eISSN: 1897-4252
ISSN: 1731-5530
Kardiochirurgia i Torakochirurgia Polska/Polish Journal of Thoracic and Cardiovascular Surgery
Current issue Archive Manuscripts accepted About the journal Supplements Editorial board Reviewers Abstracting and indexing Contact Instructions for authors Publication charge Ethical standards and procedures
Editorial System
Submit your Manuscript
SCImago Journal & Country Rank
3/2023
vol. 20
 
Share:
Share:
Original paper

Computed tomography-guided biopsy for sub-centimetre pulmonary nodules: a meta-analysis

Jin-Ling Feng
1
,
Yu-Fei Fu
1
,
Yu Li
1

  1. Department of Radiology, Xuzhou Central Hospital, Xuzhou, China
Kardiochirurgia i Torakochirurgia Polska 2023; 20 (3): 139-145
Online publish date: 2023/10/30
Article file
Get citation
 
PlumX metrics:
 

Introduction

Pulmonary nodules (PNs) are non-transparent, ovoid or round lesions with a diameter ≤ 30 mm that are surrounded by the lung parenchyma [13]. The establishment of computed tomography (CT)-based screening efforts has led to a marked rise in the rate of PN detection [4]. Differentiating between malignant and benign PNs is generally performed by testing for tumour markers and assessing the morphology, size, and CT density of the target lesions [57]. The odds that a given PN is malignant tend to rise with lesion size [810], and lesions with a diameter of 5–10 mm exhibit malignancy rates between 47.5% and 61.5% [1120].

At present, recommendations from the Fleischner Society indicate that solitary solid nodules over 8 mm in diameter or partially solid nodules with solid components greater than 6 mm in diameter should undergo biopsy or surgical resection if persistent [8]. The small size of sub-centimetre PNs (≤ 10 mm), however, makes the CT-guided biopsy of these lesions more difficult. As such, there has been a high degree of variability among published studies employing various needle types, CT methods, and co-axial method use with respect to the diagnostic accuracy (79–98%), pneumothorax (7–62%), and pulmonary haemoptysis (6–22%) rates among patients with sub-centimetre PNs undergoing biopsy procedures [1120]. There is thus a pressing need for large-scale, systematic analysis of these extant studies in an effort to provide a robust foundation with which clinicians can more effectively evaluate the safety, diagnostic accuracy, and feasibility of CT-guided biopsy approaches such that they can select the most effective biopsy approach.

Aim

This meta-analysis was performed to evaluate the diagnostic performance and safety profile associated with the CT-guided biopsy of sub-centimetre PNs.

Material and methods

Study selection

This study was conducted based on the Meta-analysis Of Observational Studies in Epidemiology (MOOSE) checklist [21] and was registered at inplasy.com (No. INPLASY202350031). Relevant studies published through April 2023 were identified in the PubMed, Web of Science, and Wanfang databases with the search strategy: (((((computed tomography) OR (CT)) AND ((lung) OR (pulmonary))) AND (biopsy)) AND (((1 cm) OR (10 mm)) OR (subcentimeter))) AND ((nodule) OR (lesion)).

Studies eligible for inclusion were as follows: (i) those that were specifically developed to analyse CT-guided biopsy outcomes in patients with sub-centimetre PNs; (ii) studies with a sample size greater than 20; and (iii) studies in which a minimum of one of the technical or clinical endpoints of interest (technical success, diagnostic yield, diagnostic accuracy, pulmonary haemorrhage, and pneumothorax rates) was evaluated. Studies were excluded if they were: (i) reviews, (ii) conference abstracts, or (iii) non-human studies.

Data extraction

Two authors independently extracted relevant data from all studies, and any discrepant results were resolved through discussion with a third investigator. The baseline data for included studies are presented in Table I.

