Introduction
With the spread of coronavirus disease 2019 and the popularization of low-dose spiral computed tomography (CT) in physical examination, increasing asymptomatic pulmonary nodules have been identified [
1]. Pulmonary nodules [
2,
3] are round or irregular lesions with a diameter of ≤ 3 cm in the lungs that appear as dense shadows on imaging. They can be well-defined or poorly demarcated lesions with single or multiple occurrences. Lesions with a diameter of 5–10 mm are defined as small pulmonary nodules. According to related study [
4], the prevalence of malignant tumors among small pulmonary nodules with a diameter of 5–10 mm is 6%–28%. Therefore, a definite pathological diagnosis of small pulmonary nodules is urgently needed. However, it is challenging to determine the nature of small pulmonary nodules on imaging alone and accurately diagnose small pulmonary nodules even with the application of techniques such as fiberoptic bronchoscopy with biopsy and CT-guided fine-needle aspiration biopsy.
In recent years, thoracoscopic surgery has played an important role in the pathological diagnosis and resection of small pulmonary nodules. However, thoracoscopic surgery has limitations in the accurate resection of small pulmonary nodules, and the accurate localization of small pulmonary nodules before surgery has accordingly been the key to its success. Therefore, the clinical application of the CT-guided hook-wire localization technique in thoracoscopic surgery for small pulmonary nodules is necessary. At present, the pre- and intraoperative positioning methods in thoracoscopic surgery include CT-guided hook-wire positioning, micro-coils positioning, percutaneous injection of materials (methylene blue, agar localization, barium, lipiodol, medical glue, etc.) for positioning, intraoperative ultrasound positioning, finger palpation positioning, etc. Among them, CT-guided hook-wire positioning technology is most commonly used [
5,
6]. This study aimed to investigate the practicability and safety of the clinical application of the CT-guided hook-wire localization technique in thoracoscopic surgery for small pulmonary nodules.
Results
A total of 50 cases in the localization group (58 nodules) underwent CT-guided hook-wire localization for puncture. Of them, 57 lesions (98.3%) were successfully located, while localization failed in one (1.7%). The patients included 13 men (26%) and 37 women (74%) aged 28–73 (mean, 54.66 ± 9.373) years old. The simultaneous localization of two pulmonary nodules was performed in eight patients; the mean nodule diameter was 7.046 ± 2.248 (range, 2.8–10.0 mm) mm. Ten patients (20%) had a history of smoking and six (12%) had a history of lung disease. Nine lesions (15.5%) were solid, 41 (70.7%) were pure ground glass nodules, and eight (13.8%) were part-solid nodules.
Twenty-two lesions (37.9%) were in the right upper lobe of the lung, 12 (20.7%) were in the right lower lobe, seven (12.1%) were in the right middle lobe, 11 (18.9%) were in the left upper lobe, and six (10.3%) were in the left lower lobe. The postoperative pathology was malignant in 68.9% of the lesions. There were 100 patients (35 men [35%], 65 women [65%]) in the control group aged 29–77 (mean, 54.75 ± 10.032) years. Simultaneous resection of two ipsilateral small pulmonary nodules was performed in 10 patients. The mean nodule diameter was 7.795 ± 2.055 (range, 3–10.0) mm. There were 13 (11.8%) solid nodules, 81 (73.6%) pure ground glass nodules, and 16 (14.6%) mixed ground glass nodules. A total of 32 lesions (29.1%) were in the right upper lobe of the lung, 21 (19.1%) were in the right lower lobe, 12 (10.9%) were in the right middle lobe, 26 (23.6%) were in the left upper lobe, and 19 (17.3%) were in the left lower lobe. The postoperative pathology of 76.3% of the nodules was malignant. There was no significant intergroup differences in the general data (
P ≥ 0.05) (Table
1).
