Low-dose versus standard-dose computed tomography-guided core needle biopsy for lung nodules: a randomized controlled trial

doi:10.21203/rs.3.rs-1438386/v1

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Low-dose versus standard-dose computed tomography-guided core needle biopsy for lung nodules: a randomized controlled trial

https://doi.org/10.21203/rs.3.rs-1438386/v1

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Background

To assess relative safety and diagnostic performance for low- and standard-dose computed tomography (CT)-guided core needle biopsy (CNB) for lung nodules (LNs).

Materials and Methods

This is a prospective randomized controlled trial (RCT) from a single-center. From June 2020 to December 2020, consecutive patients with LNs were randomly assigned into low- or standard-dose groups. The primary outcome was diagnosis accuracy, while secondary outcomes encompassed technical success, diagnostic yield, operative time, radiation dose, and CNB-related complications. This RCT was listed within ClinicalTrials.gov (NCT04217655), registered 3 January 2020.

Results

A total of 200 patients were randomly assigned to low-dose (n = 100) and standard-dose (n = 100) groups. All patients achieved technical success of CT-guided CNB and the definite final diagnoses. No significant difference was found for operative times (n = 0.231) between 2 groups. The mean dose-length product was markedly reduced within low-dose group in comparison to standard-dose group (34.6 ± 11.1 vs. 351.4 ± 107.4 mGy-cm, P < 0.001). Within low-dose group, the diagnostic yield, sensitivity, specificity, and diagnosis accuracy were 68%, 91.5%, 100%, and 94%, respectively. Within standard-dose group, the diagnostic yield, sensitivity, specificity, and diagnosis accuracy were 65%, 88.6%, 100%, and 92%, respectively. There were no significances in diagnostic yield (P = 0.653) and diagnostic accuracy (P = 0.579) between 2 groups. No significant differences within rates of pneumothorax (P = 0.836) and lung hemorrhage (P = 0.744) between 2 groups were observed.

Conclusions

Compared with standard-dose CT-guided CNB for LNs, low-dose CT can significantly reduce radiation dose, while yield comparable safety and diagnostic accuracy.

Low-dose

Computed tomography

Biopsy

Lung nodule

Computed tomography (CT) screening for lung cancer has been become a routine item in the body examination at recent years [1–3]. Therefore, the detection rate of lung nodules (LNs) is also increased. According to the guidelines for management of incidental LNs on CT, no routine follow-up or optional CT at 12 month is recommended for LNs ≤ 5 mm because the chances of malignancy in nodules of this size are very low [4]. However, the malignant rate ranged from 43%-63% when the LNs > 5 mm [5, 6]. At present, CT-guided core needle biopsy (CNB) is commonly employed for differential diagnosis in LNs, owing to its simplicity and minimal invasiveness, with the diagnostic accuracy of 92.7%-97.0% [6–8].

Compared to CT-guided CNB for lung masses, CNB for LNs is more difficult in technique due to its smaller size. Therefore, when performing CT-guided CNB for LNs, more times of CT scans are usually required to adjust the needle position and angle [9, 10]. Consequently, exposing individual patients to additional radiations. So as to decrease such unnecessary dosing during CT-guided interventions, low-dose CT procedures were employed [11]. There are also some past investigations describing low-dose CT-guided CNB in diagnosis of LNs [9, 10]. However, these previous studies are retrospective in nature with the high risk of selection, comparability, and outcome. Therefore, a well-designed randomized controlled trial (RCT) should be conducted to validate the conclusions in the previous studies.

In this study, we aim to conduct a RCT to evaluate the relative safety and diagnostic performance of low- and standard-dose CT-guided CNB for LNs.

Study design

This single-center RCT was accepted through our center’s Institutional Review Board. All participants gave written, informed-consent. This RCT was listed within ClinicalTrials.gov (NCT04217655).

From June 2020 to December 2020, consecutive eligible patients with LNs were randomly assigned into low-dose and standard-dose groups. The inclusion criteria consisted of: (a) clinical cases with LNs, detected on CT; (b) solid LNs; (c) LNs > 5 mm; (d) LNs having intermediate-high risk for lung cancer, depending upon clinical/radiology-based characteristics [4]. Inclusion criteria consisted of: (a) patients who underwent CT-guided CNB previously; (b) LNs which were stable in size for at least 1 year; (c) LNs which decreased in size during follow-up; (d) clinical cases having intense cardiac, pulmonary, renal or coagulatory dysfunctional conditions; and (e) patients who refused to join this RCT.

