Retrospective study on preoperative hook wire localisation of pulmonary ground-glass nodules: risk factors for complications and preventive strategies
Original Article

Retrospective study on preoperative hook wire localisation of pulmonary ground-glass nodules: risk factors for complications and preventive strategies

Chuanxi Wang1, Chang Chen2, Gaohua Liu1, Zhiquan Li3, Delai Zheng1, Xiaoliang Li1

1Department of Cardiothoracic Surgery, The First People’s Hospital of Neijiang, Neijiang, China; 2Department of Pathology, West China Hospital of Sichuan University, Chengdu, China; 3Department of Nuclear Medicine, The First People’s Hospital of Neijiang, Neijiang, China

Contributions: (I) Conception and design: C Wang, C Chen; (II) Administrative support: X Li; (III) Provision of study materials or patients: G Liu, Z Li; (IV) Collection and assembly of data: C Wang, D Zheng; (V) Data analysis and interpretation: C Wang, G Liu; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Xiaoliang Li, MMed, PhD. Department of Cardiothoracic Surgery, The First People’s Hospital of Neijiang, No. 1866, West Section of Hanan Avenue, Shizhong District, Neijiang 641000, China. Email: lixiaoliang_ys@yeah.net.

Background: Adjusting the angle of the trajectory needle may help reduce the occurrence of complications associated with preoperative hook and thread localisation. This study aims to examine the risk factors for complications associated with preoperative hook wire localisation of pulmonary ground-glass nodules (GGNs).

Methods: In this single-centre retrospective study, an analysis was conducted on 230 preoperative hook wire implantations for 230 pulmonary GGNs. We assessed the angle of needle trajectory by analysing the computed tomography (CT) images at the point of needle insertion. We evaluated the main variables related to patient demographics, lesion size and location and preoperative conditions to determine the risk factors for complications. Univariate and multivariate logistic regression analyses were used to establish a predictive model to evaluate the incidence of hook wire localisation complications.

Results: A total of 230 patients were included in the final analysis. Pneumothorax and intrapulmonary hemorrhage were the primary complications, occurring in 38.7% and 18.7% of cases, respectively. The results from the multivariate logistic regression analysis demonstrated a positive correlation between the needle insertion angle and the occurrence of pneumothorax [odds ratio (OR): 1.035, 95% confidence interval (CI): 1.008–1.063, P=0.011] as well as intrapulmonary hemorrhage (OR: 1.057, 95% CI: 1.020–1.095, P=0.002). Pneumothorax was associated with factors such as emphysema (OR: 12.286, 95% CI: 3.687–40.938, P<0.001), the nearest pleural distance (OR: 0.944, 95% CI: 0.907–0.983, P=0.005), and the number of punctures (OR: 3.443, 95% CI: 2.006–5.907, P<0.001). Similarly, pulmonary hemorrhage was correlated with variables such as the number of punctures (OR: 1.894, 95% CI: 1.080–3.322, P=0.026), chest wall access thickness (OR: 0.951, 95% CI: 0.915–0.988, P=0.010), and the length of intrapulmonary access (OR: 1.060, 95% CI: 1.016–1.106, P=0.007).

Conclusions: In summary, reducing the needle trajectory angle can alleviate complications linked to preoperative hook wire localisation, and employing predictive models before puncture site selection, along with strategic needle insertion planning, can effectively minimise procedural risks.

Keywords: Pulmonary ground-glass nodules (pulmonary GGNs); complications; preoperative localisation; angle of the needle trajectory; predictive models


Submitted May 27, 2024. Accepted for publication Jan 27, 2025. Published online Mar 28, 2025.

doi: 10.21037/qims-24-1051


Introduction

An increasing number of ground-glass nodules (GGNs) are being incidentally discovered due to the heightened awareness of health examinations and the expanded use of low-dose computed tomography (CT) for lung cancer screening (1). Current treatment options for high-risk pulmonary GGNs include follow-up observation, surgical resection, needle biopsy and radiofrequency ablation (2). Video-assisted thoracoscopic sublobar resection—comprising lung wedge resection, segmentectomy and combination segmentectomy—has become a primary surgical approach for GGNs (3,4). However, thoracic surgeons may struggle to locate small lesions or those situated far from the pleura during palpation or thoracoscopy. Thus, effective preoperative localisation is critical for the successful surgical management of these nodules. Prior research indicates that the ability to detect pulmonary nodules during thoracoscopy visually is hindered when the nodule’s diameter is smaller than 15 mm or more than 10 mm under the pleurae (5).

