Preoperative percutaneous localization of multiple ipsilateral pulmonary nodules: A systematic review
Chun-Ling Chi1, Xing Gao1, Cheng-Chen Tai2, Yin-Kai Chao1
1 Division of Thoracic Surgery, Chang Gung Memorial Hospital-Linkou, Chang Gung University, Taoyuan, Taiwan
2 Department of Medical Education, Chang Gung Memorial Hospital-Linkou, Chang Gung University, Taoyuan, Taiwan
Correspondence Address:
Yin-Kai Chao
Division of Thoracic Surgery, Chang Gung Memorial Hospital-Linkou, No 5. Fu-Hsing Street, Taoyuan
Taiwan
Source of Support: None, Conflict of Interest: None
DOI: 10.4103/fjs.fjs_108_22
With the increased radiological investigations applied to lung cancer screening, a growing number of small pulmonary nodules that should undergo biopsy or surgical removal are being identified. Accurate lesion localization is a key prerequisite for successful excision. Unfortunately, repeated pleural punctures in patients with multiple pulmonary nodules (MPNs) may significantly increase the risk of pneumothorax. To illustrate the role and limitations of current techniques for simultaneous localization of MPNs, we searched PubMed, Embase, and the Chinese Electronic Periodical Services for published articles from January 2000 to February 2022. A total of eight references were selected for this systematic review. Compared with techniques for localizing single pulmonary nodules (SPNs), localization of MPNs required a longer procedural time (14−56 min) and demonstrated lower success rates (83.5%−100%). The rates of pneumothorax were markedly higher in patients with MPNs (up to 57.9%) than in those with SPNs (12.7%−32.5%). Various localization methods have been proposed to deal with MPNs, including hook wire, microcoils, and dye localization. Failures most commonly occurred after localization of the first nodule, and the main causes (i.e., hook wire dislodgement, dye diffusion, patient repositioning, or pneumothorax) differed according to the localization technique. Novel approaches – including simultaneous multiple needle insertion and the use of hybrid operating room – hold promise for reducing complications rates and procedural times. Collectively, preoperative percutaneous localization of ipsilateral MPNs is safe and feasible, but future technological innovations are needed in order to enhance localization safety and accuracy.
Keywords: Hybrid operating room, multiple pulmonary nodules, preoperative localization, simultaneous needle insertion
With an increased volume of radiological investigations applied to lung cancer (LC) screening, a growing number of small pulmonary nodules that should undergo biopsy or surgical removal are being identified. Accurate lesion localization is a key prerequisite for successful removal through video-assisted thoracoscopic surgery. Various localization methods have been proposed to deal with small pulmonary nodules, including hookwire, microcoils, and dye localization.[1],[2] However, all of these techniques rely on pleural puncture for which the risk of iatrogenic pneumothorax is not negligible. This is especially important if repeated punctures are needed in patients with ipsilateral multiple pulmonary nodules (MPNs).[3],[4],[5] Several studies have reported on the feasibility and outcomes of MPNs localization, with success rates ranging from 88% to 100%. However, the incidence of iatrogenic pneumothorax may be as high as 50% after the first hook wire placement and may further increase to 89.5% at the end of the procedure.[3],[6] In this scenario, it is important to weigh the advantages and disadvantages of each method. Hence, we performed a systematic review to illustrate the role and limitations of current techniques for simultaneous localization of MPNs.
MethodsStudy selection
This systematic review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines.[7][Figure 1] visually summarizes the study selection process. With the involvement of a senior librarian at the Chang Gung University as an expert searcher, PubMed, Embase, and the Chinese Electronic Periodical Services were queried by two authors (Chun-Ling Chi and Xing Gao) for relevant articles published from January 2000 to February 2022. Search terms included all subject headings and/or keywords associated with “localization” (AND) “lung nodules” (AND) “multiple” in all fields. The full search strategy is available in Supplementary File 1. After excluding duplicates, two authors (CLC and XG) independently screened titles and abstracts. Studies that described the preoperative localization of ipsilateral MPNs were eligible for inclusion. While references were excluded if the research was solely focused on contralateral nodules or single pulmonary nodules (SPNs). Studies that comprised a limited number of contralateral nodules were considered for inclusion. All retrieved references were reviewed to determine which articles met the predefined inclusion criteria. Any discrepancies were resolved by consensus and discussion with an independent, third investigator (Yin-Kai Chao).
