Journal of Medical Imaging and Radiation Oncology 58 (2014) 657–662 bs_bs_banner
R ADIOLO GY—OR I G I N AL A RT I C L E
Usefulness of CT-guided hookwire marking before video-assisted thoracoscopic surgery for small pulmonary lesions Kazushi Suzuki,1 Masashi Shimohira,1 Takuya Hashizume,1 Yoshiyuki Ozawa,1 Ryoji Sobue,2 Mikio Mimura,2 Yuji Mori,3 Hidenori Ijima,4 Kenichi Watanabe,4 Motoki Yano,5 Hiromu Yoshioka6 and Yuta Shibamoto1 1 Department of Radiology, Nagoya City University Graduate School of Medical Sciences, Departments of 2Radiology and 6Thoracic Surgery, Japanese Red Cross Nagoya Daini Hospital, 3Department of Radiology, Nagoya City East Medical Center, 5Department of Thoracic Surgery, Nagoya City University Medical School, Nagoya and 4Department of Radiology, Okazaki City Hospital, Okazaki, Japan
K Suzuki MD; M Shimohira MD; T Hashizume MD; Y Ozawa MD; R Sobue MD; M Mimura MD; Y Mori MD; H Ijima MD; K Watanabe MD; M Yano MD; H Yoshioka MD; Y Shibamoto MD. Correspondence Dr Kazushi Suzuki, Department of Radiology, Nagoya City University Graduate School of Medical Sciences, Nagoya, 467-8601, Japan. E-mail: [email protected] Conflict of interest: The authors have no conflicts of interest regarding this article. Submitted 26 February 2014; accepted 27 June 2014. doi:10.1111/1754-9485.12214
Abstract Purpose: The aim of this study was to evaluate the technical and clinical efficacy and safety of CT-guided hookwire marking before video-assisted thoracoscopic surgery (VATS) for small pulmonary lesions. Materials and Methods: This procedure was performed on 161 lesions in 154 patients (75 men and 79 women; median age, 62 years; age range 23–89 years). Medical records and images were reviewed, and the technical success rate, surgical success rate and complications were evaluated. Technical success was defined as successful hookwire marking at the target site without marker dropping before VATS. Surgical success was defined as negative surgical margins on pathological examination after VATS. Results: There were 97 nodules and 64 ground-glass opacities, and their mean size was 9.8 mm (range 2–34). The technical success rate was 97.5% (157/161). In three of the four failed cases, another hookwire marker was placed, and in the remaining case, VATS was performed without a marker. The surgical success rate was 98.1% (158/161). In the three failed cases, the margin was positive, so lung lobectomy was performed in one case, and the other two cases were observed carefully. Complication rates were as follows: pneumothorax, 37.9% (61/161); focal intrapulmonary haemorrhage, 34.8% (58/139); haemoptysis, 0.6% (1/161); haemothorax, 0% (0/161); air embolism, 0.6% (1/161); dissemination, 0% (0/161); and death, 0% (0/161). Conclusion: CT-guided hookwire marking appears to be useful for VATS, but the procedure may, although rarely, cause severe complications such as air embolism. Key words: air embolism; CT-guided marking; hookwire; video-assisted thoracic surgery.
Introduction A lung nodule is defined as an intraparenchymal lung mass that is ≤3 cm in diameter. Frequently, these nodules are detected incidentally by thin-slice helical CT upon examination for another medical reason. Furthermore, screening for lung tumour with spiral CT has become available, and many otherwise undetectable small lung nodules are now detected.1 Conventional diagnostic modalities, such as bronchoscopic or tran© 2014 The Royal Australian and New Zealand College of Radiologists
sthoracic needle biopsy, are not very useful in the diagnosis of some of these small lung nodules, and videoassisted thoracoscopic surgery (VATS) now plays a more important role.2,3 VATS has gained widespread acceptance, because it can minimise post-operative morbidity and remove as small a volume of lung tissue as possible. In addition, pulmonary function and prognosis are far better after VATS than after open thoracotomy.4 However, the disadvantage of VATS is the difficulty in detecting small subpleural nodules, which are frequently 657
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neither visible nor palpable. Therefore, preoperative marking of a pulmonary nodule often becomes necessary. In this study, we evaluated the technical and clinical efficacy and safety of CT-guided hookwire marking before VATS for small pulmonary lesions.
Methods Study aim and approval This retrospective study was performed to evaluate the technical and clinical efficacy and safety of CT-guided hookwire marking before VATS for small pulmonary lesions. This study was approved by the institutional review board, and written informed consent was obtained from all patients.
Patients From July 2004 through July 2014, 161 pulmonary lesions in 154 patients underwent hookwire marking for pulmonary lesions using CT or CT fluoroscopy guidance. The patients comprised 75 men and 79 women, with a median age of 62 years (range 23–89 years), and all were inpatients. For four patients, multiple marking procedures were performed. The mean diameter of the lesions was 9.8 mm (range 2–34). Ninety-seven lesions (60.3%) had solid opacity, and 64 (39.7%) had groundglass opacity (GGO).
