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© AME Publishing Company. J Thorac Dis 2024;16(10):6347-6356 | https://dx.doi.org/10.21037/jtd-24-1052
Original Article
The use of electromagnetic navigation bronchoscopy-guided
microwave ablation in patients with multiple bilateral pulmonary
nodules: a retrospective study of 26 cases
Siwei Wang1#, Chi Su1#, Jing Li2#, Na Yin3, Chunpei Wu4, Rong Gao4, Shuai Zhang1, Xiaojun Wang1,
Zhenzhong Lin5, Dongxue Li3, Jingwen Hu2*, Ming Li1*
1Department of Thoracic Surgery, Jiangsu Key Laboratory of Molecular and Translational Cancer Research, Nanjing Medical University Afliated
Cancer Hospital & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research, Nanjing, China; 2Department of Endoscope, Nanjing Medical
University Afliated Cancer Hospital & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research, Nanjing, China; 3Department of Radiology,
Nanjing Medical University Affiliated Cancer Hospital & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research, Nanjing, China;
4Department of Anesthesiology, Nanjing Medical University Afliated Cancer Hospital & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer
Research, Nanjing, China; 5Department of Pathology, Nanjing Medical University Afliated Cancer Hospital & Jiangsu Cancer Hospital & Jiangsu
Institute of Cancer Research, Nanjing, China
Contributions: (I) Conception and design: M Li, J Hu, S Wang; (II) Administrative support: S Zhang, X Wang; (III) Provision of study materials or
patients: C Su, J Li, N Yin, C Wu, R Gao; (IV) Collection and assembly of data: S Wang, C Su, Z Lin, D Li; (V) Data analysis and interpretation:
S Wang, J Hu; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.
#These authors contributed equally to this work as co-rst authors.
*These authors contributed equally to this work.
Correspondence to: Ming Li, MD, PhD. Department of Thoracic Surgery, Jiangsu Key Laboratory of Molecular and Translational Cancer Research,
Nanjing Medical University Afliated Cancer Hospital & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research, Baiziting 42, Nanjing
210009, China. Email: liming750523@163.com; Jingwen Hu, MD, PhD. Department of Endoscope, Nanjing Medical University Afliated Cancer
Hospital & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research, Baiziting 42, Nanjing 210009, China. Email: h136271114@163.com.
Background: To treat multiple bilateral ground-glass opacities (GGOs), surgical treatments and
electromagnetic navigation bronchoscopy (ENB)-guided ablation therapy are recommended therapeutic
measures. However, the differences between bilateral and unilateral ablation, with or without surgery, remain
unknown. This study aims to evaluate the differences in efcacy among various strategies.
Methods: This retrospective study reports a single-center experience with ENB-guided microwave ablation
(MWA) for patients with multiple bilateral GGOs. A total of 26 cases from December 2020 to February
2023 were reviewed. The primary end points were technical safety and efciency.
Results: This study compared three therapeutic strategies for patients with multiple bilateral GGOs
based on ENB-guided MWA. Five cases simultaneously underwent video-assisted thoracoscopic surgery
(VATS) and ENB-guided MWA, namely simultaneous VATS-MWA group. Eight cases received VATS
followed by the second period ENB-guided MWA, namely two-step VATS-MWA group. Thirteen cases
were performed with only ENB-guided MWA for bilateral lesions. All conducted treatments were consistent
with preoperative assessment. The group of only ENB-guided MWA had the worst pulmonary function and
performance status but the highest proportion of pure GGOs. Intriguingly, the use of only ENB-guided
MWA showed a favorable performance in pathological detection, while no signicant differences were found
between the simultaneous VATS-MWA group and the two-step VATS-MWA group.
Conclusions: The use of ENB-guided MWA shows efcacy in treating multiple bilateral GGOs suspected
of having multiple primary lung cancers. Bilateral ENB-guided MWA is feasible in patients who cannot
tolerate surgery, and VATS combined with ENB-guided MWA is safe and can also preserve as much
pulmonary function as possible.