Since Plunkett et al. (6) developed a short hook wire and suture system as a preoperative CT-guided localisation method in 1992, this system has been frequently used because of its high feasibility and clinical usefulness. Although numerous recent studies have validated the safety and efficacy of preoperative localisation (7), it is important to note that hook wire localisation carries the risk of puncturing the visceral pleura and lung, leading to complications such as pneumothorax, pulmonary haemorrhage and haemothorax (8). Moreover, a few patients may experience serious complications such as air embolism (9). Most complications do not pose a threat to the patient’s life, but they frequently affect the outcome of the procedure and the patient’s overall experience. Currently, there is no viable method for preventing and detecting these potential risks. Several investigations have indicated that the translobar fissure pathway (7), numerous punctures (10) and emphysema (11) are significant risk factors for pneumothorax in the context of localised nodules and lung biopsies. At the same time, some studies have suggested that the supine position (12) and the length of intrapulmonary access (13) are high-risk factors for intrapulmonary haemorrhage. A study on needle biopsy procedures revealed that a needle-pleural angle of ≥51° was identified as a risk factor for a high incidence of pneumothorax (14). Previous studies have identified several risk factors and protective factors associated with preoperative hook wire localization. For example, one study found that a single puncture through the visceral pleura was an independent protective factor for pneumothorax, while pneumothorax itself was a risk factor for wire dislodgement (15). Another study reported that multiple punctures and specific locations of punctures on the chest wall were significantly associated with moderate to severe pain after needle localization (16). However, none of these studies have considered the needle angle as a contributing factor to complications. Adjusting the angle of the trajectory needle may help reduce the occurrence of complications associated with preoperative hook and thread localisation.

This study involves a retrospective analysis of the complications and risk factors associated with preoperative hook wire localisation under CT guidance. The incidence of complications is evaluated by developing a prediction model. Additionally, the risk factors for complications during preoperative localisation are analysed, and the relationship between needle angle and surgical complications is explored. We present this article in accordance with the STROCSS reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1051/rc).


Methods

Instruments

This study used a GE Lingspeed (Wisconsin, USA) double-row spiral CT scanner for puncturing. The CT scan was performed with calm breathing using a layer thickness of 2.5 mm, a layer spacing of 2.5 mm and a screw pitch of 1.375:1. Additionally, a disposable hook wire needle (Model SS510-10, 20 G ×100 mm) from Ningbo Shengjiekang Biotechnology Co., Ltd. (Ningbo, China) was used to identify pulmonary nodules (17).

Patients

This was a single-centre retrospective study. The criteria for preoperative hook wire localisation were as follows: a maximum diameter of ≤10 mm and the use of only one hook wire. The exclusion criteria were as follows: the presence of metastatic tumours or a history of ipsilateral lung surgery, radiation and/or chemotherapy. Between March 2021 and May 2022, 247 localisation procedures using a short hook wire were conducted for 247 small pulmonary lesions before performing a video-assisted thoracoscopic surgery (VATS) at the hospital. Out of them, 17 procedures that involved solid nodules or nodules with a diameter of >10 mm were not considered. In this study, a total of 230 preoperative hook wire implantations were performed for 230 pulmonary GGNs. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The current retrospective study was approved by the ethics committee of The First People’s Hospital of Neijiang (No. 2020-07). Since we only reviewed medical records of the patients, and no individual patient could be identified from the data, the requirement for informed consent was waived by the ethics committee of The First People’s Hospital of Neijiang.

Procedures

The treatment involved the collaboration of a thoracic surgeon and a radiologist, each with over 10 years of experience. Preoperative hook wire placements were performed under local anaesthesia, with the patient remaining conscious. The process began with the patient positioned appropriately (supine, lateral or prone) based on preoperative CT imaging, which also guided the precise placement of the CT fast-guiding pad over the insertion area, optimising the puncture location near the chest wall close to the nodule. Special attention was required to avoid critical structures, such as the scapula and subclavian arteries, especially when targeting nodules in the middle or upper lobes, occasionally necessitating repositioning. A CT scan confirmed the nodule’s location, and a trajectory avoiding major blood vessels, interlobar fissures, the liver and existing lesions was planned. Following sterilisation and local anaesthesia at the puncture site, a hook wire was carefully inserted and advanced within 10 mm of the lesion under CT guidance. A follow-up CT ensured accurate placement, with adjustments made if the needle’s angle was off-target, involving retraction and reinsertion as needed. Once positioned correctly, the hook wire was released, and the needle was withdrawn, embedding the thread in subcutaneous tissue. A CT scan was then performed 5 minutes later to check the final position of the hook wire and assess for complications such as pneumothorax, parenchymal haemorrhage or haemothorax. Finally, the patient was transported to their hospital room in a wheelchair to await surgery.