Table 1
Patients’ general characteristics by study group
Number of patients (n) | 50 | 100 | |
Sex, n (%) | | | 0.265 |
Male | 13 (26) | 35 (35) | |
Female | 37 (74) | 65 (65) | |
Mean age, years, \(\overline{x}\) ± s | 54.66 ± 9.373 | 54.75 ± 10.032 | 0.734 |
History of lung disease, n (%) | | | 0.473 |
Positive | 6 (12) | 7 (7) | |
Negative | 44 (88) | 93 (93) | |
History of smoking, n (%) | | | 0.767 |
Positive | 10 (20) | 18 (18) | |
Negative | 40 (80) | 82 (82) | |
Nodule type, n (%) | 58 | 110 | 0.286 |
Single occurrence | 42 (84) | 90 (90) | |
Multiple occurrences | 8 (16) | 10 (10) | |
Nodule diameter, mm, \(\overline{x}\) ± s | 7.046 ± 2.248 | 7.795 ± 2.055 | 0.053 |
Nodule properties, n (%) | | | 0.796 |
Solid nodules | 9 (15.5) | 13 (11.8) | |
Pure ground glass nodules | 41 (70.7) | 81 (73.6) | |
Mixed ground glass nodules | 8 (13.8) | 16 (14.6) | |
Nodule location, n (%) | | | 0.623 |
Right upper lobe | 22 (37.9) | 32 (29.1) | |
Right middle lobe | 7 (12.1) | 12 (10.9) | |
Right lower lobe | 12 (20.7) | 21 (19.1) | |
Left upper lobe | 11 (19.0) | 26 (23.6) | |
Left lower lobe | 6 (10.3) | 19 (17.3) | |
Type of final surgical approach after pathological diagnosis, n (%) | | | 0.056 |
Pulmonary wedge resection | 38 (76) | 56 (56) | |
Segmentectomy | 6 (12) | 24 (24) | |
Lobectomy | 6 (12) | 20 (20) | |
Postoperative pathology, n (%) | | | 0.282 |
Adenocarcinoma in situ | 27 (46.6) | 49 (44.5) | |
Invasive adenocarcinoma | 10 (17.2) | 30 (27.3) | |
Minimally invasive adenocarcinoma | 3 (5.2) | 5 (4.5) | |
Atypical adenomatous hyperplasia | 6 (10.3) | 9 (8.2) | |
Benign lesions | 12 (20.7) | 17 (15.5) | |
CT-guided localization and puncture outcomes
There were 50 patients in the localization group, in which a total of 58 pulmonary nodules were localized. The localization success rate was 98.3% (57/58). The reason for the failure to locate one pulmonary nodule was that it was found to fall off during surgery after successful localization. Finally, according to the location of the bleeding point of the puncture needle, the video-assisted thoracoscopic wedge resection of the lung was successfully performed. The mean puncture depth was 54.89 ± 13.915 (range, 30.56–84.8) mm, and the mean puncture time was 14.66 ± 5.181 (range, 10–35) min. The incidence of localization-related complications was 24% (12/50), while the incidence of pneumothorax was 16% (8/50); all were asymptomatic pneumothorax requiring no specific treatment. The incidence of intrapulmonary hematoma was 4% (2/50); no relevant treatment was adopted since the patient did not complain of discomfort after positioning. There was one case (2%) of pleural reaction that was relieved after rest; no special treatment was provided. One patient (2%) successfully underwent wedge resection of the lung according to the hematoma at the puncture point on the lung surface and the localization depth after unhooking of the locating needle. No serious complications such as severe pneumothorax, massive hemorrhage, or embolism occurred during the puncture process (Table
2).
Table 2
Computed tomography-guided localization and puncture outcomes
Nodule diameter, mm | 7.05 ± 2.248 (2.8–10.0) |
Distance from pleura, mm | 22.40 ± 11.395 (5.47–79.47) |
Puncture depth, mm | 54.89 ± 13.915 (30.56–84.8) |
Puncture time, min | 14.66 ± 5.181 (10–35) |
Single occurrence | 13.31 ± 2.542 (10–18) |
Multiple occurrences | 22.75 ± 7.924 (15–35) |
Localization-related complications | 12 (24.0) |
Pneumothorax | 8 (16.0) |
Intrapulmonary hematoma | 2 (4.0) |
Pleural reaction | 1 (2.0) |
Half-shedding | 1 (2.0) |
The mean operation time of the localization group was 103.88 ± 41.72 min, which was significantly shorter than that of the control group (133.30 ± 45.42 min,
P < 0.05). The mean intraoperative blood loss (44.20 ± 34.17 mL) was significantly lower in the localization group than in the control group (100.60 ± 132.78 mL,
P < 0.05). The mean days of hospitalization was significantly shorter in the localization (7.96 ± 2.34 days) than in the control group (9.21 ± 3.25 days,
P < 0.05) (Table
3).
Table 3
Surgery-related indicators by study group (\(\overline{x}\) ± s)
Operation time, min | 103.88 ± 41.72 | 133.30 ± 45.42 | 0.000 |
Intraoperative blood loss, mL | 44.20 ± 34.17 | 112.30 ± 219.90 | 0.000 |
Hospital stay, days | 7.96 ± 2.34 | 9.21 ± 3.25 | 0.025 |
Uni- and multivariate analysis of localization-related pneumothorax
In our attempt to further clarify the risk factors for localization-related pneumothorax in the localization group, three variables were identified as likely associated with localization-related pneumothorax through univariate analysis. In the multivariate logistic regression analysis, the localization times of nodules was an independent risk factor for localization-related pneumothorax. (odds ratio, 10.966; 95% confidence interval, 1.333–90.236;
P = 0.026) (Table
4).
