factors of CT-guided transthoracic needle biopsy’s complication

One of our new findings is the possible correlation between the incidence of pneumothorax complications and the distance between the tumor and the skin as well as the tumor and the chest, which is consistent with findings from earlier studies that have not yet clearly shown parameters such as sensitivity, specificity, and accuracy of a specific distance cutoff threshold (15,18,27). Additional risk factors for pneumothorax complications, as reported by other authors, include the puncture of needles into interlobar fissures, fibrotic lung areas, or emphysema (15,18). Meanwhile, at some medical centers, there is no statistically significant relationship between the number of biopsies and the rate of complications (26). Wu et al. mentioned that the risk of pneumothorax is higher with increased depth of the lesions from the skin or long needle path (>4 cm), consistent with our above findings (23).

Zhao et al., in a study with a 31.4% pneumothorax rate, by using multivariable logistic regression, found that independent risk factors of pneumothorax include emphysema (P<0.001), no physical contact between lesions, and pleura (P<0.001), prone or side sleeping posture (P=0.002) and the number of needle insertions (P<0.001) (28). The pneumothorax prediction model’s sensitivity, specificity, and accuracy figures are 56.8%, 79.6%, and 72.5%, respectively (28). While clinicians probably can somehow predict the posture and the number of needle insertions beforehand, our study, instead, focuses on the risk factor relating to the determined distance between a tumor and the chest wall, the tumor, and the skin, which can consistently and quickly be determined before the procedure. Both of our ROC curves have good AUC values. The first curve refers to the risk associated with the length of the chest wall tumor. A 23-mm or above length might be considered a significant threshold for pneumothorax complications. Regarding the second distance, which corresponds to the size of the skin tumor, a measurement of 42 mm or greater might indicate the possibility of pneumothorax complications. These two numbers can provide further information about the potential complications of a biopsy.

Various measures, nevertheless, can be adopted to mitigate the development of pneumothorax and minimize the number of pneumothoraces requiring chest tube placement. During and right after the procedure, clinicians should instruct patients not to move, talk rigorously, cough, or breathe deeply. Interlobar fissures should be avoided to reduce the number of pleural punctures. Careful discussion and planning are essential to minimize the traversal of aerated lung tissue without puncturing bullae or pneumatoceles, if feasible (23). In patients at high risk for developing pneumothorax, it may be suggested to use a procedure called needle track obliteration, or “patching”, where 2–3 mL of the patient’s blood is injected during the final withdrawal of the introducer needle (29). The efficacy of this technique remains controversial. Finally, after the biopsy, it is essential to position patients immediately with the puncture site facing downwards once the introducer needle has been removed (30,31). To facilitate the absorption of a pneumothorax, if it occurs, oxygen is delivered via a nasal cannula both during and after the procedure (32).

Our study also found no correlation between tumor sizes and biopsy complications, which aligns with the finding from Polat et al. (33). Remarkably, this study found that the depth of lesion measured from the pleura is 34.62±19.80 mm for patients with chest drainage and 22.81±17.82 mm for those without (P<0.01), which can be postulated that the length from the tumor to the pleura can correlate with severe pneumothorax complications. Polat et al. also conducted ROC analysis to estimate the probability of assisted drainage according to the distance of lesion calculated from the pleura surface. If the length exceeds 24 mm, the sensitivity would be 70.1%, and the specificity would be 64.5% (33). Similarly, our study found that a tumor-chest wall of more than 23 mm can be considered a threshold for risk prediction.

Study limitations

Due to the retrospective nature of our study and ethical limits, we were unable to include control groups, although having an adequately large sample size. Furthermore, the data was not initially collected prospectively, meaning certain information may be missed. Therefore, the complication predictors identified in our studies should be cautiously adopted and cannot be generalized until a formal prospective is thoroughly conducted.

Conclusions

Ninety-five percent first-attempt sampling rate among the patients, with the rate of pneumothorax complication being 27.6% (61/221 patients). Additionally, 19.9% showed signs of hemoptysis, and 5.4% showed both signs of pneumothorax and hemoptysis. All 221 patients underwent transthoracic biopsy, with the case with the longest distance from the chest wall being 63.2 mm and the average distance recorded being 37.2 mm. Moreover, the average needle insertion range recorded is 57.4±8.8 mm, with the shortest being 30 mm and the greatest being 92.7 mm. The smallest tumor was 10 mm³, and the greatest was 325 mm³.