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Introduction
In recent years, the detection rate of ground-glass
opacities (GGOs) has increased signicantly, and a relative
proportion of GGOs would nally be conrmed malignancy
pathologically. Although minimally invasive surgical
approaches have become the answer for these suspicious
GGOs, a consensus on the diagnosis and treatment is still
lacking for patients with bilateral multiple GGOs.
Electromagnetic navigation bronchoscopy (ENB) is a
recommended minimally invasive technology to approach
pulmonary lesions (1), especially for peripheral lesions
difficult to reach with bronchoscopy alone (2). To find a
more effective interventional treatment for patients with
multiple GGOs, thermal ablation therapy has been used
in these patients, including radiofrequency ablation and
microwave ablation (MWA). Presently, the use of ENB-
guided MWA has become a proven therapeutic strategy,
which may be particularly advantageous in patients with
poor pulmonary function.
Jiang et al. first performed the combination of ENB-
guided MWA and thoracoscopic resection on patients with
multiple GGOs (3). In this case, the target GGO of ENB-
guided MWA was located in the right upper lobe, and, after
the procedure, the remaining lesions in left lung were all
successfully resected by video-assisted thoracoscopic surgery
(VATS). Presently, a total of two studies reported a single-
centered systematical application of ENB-guided MWA
in multiple, unilateral or bilateral GGOs (4,5). The results
indicated that ENB-guided MWA combined with VATS is
safe and feasible in patients with multiple GGOs suspected
of having multiple primary lung cancers.
In this study, we conducted a retrospective study to
investigate the differences in patient characteristics and
efficacy among three treatment strategies based on ENB-
guided MWA: receiving only ENB-guided MWA, receiving
simultaneous VATS and ENB-guided MWA, and receiving
VATS followed by a second round of ENB-guided MWA.
Our results revealed selection tendencies within different
strategies, which provided a theoretical basis for treatment
optimization in patients with bilateral GGOs. We present
this article in accordance with the PROCESS reporting
checklist (available at https://jtd.amegroups.com/article/
view/10.21037/jtd-24-1052/rc).
Methods
Patients and procedures
The study was conducted in accordance with the Declaration
of Helsinki (as revised in 2013). The study was approved
by the institutional ethics board of Jiangsu Cancer Hospital
(No. JSLMTCR-2020-062) and individual consent for this
retrospective analysis was waived. We reviewed a total of 26
patients underwent ENB-guided MWA from Jiangsu Cancer
Hospital between December 2020 to February 2023. The
clinical criteria for ENB-guided MWA in our center were as
follows: (I) bilateral GGOs [pure GGO (pGGO) or mixed
GGO (mGGO)] conrmed by chest computed tomography
(CT); (II) predominant lesion (in size and solidity) diameter
Highlight box
Key ndings
• The use of electromagnetic navigation bronchoscopy (ENB)-
guided microwave ablation (MWA) is safe and efcacy in treating
patients with multiple bilateral ground-glass opacities (GGOs).
• The combination of ENB-guided MWA and video-assisted
thoracoscopic surgery (VATS) exhibits advantages over bilateral
surgical procedure in certain cases.
What is known and what is new?
• ENB-guided MWA has become a proven therapeutic strategy in
treating GGOs, which is recommended for patients with poor
pulmonary function.
• The combination of ENB-guided MWA and VATS provided a
potential for treatment optimization in patients with multiple
bilateral GGOs.
What is the implication, and what should change now?
• Bilateral ENB-guided MWA is feasible in patients who cannot
tolerate surgery, and VATS combined with ENB-guided MWA is
safe and can also preserve as much pulmonary function as possible.