Treatment of common complications

  • Pneumothorax: if the pneumothorax volume was <30%, the patient was returned to the ward for oxygen treatment and waited for surgery. When the pneumothorax volume was ≥30%, a chest tube was inserted simultaneously with oxygen inhalation, and the patient waited for surgery.
  • Intrapulmonary haemorrhage: the severity of intrapulmonary haemorrhage was graded as follows: Grade 0 indicated no haemorrhage, Grade 1 was defined as needle tract haemorrhage up to 2 cm, Grade 2 as haemorrhage more than 2 cm, Grade 3 included lobar haemorrhage or greater and Grade 4 denoted a haemothorax (18). If the intrapulmonary haemorrhage was limited to a single lung segment, it indicated a small quantity of bleeding. In such cases, oxygen therapy was administered. However, if the bleeding affected more than one lung segment, it was considered a significant amount of bleeding. In these instances, the patient was placed in the lateral decubitus position with the surgical side down, and oxygen and haemostatic drugs were administered. Subsequently, the patient was promptly transferred to the operating room for immediate surgical intervention.
  • Pleural reaction and pain: dexamethasone (10 mg), tramadol (100 mg) or oxygen were injected.
  • Haemothorax: the patient was immediately admitted to the operating room for VATS.

VATS

All patients underwent single-port thoracoscopic surgery within 10 hours of preoperative hook wire placement. Surgical planning included selecting the appropriate procedure among segmentectomy, combined segmentectomy, wedge resection and lobectomy, depending on the location of the GGNs. A distance of at least 2 cm from the lesion was necessary for the resection margin in sublobar resection. Lobectomy was performed when sublobar resection was deemed unreliable or when intraoperative frozen section analysis indicated the presence of a persistent tumour at the margins. An experienced pathologist conducted the intraoperative frozen pathological diagnosis. If the pathology indicated primary lung malignant tumours, systemic lymph node dissection or sampling was conducted. Finally, special staining and immunohistochemistry were performed on each resected lesion after surgery to determine the final pathological diagnosis (19).

Data collection

This study assessed several patient characteristics, lesions and preoperative procedures to identify the risk factors associated with complications. Data were collected starting from the immediate postoperative period until the patient’s discharge from the hospital. Key follow-up points were set at 24 and 48 hours and at the time of discharge to assess immediate surgical outcomes and any short-term complications. Additional follow-up data were collected during the post-discharge period at 1 week, 1 month and 3 months post-surgery through outpatient visits and telephone interviews. This structured approach allowed for a detailed assessment of both the immediate and extended postoperative recovery phases. The patient variables considered in this study were age, sex, smoking index, the presence of pulmonary emphysema on CT scans and the presence of adhesions between the visceral and parietal pleurae found during VATS. The smoking index was calculated by multiplying the number of cigarettes smoked per day by the number of years of smoking. The lesion variables included size (diameter of the long axis, in mm), position (left upper lobe, left lower lobe, right upper lobe, right lower lobe or right mid-lung), the closest distance to the pleura (in mm) and pathological diagnosis (benign lesions, carcinoma in situ, microinvasive carcinoma or invasive carcinoma). The procedure variables included puncture positioning, the number of punctures of the pleura, the angle of the introducer needle trajectory, the distance the hook wire travelled within the lung parenchyma from the pleural surface to the nodule [length of the intrapulmonary pathway (in mm)], the distance from the outer surface of the chest wall to the pleural entry point where the hook wire was inserted [the length of the chest wall path (in mm)] and the distance from the tip of the inserted hook wire to the actual nodule, ensuring accurate placement for surgical procedures [nodule distance to locate the hook wire (in mm)]. The angle of the needle trajectory was the acute angle between the needle trajectory and the vertical line at which the needle passed through the pleura (Figure 1). Before the needle was inserted into the desired position near the nodule and prepared for release, a reference line was established perpendicular to the pleura at the point of needle insertion on the CT image. The angle between the needle and the reference line was then measured as the trajectory angle of the needle.

Figure 1 The angle of the needle trajectory (α). The angle of the needle trajectory (α) is the acute angle between the needle trajectory and the vertical line at which the needle passes through the pleura.

This study evaluated complications, including pneumothorax, haemothorax, intrapulmonary haemorrhage, chest wall haematoma, pleural response, severe pain (measured using a visual analogue scale with a score of ≥8), lack of lesion during surgery and failure of hook wire implantation.

Statistical analysis

Data analysis was conducted using the R software (R Core Team 2022, version 4.1.1). Descriptive statistics were calculated as means ± standard deviations for continuous variables and absolute and relative frequencies for categorical data. Clinical and demographic variables were compared between the pneumothorax and control groups, as well as between the pulmonary haemorrhage and control groups, using independent sample t-tests and χ2 tests. Nonparametric methods were applied to data that did not meet normal distribution assumptions or when sample sizes were small. Least absolute shrinkage and selection operator (LASSO) regression was performed on variables associated with pulmonary haemorrhage or pneumothorax, and the results were visualised. Multivariate logistic regression was used to estimate the regression coefficients, and a P value of less than 0.05 was considered statistically significant.


Results

Characteristics of the included patients

A total of 230 patients were included in the final analysis, with an average age of 51.43±12.35 years. One patient failed to undergo preoperative hook wire localisation due to a faulty hook wire, resulting in a localisation success rate of 99.6%. Fifty-seven (24.8%) of the patients were men and 173 (75.2%) were women. Other relevant characteristics are listed in Table 1.