Table I

Characteristics of studies included in the meta-analysis

StudiesYearCountry/areaPatients numberMean ageM/FMean lesion sizeType of needleGuidance methodsCo-axial techniqueMean number of samplesNOS
Chang [11]2018Taiwan259Not given111/148Not givenCoreCTYesNot given8
Choi [12]2013Korea268Not givenNot given9.3 mmCore and FineCTNo2.07
Choo [13]2013Korea10562 y55/508.5 mmCoreCBCTYesNot given8
Dominguez-Konicki [14]2020USA19365.5 y114/79Not givenCore and FineCTFYesNot given8
Hui [15]2022China10558.9 y57/489.1 mmCoreCTNo1.78
Hwang [16]2018Korea21362.1 y99/1149 mmCore and FineCBCTYesNot given8
Li [17]2020China10157.8 y55/469 mmCoreCTNo1.78
Ng [18]2008Canada5463.3 y28/269 mmFineCTYesNot given8
Portela de Oliveira [19]2020Canada12765.4 y65/629.2 mmCore and FineCTNoNot given8
Wallace [20]2002USA5761.3 y30/27Not givenFineCTNoNot given7

[i] M – male, F – female, CT – computed tomography, CBCT – cone-beam CT, CTF – CT fluoroscopy, NOS – Newcastle-Ottawa scale.

Technical success for CT-guided biopsy procedures was defined by the successful collection of a sample of quality that was adequate to permit visual inspection [15]. Diagnostic yield was assessed by dividing the diagnostic results based upon CT-guided biopsy procedures by the total results [15]. Diagnostic accuracy was calculated based on the sum of the numbers of true positive and true negative results [15].

Quality assessment

The quality of non-randomized controlled trials was assessed with the Newcastle-Ottawa scale (NOS) [10]. These studies were scored based on selection, comparability, and outcome criteria, which were awarded up to 4, 2, and 3 points each, respectively. Studies with a total NOS score of 7 or higher were considered to be of high quality.

Statistical analysis

Random-effects models were used to evaluate pooled data for all study endpoints. Pooled result heterogeneity was assessed using the Q test and I2 values, with significant heterogeneity being defined by an I2 value > 50%. Sensitivity analyses were performed with a leave-one-out approach, and subgroup analyses were performed based on guidance methods, needle types, and whether a co-axial method was employed. Egger’s test was used to assess the potential for publication bias, and p < 0.05 was the cut-off for statistical significance. Stata 12.0 was used to conduct all pooled analyses.

Results

Study selection

Of 6522 initially identified studies, 10 were ultimately incorporated into this meta-analysis, as detailed in Figure 1. These studies included a total of 1482 patients undergoing CT-guided biopsy procedures for the evaluation of sub-centimetre PNs (Table I). Biopsies in 4, 2, and 4 of these studies were performed using core needles, fine needles, or both needle types, respectively. In addition, 7, 2, and 1 of these studies employed conventional CT, cone-beam CT (CBCT), and CT fluoroscopy (CTF) guidance, respectively, while the co-axial technique was employed for the biopsy procedures in 4 of these studies. All these studies were of high quality, with NOS scores ranging from 7 to 8.

Figure 1

Flowchart of this meta-analysis

/f/fulltexts/KiTP/51615/KITP-20-51615-g001_min.jpg

Technical success

Technical success rates were reported in 3 studies [12, 17, 20], with a pooled technical success rate of 90% (95% CI: 0.81–0.99, Figure 2 A). Significant heterogeneity was detected (I2 = 93.6%), but there was no evidence of publication bias (p = 0.247). Sensitivity analyses failed to establish the sources of heterogeneity for this endpoint.

Figure 2

Forest plots of the technical success rate (A), diagnostic yield (B), diagnostic accuracy (C), Pneumothorax rate (D) and pulmonary haemorrhage rate (E)

/f/fulltexts/KiTP/51615/KITP-20-51615-g002_min.jpg

Diagnostic yield

Diagnostic yield was reported in 4 studies [14, 15, 17, 19], with an overall pooled yield rate of 60% (95% CI: 0.41–0.79, Figure 2 B). Both significant heterogeneity (I2 = 96%) and publication bias (p = 0.008) were detected, but sensitivity analyses failed to establish the sources of heterogeneity for this endpoint.