Keywords: Electromagnetic navigation bronchoscopy (ENB); microwave ablation (MWA); bilateral pulmonary
nodules; ground-glass opacities (GGOs)
Submitted Jul 01, 2024. Accepted for publication Sep 13, 2024. Published online Oct 30, 2024.
doi: 10.21037/jtd-24-1052
View this article at: https://dx.doi.org/10.21037/jtd-24-1052
Journal of Thoracic Disease, Vol 16, No 10 October 2024 6349
© AME Publishing Company. J Thorac Dis 2024;16(10):6347-6356 | https://dx.doi.org/10.21037/jtd-24-1052
Figure 1 The procedure of simultaneous video-assisted thoracoscopic surgery and ENB-guided MWA. (A) The formation of three different
therapeutic strategies, which were receiving only ENB-guided MWA, simultaneous VATS and ENB-guided MWA, and two-step VATS and
ENB-guided MWA. (B) The most recent chest computed tomography before treatment (patient No. 25) shows the nodule that underwent
ablation and the nodule that underwent surgical resection. (C) Planning the ablation of the lesion in right upper lobe: real-time electromagnetic
navigation displays the sensor probe targeting the nodule, complemented by endobronchial ultrasonography with a guide sheath imaging the
nodule. (D) The surgically resected left lower lung sample for intraoperative histopathology. MWA, microwave ablation; VATS, video-assisted
thoracoscopic surgery; ENB, electromagnetic navigation bronchoscopy.
MWA
MWA-only
Simultaneous
VATS-MWA
Two-step
VATS-MWA
MWA
VAT S MWA
1st VAT S 2nd MWA
B
D
A
C
>7 mm and with highly suspicious of malignancy; (III)
Eastern Cooperative Oncology Group performance status
(PS) of 0 to 2; (IV) no previous history of tumors; (V) no
regional lymph nodes or distant metastases observed in the
preoperative examination.
We chose ablation or resection for the lesions based
on the following principles: (I) for the predominant
lesion, we chose VATS or ENB-guided MWA based on
cardiopulmonary function, and we would perform ENB-
guided biopsy before proceeding the ablation; (II) for the
minor lesions in the ipsilateral lung, we preferred surgical
resection when performing VATS on the predominant
lesion; (III) for the other lesions in the contralateral
lung, we conducted ENB-guided MWA. Finally, the
result was the formation of three different therapeutic
strategies, which were receiving only ENB-guided MWA,
simultaneous VATS and ENB-guided MWA, and two-step
VATS and ENB-guided MWA (Figure 1A).
ENB-guided MWA and biopsy
In our center, we used SuperDimension navigation
Wang et al. The use of ENB-MWA in patients with bilateral GGOs
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system (SuperDimension Inc., Minneapolis, MN, USA)
to proceed ENB procedures, and the MWA procedures
were performed using the MTC-3 MWA system (Vision-
China Medical Devices, Nanjing, China). ENB procedures
were carried out as follows: (I) High-resolution chest
CT scan data were imported into the system to conduct
three-dimensional reconstruction and plan navigation
paths for lung and bronchial images (Figure 1B). (II) Six
positioning points were set within the virtual bronchial
tree reconstructed from imaging, and the images from the
fiberoptic bronchoscope (BF-1TQ290, Olympus, Tokyo,
Japan) were aligned with the virtual bronchial tree based on
these points. (III) The computer automatically planed the
path based on the lesion’s position, and the lesion position
and size were marked on CT images. (IV) Patients were
placed in a supine position under general anesthesia with a
laryngeal mask or endotracheal intubation for ventilation.
(V) Three magnetic poles were symmetrically placed
on the anterior chest, between the sternal angle and the
eighth intercostal space on both sides, forming an isosceles
triangle layout, above the electromagnetic positioning
board. (VI) During navigation, a conventional bilateral
bronchial examination was conducted using the fiberoptic
bronchoscope, and then the positioning guide tube was
inserted into the bronchoscope’s working channel, with
the sensor exposed at the front end. (VII) Under real-time
navigation, the guide tube was controlled to enter the lesion
site, and the lesion was confirmed using an ultrasound
probe (Figure 1C). (VIII) Tissue samples were obtained or
area staining was performed through the extension working
tunnel using biopsy needles, forceps, brush forceps, or ne
catheters. (IX) For the ablation procedure, parameters such
as tumor size, location, morphology, adjacent structures,
access route, and vessel diameter near the nodules were
adjusted. Microwave energy at 0 to 100 W power and
a frequency of 2,450±50 MHz was used. A microwave
antenna (1.8 mm diameter, 1,200 mm effective length, with
water circulation cooling system) was inserted into the
lesion through the ENB’s working channel. Ablation was
conducted with 60 to 80 W power for 4 to 8 minutes per
site, guided by cone beam CT.
