Temporary Pulmonary Stent Placement as Emergency Treatment of Pulmonary Embolism First Experimental Evaluation
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1 Journal of the American College of Cardiology Vol. 48, No. 4, by the American College of Cardiology Foundation ISSN /06/$32.00 Published by Elsevier Inc. doi: /j.jacc PRECLINICAL STUDIES as Emergency Treatment of Pulmonary Embolism First Experimental Evaluation Thomas Schmitz-Rode, MD,* Rajeev Verma, MD, Joachim G. Pfeffer,* Ralf-Dieter Hilgers, PHD, Rolf W. Günther, MD Aachen, Germany OBJECTIVES BACKGROUND METHODS RESULTS CONCLUSIONS We aimed to evaluate the performance of a newly designed temporary stent device as a percutaneous emergency treatment of pulmonary embolism. If thrombolysis is contraindicated or recanalization by thrombolysis delayed in patients with severe pulmonary embolism who are threatened by acute circulatory failure, percutaneous temporary pulmonary stent placement may represent an additional option before surgical embolectomy is considered. The newly designed temporary pulmonary stent is made from woven Nitinol and has a distal blunt end and a proximal crimped end, which is firmly fixed to a inch guidewire. It is delivered through a 9.5-F polytetrafluoroethylene sheath using a pusher tube. Stent placement and removal were examined in 9 anesthetized sheep with experimentally induced pulmonary embolism. Hemodynamic parameters were recorded in 7 animals. Delivery and removal of the stent was uneventful and rapidly accomplished. Stent placement was associated with a significant decrease in Miller angiographic index (from to ; p ), heart rate (from beats/min to beats/min; p ), and mean pulmonary artery pressure (from mm Hg to mm Hg; p ) and a significant increase in mean aortic pressure (from mm Hg to 61 8 mm Hg; p ). Autopsy revealed neither wall damage nor parenchymal hemorrhage. Our preliminary study proves the technical feasibility of temporary placement and removal of a newly designed dedicated pulmonary stent to recanalize centrally located embolic occlusions in severe pulmonary embolism. Animal experimental evaluation revealed rapid and significant circulatory improvement after stent placement. (J Am Coll Cardiol 2006;48:812 6) 2006 by the American College of Cardiology Foundation The mainstay of treatment in severe pulmonary embolism (PE) is systemic thrombolytic therapy and, if thrombolysis is foreseen to fail, surgical embolectomy (1,2). Catheterdirected techniques, such as embolus fragmentation or aspiration, are not widely established (3,4). Our study introduces a new percutaneous mode of therapy that may serve as an additional option before resorting to surgical embolectomy. We present the first animal experimental evaluation of a percutaneous temporary stent implantation into the obstructed central pulmonary artery as a short-term treatment that is intended to bridge to circulatory stabilization. The removable stent is expanded alongside the main pulmonary embolus to create a patent channel to provide for reperfusion of the dependent periphery and immediate relief of right ventricular afterload. From the *Department of Applied Medical Engineering, Helmholtz Institute, Department of Diagnostic Radiology, and the Institute for Medical Statistics, RWTH Aachen University and University Hospital, Aachen, Germany. Supported by the Aachen Center of Competence in Medical Technology (AKM) and the German Federal Ministry of Education and Research (BMBF). Manuscript received December 14, 2005; revised manuscript received April 6, 2006, accepted April 18, METHODS Temporary pulmonary stent device. The pulmonary stent (custom-made, Helmholtz Institute, Aachen, Germany) consists of woven, self-expanding, shape-memory alloy wire (Nitinol; Euroflex, Pforzheim, Germany) with a maximum expanded diameter of 20 mm and a length of 100 mm (Fig. 1). Its distal open end features wire U-bends and thus a smooth crown-like edge. The proximal crimped end is firmly fixed to a inch highly flexible hydrophilically coated guidewire (Radifocus; Terumo, Tokyo, Japan). The stent device is delivered through a pre-placed 9.5-F custom-made polytetrafluoroethylene (PTFE) sheath (Helmholtz Institute), using a 6.5-F custom-made PTFE pusher tube (Helmholtz Institute). The stent is deployed under fluoroscopic control by holding the pusher tube and withdrawing the sheath. After placement, both sheath and pusher tube are removed, leaving the stent with the attached floppy guidewire in place. For stent removal, the wire serves as a guide axis, over which the 9.5-F sheath is re-advanced. The stent is removed by withdrawal into the sheath. Pulmonary embolism animal model. The pulmonary stent device was examined in 9 anesthetized sheep (body weight 70 to 80 kg) with experimentally induced PE (5,6). Pre-