The primary endpoint of this RCT was diagnostic accuracy, while the second endpoints included technical success, diagnostic yield, operative time, radiation dose, and CNB-related complications.

Randomization and blind

The eligible patients were randomly assigned into 1:1 low-dose and standard-dose groups through block-randomization technique (block size: 8), whereby randomized computer-generated numbers were placed within sequentially-numbered, opaque, sealed envelopes. Prior to biopsy, envelopes were opened by a member of the Science and Education department without any further role in the trial. This RCT was single-blind for the patients.

CT-guided CNB protocols

All procedures were performed under the guidance of a 16-row CT (Philips™, Ccategoryand, OH, USA) operated through a CT-guided interventional radiology expert (10 + years). Table 1 showed the scanning parameters of 2 groups.

Table 1

Scanning parameters between 2 groups
	Low-dose group	Standard-dose group
Tube voltage	120 kV	120 kV
Tube current	15 mA/s	150 mA/s
Thickness	2 mm	2 mm
Collimation	16 × 0.75 mm	16 × 0.75 mm
Pitch	1.063	1.063
Rotation time	0.5 s	0.5 s
Field of view	350 mm	350 mm

The patients’ position was decided according to the sites of LNs. The needle-paths were chosen depending upon preoperative CT outcomes. Co-axial technique was employed during procedures. A 17G outer needle (DuoSmart™, Modena, Italy) was pierced within lung-parenchyma, followed by a second CT scan for establishing needle-tip displace it accordingly. Once outer needle-tip touched LN, an 18G inner semi-automatic core-needle (Wego™, Weihai, China) was inserted via outer needle to obtain the samples from the LNs. Each LN was obtained for 3–4 samples, consequently submerged within 10% formaldehyde until pathology assessments were done.

After biopsy, another CT intervention was conducted for assessing the procedure-linked issues.

Imaging subjectivity

Two radiologists evaluated imaging standards independently. One radiologist had 15 years of experience in CT-guided intervention and another one had 8 years of experience in CT-guided intervention. Imaging-quality was evaluated across four categories: category A: needle/LN were distinctly observable; category B: needle/LN were adequately observable; category C: needle/LN were only somewhat observable; and category D: needle/LN could not be seen [12, 13]. Category A and B could be used for CT-guided CNB procedures. If category C or D images occurred, tube voltage and/or current were adjusted to obtain the higher quality images. However, the procedures should be considered as technical failure.

Definitions and diagnoses

LN was defined as spherical/oval image of non-transparent lesions ≤ 3cm in diameter with neighboring pulmonary parenchyma/non-linked to atelectasis, mediastinal lymphadenopathy, or pleural effusion [4]. Technical success for CT-guided CNB was confirmed once pathologists placed their diagnosis from extracted specimens [12]. CNB-based diagnoses could be classified into four categories: (a) malignancy; (b) suspected malignancy; (c) specific benignity; and (d) non-specific benignity. Suspected malignancy was defined as atypical cells suspected for indicating malignancy [14]. Specific benignity was defined as dataset outcomes suggested defined benign-diagnosis, including hamartomas and tuberculosis [14]. Non-specific benignity was defined as benign pathology characteristics existed, through did not suffice for a formal diagnosis [14].

Resection could make the final diagnoses for both malignant and benign LNs. CNB-based malignancy and specific benignity could be accepted as the final diagnosis [8–13]. CNB-based suspected malignancy and non-specific benignity could not be accepted as the final diagnoses, if they were not confirmed by resection, the CT medical observation would be useful for attaining a finalized diagnostic outcome. Whenever a LN with ≥ 20% size-reduction (without anticancer treatments), or maintained dimensions (no change or decreased < 20%) for a 12 month-minimum period (with no anti-cancer treatments), the final benign diagnosis could be accepted [6, 14].

True-positive was postulated when CNB-based malignancy/suspicious confirmed as malignant at finalized-diagnosis, and true-negative was postulated when CNB-based benignities confirmed benignities at finalized-diagnosis. Diagnosis yield = (CNB-based malignancy + CNB-based specific benignity)/all cases. Diagnostic accuracy = (true positive + true negative)/all cases with the final diagnosis. Pneumothorax and lung hemorrhage were assessed by chest CT. Lung hemorrhage was deemed a novel consolidating/ground-glass opacity around needle tract [15]. High-grade hemorrhage is defined as the width of needle tract hemorrhage > 2 cm [15].