Intraoperative histopathology testing involved the
use of rapid on-site evaluation (ROSE). A cytologist
conducted ROSE of specimens, verifying their adequacy,
and identifying tumor cells. Whenever feasible, diagnostic
suspicion was formed based on this assessment. Following
tumor biopsy using ENB, pathology of frozen specimens
was promptly carried out, with two levels of each specimen
utilized for diagnosis. The frozen sections were analyzed by
two senior pathologists, and any discrepancies were resolved
by a third senior pathologist.
VAT S
The patient-specic surgical planning was based on the size,
location, or ENB-guided biopsy of predominant lesions
and the lung function reserve. The VATS were performed
based on the following principles: (I) anatomical sublobar
resection was recommended for the predominant lesion;
(II) pGGOs and mGGOs were preferentially treated with
wedge resection and segmentectomy, respectively; (III)
lobectomy was preferentially chosen for central lesions,
especially for mGGOs; (IV) when the lesion is larger than
2 cm, radiologically or ROSE diagnosed as an invasive
lesion, which will also be considered lobectomy (Figure 1D).
Follow-up
After undergoing ENB-guided treatment or surgery, all
patients received consistent follow-up care, either through
regular outpatient visits or via telephone communication.
The follow-up period began immediately after the surgery
and continued until December 2023. In the first year
following surgery, patients underwent chest CT scans,
tumor marker assessments, and abdominal ultrasonography
every three months. In the second year post-surgery,
these evaluations were performed every six months, and
subsequently, annually.
Statistical analysis
The analyses were performed utilizing R version 4.3.3.
Characteristic data were summarized employing descriptive
statistics, encompassing frequency distributions and cross-
tabulations for discrete variables, and providing mean,
standard deviation, median, interquartile range, minimum,
and maximum values for continuous variables.
We visualized the significant differential or differential
trend of variables using point-plots (6). To annotate
included cases in point-plots, the maximum diameter and
number of GGOs of each case were respectively used as the
x-axis and y-axis. Then, the median value and distinguished
stage were used for the selected continuous and discrete
variables, respectively, to distinguish cases. The condence
intervals of ellipsoidal shape were calculated based on
the distribution of points’ positions. Finally, all included
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variables were compared within each group. The distance
between the centers of condence intervals represented the
degree of difference between the advantageous samples and
the ingroup samples, and the length of distance represented
the contribution in the group selection.
Results
Patient and lesion characteristics
A total of 26 patients with bilateral multiple GGOs
who underwent ENB-guided MWA were included in
this post-analysis. According to the different treatment
procedures received by patients, the detailed information
of characteristics is summarized in Table 1. All patients
underwent preoperative examinations, which included
evaluations of cardiopulmonary function, enhanced chest
CT scans, head magnetic resonance imaging, bone scans,
and positron emission tomography (PET)-CT scans if
deemed necessary. Thirteen men and 13 women were
included, with an overall mean age was 67.7±10.7 years
and a smoking rate of 42.3%. Among male patients, the
majority had a history of smoking (10 in 13). In the MWA-
only group, there were 32 GGOs with a mean size of
18.2±8.0 mm, comprising 28 pGGOs and 4 mGGOs.
The simultaneous VATS-MWA group had 14 GGOs with
a mean size of 15.7±5.3 mm, including 7 pGGOs and
7 mGGOs. The two-step VATS-MWA group exhibited
20 GGOs with a mean size of 14.9±7.6 mm, consisting of
9 pGGOs and 11 mGGOs.
Comparison among three treatment groups
According to the characteristics in Table 1, we further
compared the differences among three treatment groups.
