Incidence and risk factor analysis of moderate-to-severe pain after preoperative CT-guided hook-wire puncture localization of pulmonary nodules

Abstract

Background

Pain is a relatively common complication after hook-wire puncture localization. However, the problem of pain occurrence following this localization procedure has not been sufficiently examined. In this prospective study, we aimed to investigate the incidence and risk factors associated with acute pain after preoperative CT-guided hook-wire puncture localization of pulmonary nodules.

Methods

Clinical data were collected prospectively from patients with small pulmonary nodules who underwent preoperative CT-guided hook-wire puncture localization between May 2022 and May 2023 at the Affiliated Hospital of Xuzhou Medical University. Patients were divided into two groups on the basis of the presence or absence of moderate-to-severe pain following the localization process. Univariate logistic analysis was conducted to analyse the clinical data of the two groups. Subsequently, the significant variables (P < 0.1) from the univariate analysis were subjected to multivariate logistic analysis, followed by the establishment of regression equations to determine the significant risk factors related to moderate-to-severe pain after hook-wire puncture localization.

Results

A total of 281 patients with small pulmonary nodules undergoing preoperative CT-guided hook-wire puncture localization were finally included, with a mean age of 54.86 years (SD = 12.1 years) and female predominance (67.6%). In the resting state, 53% of the patients reported moderate-to-severe pain. Univariate analysis revealed that age (P = 0.085), the depth of localization needle insertion into the lung (P = 0.024) and the location of the chest wall puncture (P = 0.07) were associated with moderate-to-severe pain occurrence after hook-wire puncture localization (P < 0.1). Furthermore, multivariate logistic regression analysis demonstrated that the depth of localization needle insertion into the lung (OR = 0.953, 95% CI: 0.914–0.992, P = 0.02) and the location of the chest wall puncture (lateral chest wall vs. anterior chest wall: OR = 2.101, 95% CI: 1.166–3.784, P = 0.013; posterior chest wall vs. anterior chest wall: OR = 1.163, 95% CI: 0.895–2.971, P = 0.11) were independent predictors of moderate-to-severe pain incidence following CT-guided hook-wire puncture localization (P < 0.05).

Conclusion

Moderate-to-severe pain is prevalent in patients with pulmonary nodules who undergo preoperative CT-guided hook-wire puncture localization. The depth of needle insertion into the lung and the location of the chest wall puncture are significant predictors of moderate-to-severe pain onset.

Introduction

Lung cancer is one of the most common malignant tumors and the leading cause of cancer-related death globally, posing a serious threat to human life and health [1]. Moreover, the implementation of screening procedures for high-risk groups and the rapid development of modern imaging technologies have led to the extensive use of high-resolution spiral computed tomography, contributing to the increased detection of cases of small lung nodules with suspicion of lung cancer. Consequently, clinical management and decision-making in patients with pulmonary nodules are critical for clinicians.

In the context of surgical treatment, rapid and accurate localization of pulmonary nodules is a crucial factor for the success of modern minimally invasive thoracic surgery [2]. Hook-wire puncture localization is widely employed by thoracic surgeons for the precise preoperative localization of pulmonary nodules for resection. This localization method significantly reduces the time required for thoracoscopic nodule exploration and accelerates the process of lung resection by pulling the anchored lung tissue close to the lung surface, thus substantially improving surgical efficiency. Compared with other localization techniques, hook-wire puncture localization offers the advantages of simplicity, a high success rate, and low cost; however, it may lead to puncture-related complications such as pneumothorax, pulmonary hemorrhage, moderate-to-severe pain, and wire dislocation [3, 4]. Although numerous studies have examined the efficacy and safety of hook-wire puncture localization, research on the pain associated with this localization method is relatively rare and no recent studies are available [5,6,7]. Currently, studies on acute pain incidence after hook-wire puncture localization have reported inconsistent results, along with inadequate descriptions of the degree of pain in the patients and the specific methods utilized for pain assessment [8,9,10]. Therefore, exploring the potential risk factors may help prevent or decrease acute pain occurrence following hook-wire puncture localization in high-risk populations.

Here, we aimed to systematically acquire data on acute pain in a prospective cohort of patients with pulmonary nodules who underwent preoperative CT-guided hook-wire puncture localization and to conduct logistic regression analysis to explore the prevalence and associated risk factors of acute pain after this localization procedure. We hope our findings will provide relevant clinical guidance for hook-wire puncture localization in this patient population.

Materials and methods

Ethical review

This study prospectively analyzed the clinical data of patients with small pulmonary nodules who underwent preoperative CT-guided hook-wire puncture localization between May 2022 and May 2023 at the Affiliated Hospital of Xuzhou Medical University. This study received approval from the Hospital Ethics Committee of the Affiliated Hospital of Xuzhou Medical University (approval no.: XYFY2022-KL097-01) and complied with the principles of the Declaration of Helsinki and related ethical requirements. All patients participating in this study provided a signed informed consent form.