In the figure for prognosis of pneumothorax complication, the chest wall-tumor edge distance has a value of area under ROC curve of 0.8414. A threshold of 23 mm shows that sensitivity, specificity, and accuracy are 72.13%, 80.5% and 78.18% respectively. The skin-tumor edge distance also shows a value of area under ROC curve of 0.8396. A threshold of 39.4 mm shows that sensitivity, specificity, and accuracy are 83.61%, 72.50%, and 75.57%, respectively. The skin-chest wall has a value of area under ROC curve of 0.5011, that of the skin-tumor center is 0.6782, and that of tumor size is 0.3087. The results found that there is a correlation between distances and pneumothorax complications. The rate of pneumothorax is 51.5% for patients with chest wall-tumor edge that is greater or equal to 20 mm; the rate is 8.2% for distances less than 20 mm (P<0.001).

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-955/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-955/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-955/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-955/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). The study was approved by the Ethics Committee of Thu Duc City Hospital (No. 1455/QD-BV) and individual consent for this retrospective analysis was waived due to the retrospective nature of the study.

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/.

References

1. Thandra KC, Barsouk A, Saginala K, et al. Epidemiology of lung cancer. Contemp Oncol (Pozn) 2021;25:45-52. [Crossref] [PubMed]
2. Pham T, Bui L, Kim G, et al. Cancers in Vietnam-Burden and Control Efforts: A Narrative Scoping Review. Cancer Control 2019;26:1073274819863802. [Crossref] [PubMed]
3. Nguyen SM, Nguyen QT, Nguyen LM, et al. Delay in the diagnosis and treatment of breast cancer in Vietnam. Cancer Med 2021;10:7683-91. [Crossref] [PubMed]
4. Ost D. Approach to the patients with Pulmonary Nodules. In: Grippi MA, Elias JA, Kotloff RM, et al. editors. Fishman’s Pulmonary Diseases and Disorders. 5th ed. New York: The McGraw-Hill Companies, Inc.; 2015:1815-30.
5. Nooreldeen R, Bach H. Current and Future Development in Lung Cancer Diagnosis. Int J Mol Sci 2021;22:8661. [Crossref] [PubMed]
6. Rivera MP, Mehta AC, Wahidi MM. Establishing the diagnosis of lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e142S-65S.
7. Benn BS, Gmehlin CG, Kurman JS, et al. Does transbronchial lung cryobiopsy improve diagnostic yield of digital tomosynthesis-assisted electromagnetic navigation guided bronchoscopic biopsy of pulmonary nodules? A pilot study. Respir Med 2022;202:106966. [Crossref] [PubMed]
8. Winokur RS, Pua BB, Sullivan BW, et al. Percutaneous lung biopsy: technique, efficacy, and complications. Semin Intervent Radiol 2013;30:121-7. [Crossref] [PubMed]
9. Beslic S, Zukic F, Milisic S. Percutaneous transthoracic CT guided biopsies of lung lesions; fine needle aspiration biopsy versus core biopsy. Radiol Oncol 2012;46:19-22. [Crossref] [PubMed]
10. Harrison BD, Thorpe RS, Kitchener PG, et al. Percutaneous Trucut lung biopsy in the diagnosis of localised pulmonary lesions. Thorax 1984;39:493-9. [Crossref] [PubMed]
11. Heyer CM, Reichelt S, Peters SA, et al. Computed tomography-navigated transthoracic core biopsy of pulmonary lesions: which factors affect diagnostic yield and complication rates? Acad Radiol 2008;15:1017-26. [Crossref] [PubMed]
12. Yamagami T, Terayama K, Yoshimatsu R, et al. Role of manual aspiration in treating pneumothorax after computed tomography-guided lung biopsy. Acta Radiol 2009;50:1126-33. [Crossref] [PubMed]
13. Sokolowski JW Jr, Burgher LW, Jones FL Jr, et al. Guidelines for percutaneous transthoracic needle biopsy. This position paper of the American Thoracic Society was adopted by the ATS Board of Directors, June 1988. Am Rev Respir Dis 1989;140:255-6. [Crossref] [PubMed]