Table 4
Univariate and multivariate analyses of localization-related pneumothorax
Age | 0.951 (0.882–1.026) | 0.192 | | |
Sex | 1.920 (0.388–9.489) | 0.424 | | |
History of smoking | 6.000 (1.172–30.725) | 0.032 | 2.341 (0.287–19.108) | 0.427 |
History of lung disease | 7.800 (1.225–49.677) | 0.030 | 4.136 (0.450–38.056) | 0.210 |
Localization time | 0.719 (0.502–1.028) | 0.071 | | |
Puncture depth | 0.975 (0.918–1.036) | 0.412 | | |
Localization times of nodules | 21.667 (3.402–137.992) | 0.001 | 10.966 (1.333–90.236) | 0.026 |
Distance from pleura | 0.890 (0.792–1.000) | 0.050 | | |
Nodule diameter | 1.284 (0.879–1.876) | 0.197 | | |
Reasons for conversion to thoracotomy and lobectomy
In the control group, 16 cases (16%) were converted to thoracotomy and lobectomy during surgery (Table
5). The main reason for the conversion to lobectomy was that the finger palpation did not touch the pulmonary nodules during the operation (11 cases) and the conversion thoracotomy was the discovery of severe pleural adhesions (5 cases). One case (2%) in the localization group was converted to thoracotomy due to severe pleural adhesions. The conversion rate to thoracotomy and lobectomy was 2% in the localization group versus 16% in the control group (Table
5).
Table 5
Reasons for conversion to thoracotomy and lobectomy by study group
Failed preoperative localization | – | – |
Decoupling | – | – |
Failed intraoperative localization | – | 11 |
Severe pleural adhesions | 1 | 5 |
Total converted to thoracotomy and lobectomy | 1 (2%) | 16 (16%) |
Discussion
In recent years, the incidence of lung cancer has been second only to breast cancer; however, it still has the highest mortality rate [
8]. With the increasing popularity of low-dose spiral CT in physical examination, the detection rate of small pulmonary nodules has increased significantly. Approximately 50% of small pulmonary nodules are malignant [
9]. However, it is difficult to identify the pathology using traditional CT-guided percutaneous lung puncture and bronchoscopy with biopsy, and false-negative results occur. According to relevant reports [
10,
11], in 29% of cases, the possibility of malignancy cannot be ruled out due to insufficient histological evidence. VATS has the advantages of a high diagnostic rate, short operation time, and minimal trauma; thus, it has become an important method for the diagnosis and treatment of small pulmonary nodules [
11]. However, VATS has limitations in terms of resection of small pulmonary nodules due to the small size of the pulmonary nodules and difficulty with lesion localization. As a result, accurate positioning has become the key to the diagnosis and treatment of small pulmonary nodules. Multiple positioning methods used in the clinical setting can be broadly divided into two categories: intraoperative non-invasive localization and preoperative invasive localization. Among them, the common non-invasive localization methods include intraoperative finger palpation and intraoperative ultrasound localization.
Invasive localization methods include CT-guided hook-wire localization, CT-guided percutaneous injection of material (micro-coil positioning, methylene blue, agar positioning, barium, lipiodol, medical glue, etc.) for positioning and other positioning methods.
In recent years, relevant medical practitioners have used electromagnetic navigation bronchoscopy (ENB) for intraoperative localization. Awais and Luo et al [
12,
13] confirmed the successful application of ENB in the localization and resection of pulmonary nodules, Chao [
14] et al. performed intraoperative localization in a hybrid operating room (HOR), which has a similar diagnostic rate compared to other invasive preoperative localization such as percutaneous lung puncture localization. The rates of complications such as pneumothorax and bleeding was also significantly reduced [
15]. However, ENB has high technical requirements for operation, high costs of mixed laboratories, and expensive inspection equipment. Only a few hospitals in China have such equipment and mixed operating rooms, which limits its clinical popularity.