Inclusion and exclusion criteria

Patient inclusion criteria were as follows: (1) aged between 18 and 75 years; (2) American Society of Anaesthesiologists (ASA) classification of I to III; (3) needle puncture and positioning in CT-guided hook-wire puncture localization conducted under local anaesthesia on surgery day; (4) only one hook-wire puncture needle utilized for localization. Patient exclusion criteria were as follows: (1) long-term use of analgesics, anxiolytics, or sleeping pills; (2) a previous history of chronic pain; (3) the presence of psychiatric or neurological disorders or other conditions such as cognitive or language dysfunction.

Data collection

• (1) General data: age, sex, body mass index, ASA classification, smoking history, drinking history, and comorbidities (diabetes, hypertension, coronary heart disease, or arrhythmia).

• (2) Imaging data: location of pulmonary nodules; longitudinal diameter of the largest cross-section of pulmonary nodules; density of pulmonary nodules (ground glass, partially solid, or solid); depth of pulmonary nodules (shortest distance of the nodule from the pleura); success of the hook-wire puncture localization (i.e. observing whether the localization needle appears to be decoupled to determine whether localization was successful or not); location of the chest wall puncture (including the anterior chest wall [from the parasternal line to the anterior axillary line], the lateral chest wall [from the anterior axillary line to the posterior axillary line], and the posterior chest wall [from the posterior axillary line to the spine]; skin-to-needle tip distance (the shortest distance from the skin to the needle tip after needle release); the depth of localization needle into the lung (the depth of the needle in the lung tissue after needle release); the depth of the chest wall puncture (the depth of needle insertion into the chest wall after needle release); and the puncture angle (the angle between the needle and the ground vertical line).

• (3) Complications: e.g. pneumothorax, intra-pulmonary hemorrhage (i.e. chest CT showing new patchy ground glass opacities in the lungs) and pleural reaction.

Localization process

Before the localization procedure, a chest CT scan was performed to observe the size and location of the lung nodule and select a suitable puncture access method (Fig. 1A). Initially, the patient was routinely disinfected, and a sterile towel was spread. Next, 2% lidocaine was administered as local anaesthesia, allowing the anaesthesia to infiltrate layer by layer to the wall layer of the subpleural membrane. The unreleased hook-wire puncture localization needle was then slowly inserted from the entry point along the established puncture path without passing through the wall layer of the pleural membrane (Fig. 1B). Subsequently, the patient was instructed to hold their breath after a deep inhalation to perform a second CT scan. After determining that the needle path did not deviate from the proposed puncture path, the needle was further inserted into the lung until the tip of the hook-wire puncture needle was near the pulmonary nodule. A third CT scan was conducted (Fig. 1C) to confirm that the needle tip was located within 5–10 mm of the nodule. The needle was then released to anchor the lung tissue, followed by retrieval of the trocar and fixing the wound with gauze. Finally, a fourth CT scan (Fig. 1D) was performed to verify successful hook-wire puncture localization and detect any complications related to the localization technique, such as pain, intra-pulmonary hemorrhage, pneumothorax and pleural reaction.All localization were performed by the same experienced thoracic surgeon.

Fig. 1

Process of preoperative CT-guided hook-wire puncture localization

A: Defining the location of the pulmonary nodule; B: Inserting the localization needle into the chest wall, but not through the pleura; C: Locating the tip of the needle at the appropriate position around the pulmonary nodule; D: Releasing the core of the needle to anchor the lung tissue (a: the core of the needle, b: the pulmonary nodule).

Pain assessment

Within 10–15 min after the localization procedure, the research team assessed the patient’s pain perception at rest in the ward via a visual analogue scale (VAS)(Fig. 2). According to the VAS score, patient pain was categorized as follows: no pain (0 points), mild pain (1–3 points), moderate pain (4–6 points), and severe pain (7–10 points).

Fig. 2

Visual analogue scale

Statistical analysis

All the data analyses were performed via SPSS version 25.0. Normally distributed measurement data are expressed as the mean ± standard deviation ($\:\stackrel{-}{\text{X}}$ ± SD), and a t-test was applied for comparisons between two groups. Non-normally distributed measurement data are presented as medians (M) (upper quartile [QU], lower quartile [QL]), and the Mann–Whitney U test was employed for between-group comparisons. Categorical variables are described as frequencies and percentages, with the Pearson χ² test for comparing rates or constitutive ratios and the Mann–Whitney U test for the ordered multiclassification. A test level of α = 0.05 with P < 0.05 indicated statistically significant differences. According to the VAS pain scores, the intensity of acute pain in patients at rest after preoperative CT-guided hook-wire puncture localization of pulmonary nodules was used to divide them into a “no-to-mild pain group” and a “moderate-to-severe pain group”. Furthermore, univariate logistic analyses were performed on the general clinical data of the patients and data related to hook-wire puncture localization. Subsequently, the significant variables with P < 0.1 in the univariate logistic analysis were incorporated in the multivariate logistic analysis, followed by the development of regression equations to calculate the odds ratios (ORs) and 95% confidence intervals (CIs) of each variable, with P < 0.05 indicating statistical significance.