2 JACC Vol. 48, No. 4, 2006 August 15, 2006:812 6 Schmitz-Rode et al. 813 Abbreviations and Acronyms AP aortic pressure CVP central venous pressure PAP pulmonary artery pressure PCWP pulmonary capillary wedge pressure PE pulmonary embolism PTFE polytetrafluoroethylene formed thrombi (mean weight g) were made from porcine blood, which was stored at 4 C for 10 days to increase thrombus consistency. One thrombus per animal was introduced through a 32-F jugular sheath and released at the sheath tip into the right atrium. The thrombus was directed by perfusion through the right ventricle into the pulmonary arterial system without disintegration, causing a centrally located embolic occlusion of one of the main arteries. Pulmonary angiography before and after embolus injection was performed via right femoral venous access, using a standard pulmonary 7-F pigtail catheter (Grollman; Merit Medical, South Jordan, Utah) and by producing angiograms in 3 standard projections. The 9.5-F stent delivery sheath was placed in the occluded pulmonary artery. The wire-mounted stent was pushed with its proximal edge up to the tip of the delivery sheath using the coaxial pusher tube. Deployment of the stent was observed under fluoroscopy. Final angiograms documented the extent of recanalization. After the procedure the stent was removed. In all 9 animals the angiographic index was determined after embolus injection and pulmonary stent placement. In the last 7 animals, the following hemodynamic parameters were recorded before and after embolus injection and after stent placement: heart rate, mean pulmonary artery pressure (PAP), mean aortic pressure (AP), arterial oxygen saturation, central venous pressure (CVP), and pulmonary capillary wedge pressure (PCWP). Autopsy. At the completion of the trial, all subjects were killed. After en bloc resection of heart and lungs, all cardiac structures, particularly the right atrium, tricuspid valve, right ventricle, and pulmonic valve, were inspected macroscopically for wall damage such as perforation or hemorrhage. Main and lobar pulmonary arteries were evaluated in the same way, with emphasis on the treated area. Statistics. Heart rate (beats/min), mean PAP (mm Hg), mean AP (mm Hg), arterial oxygen saturation (%), Miller angiographic index, CVP (mm Hg), and PCWP (mm Hg) were analyzed separately using a 1-factor repeated-measures analysis of variance (within-subjects factor: conditions baseline, embolus, and stent ) and linear contrasts for the within-subjects factor. The log-likelihood criterion was used to specify the covariance structure (unstructured, autoregressive, or compound symmetry). We used a significance level of 0.05 in this explorative evaluation. Computations were performed using the MIXED procedure of SAS version 9.0 (SAS Institute, Cary, North Carolina) under Windows XP (Microsoft, Redmond, Washington). Figure 1. Phases of deployment of a removable pulmonary stent for emergency treatment of acute massive pulmonary embolism, made from self-expanding woven shape-memory wire (maximum expanded diameter 20 mm). The attached guidewire (arrow, bottom panel) facilitates removal by withdrawal into the 9.5-F sheath. RESULTS Thrombus injection and creation of PE was successful in all animals, with embolic occlusion of a main or intermediate/ interlobar pulmonary artery. Pulmonary embolization of the injected thrombus was associated with a decrease in mean AP and arterial oxygen saturation and an increase in mean PAP, heart rate, and CVP (Table 1). Delivery and deployment of the stent was rapidly accomplished. The delivery sheath could be navigated adequately and the stent device could be quickly placed in the occluded pulmonary arteries of all 9 sheep by bridging the occluding embolus on its entire length. The average procedure time of stent placement, including positioning of the sheath, was min (range 14 to 38 min). Angiography after stent placement revealed partial recanalization, with improved flow in all treated main, intermediate, and lobar pulmonary arteries (Fig. 2). Correspondingly, the Miller