Diagnostic accuracy

Diagnostic accuracy rates were reported in 8 studies [1113, 1518, 20], with an overall pooled rate of 91% (95% CI: 0.88–0.95, Figure 2 C). Both significant heterogeneity (I2 = 76.9%) and publication bias (p = 0.001) were detected, but sensitivity analyses failed to establish the sources of heterogeneity for this endpoint.

Pneumothorax

Pneumothorax rates were reported by 8 studies [1113, 1517, 19, 20], with an overall pooled incidence rate of 24% (95% CI: 0.16–0.33, Figure 2 D). Significant heterogeneity was detected (I2 = 93.6%), but there was no evidence of publication bias (p = 0.656). Sensitivity analyses failed to establish the sources of heterogeneity for this endpoint.

Pulmonary haemorrhage

Pulmonary haemorrhage rates were reported by 6 studies [11, 13, 1517, 19], and the pooled rate was 11% (95% CI: 0.06–0.16, Figure 2 E). Significant heterogeneity was detected (I2 = 80.8%), but there was no evidence of publication bias (p = 0.942). Sensitivity analyses identified the study conducted by Chang et al. [11] as the source of detected heterogeneity.

Subgroup analyses

The results of subgroup analyses conducted for diagnostic accuracy rates are compiled in Table II. The respective pooled rates for patients who underwent fine-needle and core-needle procedures were 85% and 95% respectively, while the respective rates for patients who underwent biopsy procedures performed with conventional CT and CBCT guidance were 92% and 95%, and the pooled rates for patients that underwent biopsy procedures that did and did not utilize the co-axial method were 94% and 93%, respectively.

Table II

Subgroup analyses of diagnostic accuracy

VariableStudies (n)Pooled rate (%)95% CII2 (%)
Type of needle:
 Fine needle2850.78–0.9233.6
 Core needle4950.93–0.9675.9
Guidance method:
 Conventional CT6920.91–0.9454.1
 CBCT2950.93–0.9893.8
Co-axial method:
 Yes4940.92–0.9687.8
 No4930.91–0.9544.5

[i] CI – confidence interval, CT – computed tomography, CBCT – cone-beam CT.

The results of subgroup analyses conducted for pneumothorax rates are compiled in Table III. The respective pooled rates for patients who underwent fine-needle and core-needle procedures were 62% and 15%, respectively, while the respective rates for patients who underwent biopsy procedures performed with conventional CT and CBCT guidance were 22% and 15%, and the pooled rates for patients that underwent biopsy procedures that did and did not utilize the co-axial method were both 20%.

Table III

Subgroup analyses of pneumothorax

VariableStudies (n)Pooled rate (%)95% CII2 (%)
Type of needle:
 Fine needle1620.50–0.74
 Core needle4150.13–0.1892.3
Guidance method:
 Conventional CT6220.19–0.2493.1
 CBCT2150.12–0.1996.7
Co-axial method:
 Yes3200.17–0.2395.9
 No5200.17–0.2393.5

[i] CI – confidence interval, CT – computed tomography, CBCT – cone-beam CT.

The results of subgroup analyses conducted for pulmonary haemorrhage rates are compiled in Table IV. Respective pooled pulmonary haemorrhage rates for patients who underwent biopsy procedures performed with conventional CT and CBCT guidance were 12% and 9%. Respective pooled rates for patients who underwent biopsy procedures that did and did not utilize the co-axial method were 12% and 9%.