Data extraction
Data extraction from the full texts of relevant papers was performed by CLC and checked by XG and YKC. For all studies, data were extracted on (1) general information (title, authors, journal, and year of publication), (2) number of patients who had undergone MPNs localization, (3) number of nodules, (4) mean nodule size, (5) localization approach (i.e., hook wire placement, microcoil positioning, or dye localization), (6) duration of localization (i.e., time elapsed from the beginning of the localization until its completion), (7) success rate (i.e., the ratio of successful nodule localization attempts over all attempts not including the occurrence of dislodgement afterward), (8) resection rate (i.e., the ratio of MPNs successfully excised over all identified MPNs), (9) needle insertion techniques (i.e., multiple punctures performed individually vs. simultaneously), (10) localization-related complications (including pneumothorax and pulmonary hemorrhage), (11) occurrence of severe pneumothorax requiring chest tube positioning or pigtail catheter drainage, and (12) occurrence of progressive pneumothorax requiring interruption of localization.
ResultsStudy characteristics
A total of eight studies met the inclusion criteria [Table 1]. All selected references were two-arm cohort studies published between 2015 and 2022. The largest investigation included 81 patients harboring a total of 169 MPNs. Three references focused on MPNs only, whereas the remaining five included both SPNs and MPNs. The mean nodule size ranged from ~6-8 mm. Two studies included two distinct cohorts of patients who had undergone MPNs localization with different techniques. Specifically, Kadeer et al.[8] compared multiple individual versus simultaneous hook wire insertions, whereas Chao et al.[9] compared preoperative versus intraoperative computed tomography (CT)-guided MPNs localization. Most patients presented with ipsilateral MPNs. In two studies, there was a small proportion of patients with nodules on the contralateral side.
Table 1: Characteristics of the studies included in the systematic reviewNeedle insertion techniques and marker selection
[Table 2] shows the technical details of lesion localization. The most common approach was hook wire localization, followed by microcoil positioning and dye localization. Most procedures took place in an interventional radiology suite and were carried out in a two-step fashion. Only one study was conducted using a single-step procedure for lesion localization and removal within a hybrid operating room (HOR).
Efficacy and safety
The reported success rates for hook wire localization ranged from 83.5% to 98.8%. The lowest success rate (83.5%) was reported in a study in which multiple hook wires were inserted in an individual fashion.[8] Two studies reported on dislodgement rates, which varied from 3.8% to 6%. The mean procedural time ranged from 13 to 56 min.
The main complication of percutaneous approaches was pneumothorax, which occurred in up to 57.9% of patients who had undergone MPNs localization [Table 3]. Only two studies specifically reported the occurrence of severe pneumothorax, whereas three references lacked details on the severity of this complication. Five studies compared MPNs versus SPNs localization. In general, the rates of pneumothorax were markedly higher in patients with MPNs than in those with SPNs, the only exception being the study by Xu et al.[14] Pulmonary hemorrhage was reported in up to 23% of patients who had undergone MPNs localization.
DiscussionLC screening programs have increased the number of MPNs being detected. While accurate preoperative localization is crucial for successful surgical outcomes, there are still significant technical hurdles to overcome. Specifically, the key procedural consideration is to reduce the risk of iatrogenic pneumothorax while multiple pleural punctures are being performed. In the present systematic review, we summarized the feasibility, safety, and clinical efficacy of preoperative MPNs localization based on the published literature.
Safety and efficacy of multiple pulmonary nodules versus single pulmonary nodules localization
Compared with SPNs, simultaneous MPNs localization is expected to be associated with a longer procedural time and lower success rates. Of the eight studies included in our systematic review, five compared the outcomes of MPNs versus SPNs localization. As expected, the technical success rate of MPNs localization was lower compared with that of SPNs, with the most unfavorable outcomes being reported in the study by Kadeer et al.[8] when multiple needles were inserted one after the other. These results were attributed to the localization success criterion (i.e., distance between localizer and lesion <3 cm) and the mean number of lesions (2.51 per patient). In other studies, failures most commonly occurred after localization of the first nodule – with the main causes including hook wire dislodgement, dye diffusion, position changes, and pneumothorax. The lower technical success rate of MPNs versus SPNs localization is also consistent with the meta-analysis by Park et al.,[16] which mainly included studies focusing on SPNs. The reported success rates obtained with different techniques – including hook wire, microcoils, and dye localization – were as high as 98%−99%.[16] In our systematic review, we found that the localization technique affected failure rates. The two principal causes of failed hook wire localization were dislodgement before completion of the localization procedure and massive pneumothorax. In the study by Kadeer et al.,[8] failures occurred only when the authors attempted to identify a third nodule in patients who harbored at least two pulmonary lesions. The physical characteristics of tissue marking dyes have been related to the risk of failure when this technique was applied. In general, surgery should be conducted on the same day of the dye marking procedure. This is because surgeons cannot resort to palpation in the event of dye diffusion, differently from what can be implemented in case of hook wire or microcoil localization. In the study by Xu et al.,[13] cyanoacrylate used for dye marking caused small airway irritation when given through rapid injection. The correct identification of MPNs was ultimately compromised by changes in patient positioning as a result of cough and difficulty in breathing.[13] Other technical challenges – including the limited visualization in anthracotic regions of the lung surfaces – are similar to those encountered during SPNs localization. The lower localization rates for MPNs were not paralleled by reduced resection rates. However, excision was mainly accomplished using segmentectomy or lobectomy. In the presence of successful localization, more conservative approaches (e.g., wedge resection) would have been feasible without compromising clinical outcomes. In the study by Hu et al.[11] where a resection rate of 98.7% was reported, there was only a single case of iatrogenic pneumothorax occurring during localization. The patient had a 3-mm pure ground-glass nodule and the puncture needle failed to enter into the visceral pleura.