Table 1

Characteristics of the patients, nodules, and procedures

Variables Value
Sex, male/female 57/173
Age (years) 51.43±12.35
Pulmonary emphysema, yes/no 21/209
Smoking index 68.7±215.1
Pleural adhesion, yes/no 6/224
Lesion location
   Right upper lobe 80 (34.8)
   Right middle lobe 17 (7.4)
   Right lower lobe 56 (24.3)
   Left upper lobe 55 (23.9)
   Left lower lobe 22 (9.6)
Distance to the nearest pleura (mm) 13.2±10.6
Nodules size (mm) 7.0±1.8
Pathological diagnosis
   Benign lesion/carcinoma in situ/microinvasive carcinoma/invasive carcinoma 28/40/105/57
Number of punctures, 1/2/3/4 163/54/11/2
Distance to the hookwire (mm) 6.09±3.30
Angle of the needle trajectory (°) 18.0±11.7
Length of the chest wall pathway (mm) 38.7±12.1
Length of the intrapulmonary pathway (mm) 17.4±9.9
Patient positioning, supine/side sleeper/prone 61/99/70

Data are presented as number, n (%), or mean ± standard deviation.

Complications and surgery of the included patients

In all cases, single-port VATS was successfully performed within 6 hours of localisation without conversion to thoracotomy. Eighty-two patients (35.7%) underwent wedge resection, 127 (55.2%) underwent segmentectomy and 21 (9.1%) underwent lobectomy. In two patients, lung lesions could not be detected due to intrapulmonary haemorrhage masking, and tumour cells were not found in the final pathological tissue. The overall complication rate was 61.3%. Pneumothorax was the most common complication, observed in 89 patients (38.7%), four of whom (1.7%) required drainage tubes. Most cases of pneumothorax were mild, and there were no obvious symptoms after oxygen inhalation. Out of the total number of patients, only four (1.7%) experienced dyspnoea due to moderate pneumothorax. However, their symptoms were alleviated following the insertion of drainage tubes, and no cases of tension pneumothorax were seen. Subsequently, intrapulmonary haemorrhage was observed in 18.7% of cases, but there were no instances of significant coughing up of blood. Most instances of intrapulmonary haemorrhage were either asymptomatic or presented with minimal haemoptysis and did not experience significant haemoptysis. Chest wall haematoma is defined as a large haematoma around the puncture point of the chest wall found during surgery but with no obvious blood in the chest cavity, and it has an incidence of 11.3%. Additional complications are presented in Table 2.

Table 2

The description of complications

Variables Value, n (%)
Pneumothorax 89 (38.7)
Pulmonary hemorrhage 43 (18.7)
Chest wall hematoma 26 (11.3)
Pleural reaction 21 (9.1)
Pain 20 (8.7)
Hemothorax 5 (2.2)
Placement drainage 4 (1.7)
Lack of lesion 2 (0.9)
Failure of hookwire implantation 1 (0.4)

Comparing the characteristics of the pneumothorax and control groups

The characteristics of the pneumothorax and control groups were compared, revealing significant differences in terms of pulmonary emphysema, the distance to the nearest pleura, patient positioning, the number of punctures, the angle of the needle trajectory and the length of the intrapulmonary pathway (Table 3). LASSO regression was further applied to select the variable related to the probability of pneumothorax (coefficients of unrelated variables were reduced to zero) (Figures 2,3). Finally, multivariate logistic regression was utilised to calculate the remaining coefficients in the final model, and a nomogram was implemented to visually represent the final multivariate logistic regression model (Figure 4).

Table 3

Comparing the characteristics of the pneumothorax and no pneumothorax groups

Variables No pneumothorax (N=141) Pneumothorax (N=89) P value
Sex (male) 29 (20.6) 28 (31.5) 0.062
Age (years) 51.4±12.2 51.4±12.7 0.99
Pulmonary emphysema (yes) 4 (2.8) 17 (19.1) <0.001
Smoking index 46.7±163.6 103.4±275.3 0.082
Pleural adhesion (yes) 6 (4.3) 0 (0.0) 0.122
Lesion location 0.187
   Right upper lobe 46 (32.6) 34 (38.2)
   Right middle lobe 11 (7.8) 6 (6.7)
   Right lower lobe 29 (20.6) 27 (30.3)
   Left upper lobe 40 (28.4) 15 (16.9)
   Left lower lobe 15 (10.6) 7 (7.9)
Distance to the nearest pleura (mm) 14.6±10.9 10.9±9.7 0.008
Nodules size (mm) 6.9±1.8 7.2±1.8 0.167
Pathological diagnosis 0.687
   Benign lesion 15 (10.6) 13 (14.6)
   Carcinoma in situ 23 (16.3) 17 (19.1)
   Microinvasive carcinoma 68 (48.2) 37 (41.6)
   Invasive carcinoma 35 (24.8) 22 (24.7)
Patient positioning 0.001
   Supine 49 (34.8) 12 (13.5)
   Side sleeper 50 (35.5) 49 (55.1)
   Prone 42 (29.8) 28 (31.5)
Number of punctures <0.001
   1 113 (80.1) 50 (56.2)
   2 25 (17.7) 29 (32.6)
   3 3 (2.1) 8 (9.0)
   4 0 (0.0) 2 (2.2)
Distance to the hookwire (mm) 5.9±3.2 6.4±3.4 0.201
Angle of the needle trajectory (°) 16.4±11.2 20.5±12.1 0.011
Length of the chest wall pathway (mm) 39.4±11.8 37.7±12.5 0.319
Length of the intrapulmonary pathway (mm) 18.4±10.9 15.7±7.8 0.031