While no signicant differences were found in the baseline
information, the MWA-only group exhibited the worst
pulmonary function (P<0.001) and a trend of poorer
performance status (P=0.06). A higher proportion of cases
with mGGOs was observed in the simultaneous and two-
step groups (P=0.07), although no significant differences
were indicated among the treated GGOs. Additionally,
although the MWA-only group showed the longest ablation
time (P=0.02), a better perioperative efficacy (vs. the
simultaneous group) and comparable lower complication
rates were revealed compared to the other two groups.
There were no significantly different results found in
intraoperative pathology and non-detectable rates among
these three groups. However, earlier stages were indicated
in the postoperative pathology of the simultaneous and two-
step groups (P=0.01).
Analysis of ENB-guided procedure selection
Accordingly, we visualized the statistical differences
in pulmonary function level, PS score, disease pattern
of mGGOs, ablation time length, and postoperative
pathology among the various treatment groups (Figure 2,
see the “Methods” section). We observed that the three
treatment groups exhibit variations across all included
point plots. The MWA-only group displayed significantly
different trends in pulmonary function, PS, disease pattern,
and pathology. Similarly, the simultaneous group exhibited
significant differences in pulmonary function, disease
pattern, ablation time, and pathology. Notably, the two-step
group demonstrated significantly different trends across
all indicators. Further, to conduct intra-group analysis to
identify the variables contributing most to the grouping,
we reorganized the results to visualize the group-based
differences (Figure 3). The intra-group analyses indicated
that disease pattern plays a key role in the selection of
only ENB-guided MWA, while PS score predominantly
inuences the selection of two-step VATS and ENB-guided
MWA.
Discussion
The detection rate of patients presenting as multiple GGOs
is increasing (7). The previous research indicated that
multiple GGOs are mostly multifocal adenocarcinomas,
such as atypical adenomatous hyperplasia, adenocarcinoma
in situ, minimally invasive adenocarcinoma, and invasive
adenocarcinoma (8). The natural history between isolated
and multiple GGOs has not been fully revealed, and the
selection of appropriate intervention for multiple GGOs
remains controversial (9). Surgical resection, particularly
via VATS, is regarded as the preferred treatment for
multiple GGOs. However, when GGOs are dispersed
across different lobes and even involve bilateral lesions, it
poses a signicant challenge for thoracic surgeons (10). The
simultaneous treatment of all lesions presents difficulties
for many cases, particularly those with compromised
cardiopulmonary function unable to tolerate concurrent
resections, and those with bilateral GGOs. Consequently,
our center has tried different hybrid procedures designed
for those patients with multiple GGOs, particularly those
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Table 1 Clinical characteristics and therapeutic summaries
Variables MWA-only (n=13) Simultaneous (n=5) Two-step (n=8) P value
Gender 0.35
Male 8 1 4
Female 5 4 4
Age (years) 0.64
≥60 11 5 6
<60 2 0 2
Tabaco 0.13
Smoking 7 0 4
Non-smoking 6 5 4
Pulmonary function <0.001
FEV1/FVC ratio 0.75±0.05 0.89±0.04 0.82±0.06
ECOG PS 0.06
0 4 5 5
1 8 0 3
2 1 0 0
Disease pattern 0.07
pGGO + pGGO 10 1 2
mGGO + pGGO 2 2 4
mGGO + mGGO 1 2 2
Ablation side >0.99
Left – 2 3
Right – 3 5
GGO treatment >0.99
Number of GGOs by ablation 32 7 9
Number of GGOs by resection – 7 11
Surgical strategy 0.34
Wedge resection – 1 5
Segmentectomy – 3 2
Lobectomy – 1 1
Perioperative efficacy
Ablation time, min 8±4.3 4.6±0.9 3.9±1.8 0.02
Operation time, min 73.1±16.1 108±9.1 103.1±19.3/42.5±5.3 –
Postoperative hospital stay, d 1.3±1.1 8±4.5 4.4±0.5/1.5±0.9 –
Postoperative pain, level 0.9±0.9 1.8±0.4 1.5±0.8/0.5±0.5 –
Table 1 (continued)
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Table 1 (continued)
Variables MWA-only (n=13) Simultaneous (n=5) Two-step (n=8) P value
Complications/adverse events 0.74
Pneumonia (grade I) 1 0 1
Pneumothorax (grade I) 0 0 1
Pneumothorax (grade II) 1 1 0
Intraoperative pathology 0.66
AAH 1 1 0
AIS 2 1 2
MIA 5 2 1
IA 1 0 0
Undetermined 4 1 5 0.32
Postoperative pathology 0.01
AAH 5 2 1
AIS 6 0 1
MIA 0 0 4
IA 2 3 2
Data are expressed as n and mean ± standard deviation. MWA, microwave ablation; FEV1, forced expiratory volume in one second; FVC,
forced vital capacity; ECOG PS, Eastern Cooperative Oncology Group performance status; GGO, ground-glass opacity; pGGO, pure GGO;
mGGO, mixed GGO; AAH, atypical adenomatous hyperplasia; AIS, adenocarcinoma in situ; MIA, minimally invasive adenocarcinoma; IA,
invasive adenocarcinoma.