Statistical analyses

The sample size was calculated based on diagnostic accuracy with the non-inferiority analysis. Based upon past investigations linked to CT-guided CNB for LNs, we estimated that the diagnostic accuracy was 94% [6, 8, 12]. Based on the − 10% of non-inferiority margin with the one-sided significance category of 0.025, we estimated that 200 patients (100 patients per group) were needed after considering 10% drop out rate.

Intention-to-treat (ITT) evaluations were performed depending on total patient group quantity enrolled in this study, while per-protocol (PP) evaluations were performed depending total patients who achieved technical success and definite final-diagnoses.

The continuous data were compared through independent sample t test, while categorical data were compared through Pearson χ²/Fisher exact test. Predictive indicators for diagnosis accuracy and complications were found through univariate and multivariate logistic regression tests. Kappa analysis was conducted for assessing inter-observer agreement regarding imaging-quality. All statistical analyses were conducted through SPSS® v.16.0 (SPSS Inc™, Chicago, Illinois, USA).

Patients

During the enrolled period, a total of 200 patients who fulfilled the inclusion criteria were randomly assigned to low-dose (n = 100) and standard-dose (n = 100) groups (Fig. 1). All patients achieved technical success of CT-guided CNB and the definite final diagnoses. Therefore, ITT and PP analyses were conducted based on the same population (Table 2).

Table 2

Baseline data and procedure details between 2 groups.
	Low-dose group (n = 100)	Standard-dose group (n = 100)	P value
Normal data
Age (y)	63.7 ± 10.5	61.1 ± 13.0	0.144
Gender (male/female)	68/32	62/38	0.374
Smoking history	49	40	0.200
Tumor history	7	10	0.447
BMI (kg/m²)	23.1 ± 3.6	22.8 ± 3.2	0.590
Imaging feature
Emphysema	28	33	0.229
Size (mm)	24.8 ± 4.2	23.5 ± 5.0	0.045
Lung (left/right)	42/58	45/55	0.669
Lobe (upper/non-upper)	45/55	42/58	0.669
Biopsy procedure
Lesion-pleura distance (</≥ 30 mm)	85/15	75/25	0.077
Needle- pleura angle (</≥ 50 degrees)	13/87	11/89	0.663
Prone/Supine/Decubitus	67/30/3	54/44/2	0.120
Number of needle pathways	1.3 ± 0.7	1.3 ± 0.7	0.694
Number of samples	3.3 ± 0.5	3.3 ± 0.5	0.880
Duration of procedure (min)	10.8 ± 4.1	11.6 ± 5.3	0.231
Complications
Pneumothorax (chest tube insertion)	14 (4)	13 (3)	0.836
Lung hemorrhage (high-grade hemorrhage)	24 (14)	26 (14)	0.744
Radiation dose
DLP (mGy-cm)	34.6 ± 11.1	351.4 ± 107.4	< 0.001
BMI: body mass index; DLP: dose-length product.

Procedure details

Table 2 showed the procedure details of low-/standard-dose CT-guided CNB. There were no significant differences within number of needle pathways (n = 0.694), number of samples (P = 0.880), and duration of procedures (n = 0.231) between 2 groups. The mean dose-length product (DLP) was markedly reduced within low-dose group in comparison to standard-dose group (P < 0.001), and the radiation dose was reduced more than 90% by the low-dose protocol.

Imaging-quality

Within low-dose group, 72 images (72%) were considered as category A and 28 images (28%) were considered as category B. Within standard-dose group, all imaging scans were considered as category A. The inter-observer agreements were very good across both groups (kappa value = 0.926 and 1.000, respectively). The category A images occurred more frequently within standard-dose group (P < 0.001).

Diagnosis

In low-dose group (Fig. 2), CNB-based diagnoses encompassed malignancy (n = 64), suspicious malignancy (n = 1), specific benignity (n = 4), and non-specific benignity (n = 31). Among them, malignancy/specific benignity results could be approved as finalized-diagnoses. Suspicious malignancy was validated as lung adenocarcinoma through surgical resection. Twenty-five non-specific benignities were confirmed as true benignities by CT medical observation (n = 23) or surgical resection (n = 2), while 6 non-specific benignities were confirmed as false benignities by surgical resection. Therefore, the diagnostic yield, sensitivity, specificity, and diagnostic accuracy were 68%, 91.5%, 100%, and 94%, respectively.

Within standard-dose group (Fig. 3), CNB-based diagnoses encompassed malignancy (n = 61), suspicious malignancy (n = 1), specific benignity (n = 4), and non-specific benignity (n = 34). Among them, the malignancy and specific benignity results could be approved as finalized- diagnoses. Suspicious malignancy was validated as lung adenocarcinoma through surgical resection. Twenty-six non-specific benignities were confirmed as true benignities by CT medical observation (n = 22) or surgical resection (n = 4), while 8 non-specific benignities were confirmed as false benignities by surgical resection. Therefore, the diagnostic yield, sensitivity, specificity, and diagnostic accuracy were 65%, 88.6%, 100%, and 92%, respectively.