14. Zhou Q, Dong J, He J, et al. The Society for Translational Medicine: indications and methods of percutaneous transthoracic needle biopsy for diagnosis of lung cancer. J Thorac Dis 2018;10:5538-44. [Crossref] [PubMed]
15. Takeshita J, Masago K, Kato R, et al. CT-guided fine-needle aspiration and core needle biopsies of pulmonary lesions: a single-center experience with 750 biopsies in Japan. AJR Am J Roentgenol 2015;204:29-34. [Crossref] [PubMed]
16. Nahm FS. Receiver operating characteristic curve: overview and practical use for clinicians. Korean J Anesthesiol 2022;75:25-36. [Crossref] [PubMed]
17. Park B, Kim Y, Lee J, et al. Sex Difference and Smoking Effect of Lung Cancer Incidence in Asian Population. Cancers (Basel) 2020;13:113. [Crossref] [PubMed]
18. Shin YJ, Yi JG, Son D, et al. Diagnostic Accuracy and Complication of Computed Tomography (CT)-Guided Percutaneous Transthoracic Lung Biopsy in Patients 80 Years and Older. J Clin Med 2022;11:5894. [Crossref] [PubMed]
19. Heerink WJ, de Bock GH, de Jonge GJ, et al. Complication rates of CT-guided transthoracic lung biopsy: meta-analysis. Eur Radiol 2017;27:138-48. [Crossref] [PubMed]
20. Bozbaş Ş, Akçay Ş, Ergür F, et al. Transthoracic lung and mediastinal biopsies obtained with the Tru-Cut technique: 10 years' experience. Turk J Med Sci 2010;40:495-501.
21. Tongbai T, McDermott S, Fintelmann FJ, et al. Complications and Accuracy of Computed Tomography-guided Transthoracic Needle Biopsy in Patients Over 80 Years of Age. J Thorac Imaging 2019;34:187-91. [Crossref] [PubMed]
22. Wiener RS, Schwartz LM, Woloshin S, et al. Population-based risk for complications after transthoracic needle lung biopsy of a pulmonary nodule: an analysis of discharge records. Ann Intern Med 2011;155:137-44. [Crossref] [PubMed]
23. Wu CC, Maher MM, Shepard JA. Complications of CT-guided percutaneous needle biopsy of the chest: prevention and management. AJR Am J Roentgenol 2011;196:W678-82. [Crossref] [PubMed]
24. Chassagnon G, Gregory J, Al Ahmar M, et al. Risk factors for hemoptysis complicating 17-18 gauge CT-guided transthoracic needle core biopsy: multivariate analysis of 249 procedures. Diagn Interv Radiol 2017;23:347-53. [Crossref] [PubMed]
25. Wang S, Dong K, Chen W. Development of a hemoptysis risk prediction model for patients following CT-guided transthoracic lung biopsy. BMC Pulm Med 2020;20:247. [Crossref] [PubMed]
26. Wiener RS, Wiener DC, Gould MK. Risks of Transthoracic Needle Biopsy: How High? Clin Pulm Med 2013;20:29-35. [Crossref] [PubMed]
27. Beşir FH, Altın R, Kart L, et al. The results of computed tomography guided tru-cut transthoracic biopsy: complications and related risk factors. Wien Klin Wochenschr 2011;123:79-82. [Crossref] [PubMed]
28. Zhao Y, Wang X, Wang Y, et al. Logistic regression analysis and a risk prediction model of pneumothorax after CT-guided needle biopsy. J Thorac Dis 2017;9:4750-7. [Crossref] [PubMed]
29. McCartney R, Tait D, Stilson M, et al. A technique for the prevention of pneumothorax in pulmonary aspiration biopsy. Am J Roentgenol Radium Ther Nucl Med 1974;120:872-5. [Crossref] [PubMed]
30. Covey AM, Gandhi R, Brody LA, et al. Factors associated with pneumothorax and pneumothorax requiring treatment after percutaneous lung biopsy in 443 consecutive patients. J Vasc Interv Radiol 2004;15:479-83. [Crossref] [PubMed]
31. Moore EH, Shepard JA, McLoud TC, et al. Positional precautions in needle aspiration lung biopsy. Radiology 1990;175:733-5. [Crossref] [PubMed]
32. Shepard JA. Complications of Percutaneous Needle Aspiration Biopsy of the Chest: Prevention and Management. Semin Intervent Radiol 1994;11:181-6.
33. Polat G, Özdemir Ö, Serçe Unat D, et al. Pneumothoraxes after CT-guided percutaneous transthoracic needle aspiration biopsy of the lung: A single-center experience with 3426 patients. Tuberk Toraks 2023;71:67-74. [Crossref] [PubMed]