The eight studies included in our systematic review reported procedural times ranging from 13 to 56 min. This variable, however, varies greatly according to localization materials, needle insertion technique, how many nodules need to be localized, and whether the patient has to be repositioned or not.
The main concern for MPN procedure is the incidence of iatrogenic pneumothoraxes, this rate is as high as 57.9% in our included studies. While the incidence of severe cases was markedly lower (4.8%−8.6%) and more data are required to draw definitive conclusions, it should be noted that even mild pneumothorax may compromise visceral pleural puncture. In this scenario, localization can be further complicated even in the presence of superficial lesions. Based on the five studies that compared MPNs versus SPNs localization [Table 3], the rates of pneumothorax were markedly higher in patients with MPNs (up to 57.9%) than in those with SPNs (12.7%−32.5%).
Applying novel techniques to minimize complications during multiple pulmonary nodules localization: simultaneous needle insertion and/or hybrid operating rooms
Novel techniques have been designed to overcome the difficulties in localizing MPNs, including simultaneous multiple needle insertion and the use of HORs. The former is a modification of the approach proposed by Kadeer et al.[8] in which a row of wires is attached to the skin in the position of each nodule according to projection images. After positioning of needles in the correct direction and depth, they are introduced simultaneously into the target lesions and subsequently released. Compared with the traditional approach according to which multiple needles are inserted one after the other, this method decreased the risk of pneumothorax from 54.7% to 21.8%. Moreover, this technique was associated with a higher success rate (96.7% vs. 83.5%, respectively) and a markedly lower procedural time (14 min vs. 23 min, respectively) compared with traditional hook wire localization. This approach has been recently successfully replicated with promising results.[8]
Another novel technique for MPNs localization has been recently described by Chao et al.[9] who compared traditional preoperative localization performed in a radiology suite versus intraoperative CT-guided localization performed in a HOR equipped with C-arm cone-beam CT. Within the HOR, the authors simultaneously accomplished both localization and removal of MPNs. The advantages offered by the use of a HOR included a reduction of the time at risk (i.e., procedural time and transfer time), a lower radiation exposure, and a reduced risk of patient repositioning (due to the wide range of the cone-beam CT unit). Both procedural time and the need for intraprocedural patient repositioning have been associated with an increased risk of pneumothorax; therefore, the use of HORs may offer inherent advantages for MPNs localization. However, a potential caveat is the longer general anesthesia time required for HOR localization, especially when at least three nodules are present. In this scenario, benefits should be weighed against the availability of HORs and the potential risks of prolonged general anesthesia.
Bronchoscopic localization of multiple pulmonary nodules: new hope for the future?
Electromagnetic navigation bronchoscopy generates a three-dimensional representation of the tracheobronchial tree starting from CT data. An electromagnetic tracking device can subsequently be used to navigate a steerable probe to target peripheral lung lesions. This approach, coupled with dye marking, allows performing one-stage surgery for multiple lung nodules. Previous investigations focusing on preoperative localization of pulmonary nodules reported success rates of 94%−94.5% with a limited occurrence of complications (i.e., pneumothorax and pulmonary hemorrhage).[15],[17],[18] The mean procedural time ranged between 25 and 29.4 min.[17],[18] However, the reliability of the conclusions should be interpreted cautiously given the limited number of patients with MPNs included in these studies.
Limitations
There are limitations to our systematic review. We acknowledge that all included studies had a retrospective design. It is also possible that several confounding variables (e.g., operator experience, needle direction, and puncture depth) were not properly taken into account. Finally, the lack of technical standardization may jeopardize the effectiveness of localization and result in healthcare disparities.
ConclusionsPreoperative percutaneous localization of ipsilateral MPNs is safe and feasible. However, compared with techniques for localizing SPNs, localization of MPNs required a longer procedural time and demonstrated lower success rates and a higher burden of complications. Future technological innovation is going to increase the number of alternatives to enhance localization safety and accuracy.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
Comments (0)