Data are presented as n (%) or mean ± standard deviation.

Figure 2 The relationship between binomial deviance and log(λ) in model of pneumothorax. Lasso regression was further applied to select the variate that was related to the probability of pneumothorax (coefficients of unrelated variables were reduced to zero). Binomial deviance decreased first with the increase of log(λ) and then obviously increased with the increase of log(λ) later. Then the optimal log(λ) was chosen based on the corresponding minimal binomial deviance.
Figure 3 Log(λ) and corresponding penalized coefficients in model of pneumothorax. Heavier penalty was given on the coefficients as the log(λ) increased, the log(λ) was chosen based on the optimal value at −4.131 in Figure 2.
Figure 4 Nomogram for incidence of pneumothorax based on the multivariate logistic regression in Table 4. To predict the risk of pneumothorax in patients, a vertical scale is placed on the nomogram, with each predictor corresponding to the points, and the sum of all predictor points is calculated, which is expressed as the total points. Place a vertical scale on the nomogram at the total points to determine the risk of pneumothorax. For example, a patient without emphysema, distance to the nearest pleura is 45 mm, patient positioning is supine, number of punctures is 1 time, angle of the needle trajectory is 50°, length of the intrapulmonary pathway is 55 mm, the total point is 47, corresponding to the risk of pneumothorax is from >0.05 to <0.1.

The multivariate logistic regression analysis demonstrated substantial correlations between the risk of pneumothorax incidence and variables including pulmonary emphysema, the distance to the nearest pleura, the number of punctures and the angle of the needle trajectory. Among these variables: (I) the angle of the needle trajectory had an odds ratio (OR) of 1.035, with P=0.011, indicating that the OR for the occurrence of pneumothorax was 1.035 with a 1-unit increase in the angle of the needle trajectory while holding other variables constant; (II) several punctures had an OR of 3.443, with P<0.001, indicating that the OR for the occurrence of pneumothorax was 3.443 with a 1-unit increase in the number of punctures while holding other variables constant; (III) distance to the nearest pleura had an OR of 0.944, with P=0.005, indicating that the OR for the occurrence of pneumothorax was 0.944 with a 1-unit increase in the distance to the nearest pleura while holding other variables constant; and (IV) pulmonary emphysema had an OR of 12.286, with P<0.001, indicating that the OR for the occurrence of pneumothorax was 12.286 with a 1-unit increase in pulmonary emphysema while holding other variables constant (Table 5).

Table 5

Multivariate logistic regression for factors related to pneumothorax, based on covariates with non-zero penalized coefficients

Variables B SE Z P value OR 95% CI
Intercept −2.858 0.689 −4.151 <0.001 0.057 0.015–0.221
Pulmonary emphysema 2.508 0.614 4.085 <0.001 12.286 3.687–40.938
Distance to the nearest pleura −0.057 0.02 −2.821 0.005 0.944 0.907–0.983
Patient positioning 0.294 0.208 1.415 0.157 1.342 0.893–2.017
Number of punctures 1.236 0.275 4.488 <0.001 3.443 2.006–5.907
Angle of the needle trajectory 0.034 0.014 2.534 0.011 1.035 1.008–1.063
Length of the intrapulmonary pathway −0.003 0.02 −0.163 0.871 0.997 0.959–1.036

Intercept: represents the baseline log odds of the outcome (pneumothorax) when all predictor variables are set to zero. It serves as the constant term in the regression equation. CI, confidence interval; OR, odds ratio; SE, standard error.

Comparing the characteristics of the pulmonary haemorrhage and control groups

A comparison of the characteristics of the pulmonary hemorrhage and control groups revealed significant differences between the two groups in terms of distance to the nearest pleura, number of punctures, angle of the needle, length of the chest wall pathway, and length of the intrapulmonary pathway (Table 4). LASSO regression was utilised to identify the variables that were associated with pulmonary haemorrhage. The coefficients of unrelated variables were effectively lowered to 0 (Figure 5). In the analysis of pneumothorax, a multivariate logistic regression was employed to estimate the remaining coefficients in the final model. Additionally, a nomogram was utilised to represent the final multivariate logistic regression model visually (Figure 6).