Table IV

Subgroup analyses of pulmonary haemorrhage

VariableStudies (n)Pooled rate (%)95% CII2 (%)
Type of needle:
 Fine needle0
 Core needle4110.09–0.1488.2
Guidance method:
 Conventional CT4120.10–0.1585.4
 CBCT290.06–0.1260.5
Co-axial method:
 Yes3120.10–0.1590.9
 No390.06–0.120

[i] CI – confidence interval, CT – computed tomography, CBCT – cone-beam CT.

Discussion

The present meta-analysis examined the diagnostic accuracy, feasibility, and safety of using CT-guided biopsy as an approach to the diagnosis of sub-centimetre PNs. The 90% pooled rate of technical success computed for the included studies suggests that CT-guided biopsy is a reliable means of collecting samples from sub-centimetre PNs that are large enough to permit pathological examination. This pooled rate, however, was below the 99–100% rates that have been reported in other analyses focused on the CT-guided biopsy of PNs [6, 22, 23]. Of the studies incorporated into this meta-analysis, the article published by Wallace et al. [20] reported a low 77% technical success rate, whereas the other studies reporting this endpoint exhibited rates greater than 90% [12, 17]. This may be attributable to the fact that the CT-guided biopsy procedures included in the Wallace et al. study were conducted from 1999 to 2001, and technical success rates may have improved over time with advances including the development of CT multiplanar reformation, CTF, and CBCT approaches.

In this meta-analysis, the pooled diagnostic yield rate indicated that CT-guided biopsy procedures alone can yield a definitive diagnosis in roughly 60% of patients being evaluated for sub-centimetre PNs, in line with rates of 65–71% that have previously been reported for the CT-guided biopsy of PNs [22, 24].

In this meta-analysis, the pooled diagnostic accuracy rate for CT-guided biopsy procedures was 91%, demonstrating the value of this approach as an accurate means of diagnosing sub-centimetre PN diagnosis. In subgroup analyses, the use of guidance methods (conventional CT vs. CBCT) or the co-axial method had no impact on this diagnostic accuracy rate. However, a notable difference in this rate was evident when comparing fine- and core-needle biopsy procedures (85% vs. 95%). Supporting this finding, core-needle biopsy procedures have been demonstrated to achieve sample adequacy superior to that associated with fine-needle biopsy procedures [25]. Core-needle biopsy procedures are also better suited to the evaluation of specific molecular markers of interest, providing supplemental information that can support traditional pathological diagnostic findings [26].

Rates of pulmonary haemorrhage and pneumothorax were analysed as a metric to gauge the safety of CT-guided biopsy procedures in patients with sub-centimetre PNs. The respective pooled incidence rates of these 2 complications were 11% and 24% among the included studies, in line with similar rates reported in a prior meta-analysis focused on the CT-guided biopsy of small PNs (≤ 20 mm) [27]. Some prior meta-analyses have reported no differences in rates of pulmonary haemorrhage or pneumothorax as a function of needle type (core vs. fine needle) or guidance methods used (conventional CT vs. CTF) [25, 28]. While the subgroup analyses conducted herein indicated that the pneumothorax rate associated with fine-needle biopsy procedures was 62%, this result was only derived from a single report [20], highlighting the need for further research to better gauge this procedural risk.

There are certain limitations to this meta-analysis. Firstly, all included studies were retrospective in design and may thus be associated with a higher risk of bias, emphasizing a need for prospective validation. Secondly, only single-arm results were taken into consideration in this study, precluding any potential comparisons between 2 different methods. And thirdly, some of the included studies utilized 2 different needle types and did not report which needles were used for which patients, introducing potential bias into the subgroup analyses conducted based on needle type.

Conclusions

The results of this meta-analysis indicate that CT-guided biopsy approaches are a safe and effective means of diagnostic evaluation in patients with sub-centimetre PNs.

Disclosure

The authors report no conflict of interest.

References

1 

Godoy MCB, Odisio EGLC, Truong MT, de Groot PM, Shroff GS, Erasmus JJ. Pulmonary nodule management in lung cancer screening: a pictorial review of lung-RADS Version 1.0. Radiol Clin North Am 2018; 56: 353-363.