unable to undergo simultaneous surgical resection.
Multiple GGOs could often be categorized as
synchronous multiple primary lung cancers (sMPLC).
These patients with multiple GGOs or sMPLC faced
a risk of incorrect staging from initial imaging studies.
Both clinical and radiographic assessments might lead
to either over-staging or under-staging. CT scans, when
inaccurate, tended to under-stage patients, while PET-CT
scans, when incorrect, often over-stage by interpreting a
second primary nodule as “consistent with metastasis” (11).
Accurate staging typically requires careful evaluation of the
mediastinum, often using PET-CT, to ensure no uptake in
mediastinal lymph nodes and the absence of extra-thoracic
metastases (12). Previous studies explored other therapeutic
options, including stereotactic body radiation therapy
(SBRT) and tyrosine kinase inhibitors (TKIs) (13,14). SBRT
was shown to be a safe and effective treatment for patients
with multiple GGOs or sMPLC and was considered
a viable alternative to surgery. The 1-, 3-, and 5-year
overall survival rates were 100.0%, 91.6%, and 82.8%,
respectively (13). Postoperative EGFR-TKI treatment
demonstrated efcacy in addressing persistent lesions after
surgery, offering signicant benets for patients with more
than two remaining lesions, mGGO patterns, or residual
lesion diameters ≥8 mm (14).
Presently, few studies reported the systematic application
of ENB-guided MWA in patients with multiple GGOs,
especially bilateral multiple GGOs. Narsule et al. were
the first to report that CT-guided percutaneous thermal
ablation of lung tumors, with the assistance of a magnetic
navigation system, was effective in reducing the time for
the ablation needle to reach its target and the duration of
treatment (15). Then, Jiang et al. reported the feasibility
of the combination of ENB-guided MWA and VATS
on patients with multiple GGOs (3), which showed that
ENB-guided MWA combined with VATS is an alternative
treatment strategy to deal with multiple GGOs at the
same stage of the operation in the specifical population.
Further, Qu et al. and Zeng et al. reported the systematical
application of ENB-guided MWA with or without VATS in
multiple GGOs (4,5), which conrmed that the application
of ENB-guided MWA on multiple GGOs is safe and
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Figure 2 The visualization of differential baseline information among patients receiving only ENB-guided MWA, simultaneous VATS
and ENB-guided MWA, and two-step VATS and ENB-guided MWA. The number and maximum diameter of GGOs were warranted
to demonstrate disease status of each case. The median value or distinguished stage were used to distinguish point size. For the discrete
variables, values of 1 or 2 were assigned for worse PS; including mGGO was considered as progressed disease pattern; MIA or IA was
regarded as advanced pathology stage. The ellipsoidal shape represents the condence intervals of included points. ENB, electromagnetic
navigation bronchoscopy; MWA, microwave ablation; VATS, video-assisted thoracoscopic surgery; GGO, ground-glass opacity; mGGO,
mixed GGO; PS, performance status; MIA, minimally invasive adenocarcinoma; IA, invasive adenocarcinoma.