Results

Clinical characteristics of the patient

After the patients were systematically screened according to the inclusion and exclusion criteria, 305 patients were eligible for this study. Among them, 16 patients were excluded because of cancellation of the surgery, 3 patients refused to participate in the study, and 5 patients did not undergo CT-guided hook-wire puncture localization before the resection procedure due to the reassessment of surgical risk, changes in patient health status, or other psychological factors. Ultimately, 281 patients were included in the final analysis. The mean age of the patients was 54.86 years (SD = 12.1 years), and 67.6% were female. The localization process of the patients is illustrated in Fig. 3.The general characteristics of the study patients are listed in Table 1. The localization success rate for included patients was 100%. Intraoperative data revealed that all localization needles were appropriately placed and no decoupling had occurred. The characteristics of hook-wire puncture localization in the patients with pulmonary nodules are presented in Table 2. Hook-wire puncture localization had a relatively balanced proportion of locations of chest wall punctures, with 32.4%, 32.4%, and 35.2% in the anterior, lateral, and posterior chest walls, respectively. Pain assessment of the patients after preoperative CT-guided hook-wire puncture localization of the pulmonary nodules revealed that 53% of them experienced moderate-to-severe pain at rest. Moreover, the patients were divided into two groups on the basis of the presence or absence of moderate-to-severe pain after completing the localization procedure, and the clinical data of the two groups were compared.

Fig. 3

Study flowchart showing the entire process from patient screening to final analyses

Table 1 Demographic and clinical characteristics of patients with puncture localization of pulmonary nodules

Table 2 Characteristics of puncture localization of pulmonary nodules

Univariate and multivariate analyses

Univariate logistic analysis demonstrated that age (P = 0.085), the depth of localization needle insertion into the lung (P = 0.024), and the location of the chest wall puncture (P = 0.07) were potential risk factors for moderate-to-severe pain after completing the localization procedure (P < 0.1; Table 3). After pulmonary nodule localization, 21 cases of pneumothorax (15.9%), 11 cases of intra-pulmonary hemorrhage (8.3%) and 3 cases of pleural reaction (2.3%) were recorded in the “no-to-mild pain group”. In the “moderate-to-severe pain group”, 23 cases of pneumothorax (15.4%), 8 cases of intra-pulmonary hemorrhage (5.4%) and 5 cases of pleural reaction (3.4%) were recorded. There were no statistically significant differences between the two groups in terms of pneumothorax (P = 1.000), intra-pulmonary hemorrhage (P = 0.453), pleural reaction (P = 0.853) and post-positioning complications (P = 0.889). Furthermore, variables with P < 0.1 in the univariate analysis were subjected to multivariate analysis. The results indicated that the depth of localization needle into the lung (OR = 0.953, 95% CI: 0.914–0.992, P = 0.02) and the location of the chest wall puncture (lateral chest wall vs. anterior chest wall: OR = 2.101, 95% CI: 1.166–3.784, P = 0.013; posterior chest wall vs. anterior chest wall: OR = 1.163, 95% CI: 0.895–2.971, P = 0.11) were influencing factors for moderate-to-severe pain incidence after the localization (Table 4).

Table 3 Univariate analysis of moderate-to-severe pain at rest after hook-wire puncture localization of pulmonary nodules

Table 4 Multivariate analysis of moderate-to-severe pain at rest after hook-wire puncture localization of pulmonary nodules

Discussion

Only a few studies have been conducted on the incidence of pain following pulmonary nodule localization. In one such study, the researchers compared the safety and efficacy of localization via the four-hook needle and the hook-wire needle for pulmonary nodule localization. The results of that study revealed that 17.6% (5/28) of patients in the hook-wire needle group experienced pain after the localization procedure and required analgesia [6]. This observation suggests that although hook-wire puncture localization may be useful in pulmonary nodule surgery, its potential to induce pain should also be considered. However, the method of pain assessment, the pain levels of the patients, or the status of the patients during the evaluation were not described in that study. In contrast, the primary outcome indicator in our study was the incidence of moderate-to-severe pain in patients at 10–15 min after hook-wire puncture localization. Our results demonstrated that 53% of the patients experienced moderate-to-severe pain at rest after hook-wire puncture localization.