There were no significances in diagnostic yield (P = 0.653), sensitivity (P = 0.554), and diagnostic accuracy (P = 0.579) between 2 groups (Table 3).

Table 3

Diagnostic performance between 2 groups.
	Low-dose group (n = 100)	Standard-dose group (n = 100)	P value
Technical success rate	100%	100%	-
Biopsy pathological diagnosis			0.976
Malignancy	64	61
Suspected malignancy	1	1
Specific benign	4	4
Non-specific benign	31	34
Final diagnosis			0.877
Malignancy	71	70
Benign	29	30
Diagnostic performance
Diagnostic yield	68/100 (68%)	65/100 (65%)	0.653
Sensitivity	65/71 (91.5%)	62/70 (88.6%)	0.554
Specificity	29/29 (100%)	30/30 (100%)	-
Overall accuracy	94/100 (94%)	92/100 (92%)	0.579

At univariate logistic regression test, non-prone position (P = 0.059) and upper lobe (P = 0.038) were associated with diagnostic failure. However, when these 2 factors were put into the multivariate logistic regression test, no risk factor (P = 0.323 and 0.165, respectively) was associated with diagnostic failure (Table 4).

Table 4

Predictors of diagnostic accuracy.
Variables	Univariate analysis			Multivariate analysis
Variables	Hazard ratio	95% CI	P value	Hazard ratio	95% CI	P value
Body position
Prone	1			1
Non-prone	2.983	0.961–9.259	0.059	1.906	0.531–6.839	0.323
Lobe
Non-upper	1			1
Upper	3.539	1.071–11.699	0.038	2.592	0.675–9.947	0.165
CI: confidential interval.

Complications

Pneumothorax was observed within 14 (14%) and 13 (13%) cases for low-dose and standard-dose groups, respectively (P = 0.836). Among them, 4 (28.6%) and 3 (23.1%) patients required chest tube insertion (P = 0.745). At univariate logistic regression test, more needle pathways (P = 0.006) and longer duration of procedure (P = 0.033) were associated with pneumothorax. When these 2 factors were put into the multivariate logistic regression test, more needle pathways (P = 0.045) was the only risk factor of pneumothorax (Table 5).

Table 5

Predictors of biopsy-related complications.
Variables	Univariate analysis			Multivariate analysis
Variables	Hazard ratio	95% CI	P value	Hazard ratio	95% CI	P value
Pneumothorax
Number of needle pathways	2.322	1.280–4.214	0.006	1.975	1.015–3.845	0.045
Duration of procedure	1.151	1.011–1.310	0.033	1.082	0.934–1.254	0.292
High-grade lung hemorrhage
Lesion size	0.802	0.701–0.927	0.002	0.858	0.736–0.999	0.049
Lesion-pleura distance
< 30 mm	1			1
≥ 30 mm	10.147	2.835–36.321	< 0.001	5.720	1.402–23.339	0.015
Needle-pleura angle
< 50 degrees	1			1
≥ 50 degrees	0.185	0.050–0.686	0.012	0.314	0.057–1.725	0.183
Duration of procedure	1.187	1.041–1.355	0.011	1.092	0.917–1.301	0.325
CI: confidential interval.

Lung hemorrhage was observed in 24 (24%) and 26 (26%) patients in low-dose and standard-dose groups, accordingly (P = 0.744). Among them, 14 (28.6%) and 14 (23.1%) patients experienced high-grade hemorrhage (P = 0.749). All patients with lung hemorrhage were managed with hemostasis. At univariate logistic regression test, smaller lesion size (P = 0.002), lesion-pleura distance ≥ 30 mm (P < 0.001), and needle-pleura angle ≥ 50 degrees (P = 0.012) were associated with high-grade hemorrhage. When these 3 factors were put into the multivariate logistic regression test, smaller lesion size (P = 0.049) and lesion-pleura distance ≥ 30 mm (P = 0.015) were the risk factors of high-grade hemorrhage (Table 5).