Device and technique All marking procedures were performed on the day of VATS. A 21-gauge marker needle (Guiding-Marker System, Hakko, Tokyo, Japan; Fig. 1) was used in all procedures and it was manipulated according to Kanazawa et al.5 This marker system includes a stainless steel hookwire marker and its introducer. The hookwire is 0.28 mm in diameter and 10 mm in length. A 30-cmlong, 5-0 nylon monofilament suture is firmly attached to its proximal end. The introducer system consists of a 21-gauge, 10- or 15-cm-long cannula, and a 24-gauge, 10-cm-long hollow pusher. The hookwire is preloaded inside the tip of the cannula, the distal end of the pusher is in place immediately after the hookwire, and the attached suture passes through the pusher. During the procedure, first, chest CT scan was performed to confirm the position of the pulmonary lesion. After local anaesthesia, the needle was inserted under CT guidance or CT fluoroscopy. In 88 cases, the procedure was performed with CT guidance, and in 73, with CT fluoroscopy guidance. When it was confirmed by CT or CT fluoroscopy that the needle was near the pulmonary lesion, the marker was deployed as follows. After releasing the safe stopper of the pusher, the hookwire was ejected by full advance of the pusher. Once CT or CT fluoroscopy showed that the hookwire was just free from 658
Fig. 1. (a) Photograph of the 21-gauge marker needle (Guiding-Marker System, Hakko, Tokyo, Japan). (b) Magnified photograph of hookwire (arrowhead), hollow pusher (thin arrow) and cannula (thick arrow). (c) Monofilament nylon suture (5-0) firmly attached to the funnel-shaped proximal end of hookwire (arrow).
the cannula, the introducer system was carefully withdrawn. Chest CT scan was repeated immediately after the procedure to evaluate the marker position and complications. The portion of the suture outside the patient was loosely coiled, kept free to move and kept covered with a sterile gauze. The suture was used at VATS as a © 2014 The Royal Australian and New Zealand College of Radiologists
CT-guided marking before VATS
guide to the lesion. In all cases, VATS was performed immediately after placement of the marker, usually within 1–2 h.
Assessment To evaluate the technical success rate, surgical success rate and complications, medical records and images were reviewed. Technical success was defined as successful hookwire marking at the target site without marker dropping before VATS. Surgical success was defined as resection of the target lesion with negative margins on pathological examination after VATS. Complications evaluated were pneumothorax, alveolar haemorrhage, haemoptysis, haemothorax, air embolism, dissemination of the punctured route and technicalrelated deaths.
Results In 157 of the 161 procedures (97.5%), the marker was placed in an appropriate position (Fig. 2). In 4 of the 161 procedures (2.5%), dislodgement of the hookwire occurred. Three of the four cases underwent marker placement again. In one case, the marker was confirmed to be located in the chest wall, and subcutaneous emphysema was observed; however, VATS was performed successfully without a marker in this case. The technical success rate was therefore 97.5%. The mean distance from a marker to the lesion was 7.4 mm (range 0–39). All inserted markers were resected during VATS without any complications. The pathological margin was negative in 158 of the 161 lesions (98.1%), whereas in three cases it was positive (1.9%). Lobectomy was performed in one case, and two cases are being followed carefully. Thus, the surgical success rate was 98.1%. Their pathological diagnosis was as follows: primary lung cancer in 87 (54.0%), metastatic lung cancer in 46 (28.6%), MALT lymphoma in 1, and benign lesion in 27. Complications were as follows: alveolar haemorrhage in 66 (41.6%), pneumothorax with no drainage tube insertion in 61 (37.9%), haemoptysis in 1 (0.6%), and air embolism in 1 (0.6%). There was no haemothorax, dissemination of the punctured route or procedure-related deaths. No patients developed any new symptoms between the end of marker placement and the start of the VATS, except for one air embolism case. In one case of air embolism, difficulty in movement and numbness in the left arm developed after marking, and a small amount of air was confirmed to exist in the heart at CT after the procedure (Fig. 3). She was referred to a neurologist promptly, and was instructed to have complete bed rest and oxygen inhalation. The patient’s symptoms had disappeared when she returned to the hospital room. The air in the heart had completely disappeared on CT performed in the afternoon of the same day. VATS was performed successfully 5 days after marking. © 2014 The Royal Australian and New Zealand College of Radiologists
Fig. 2. A 61-year-old woman presenting with a pulmonary nodule in the left upper lobe. (a) CT showed a solid lesion, and the needle of the hookwire marker was inserted near the nodule in the supine position under CT fluoroscopy guidance. (b) CT showed successful placement of the hookwire marker near the lesion.