In this study, multivariate logistic regression analysis revealed that the presence or absence of moderate-to-severe pain was significantly correlated with the depth of localization needle insertion into the lung and the location of the chest wall puncture. Although some studies have reported a significant positive correlation between the increased depth of localization needle insertion into the lung and an elevated incidence of mild intra-pulmonary hemorrhage during CT-guided hook-wire puncture localization (P = 0.044), these studies have not comprehensively explored the potential link with moderate-to-severe pain occurrence [11]. Our results indicated that the shallower the depth of localization needle insertion into the lung and the closer its distance from the pleura is, the greater the likelihood of moderate-to-severe pain after localization. However, no definitive explanation has been established for the specific cause of pain after hook-wire puncture localization. We speculate that pain occurrence may be linked to tissue damage, local inflammation, and other factors. Although hook-wire puncture localization is performed via an optimal path on the basis of prior imaging data and under local anaesthetic infiltration, the skin, subcutaneous tissues, muscles, parietal or visceral pleura, lung parenchyma and even the intercostal nerves and blood vessels are inevitably damaged during the puncture process. These injuries may further lead to the pathological remodeling of the intercostal nerves or visceral pain in the lung tissue, ultimately inducing moderate-to-severe pain. The incidence of pain following hook-wire puncture localization may be related to the anatomical structure and innervation of the pleura. Specifically, the parietal pleura is innervated by pain-sensitive somatic nerves, while the visceral pleura receives innervation from the pulmonary branch of the vagus nerve and the sympathetic trunk which lacks specific nociceptors and is relatively insensitive to painful stimulus [12, 13]. However, an animal study in rats suggested that the neurosensory endings innervating the visceral pleura could transmit certain information [14]. For example, inflammatory mediators released into the pleural cavity at the injury site can stimulate local pain receptors, which then transmit nociception to the brain [12]. Additionally, the location of the chest wall puncture during the hook-wire puncture localization is a critical factor in the development of moderate-to-severe pain. The intercostal nerve, comprising sensory and motor nerve fibers, originates from the ventral branch of the thoracic spinal nerve and runs along the intercostal groove at the lower edge of the rib cage. Consequently, pain may be induced when the intercostal nerve is damaged or stimulated by peripheral inflammatory mediators. In our multivariate regression analysis, hook-wire puncture localization in the lateral chest wall compared with that in the anterior and posterior chest walls was associated with the highest incidence of moderate-to-severe pain. This finding may be attributed to the increased risk of intercostal nerve injury in the lateral chest wall. Therefore, the distribution of the intercostal nerves and injury risk should be thoroughly considered when choosing the location of the hook-wire puncture to reduce the likelihood of pain occurrence. Clinicians can develop individualized puncture positioning protocols, such as increasing the depth of anaesthesia and changing the positioning material, which may help to reduce the incidence of moderate to severe pain in patients, by identifying the important risk factors for the development of moderate-to-severe pain after preoperative CT-guided hook-and-wire puncture positioning.

Our multivariate analysis also revealed that age was not a statistically significant risk factor for pain. Nevertheless, age as a potential risk factor should not be overlooked in pain management strategies. Moreover, the alterations in pain characteristics with age have attracted increasing attention in recent years because of the increasing aging population worldwide. Hence, age-related changes in pain responses have now been extensively studied. These studies have shown that older adults are less responsive to transient cutaneous pain (e.g. thermal pain); conversely, sensitivity to more sustained painful stimuli in deeper tissues increases with increasing patient age [15, 16]. Several researchers have also demonstrated that the temporal summation of pain increases in older adults [17, 18], whereas conditioned pain modulation has been found to diminish with age [19, 20]. All these results imply that increasing age is strongly associated with the altered homeostasis of pain modulation, with patients exhibiting comparatively stronger pain facilitation and lower pain inhibition with increasing age.

This study has a few limitations that should be considered. First, given that this study was observational in nature, we could not clarify the causal relationship between relevant risk factors and moderate-to-severe pain after hook-wire puncture localization. The absence of a significant correlation between post-puncture pain and local procedure-related complications such as intra-pulmonary hemorrhage, pneumothorax and pleural reaction may be related to the small sample size of the study. Hence, future multi-center, large-sample studies are necessary to validate our findings. Second, pain occurrence following the localization procedure is subjective to the patient. Although the relationship between pain and VAS scores was explained to the patients before performing localization, some of them may have had a limited understanding. Thus, the pain assessment in this study may not have fully reflected the actual experience of the patients. Third, the risk factors included in this study were limited, whereas the true number of factors influencing the incidence of moderate-to-severe pain after the localization technique may be considerably greater.

Conclusions

In conclusion, our study revealed that the occurrence of moderate-to-severe pain is common among patients with small pulmonary nodules who undergo CT-guided hook-wire puncture localization. Furthermore, the results of the study demonstrate that the depth of localization needle insertion into the lung and the location of the chest wall puncture are crucial predictors of moderate-to-severe pain incidence.