2 

van Riel SJ, Ciompi F, Jacobs C, Winkler Wille MM, Scholten ET, Naqibullah M, Lam S, Prokop M, Schaefer-Prokop C, van Ginneken B. Malignancy risk estimation of screen-detected nodules at baseline CT: comparison of the PanCan model, Lung-RADS and NCCN guidelines. Eur Radiol 2017; 27: 4019-4029.

3 

McWilliams A, Tammemagi MC, Mayo JR, Roberts H, Liu G, Soghrati K, Yasufuku K, Martel S, Laberge F, Gingras M, Atkar-Khattra S, Berg CD, Evans K, Finley R, Yee J, English J, Nasute P, Goffin J, Puksa S, Stewart L, Tsai S, Johnston MR, Manos D, Nicholas G, Goss GD, Seely JM, Amjadi K, Tremblay A, Burrowes P, MacEachern P, Bhatia R, Tsao MS, Lam S. Probability of cancer in pulmonary nodules detected on first screening CT. N Engl J Med 2013; 369: 910-919.

4 

Choi HK, Mazzone PJ. Lung cancer screening. Med Clin North Am 2022; 106: 1041-1053.

5 

Chen G, Bai T, Wen LJ, Li Y. Predictive model for the probability of malignancy in solitary pulmonary nodules: a meta-analysis. J Cardiothorac Surg 2022; 17: 102.

6 

Li Y, Wang T, Fu YF, Shi YB. Computed tomography-based spiculated sign for prediction of malignancy in lung nodules: a meta-analysis. Clin Respir J 2020; 14: 1113-1121.

7 

Li L, Guo C, Wan JL, Fan QS, Xu XL, Fu YF. The use of carcinoembryonic antigen levels to predict lung nodule malignancy: a meta-analysis. Acta Clin Belg 2022; 77: 227-232.

8 

MacMahon H, Naidich DP, Goo JM, Lee KS, Leung ANC, Mayo JR, Mehta AC, Ohno Y, Powell CA, Prokop M, Rubin GD, Schaefer-Prokop CM, Travis WD, Van Schil PE, Bankier AA. Guidelines for management of incidental pulmonary nodules detected on CT images: from the Fleischner Society 2017. Radiology 2017; 284: 228-243.

9 

Bankier AA, MacMahon H, Goo JM, Rubin GD, Schaefer-Prokop CM, Naidich DP. Recommendations for measuring pulmonary nodules at CT: a statement from the Fleischner Society. Radiology 2017; 285: 584-600.

10 

Bueno J, Landeras L, Chung JH. Updated Fleischner Society Guidelines for managing incidental pulmonary nodules: common questions and challenging scenarios. Radiographics 2018; 38: 1337-1350.

11 

Chang YY, Chen CK, Yeh YC, Wu MH. Diagnostic feasibility and safety of CT-guided core biopsy for lung nodules less than or equal to 8 mm: a single-institution experience. Eur Radiol 2018; 28: 796-806.

12 

Choi SH, Chae EJ, Kim JE, Kim EY, Oh SY, Hwang HJ, Lee HJ. Percutaneous CT-guided aspiration and core biopsy of pulmonary nodules smaller than 1 cm: analysis of outcomes of 305 procedures from a tertiary referral center. AJR Am J Roentgenol 2013; 201: 964-970.

13 

Choo JY, Park CM, Lee NK, Lee SM, Lee HJ, Goo JM. Percutaneous transthoracic needle biopsy of small (≤ 1 cm) lung nodules under C-arm cone-beam CT virtual navigation guidance. Eur Radiol 2013; 23: 712-719.

14 

Dominguez-Konicki L, Karam AR, Furman MS, Grand DJ. CT-guided biopsy of pulmonary nodules ≤ 10 mm: diagnostic yield based on nodules’ lobar and segmental distribution. Clin Imaging 2020; 66: 7-9.