Discussion VATS for pulmonary lesions has been performed widely. VATS can significantly reduce postoperative pain, preserves respiratory function, is less invasive to the thoracic wall and maintains a better quality of life.6,7 However, it is difficult to perform for small subpleural pulmonary lesions. Yoshida et al.8 reported that 85–92% of pulmonary lesions were neither visible nor palpable during thoracoscopic resection. Furthermore, Suzuki et al.9 reported that failure to visualise or palpate the nodule was observed in 54% of patients, requiring conversion from VATS to thoracotomy for successful resection. Therefore, preoperative marker placement is important, and various methods have been reported using a hookwire, a spiral wire, a platinum microcoil, methylene blue, technetium-99m macroaggregated albumin, lipiodol or ultrasound.8,10–20 Vandoni et al.15 659
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Fig. 3. A 29-year-old woman presenting with a pulmonary nodule in the left lower lobe. (a) CT showed a solid lesion, and the needle of hookwire marker was inserted near the nodule in the prone position under CT guidance. (b) CT showed air in her heart (white arrow).
described the use of methylene blue injections and reported a high success rate (92.6%), but they recommended that the time between labelling and operation should be kept within a maximum of 3 h because the coloured substances frequently spread into the surrounding normal tissues. Santambrogio et al.20 reported that localisation using thoracoscopic ultrasound was noninvasive, with a high success rate (100%) in their 18 cases, but it had some limitations, requiring a great deal of experience and a special flexible probe. Also, it is limited by the presence of air in the lung when complete lung collapse is not feasible. Injection of radionuclides also achieved a high success rate (96–100%)17,18; nevertheless, it seems to have most of the same problems as thoracoscopic ultrasound and methylene blue injection. These include the need for a special flexible probe during thoracoscopic surgery and no opportunity to inject again if a technical mistake occurs. Gonfiotti et al.18 experienced contamination of the pleural cavity with a contrast 660
medium, including radionuclides due to a technical mistake during CT-guided injection. They missed the localisation of the lesion and also finger palpation was unable to localise the lesion. The lipiodol marking procedure showed a high success rate (100%), but a C-arm-shaped fluoroscopic unit is required to detect the infused lipiodol.19 Short hookwire marking also has a high success rate (93.6–97.6%).10,11 Dendo et al.11 mentioned that the design with a short hookwire and long suture is an advantage of this system. Because the flexible suture protrudes from the skin, patients do not complain of pleural pain associated with breathing. In addition, there is reliability in that an operator does not need to not push or pull the hookwire embedded in the lung. It is possible to move the patient to an operating table or stretcher without special care. Some minor complications, such as pneumothorax, pulmonary haemorrhage and haemothorax, may occur by insertion of the needle into the lung, but this is not specific to hookwire placement. Thus, we think that hookwire placement is the most appropriate procedure. It was reported that asymptomatic pneumothorax was observed in 7.5–49% of cases, pulmonary bleeding in 14.9–29.8%, haemorrhage into the pleural cavity in 0.6– 3.5% and dislodgment of the marker in 1.8–7.5%.10–12 In our study, the results were almost the same: pneumothorax in 37.9%, pulmonary haemorrhage in 41.6% and dislodgment of the marker in 2.5%. Although relatively rare, systemic air embolism is an important serious complication during hookwire placement. Fortunately, in our case the patient’s neurological impairment was transient, with no permanent sequelae. In the English literature, five cases of air embolism during hookwire marking have been reported since 200221–25 (Table 1). However, all of these are described as case reports, so its incidence is unknown. On the other hand, the incidence of air embolism during transthoracic needle biopsy, which is a similar procedure to hookwire placement, has been estimated to be 0.02– 0.07%.26–28 Three cases of air embolism have been reported among about 20 000 shipments of a marker system, so the incidence is estimated to be about 0.015%.29 However, all cases of air embolism might not necessarily have been detected and reported to the manufacturer. Also, all of the shipped markers might not necessarily have been used. Therefore, the actual incidence of air embolism may be higher. Thus, we think that the 0.6% (1/161) rate of air embolism in our study might be a reasonable rate. The mechanism of air embolism during hookwire marking is the communication between the airway and pulmonary vein.20–22 In some situations, such as coughing and placement while breath-holding during inspiration, and repositioning after placement, intra-alveolar pressure is increased, and the risk of air embolism might increase. Lalli et al.30 also mentioned that an increase of airway pressure caused by © 2014 The Royal Australian and New Zealand College of Radiologists
CT-guided marking before VATS
Table 1. Air embolism complication during CT-guided pulmonary marking
Kamiyoshihara et al.21 Horan et al.22 Sakiyama et al.23 Sato et al.24 Iguchi et al.25 Our study
Age
Sex
Location
Size (mm)
Needle
Position
Cardiac symptoms
Neurological symptoms
Outcome
24 32 79 59 75 27
F M F M M F
RLL LLL RLL RLL RUL RLL
4 10 15 7 6 13
22G 20G 21G 21G 21G 21G
Left lateral Right lateral Left semilateral Prone Supine Prone
No Yes Yes Yes Yes No
Yes No No Yes No Yes
Alive Alive Died Alive Alive Alive
RLL, right lower lobe; LLL, left lower lobe; RUL, right upper lobe.