It is generally believed that the CT-guided hook-wire localization technique is the most commonly used pulmonary nodule localization technology [
5,
6,
9]. This localization technique requires the placement of an anchor needle (first used in the localization of breast lumps) in the lung tissue adjacent to the pulmonary nodule under CT guidance. This locating needle is a disposable pulmonary nodule locating needle improved by Fan [
16] et al. based on the traditional hook-wire positioning device. The most common complication of this positioning technique is pneumothorax. Hanauer [
17] et al. studied 181 cases of solitary pulmonary nodules and found that the rate of pneumothorax in patients underwent hook-wire localization could reach 38%. The incidence of pneumothorax in this study was 16% (8/50), which was lower than that reported in the above study. This may be related to the skilled operation of the surgeons and their mastery of the indications for preoperative hook-wire puncture positioning. Upon studying 276 patients with hook-wire positioning, Iguchi et al. [
18] concluded that increased respiratory motion during positioning, pulmonary nodules that are located in the lower lobe of the lung, pulmonary nodules with solid components, prone patient position, and puncture path that passes through the interlobar fissures are all factors that may cause pneumothorax.
Most patients have mild symptoms that do not require special treatment. Li et al. [
19] reported that the incidence of hook-wire pulmonary hemorrhage was 13.9%–36%. In this study, the incidence of intrapulmonary hemorrhage was 4% (2/50), which is much lower than those reported in the above-mentioned studies. This may be related to the small number of cases in the localization group. Hwang et al. [
20] performed hook-wire localization in 45 patients and found that hook-wire displacement occurred in 8.9% of patients. In our study, half-shedding occurred only in one patient (2%) after positioning. The displacement rate was much lower than that reported in the other hook-wire studies. In the one case in which the locating needle fell off in this study, the lesion was relatively close to the pleura. The displacement of the locating needle is related to the depth of the release position of the puncture needle and preoperative pulling to the locating needle. Pleural reactions are generally caused by irritation of the pleura by detachment of the positioning line or the locating needle, which is common in elderly and frail patients. In this patient, the occurrence of pleural reaction was due to his excessive tension and weakness, leading to dizziness and a decrease in blood pressure after the puncture; his symptoms were relieved after rest, and no serious complications occurred. However, in clinical practice, it is necessary to prevent the occurrence of severe pleural reactions.
In the diagnosis and treatment of small pulmonary nodules, CT-guided hook-wire localization technology can reportedly [
21] help accurately locate and rapidly remove lesions during thoracoscopic surgery, thus effectively shortening the operation time. The duration of thoracoscopic surgery, intraoperative bleeding and hospital stay of patients in both groups were recorded, and the results showed that the operation time, intraoperative bleeding and hospital stay in the positioning group were significantly lower than those in the control group, which is consistent with the results of the above studies.
This study explored the efficacy and safety of CT-guided hook-wire localization in thoracoscopic surgery for small pulmonary nodules through clinical practice with a certain number of cases. The univariate analysis revealed that three variables were associated with localization-related pneumothorax. The number of localized small pulmonary nodules was an independent risk factor for localization-related pneumothorax, as was indicated by multivariate regression analysis, consistent with previous findings [
22]. Considering that relatively more holes were created by the insertion of multiple locating needles into the visceral pleura due to the simultaneous placement of two locating needles in our study, the chance of air entering the pleural cavity was increased [
23]. In the course of clinical diagnosis and treatment, many patients have multiple occurrences of pulmonary nodules. The incidence of pneumothorax in patients during localization process may be relatively high, so effective measures to prevent pneumothorax should be prepared before the procedure. The rate of conversion to thoracotomy in the two groups was 2% versus 16% (control versus localization group), and the difference was statistically significant. In this study, 68.9% and 76.3% of the resected small pulmonary nodules in the localization group and the control group, respectively, were finally diagnosed as malignant; both were higher than the previously reported malignancy rate of small pulmonary nodules with a diameter of < 10 mm (6%–28%); this may be due to the fact that only those small pulmonary nodules that are highly suspected as malignant by the observation of their imaging properties are further inspected surgically for diagnosis and treatment in clinical practice; no further analysis would be performed because the localization was not necessarily related to the postoperative nature of the nodules. Once the hook-wire localization technique guided by CT is practiced in a large number of cases, it can be developed into a localization technique that is mastered by physicians in clinical departments. This can significantly improve the early diagnosis and resection rates of small pulmonary nodules and provide effective help for the detection and treatment of early-stage lung cancer (Additional file
1).
This retrospective study was performed at a single center with a small sample size. Thus, future multicenter studies with large sample sizes are needed to validate our findings.
In conclusion, CT-guided hook-wire localization technique has certain clinical application value in thoracoscopic surgery for small pulmonary nodules. It can accurately locate small pulmonary nodules, reduce intraoperative blood loss, shorten operation time and hospitalization days, and reduce the conversion rate to thoracotomy, thereby facilitating the early diagnosis and treatment of lung cancer. Simultaneous localization of multiple nodules can easily lead to the occurrence of localization-related pneumothorax. Thus, this technique is worth spreading.
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