Table 4

Comparing the characteristics of the pulmonary hemorrhage and no pulmonary hemorrhage groups

Variables No pulmonary hemorrhage (N=187) Pulmonary hemorrhage
(N=43)
P value
Sex (male) 50 (26.7) 7 (16.3) 0.152
Age (years) 52.0±12.2 48.9±12.9 0.135
Pulmonary emphysema (yes) 20 (10.7) 1 (2.3) 0.154
Smoking index 73.7±222.6 46.5±179.1 0.455
Pleural adhesion (yes) 5 (2.7) 1 (2.3) >0.99
Lesion location 0.774
   Right upper lobe 64 (34.2) 16 (37.2)
   Right middle lobe 13 (7.0) 4 (9.3)
   Right lower lobe 48 (25.7) 8 (18.6)
   Left upper lobe 43 (23.0) 12 (27.9)
   Left lower lobe 19 (10.2) 3 (7.0)
Distance to the nearest pleura (mm) 11.8±9.8 19.1±12.1 0.001
Nodules size (mm) 7.0±1.9 7.0±1.5 0.980
Pathological diagnosis 0.784
   Benign lesion 24 (12.8) 4 (9.3)
   Carcinoma in situ 32 (17.1) 8 (18.6)
   Microinvasive carcinoma 83 (44.4) 22 (51.2)
   Invasive carcinoma 48 (25.7) 9 (20.9)
Patient positioning 0.225
   Supine 46 (24.6) 15 (34.9)
   Side sleeper 80 (42.8) 19 (44.2)
   Supine 61 (32.6) 9 (20.9)
Number of punctures 0.001
   1 143 (76.5) 20 (46.5)
   2 35 (18.7) 19 (44.2)
   3 8 (4.3) 3 (7.0)
   4 1 (0.5) 1 (2.3)
Distance to the hookwire (mm) 6.0±3.3 6.5±3.3 0.351
Angle of the needle trajectory (°) 17.1±11.7 21.9±11.1 0.015
Length of the chest wall pathway (mm) 39.7±12.3 34.51±10.2 0.005
Length of the intrapulmonary pathway (mm) 15.8±8.9 24.3±11.0 <0.001

Data are presented as n (%) or mean ± standard deviation.

Figure 5 The relationship between binomial deviance and log(λ) in model of pulmonary hemorrhage. Lasso regression was further applied to select the variate that was related to the probability of pulmonary hemorrhage (coefficients of unrelated variables were reduced to zero). Binomial deviance decreased first with the increase of log(λ) and then obviously increased with the increase of log(λ) later. Then the optimal log(λ) was chosen based on the corresponding minimal binomial deviance.
Figure 6 Log(λ) and corresponding penalized coefficients in model of pulmonary hemorrhage. Heavier penalty was given on the coefficients as the log(λ) increased, the log(λ) was chosen based on the optimal value at −4.605 in Figure 5.

Multivariate logistic regression showed that variables such as the number of punctures, the angle of the needle trajectory, the length of the chest wall pathway and the length of the intrapulmonary pathway were significantly correlated with the probability of pulmonary haemorrhage. Among these variables, the angle of the needle trajectory had an OR of 1.057, with P=0.002. This indicates that the odds of pulmonary haemorrhage increased by 1.057 times with a 1-unit increase in the angle of the needle trajectory while keeping other variables constant. Similarly, the number of punctures had an OR of 1.894, with P=0.026, indicating that the odds of pulmonary haemorrhage increased by 1.894 times with a 1-unit increase in the number of punctures while keeping other variables constant. However, the length of the chest wall pathway had an OR of 0.951, with P=0.010, indicating that the odds of pulmonary haemorrhage decreased by 0.951 times with a 1-unit increase in the length of the chest wall pathway while keeping other variables constant. Lastly, the length of the intrapulmonary pathway had an OR of 1.060, with P=0.007, implying that the odds of pulmonary haemorrhage increased by 1.060 times with a 1-unit increase in the length of the intrapulmonary pathway while keeping other variables constant (Table 6 and Figure 7).

Table 6

Multivariate logistic regression for factors related to pulmonary hemorrhage, based on covariates with non-zero penalized coefficients

Variables B SE Z P value OR 95% CI
Intercept −3.076 1.216 −2.53 0.011 0.046 0.004–0.500
Sex (male) −0.595 0.523 −1.138 0.255 0.551 0.198–1.537
Age (years) −0.004 0.016 −0.285 0.776 0.996 0.965–1.027
Distance to the nearest pleura (mm) 0.042 0.022 1.933 0.053 1.043 0.999–1.088
Number of punctures 0.639 0.287 2.23 0.026 1.894 1.080–3.322
Angle of the needle trajectory (°) 0.055 0.018 3.03 0.002 1.057 1.020–1.095
Length of the chest wall pathway (mm) −0.05 0.020 −2.568 0.010 0.951 0.915–0.988
Length of the intrapulmonary pathway (mm) 0.058 0.022 2.683 0.007 1.060 1.016–1.106

Intercept: represents the baseline log odds of the outcome (pulmonary hemorrhage) when all predictor variables are set to zero. It serves as the constant term in the regression equation. CI, confidence interval; OR, odds ratio; SE, standard error.