a cough, the Valsalva manoeuvre or positive pressure ventilation increases the risk of air embolism. Considering such mechanisms, placement with breath-holding under submaximal inspiration, slow repositioning after placement and medication for cough prevention may be effective to prevent air embolism. In addition, in five of six cases including our case, air embolism occurred when the hookwire was placed in lower lobe lesions. Freund et al.31 identified risk factors for the occurrence of systemic air embolism resulting from the biopsy technique. In their study, location of the lesion in the lower lobe was one of the risk factors for systemic air embolism. We speculate that air embolism during hookwire marking might more likely occur in the lower lobe, similar to biopsy situations, because there is no difference between the two techniques to puncture the lung. Moreover, we speculate that the lower lobe shows greater movement during breathing than the upper lobe, and makes puncture difficult. If the hookwire is placed in the lower lobe, it is necessary to make the patient breathe shallowly and to carefully check the symptoms and condition of the patient. Furthermore, we believe that whole-lung CT after hookwire marking is important and should be performed not only to confirm the hookwire position, but also to confirm the absence of pneumothorax, haemorrhage and especially air embolism. The median distance between the marker and the lesion was 7.4 mm (range 0–39) in our study. The marker should be placed as close to the lesion as possible, to readily perform VATS procedure. Considering our results, the desirable distance between the marker and a lesion might be less than 8 mm. However, in deciding the access route and site of marker placement, it is necessary to consider the lung conditions such as emphysema, the vasculature in the lung and chest wall, and the position of the patients to avoid complications. In conclusion, CT-guided hookwire marking yielded high technical and clinical success rates. As VATS has become widespread, VATS for small lesions which are neither visible nor palpable will increase. Therefore, preoperative marking for those pulmonary lesions will become more important. We believe that reliable CT-guided hookwire marking can remove as small a volume of lung tissue as possible and minimise post© 2014 The Royal Australian and New Zealand College of Radiologists
operative morbidity. However, it might, although rarely, cause severe complications such as air embolism.
References 1. Kaneko M, Eguchi K, Ohmatsu H et al. Peripheral lung cancer: screening and detection with low-dose spiral CT versus radiography. Radiology 1996 Dec; 201: 798–802. 2. Burdine J, Joyce LD, Plunkett MB, Inampudi S, Kaye MG, Dunn DH. Feasibility and value of video-assisted thoracoscopic surgery wedge excision of small pulmonary nodules in patients with malignancy. Chest 2002; 122: 1467–70. 3. Yan TD, Black D, Bannon PG, McCaughan BC. Systematic review and meta-analysis of randomized and nonrandomized trials on safety and efficacy of video-assisted thoracic surgery lobectomy for early-stage non-small-cell lung cancer. J Clin Oncol 2009 May 20; 27: 2553–62. 4. Kaseda S, Aoki T, Hangai N, Shimizu K. Better pulmonary function and prognosis with video-assisted thoracic surgery than with thoracotomy. Ann Thorac Surg 2000 Nov; 70: 1644–6. 5. Kanazawa S, Ando A, Yasui K, Tanaka A, Hiraki Y. Localization of small pulmonary nodules for thoracoscopic resection: use of a newly developed hookwire system. Cardiovasc Intervent Radiol 1995 Mar–Apr; 18: 122–4. 6. Landreneau RJ, Hazelrigg SR, Mack MJ et al. Postoperative pain-related morbidity: video-assisted thoracic surgery versus thoracotomy. Ann Thorac Surg 1993 Dec; 56: 1285–9. 7. Karasaki T, Nakajima J, Murakawa T et al. Video-assisted thoracic surgery lobectomy preserves more latissimus dorsi muscle than conventional surgery. Interact Cardiovasc Thorac Surg 2009 Mar; 8: 316–20. 8. Yoshida Y, Inoh S, Murakawa T, Ota S, Fukayama M, Nakajima J. Preoperative localization of small peripheral pulmonary nodules by percutaneous marking under computed tomography guidance. Interact Cardiovasc Thorac Surg 2011 Jul; 13: 25–8. 9. Suzuki K, Nagai K, Yoshida J et al. Video-assisted thoracoscopic surgery for small indeterminate pulmonary nodules: indications for preoperative marking. Chest 1999 Feb; 115: 563–8.