0 1 2 3 4
Max size of GGO, cm
0 1 2 3 4
Max size of GGO, cm
0 1 2 3 4
Max size of GGO, cm
0 1 2 3 4
Max size of GGO, cm
0 1 2 3 4
Max size of GGO, cm
0 1 2 3 4
Max size of GGO, cm
Control
Pattern
Pulmonary function
Ablation time
PS
Pathology
One-stage
Simultaneous
Two-stage
Number of GGONumber of GGO
Number of GGONumber of GGO
Number of GGONumber of GGO
6
4
2
6
4
2
6
4
2
6
4
2
6
4
2
6
4
2
efcient.
In this study, we summarized three therapeutic strategies
for patients with bilateral GGOs based on ENB-guided
MWA. According to the above-mentioned analyses on
ENB-guided procedures (Figure 2), patients could be
classied according to the differential status of disease and
general condition. When the density or diameter of the
predominant lesion is relatively small, the bilateral ENB-
guided MWA was the preferred choice for patients with
poor general condition. For patients with more severe
lesions and good general condition, most cases underwent
simultaneous VATS and ENB-guided MWA. For patients
with severe lesions and general overall condition, VATS
followed by a second stage ENB-guided MWA was
recommended. Notably, within the simultaneous VATS-
MWA group, one patient underwent a diagnostic ENB-
guided biopsy before VATS and ENB-guided MWA,
which indicated Biopsy-VATS-MWA process. Therefore,
further investigation is required to assess the feasibility of
conducting either VATS-MWA or Biopsy-VATS-MWA.
Conclusions
In conclusion, there are several limitations in this study.
Firstly, it was a retrospective study with a relatively small
sample size. Secondly, our follow-up of patients was limited,
and the long-term prognosis still requires validation. Large-
scale randomized studies are still needed to conduct further
investigations into the efficacy and safety of different
treatment procedures. However, the results of our study
demonstrate that this systematic hybrid technique, ENB-
guided MWA for bilateral multiple GGOs, is both safe and
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Figure 3 The visualization of intra-group differences within each treatment procedure. The number and maximum diameter of GGOs
were warranted to demonstrate disease status of each case. The ellipsoidal shapes are the summarized condence intervals in Figure 2, and
the arrows between these centroids represent differences between the included baseline information and the control group. The red arrow
represents the longest centroid distance, which indicates the highest contribution in treatment selection. GGO, ground-glass opacity; MWA,
microwave ablation.
0 1 2 3 4
Max size of GGO, cm
0 1 2 3 4
Max size of GGO, cm
0 1 2 3 4
Max size of GGO, cm
MWA-only Simultaneous Two-step
Number of GGO
Number of GGO
Number of GGO
6
4
2
6
4
2
6
4
2
effective. Furthermore, it even exhibits clear advantages
over bilateral surgical procedure in certain cases.
Acknowledgments
Funding: The study was supported by the National Natural
Science Foundation of China grants (No. 82203202), the
Research Program of Jiangsu Commission of Health (No.
ZD2022027), and the Program of Nanjing Municipal
Science and Technology Bureau (No. 2022SX00000446).
Footnote
Reporting Checklist: The authors have completed the
PROCESS reporting checklist. Available at https://jtd.
amegroups.com/article/view/10.21037/jtd-24-1052/rc
Data Sharing Statement: Available at https://jtd.amegroups.
com/article/view/10.21037/jtd-24-1052/dss
Peer Review File: Available at https://jtd.amegroups.com/
article/view/10.21037/jtd-24-1052/prf
Conicts of Interest: All authors have completed the ICMJE
uniform disclosure form (available at https://jtd.amegroups.
com/article/view/10.21037/jtd-24-1052/coif). The authors
have no conicts 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
institutional ethics board of Jiangsu Cancer Hospital (No.
JSLMTCR-2020-062) and individual consent for this
retrospective analysis was waived.