Figure 7 Nomogram for incidence of pulmonary hemorrhage based on the multivariate logistic regression in Table 6. To predict the risk of pulmonary hemorrhage in patients, a vertical scale is placed on the nomogram, with each predictor corresponding to the points, and the sum of all predictor points is calculated, which is expressed as the total points. Place a vertical scale on the nomogram at the total points to determine the risk of pulmonary hemorrhage. For example, an 80-year-old male patient with a distance to the nearest pleura is 0 mm, number of punctures is 1 time, angle of the needle trajectory is 0°, length of the chest wall pathway is 10 mm, and length of the intrapulmonary pathway is 0 mm. The total point is 100, corresponding to the risk of pulmonary hemorrhage is from >0.01 to <0.05.

Discussion

Several methods have been developed to perform preoperative lung nodule localisation for VATS, including preoperative puncture localisation, three-dimensional CT bronchography and angiography and body surface positioning (20). Preoperative puncture positioning is the most accurate and reliable of these methods. It includes the use of hook wire (21), micro-coil positioning (22) and the injection of methylene blue dye or indocyanine green (23). Methylene blue injection may cause dye spillage, contaminating the surgical field of vision, whereas the intrapulmonary injection of dyes may cause an allergic reaction or even shock. While certain studies indicate that the effectiveness of micro coil placing is not significantly different from that of hook wire (24), the most commonly employed preoperative method for localising pulmonary nodules is the implantation of a hook wire (7). Previous studies have shown that preoperative hook wire localisation has a high success rate (97.5–100%) (13,25,26), and its safety and efficacy have been proven (8). Out of the 230 patients included in this study, only a single patient was unable to undergo successful hook wire localisation. This was attributed to a failure of the localisation equipment. In general, wedge resection was conducted using VATS, targeting the puncture site of the visceral pleura, with a success rate of 99.6%.

In this study, pneumothorax and intrapulmonary haemorrhage occurred in 38.7% and 18.7%, respectively, which was consistent with the reported incidences of 8–68.1% for pneumothorax and 0–35.6% for pulmonary haemorrhage in previous studies (7,13,27-29). The current investigation has established that the angle at which the needle is directed is a significant component that affects both pneumothorax and intrapulmonary hemorrhage. Previous research did not highlight that an increase in the needle angle led to a rise in both pneumothorax and pulmonary haemorrhage incidence (7,30,31). Particularly, in a puncture biopsy study (14), a needle-pleural angle of ≥51° was identified as a risk factor for a high pneumothorax rate. Furthermore, the previous study revealed a higher probability of developing pneumothorax when the puncture was made at a right angle to the pleura, which contrasted with the findings of this study. The reason for this discrepancy may be attributed to the fact that preoperative hook wire localisation entails the insertion of a line connecting the lung parenchyma to the chest wall, whereas needle biopsy does not necessitate such a line. This correlation could be because as the angle increases, the pleural opening is pulled by the positioning needle due to respiratory activity, which is more likely to cause pneumothorax. In the context of this study, it is also important to note that pulmonary blood vessels are radially distributed. Therefore, when the needle is at a right angle to the pleura, its orientation aligns closely with that of the small blood vessels, minimising the risk of pulmonary haemorrhage during the puncture. As the needle angle increases, it intersects with delicate blood vessels, potentially puncturing them and leading to pulmonary haemorrhage in the lung. Additionally, preoperative hook wire localisation is performed under CT guidance, with some patients requiring multiple punctures, and the incidence of both pneumothorax and pulmonary haemorrhage increases as the number of punctures rises. The risk of pneumothorax is higher when there are several punctures, as this leads to an increased possibility of lung surface rupture. Likewise, the presence of multiple punctures heightens the risk of puncturing small blood vessels in the lungs, thus raising the incidence of pulmonary haemorrhage. Iguchi et al. (7) suggest that transfissural routes lead to an increase in the number of openings on the lung surface, raising the occurrence of pneumothorax. Some studies suggest that a single puncture is an independent protective factor against pneumothorax after the localisation of pulmonary nodules (15), which is consistent with the results of this study.

In this study, the incidence of pneumothorax was 38.7%, and 1.7% of the patients required the placement of drainage tubes. Risk factors for pneumothorax include proximity to the pleura and the presence of emphysema. Numerous investigations utilising lung aspiration biopsies have demonstrated a correlation between the onset of pneumothorax and emphysema (14,11,32). Patients with emphysema are prone to having the hook wire pierce the overventilated alveoli, leading to a higher occurrence of pneumothorax. When the nodule is in closer proximity to the pleura, the hook wire is more likely to cause damage to the pleura, thus increasing the probability of pneumothorax. Although most complications are not life-threatening, some patients experience discomfort and may require drainage tubes. The presence of a pneumothorax may also increase the likelihood of placement failure.