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10. Ciriaco P, Negri G, Puglisi A, Nicoletti R, Del Maschio A, Zannini P. Video-assisted thoracoscopic surgery for pulmonary nodules: rationale for preoperative computed tomography-guided hookwire localization. Eur J Cardiothorac Surg 2004 Mar; 25: 429–33. 11. Dendo S, Kanazawa S, Ando A et al. Preoperative localization of small pulmonary lesions with a short hook wire and suture system: experience with 168 procedures. Radiology 2002 Nov; 225: 511–18. 12. Miyoshi K, Toyooka S, Gobara H et al. Clinical outcomes of short hook wire and suture marking system in thoracoscopic resection for pulmonary nodules. Eur J Cardiothorac Surg 2009 Aug; 36: 378–82. 13. Eichfeld U, Dietrich A, Ott R, Kloeppel R. Video-assisted thoracoscopic surgery for pulmonary nodules after computed tomography-guided marking with a spiral wire. Ann Thorac Surg 2005 Jan; 79: 313–17. 14. Powell TI, Jangra D, Clifton JC et al. Peripheral lung nodules: fluoroscopically guided video-assisted thoracoscopic resection after computed tomography-guided localization using platinum microcoils. Ann Surg 2004 Sep; 240: 481–9. 15. Vandoni RE, Cuttat JF, Wicky S, Suter M. CT-guided methylene-blue labelling before thoracoscopic resection of pulmonary nodules. Eur J Cardiothorac Surg 1998 Sep; 14: 265–70. 16. Kerrigan DC, Spence PA, Crittenden MD, Tripp MD. Methylene blue guidance for simplified resection of a lung lesion. Ann Thorac Surg 1992 Jan; 53: 163–4. 17. Chella A, Lucchi M, Ambrogi MC et al. A pilot study of the role of TC-99 radionuclide in localization of pulmonary nodular lesions for thoracoscopic resection. Eur J Cardiothorac Surg 2000 Jul; 18: 17–21. 18. Gonfiotti A, Davini F, Vaggelli L et al. Thoracoscopic localization techniques for patients with solitary pulmonary nodule: hookwire versus radio-guided surgery. Eur J Cardiothorac Surg 2007 Dec; 32: 843–7. 19. Watanabe K, Nomori H, Ohtsuka T, Kaji M, Naruke T, Suemasu K. Usefulness and complications of computed tomography-guided lipiodol marking for fluoroscopy-assisted thoracoscopic resection of small pulmonary nodules: experience with 174 nodules. J Thorac Cardiovasc Surg 2006 Aug; 132: 320–4. 20. Santambrogio R, Montorsi M, Bianchi P, Mantovani A, Ghelma F, Mezzetti M. Intraoperative ultrasound
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during thoracoscopic procedures for solitary pulmonary nodules. Ann Thorac Surg 1999 Jul; 68: 218–22. Kamiyoshihara M, Sakata K, Ishikawa S, Morishita Y. Cerebral arterial air embolism following CT-guided lung needle marking. Report of a case. J Cardiovasc Surg (Torino) 2001 Oct; 42: 699–700. Horan TA, Pinheiro PM, Araújo LM, Santiago FF, Rodrigues MR. Massive gas embolism during pulmonary nodule hook wire localization. Ann Thorac Surg 2002 May; 73: 1647–9. Sakiyama S, Kondo K, Matsuoka H et al. Fatal air embolism during computed tomography-guided pulmonary marking with a hook-type marker. J Thorac Cardiovasc Surg 2003 Oct; 126: 1207–9. Sato K, Miyauchi K, Shikata F, Murakami T, Yoshioka S, Kawachi K. Arterial air embolism during percutaneous pulmonary marking under computed tomography guidance. Jpn J Thorac Cardiovasc Surg 2005 Jul; 53: 404–6. Iguchi T, Yoshioka T, Muro M et al. Systemic air embolism during preoperative pulmonary marking with a short hook wire and suture system under CT fluoroscopy guidance. Jpn J Radiol 2009 Nov; 27: 385–8. Sinner WN. Complications of percutaneous transthoracic needle aspiration biopsy. Acta Radiol Diagn (Stockh) 1976 Nov; 17: 813–28. Tolly TL, Feldmeier JE, Czarnecki D. Air embolism complicating percutaneous lung biopsy. AJR Am J Roentgenol 1988 Mar; 150: 555–6. Tomiyama N, Yasuhara Y, Nakajima Y et al. CT-guided needle biopsy of lung lesions: a survey of severe complication based on 9783 biopsies in Japan. Eur J Radiol 2006 Jul; 59: 60–4. Oikawa T, Nomoto Y, Kinoshita K. A case of left-sided hemiplegia due to cerebral air embolism caused by CT-guided marking for small peripheral lung cancer. J Jpn Assoc Chest Surg 2008-09-15; 22: 914–19 (Japanese article). Lalli AF, McCormack LJ, Zelch M, Reich NE, Belovich D. Aspiration biopsies of chest lesions. Radiology 1978; 127: 35–40. Freund MC, Petersen J, Goder KC, Bunse T, Wiedermann F, Glodny B. Systemic air embolism during percutaneous core needle biopsy of the lung: frequency and risk factors. BMC Pulm Med 2012 Feb 6; 12: 2.