15 

Hui H, Yin HT, Wang T, Chen G. Computed tomography-guided core needle biopsy for sub-centimeter pulmonary nodules. Kardiochir Torakochir Pol 2022; 19: 65-69.

16 

Hwang EJ, Kim H, Park CM, Yoon SH, Lim HJ, Goo JM. Cone beam computed tomography virtual navigation-guided transthoracic biopsy of small (≤ 1 cm) pulmonary nodules: impact of nodule visibility during real-time fluoroscopy. Br J Radiol 2018; 91: 20170805.

17 

Li Y, Wang T, Fu YF, Shi YB, Wang JY. Computed tomography-guided biopsy for sub-centimetre lung nodules: technical success and diagnostic accuracy. Clin Respir J 2020; 14: 605-610.

18 

Ng YL, Patsios D, Roberts H, Walsham A, Paul NS, Chung T, Herman S, Weisbrod G. CT-guided percutaneous fine-needle aspiration biopsy of pulmonary nodules measuring 10 mm or less. Clin Radiol 2008; 63: 272-277.

19 

Portela de Oliveira E, Souza CA, Inacio JR, Abdelzarek M, Dennie C, Gupta A, Bayanati H. Imaging-guided percutaneous biopsy of nodules ≤1 cm: study of diagnostic performance and risk factors associated with biopsy failure. J Thorac Imaging 2020; 35: 123-128.

20 

Wallace MJ, Krishnamurthy S, Broemeling LD, Gupta S, Ahrar K, Morello Jr FA, Hicks ME. CT-guided percutaneous fine-needle aspiration biopsy of small (< or =1-cm) pulmonary lesions. Radiology 2002; 225: 823-828.

21 

Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000; 283: 2008-2012.

22 

Li EL, Ma AL, Wang T, Fu YF, Liu HY, Li GC. Low-dose versus standard-dose computed tomography-guided biopsy for pulmonary nodules: a randomized controlled trial. J Cardiothorac Surg 2023; 18: 86.

23 

Zhang HM, Huo XB, Wang HL, Zhang X, Fu YF. Computed tomography-guided cutting needle biopsy for lung nodules: a comparative study between low-dose and standard dose protocols. Medicine (Baltimore) 2021; 100: e24001.

24 

Huang YY, Cheng H, Li GC. Computed tomography-guided core needle biopsy for lung nodules: low-dose versus standard-dose protocols. Videosurgery Miniinv 2021; 16: 355-361.

25 

Li Y, Yang F, Huang YY, Cao W. Comparison between computed tomography-guided core and fine needle lung biopsy: a meta-analysis. Medicine (Baltimore) 2022; 101: e29016.

26 

Tian P, Wang Y, Li L, Zhou Y, Luo W, Li W. CT-guided transthoracic core needle biopsy for small pulmonary lesions: diagnostic performance and adequacy for molecular testing. J Thorac Dis 2017; 9: 333-343.

27 

Liu GS, Wang SQ, Liu HL, Liu Y, Fu YF, Shi YB. Computed tomography-guided biopsy for small (≤20 mm) lung nodules: a meta-analysis. J Comput Assist Tomogr 2020; 44: 841-846.

28 

Fu YF, Li GC, Cao W, Wang T, Shi YB. Computed tomography fluoroscopy-guided versus conventional computed tomography-guided lung biopsy: a systematic review and meta-analysis. J Comput Assist Tomogr 2020; 44: 571-577.

Copyright: © 2023 Polish Society of Cardiothoracic Surgeons (Polskie Towarzystwo KardioTorakochirurgów) and the editors of the Polish Journal of Cardio-Thoracic Surgery (Kardiochirurgia i Torakochirurgia Polska). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) License (http://creativecommons.org/licenses/by-nc-sa/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited and states its license.
 
Quick links
© 2024 Termedia Sp. z o.o.
Developed by Bentus.