The lengths of the chest wall pathway and the intrapulmonary pathway are contributing factors for pulmonary haemorrhage. Huang et al. (12) identified the prone position as a risk factor for pulmonary haemorrhage, suggesting that the relative thinness of the anterior chest wall may contribute to this risk. As the length of the chest wall pathway increases, it becomes more challenging to navigate without potentially damaging small blood vessels, particularly during respiratory movements. The closer the needle is to the hilus, the denser the pulmonary vessels; the greater the length of the intrapulmonary pathway, the higher the risk of pulmonary vascular injury and the incidence of pulmonary haemorrhage (13,33). A large proportion of individuals experiencing pulmonary haemorrhage exhibit either no symptoms or only minor haemoptysis. None of the patients in this study experienced massive haemoptysis after preoperative hook wire localisation. Nevertheless, the presence of pulmonary haemorrhage can obscure smaller GGNs, posing challenges in detecting intraoperative lesions. Two patients in this study did not have nodules discovered during surgery due to the impact of pulmonary haemorrhage, necessitating a lobectomy. While most pulmonary haemorrhages do not impact surgical outcomes or patient safety, it is advisable to minimise the occurrence of pulmonary haemorrhage during puncture localisation and to avoid performing a more extensive lung resection.

Like thoracentesis (34), preoperative hook wire localisation can lead to bleeding complications such as puncture site bleeding, chest wall haematoma and haemothorax. Despite this, studies often overlook haemorrhaging in thoracic and chest wall tissues during puncture localisation, which is typically followed by surgery (35). In our study, chest wall haematomas occurred in 11.3% of cases, whereas small haemothoraces, confirmed via VATS, appeared in 2.2% of cases after CT. This rate is low compared with a study reporting a 5.2% incidence of haemothorax (28). According to Qin et al. (16), VATS can be safely performed 2–3 days post-localisation despite potential bleeding challenges.

Following localisation, the persistence of the hook wire in subcutaneous tissue complicates bleeding control, potentially escalating haemorrhage risks. Minor damage to subpleural blood vessels typically causes postoperative chest wall haematomas, highlighting the risk of subsequent haemothorax. Despite the absence of life-threatening bleeding in our study, vigilant monitoring for chest bleeding is crucial post-localisation to ensure timely surgical intervention. Procedures conducted under local anaesthesia resulted in pleural reactions and pain in 9.1% and 8.7% of cases, respectively. This study did not permit extensive multivariate analyses due to limited sample sizes. A cross-sectional study identified that the number and specific locations of localisation needles significantly influence the severity of pain during activities (36). Our study did not encounter severe complications such as air embolism (9,37), tension pneumopericardium (38) or hook wire displacement (28), which are rare but noted in other studies.

There are some limitations in this study, including its small sample size and the fact that it is a single-centre retrospective study. Besides, the subsequent progression of pneumothorax, pulmonary haemorrhage and haemothorax after localisation was not monitored in this study. The exact number of hemoptyses was not recorded in this study. Additionally, total complications and rare complications were not tracked due to the presence of numerous confounding factors. Moreover, the insertion site on the body surface, especially in areas like below the scapula, clavicle, or near the liver, may affect needle trajectory due to anatomical obstacles. Including the insertion site as a procedural variable in future studies could refine predictive models and improve outcomes. Further research could explore optimal insertion sites and their impact on complications like pneumothorax and hemorrhage.


Conclusions

The success rate of CT-guided preoperative hook wire localisation is very high. Pneumothorax and pulmonary haemorrhage are the most common complications of this procedure, and maintaining a small angle of needle trajectory can reduce these complications. Therefore, the risk of complications should be evaluated using predictive models before the procedure, and the needle insertion path should be carefully planned before preoperative hook wire localisation to minimise the occurrence of postprocedural complications.


Acknowledgments

The authors thank Qing Pan for his assistance with the statistical analysis performed in this study. The authors further thank the editors at WOSCI (www.wosci.cn) for their linguistic assistance during the preparation of this manuscript.


Footnote

Reporting Checklist: The authors have completed the STROCSS reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-1051/rc

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1051/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The current retrospective study was approved by the ethics committee of The First People’s Hospital of Neijiang (No. 2020-07). Since we only reviewed medical records of the patients, and no individual patient could be identified from the data, the requirement for informed consent was waived by the ethics committee of The First People’s Hospital of Neijiang.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.


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Cite this article as: Wang C, Chen C, Liu G, Li Z, Zheng D, Li X. Retrospective study on preoperative hook wire localisation of pulmonary ground-glass nodules: risk factors for complications and preventive strategies. Quant Imaging Med Surg 2025;15(4):3430-3444. doi: 10.21037/qims-24-1051

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