© 2014 The Royal Australian and New Zealand College of Radiologists
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R ADIOLO GY—OR I G I N AL A RT I C L E
Usefulness of CT-guided hookwire marking before video-assisted thoracoscopic surgery for small pulmonary lesions Kazushi Suzuki,1 Masashi Shimohira,1 Takuya Hashizume,1 Yoshiyuki Ozawa,1 Ryoji Sobue,2 Mikio Mimura,2 Yuji Mori,3 Hidenori Ijima,4 Kenichi Watanabe,4 Motoki Yano,5 Hiromu Yoshioka6 and Yuta Shibamoto1 1 Department of Radiology, Nagoya City University Graduate School of Medical Sciences, Departments of 2Radiology and 6Thoracic Surgery, Japanese Red Cross Nagoya Daini Hospital, 3Department of Radiology, Nagoya City East Medical Center, 5Department of Thoracic Surgery, Nagoya City University Medical School, Nagoya and 4Department of Radiology, Okazaki City Hospital, Okazaki, Japan
K Suzuki MD; M Shimohira MD; T Hashizume MD; Y Ozawa MD; R Sobue MD; M Mimura MD; Y Mori MD; H Ijima MD; K Watanabe MD; M Yano MD; H Yoshioka MD; Y Shibamoto MD. Correspondence Dr Kazushi Suzuki, Department of Radiology, Nagoya City University Graduate School of Medical Sciences, Nagoya, 467-8601, Japan. E-mail: [email protected] Conflict of interest: The authors have no conflicts of interest regarding this article. Submitted 26 February 2014; accepted 27 June 2014. doi:10.1111/1754-9485.12214
Abstract Purpose: The aim of this study was to evaluate the technical and clinical efficacy and safety of CT-guided hookwire marking before video-assisted thoracoscopic surgery (VATS) for small pulmonary lesions. Materials and Methods: This procedure was performed on 161 lesions in 154 patients (75 men and 79 women; median age, 62 years; age range 23–89 years). Medical records and images were reviewed, and the technical success rate, surgical success rate and complications were evaluated. Technical success was defined as successful hookwire marking at the target site without marker dropping before VATS. Surgical success was defined as negative surgical margins on pathological examination after VATS. Results: There were 97 nodules and 64 ground-glass opacities, and their mean size was 9.8 mm (range 2–34). The technical success rate was 97.5% (157/161). In three of the four failed cases, another hookwire marker was placed, and in the remaining case, VATS was performed without a marker. The surgical success rate was 98.1% (158/161). In the three failed cases, the margin was positive, so lung lobectomy was performed in one case, and the other two cases were observed carefully. Complication rates were as follows: pneumothorax, 37.9% (61/161); focal intrapulmonary haemorrhage, 34.8% (58/139); haemoptysis, 0.6% (1/161); haemothorax, 0% (0/161); air embolism, 0.6% (1/161); dissemination, 0% (0/161); and death, 0% (0/161). Conclusion: CT-guided hookwire marking appears to be useful for VATS, but the procedure may, although rarely, cause severe complications such as air embolism. Key words: air embolism; CT-guided marking; hookwire; video-assisted thoracic surgery.
Introduction A lung nodule is defined as an intraparenchymal lung mass that is ≤3 cm in diameter. Frequently, these nodules are detected incidentally by thin-slice helical CT upon examination for another medical reason. Furthermore, screening for lung tumour with spiral CT has become available, and many otherwise undetectable small lung nodules are now detected.1 Conventional diagnostic modalities, such as bronchoscopic or tran© 2014 The Royal Australian and New Zealand College of Radiologists
sthoracic needle biopsy, are not very useful in the diagnosis of some of these small lung nodules, and videoassisted thoracoscopic surgery (VATS) now plays a more important role.2,3 VATS has gained widespread acceptance, because it can minimise post-operative morbidity and remove as small a volume of lung tissue as possible. In addition, pulmonary function and prognosis are far better after VATS than after open thoracotomy.4 However, the disadvantage of VATS is the difficulty in detecting small subpleural nodules, which are frequently 657
K Suzuki et al.
neither visible nor palpable. Therefore, preoperative marking of a pulmonary nodule often becomes necessary. In this study, we evaluated the technical and clinical efficacy and safety of CT-guided hookwire marking before VATS for small pulmonary lesions.
Methods Study aim and approval This retrospective study was performed to evaluate the technical and clinical efficacy and safety of CT-guided hookwire marking before VATS for small pulmonary lesions. This study was approved by the institutional review board, and written informed consent was obtained from all patients.
Patients From July 2004 through July 2014, 161 pulmonary lesions in 154 patients underwent hookwire marking for pulmonary lesions using CT or CT fluoroscopy guidance. The patients comprised 75 men and 79 women, with a median age of 62 years (range 23–89 years), and all were inpatients. For four patients, multiple marking procedures were performed. The mean diameter of the lesions was 9.8 mm (range 2–34). Ninety-seven lesions (60.3%) had solid opacity, and 64 (39.7%) had groundglass opacity (GGO).
Device and technique All marking procedures were performed on the day of VATS. A 21-gauge marker needle (Guiding-Marker System, Hakko, Tokyo, Japan; Fig. 1) was used in all procedures and it was manipulated according to Kanazawa et al.5 This marker system includes a stainless steel hookwire marker and its introducer. The hookwire is 0.28 mm in diameter and 10 mm in length. A 30-cmlong, 5-0 nylon monofilament suture is firmly attached to its proximal end. The introducer system consists of a 21-gauge, 10- or 15-cm-long cannula, and a 24-gauge, 10-cm-long hollow pusher. The hookwire is preloaded inside the tip of the cannula, the distal end of the pusher is in place immediately after the hookwire, and the attached suture passes through the pusher. During the procedure, first, chest CT scan was performed to confirm the position of the pulmonary lesion. After local anaesthesia, the needle was inserted under CT guidance or CT fluoroscopy. In 88 cases, the procedure was performed with CT guidance, and in 73, with CT fluoroscopy guidance. When it was confirmed by CT or CT fluoroscopy that the needle was near the pulmonary lesion, the marker was deployed as follows. After releasing the safe stopper of the pusher, the hookwire was ejected by full advance of the pusher. Once CT or CT fluoroscopy showed that the hookwire was just free from 658
Fig. 1. (a) Photograph of the 21-gauge marker needle (Guiding-Marker System, Hakko, Tokyo, Japan). (b) Magnified photograph of hookwire (arrowhead), hollow pusher (thin arrow) and cannula (thick arrow). (c) Monofilament nylon suture (5-0) firmly attached to the funnel-shaped proximal end of hookwire (arrow).
the cannula, the introducer system was carefully withdrawn. Chest CT scan was repeated immediately after the procedure to evaluate the marker position and complications. The portion of the suture outside the patient was loosely coiled, kept free to move and kept covered with a sterile gauze. The suture was used at VATS as a © 2014 The Royal Australian and New Zealand College of Radiologists
CT-guided marking before VATS
guide to the lesion. In all cases, VATS was performed immediately after placement of the marker, usually within 1–2 h.