This RCT assessed the feasibility, safety, and diagnostic ability between low- and standard-dose CT-guided CNB in LNs. Although quality of images under the standard-dose CT were significant better, low-dose CT still resulted in similar technical success rates, number of needle pathways, and duration of procedures when compared to standard-dose CT. Unlike the conventional diagnostic images, the images for CNB procedures do not require meticulous details of the lesion, and they mainly require adequately observable of the locations of needle tip and lesion [12]. These findings may indicate that low-dose CT images made by our parameters can fulfill the CNB criteria for LNs.

Diagnostic yield usually indicates the ability of making a definite diagnosis by CNB [16–18]. We found that the diagnostic yield of CT-guided CNB was not reduced by the low-dose CT. Furthermore, the diagnostic yield rates in both groups (68% and 65%) were similar to past investigations regarding CT-guided CNB for LNs [9, 17]. Similarly, Shpilberg et al. [16] additionally revealed that low-dose CT did not reduce diagnostic yield for spine biopsies (low-dose group: 69%; standard-dose: 60%, P = 0.60).

Diagnostic accuracy was the primary endpoint for this RCT. The sensitivity and diagnostic accuracy rates in low-dose group were comparable to standard-dose group. This finding was similar to that in previous studies which compared the effectiveness across low-dose and standard-dose CT-guided lung biopsy [9, 10, 12–14]. In addition, the diagnostic accuracy rates in both groups (94% and 92%) were similar (90%-96%) as in past investigations regarding CT-guided CNB for LNs [17, 19, 20]. However, we did not find any risk factors which were associated with diagnostic failure. In past investigations regarding CT-guided CNB, the risk factors of diagnostic failure usually encompassed less sample tissues and larger lesion size [9, 12, 21, 22]. In this study, we used the co-axial technique and obtained 3–4 samples from each LN, therefore, the number of sample tissues did not interfere the diagnostic accuracy. Larger lesion size, especially more than 5 cm, the diagnostic failure usually occurred due to the higher rates of obtaining the necrosis [21]. Our RCT focused on the LNs, and therefore, the lesion size was not associated with diagnostic failure.

CNB-related complications are also the important endpoints in this RCT. The comparative results of pneumothorax and lung hemorrhage indicated that the safety of CNB was not decreased by the low-dose protocol. Furthermore, the chest tube requirement rates were only 4% and 3% in low-dose and standard-group, accordingly. Risk factors for the pneumothorax and high-grade hemorrhage included more number of needle pathways, smaller lesion size, and lesion-pleura distance ≥ 30 mm. These risk factors were also in consistent with past investigations regarding CT-guided lung biopsy [10, 20].

The low-dose CT protocol could be achieved by reducing the tube voltage and/or current [12, 23, 24]. In our study, we adjusted the tube current to 10% of the normal current and achieved a more than 90% reduction in radiation exposure. This reduction extent was largely consistent with that (53%-95%) in past investigations regarding low-dose CT-guided lung biopsy [12, 23, 24]. Although major dose reductions exacerbated noise and decreased image quality, low-dose CT at 120 kV and 15 mA/s allowed for an image quality adequate for CNB procedure.

This study has some limitations. First, we only used the block randomization method, but the randomization was not performed by stratification of the lesion size. The unbalanced data of lesion size was observed and it may cause the selective bias. However, this study only included LNs and the difference of mean lesion size between 2 groups was not large (24.8 mm vs. 23.5 mm). These findings may reduce the risk of bias. Second, the risk factor of diagnostic failure was not found in this investigation. This finding could be due to the limited sample size. Third, the patients were from a single-center and the results should be validated by further multiple-center studies.

In conclusion, compared to standard-dose CT-guided CNB for LNs, low-dose CT can significantly reduce radiation dose, while yield comparable safety and diagnostic accuracy.

CNB: core needle biopsy;

CT: computed tomography;

ITT: intention-to-treat;

LN: lung nodule;

PP: per-protocol;

RCT: randomized controlled trial.

Ethics approval and consent to participate: This single-center study was approved by Ethics Committee of Xuzhou Central Hospital. All patients provided the written informed consents. All methods were carried out in accordance with Declaration of Helsinki.

Consent for publication: The relevant patients provided informed consent for publication of the images in Fig. 2 and 3.

Availability of data and materials: The data that support the findings of this study are available from the corresponding author upon reasonable request.

Competing interests: None.

Funding: None

Authors’ contributions: GCL designed this work. HYL, ALM, and YFF collected the clinical data. TW, ALM, and ELL performed the statistical analyses. ELL wrote this article. Final manuscript was approved by all authors.

Acknowledgments: None

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No competing interests reported.

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Low-dose versus standard-dose computed tomography-guided core needle biopsy for lung nodules: a randomized controlled trial

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Background

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Discussion

Conclusions

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