Open Access Statement: This is an Open Access article
distributed in accordance with the Creative Commons
Attribution-NonCommercial-NoDerivs 4.0 International
License (CC BY-NC-ND 4.0), which permits the non-
commercial replication and distribution of the article with
the strict proviso that no changes or edits are made and the
original work is properly cited (including links to both the
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See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
References
1. Folch EE, Pritchett MA, Nead MA, et al. Electromagnetic
Navigation Bronchoscopy for Peripheral Pulmonary
Lesions: One-Year Results of the Prospective, Multicenter
NAVIGATE Study. J Thorac Oncol 2019;14:445-58.
2. 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
Wang et al. The use of ENB-MWA in patients with bilateral GGOs
6356
© AME Publishing Company. J Thorac Dis 2024;16(10):6347-6356 | https://dx.doi.org/10.21037/jtd-24-1052
2013;143:e142S-65S.
3. Jiang N, Zhang L, Hao Y, et al. Combination of
electromagnetic navigation bronchoscopy-guided
microwave ablation and thoracoscopic resection: An
alternative for treatment of multiple pulmonary nodules.
Thorac Cancer 2020;11:1728-33.
4. Qu R, Tu D, Hu S, et al. Electromagnetic Navigation
Bronchoscopy-Guided Microwave Ablation Combined
With Uniportal Video-Assisted Thoracoscopic Surgery
for Multiple Ground Glass Opacities. Ann Thorac Surg
2022;113:1307-15.
5. Zeng C, Fu X, Yuan Z, et al. Application of electromagnetic
navigation bronchoscopy-guided microwave ablation in
multiple pulmonary nodules: a single-centre study. Eur J
Cardiothorac Surg 2022;62:ezac071.
6. Maynard A, McCoach CE, Rotow JK, et al. Therapy-
Induced Evolution of Human Lung Cancer Revealed
by Single-Cell RNA Sequencing. Cell 2020;182:1232-
1251.e22.
7. Shimada Y, Saji H, Otani K, et al. Survival of a surgical
series of lung cancer patients with synchronous multiple
ground-glass opacities, and the management of their
residual lesions. Lung Cancer 2015;88:174-80.
8. Zhang Y, Fu F, Chen H. Management of Ground-Glass
Opacities in the Lung Cancer Spectrum. Ann Thorac Surg
2020;110:1796-804.
9. Jiang L, He J, Shi X, et al. Prognosis of synchronous and
metachronous multiple primary lung cancers: systematic
review and meta-analysis. Lung Cancer 2015;87:303-10.
10. Yang H, Sun Y, Yao F, et al. Surgical Therapy for Bilateral
Multiple Primary Lung Cancer. Ann Thorac Surg
2016;101:1145-52.
11. Tabrizi NS, Harris ES, Gallant BP, et al. Clinical
and pathologic staging accuracy in patients with
synchronous multiple primary lung cancers. J Thorac
Dis 2024;16:491-7.
12. Liu H, Polley L. Bilateral synchronous multiple lung
cancer: an emerging problem. Lung Cancer Manag
2023;12:LMT62.
13. Jang JY, Kim SS, Song SY, et al. Clinical Outcome
of Stereotactic Body Radiotherapy in Patients with
Early-Stage Lung Cancer with Ground-Glass Opacity
Predominant Lesions: A Single Institution Experience.
Cancer Res Treat 2023;55:1181-9.
14. Cheng B, Li C, Zhao Y, et al. The impact of postoperative
EGFR-TKIs treatment on residual GGO lesions after
resection for lung cancer. Signal Transduct Target Ther
2021;6:73.
15. Narsule CK, Sales Dos Santos R, Gupta A, et al. The
efcacy of electromagnetic navigation to assist with
computed tomography-guided percutaneous thermal
ablation of lung tumors. Innovations (Phila) 2012;7:187-90.
Cite this article as: Wang S, Su C, Li J, Yin N, Wu C, Gao R,
Zhang S, Wang X, Lin Z, Li D, Hu J, Li M. The use of
electromagnetic navigation bronchoscopy-guided microwave
ablation in patients with multiple bilateral pulmonary nodules: a
retrospective study of 26 cases. J Thorac Dis 2024;16(10):6347-
6356. doi: 10.21037/jtd-24-1052