Assessment To evaluate the technical success rate, surgical success rate and complications, medical records and images were reviewed. Technical success was defined as successful hookwire marking at the target site without marker dropping before VATS. Surgical success was defined as resection of the target lesion with negative margins on pathological examination after VATS. Complications evaluated were pneumothorax, alveolar haemorrhage, haemoptysis, haemothorax, air embolism, dissemination of the punctured route and technicalrelated deaths.
Results In 157 of the 161 procedures (97.5%), the marker was placed in an appropriate position (Fig. 2). In 4 of the 161 procedures (2.5%), dislodgement of the hookwire occurred. Three of the four cases underwent marker placement again. In one case, the marker was confirmed to be located in the chest wall, and subcutaneous emphysema was observed; however, VATS was performed successfully without a marker in this case. The technical success rate was therefore 97.5%. The mean distance from a marker to the lesion was 7.4 mm (range 0–39). All inserted markers were resected during VATS without any complications. The pathological margin was negative in 158 of the 161 lesions (98.1%), whereas in three cases it was positive (1.9%). Lobectomy was performed in one case, and two cases are being followed carefully. Thus, the surgical success rate was 98.1%. Their pathological diagnosis was as follows: primary lung cancer in 87 (54.0%), metastatic lung cancer in 46 (28.6%), MALT lymphoma in 1, and benign lesion in 27. Complications were as follows: alveolar haemorrhage in 66 (41.6%), pneumothorax with no drainage tube insertion in 61 (37.9%), haemoptysis in 1 (0.6%), and air embolism in 1 (0.6%). There was no haemothorax, dissemination of the punctured route or procedure-related deaths. No patients developed any new symptoms between the end of marker placement and the start of the VATS, except for one air embolism case. In one case of air embolism, difficulty in movement and numbness in the left arm developed after marking, and a small amount of air was confirmed to exist in the heart at CT after the procedure (Fig. 3). She was referred to a neurologist promptly, and was instructed to have complete bed rest and oxygen inhalation. The patient’s symptoms had disappeared when she returned to the hospital room. The air in the heart had completely disappeared on CT performed in the afternoon of the same day. VATS was performed successfully 5 days after marking. © 2014 The Royal Australian and New Zealand College of Radiologists
Fig. 2. A 61-year-old woman presenting with a pulmonary nodule in the left upper lobe. (a) CT showed a solid lesion, and the needle of the hookwire marker was inserted near the nodule in the supine position under CT fluoroscopy guidance. (b) CT showed successful placement of the hookwire marker near the lesion.
Discussion VATS for pulmonary lesions has been performed widely. VATS can significantly reduce postoperative pain, preserves respiratory function, is less invasive to the thoracic wall and maintains a better quality of life.6,7 However, it is difficult to perform for small subpleural pulmonary lesions. Yoshida et al.8 reported that 85–92% of pulmonary lesions were neither visible nor palpable during thoracoscopic resection. Furthermore, Suzuki et al.9 reported that failure to visualise or palpate the nodule was observed in 54% of patients, requiring conversion from VATS to thoracotomy for successful resection. Therefore, preoperative marker placement is important, and various methods have been reported using a hookwire, a spiral wire, a platinum microcoil, methylene blue, technetium-99m macroaggregated albumin, lipiodol or ultrasound.8,10–20 Vandoni et al.15 659
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Fig. 3. A 29-year-old woman presenting with a pulmonary nodule in the left lower lobe. (a) CT showed a solid lesion, and the needle of hookwire marker was inserted near the nodule in the prone position under CT guidance. (b) CT showed air in her heart (white arrow).
described the use of methylene blue injections and reported a high success rate (92.6%), but they recommended that the time between labelling and operation should be kept within a maximum of 3 h because the coloured substances frequently spread into the surrounding normal tissues. Santambrogio et al.20 reported that localisation using thoracoscopic ultrasound was noninvasive, with a high success rate (100%) in their 18 cases, but it had some limitations, requiring a great deal of experience and a special flexible probe. Also, it is limited by the presence of air in the lung when complete lung collapse is not feasible. Injection of radionuclides also achieved a high success rate (96–100%)17,18; nevertheless, it seems to have most of the same problems as thoracoscopic ultrasound and methylene blue injection. These include the need for a special flexible probe during thoracoscopic surgery and no opportunity to inject again if a technical mistake occurs. Gonfiotti et al.18 experienced contamination of the pleural cavity with a contrast 660
medium, including radionuclides due to a technical mistake during CT-guided injection. They missed the localisation of the lesion and also finger palpation was unable to localise the lesion. The lipiodol marking procedure showed a high success rate (100%), but a C-arm-shaped fluoroscopic unit is required to detect the infused lipiodol.19 Short hookwire marking also has a high success rate (93.6–97.6%).10,11 Dendo et al.11 mentioned that the design with a short hookwire and long suture is an advantage of this system. Because the flexible suture protrudes from the skin, patients do not complain of pleural pain associated with breathing. In addition, there is reliability in that an operator does not need to not push or pull the hookwire embedded in the lung. It is possible to move the patient to an operating table or stretcher without special care. Some minor complications, such as pneumothorax, pulmonary haemorrhage and haemothorax, may occur by insertion of the needle into the lung, but this is not specific to hookwire placement. Thus, we think that hookwire placement is the most appropriate procedure. It was reported that asymptomatic pneumothorax was observed in 7.5–49% of cases, pulmonary bleeding in 14.9–29.8%, haemorrhage into the pleural cavity in 0.6– 3.5% and dislodgment of the marker in 1.8–7.5%.10–12 In our study, the results were almost the same: pneumothorax in 37.9%, pulmonary haemorrhage in 41.6% and dislodgment of the marker in 2.5%. Although relatively rare, systemic air embolism is an important serious complication during hookwire placement. Fortunately, in our case the patient’s neurological impairment was transient, with no permanent sequelae. In the English literature, five cases of air embolism during hookwire marking have been reported since 200221–25 (Table 1). However, all of these are described as case reports, so its incidence is unknown. On the other hand, the incidence of air embolism during transthoracic needle biopsy, which is a similar procedure to hookwire placement, has been estimated to be 0.02– 0.07%.26–28 Three cases of air embolism have been reported among about 20 000 shipments of a marker system, so the incidence is estimated to be about 0.015%.29 However, all cases of air embolism might not necessarily have been detected and reported to the manufacturer. Also, all of the shipped markers might not necessarily have been used. Therefore, the actual incidence of air embolism may be higher. Thus, we think that the 0.6% (1/161) rate of air embolism in our study might be a reasonable rate. The mechanism of air embolism during hookwire marking is the communication between the airway and pulmonary vein.20–22 In some situations, such as coughing and placement while breath-holding during inspiration, and repositioning after placement, intra-alveolar pressure is increased, and the risk of air embolism might increase. Lalli et al.30 also mentioned that an increase of airway pressure caused by © 2014 The Royal Australian and New Zealand College of Radiologists
CT-guided marking before VATS
Table 1. Air embolism complication during CT-guided pulmonary marking
Kamiyoshihara et al.21 Horan et al.22 Sakiyama et al.23 Sato et al.24 Iguchi et al.25 Our study
Age
Sex
Location
Size (mm)
Needle
Position
Cardiac symptoms
Neurological symptoms
Outcome
24 32 79 59 75 27
F M F M M F
RLL LLL RLL RLL RUL RLL
4 10 15 7 6 13
22G 20G 21G 21G 21G 21G
Left lateral Right lateral Left semilateral Prone Supine Prone
No Yes Yes Yes Yes No
Yes No No Yes No Yes
Alive Alive Died Alive Alive Alive
RLL, right lower lobe; LLL, left lower lobe; RUL, right upper lobe.
a cough, the Valsalva manoeuvre or positive pressure ventilation increases the risk of air embolism. Considering such mechanisms, placement with breath-holding under submaximal inspiration, slow repositioning after placement and medication for cough prevention may be effective to prevent air embolism. In addition, in five of six cases including our case, air embolism occurred when the hookwire was placed in lower lobe lesions. Freund et al.31 identified risk factors for the occurrence of systemic air embolism resulting from the biopsy technique. In their study, location of the lesion in the lower lobe was one of the risk factors for systemic air embolism. We speculate that air embolism during hookwire marking might more likely occur in the lower lobe, similar to biopsy situations, because there is no difference between the two techniques to puncture the lung. Moreover, we speculate that the lower lobe shows greater movement during breathing than the upper lobe, and makes puncture difficult. If the hookwire is placed in the lower lobe, it is necessary to make the patient breathe shallowly and to carefully check the symptoms and condition of the patient. Furthermore, we believe that whole-lung CT after hookwire marking is important and should be performed not only to confirm the hookwire position, but also to confirm the absence of pneumothorax, haemorrhage and especially air embolism. The median distance between the marker and the lesion was 7.4 mm (range 0–39) in our study. The marker should be placed as close to the lesion as possible, to readily perform VATS procedure. Considering our results, the desirable distance between the marker and a lesion might be less than 8 mm. However, in deciding the access route and site of marker placement, it is necessary to consider the lung conditions such as emphysema, the vasculature in the lung and chest wall, and the position of the patients to avoid complications. In conclusion, CT-guided hookwire marking yielded high technical and clinical success rates. As VATS has become widespread, VATS for small lesions which are neither visible nor palpable will increase. Therefore, preoperative marking for those pulmonary lesions will become more important. We believe that reliable CT-guided hookwire marking can remove as small a volume of lung tissue as possible and minimise post© 2014 The Royal Australian and New Zealand College of Radiologists
operative morbidity. However, it might, although rarely, cause severe complications such as air embolism.
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