3 814 Schmitz-Rode et al. JACC Vol. 48, No. 4, 2006 August 15, 2006:812 6 Table 1. Summary of Hemodynamic Measurements in 7 Sheep and Miller Angiographic Index in 9 Sheep Parameter Baseline Embolus Stent F Value (Ndf; Ddf ) p Value Heart rate (beats/min) (n 7) (n 7) (n 7) 9.79 (2; 6) Pulmonary artery pressure (mm Hg) (n 7) (n 7) (n 7) (2; 6) Aortic pressure (mm Hg) (n 7) (n 7) (n 7) (2; 6) Central venous pressure (mm Hg) (n 7) (n 7) (n 7) 5.38 (2; 6) Arterial oxygen saturation (%) (n 7) (n 7) (n 7) 4.00 (2; 6) PCWP (mm Hg) (n 7) (n 7) (n 7) 0.03 (2; 6) Miller angiographic index (9) 0 (n 9) (n 9) (n 9) (1; 8) Values expressed as mean SD. Ddf denominator degrees of freedom; Ndf nominator degrees of freedom; PCWP pulmonary capillary wedge pressure angiographic index decreased significantly (p ) (Table 1). Heart rate (Fig. 3A) and mean PAP (Fig. 3B) increased significantly from baseline to embolus (F 1, ; p ; and F 1, ; p ) and decreased significantly from embolus to stent (F 1, ; p ; and F 1, ; p ). Mean AP (Fig. 3C) decreased from baseline to embolus (F 1, ; p ) and increased from embolus to stent (F 1, ; p ). The CVP differed slightly from baseline to embolus (F 1,6 5.03; p ) but not significantly from embolus to stent (F 1,6 1.12; p ). Although mean arterial oxygen saturation decreased and mean PCWP increased after embolus injection (and vice-versa after stent placement), these changes were not significant (Table 1). In autopsy, there was no incidence of damage to either the valves or the right ventricular and atrial endocardium in any of the 9 animals. Furthermore, there was no pulmonary parenchymal hemorrhage or hemothorax. In 2 cases, slight wall hemorrhage (once in the pulmonary trunk and once in the treated left descending pulmonary artery) was observed, which impressed macroscopically as nonprotruding dark bluish spots, less than 1 cm in diameter and without any accompanying wall tears or perforation. The 7 other cases showed no signs of damage at all. DISCUSSION Acute circulatory failure is the leading cause of death in patients with acute massive PE. Prompt reduction of right ventricular afterload is a crucial therapeutic goal to prevent a lethal course. Thrombolysis is a widely accepted and implemented standard therapy of acute massive PE (1,2). Optimized strategies in surgical pulmonary embolectomy are accompanied by a considerable reduction of mortality (7). This increases significance and acceptance of open surgery as the last resort if thrombolytic therapy is contraindicated or poor recanalization is anticipated owing to temporal constraints. There are very few alternatives to these cornerstones of therapy. Interventional catheter-based approaches include fragmentation and aspiration techniques (3,4), with the advantage of limited invasiveness. However, in severe cases with extensive PE, the degree of recanalization is limited, especially if the thrombus is partly organized. There are two reports in the literature (8,9) that describe emergent pulmonary stent placement in acute massive PE as a last choice of therapy. In both cases, patients with cor pulmonale were threatened by cardiogenic shock. Bilateral implantation of self-expanding stents created patent channels alongside the emboli and led to rapid circulatory stabilization due to instant recanalization. The principle of recanalization, the compression of the embolic occlusion material by the radial expansion force of a stent, is similar to the approach presented in our experimental study. In contrast to the cited reports, which used permanently implantable standard stents that were neither shapeoptimized to the pulmonary arteries nor removable, the present study reports the development and first experimental evaluation of a dedicated temporary pulmonary stent. Such a stent should completely bridge and recanalize the embolic occlusion, and should be rapidly insertable and removable. To avoid floating of the proximal half of the stents in the pulmonary arterial trunks (8,9), the stent should have an appropriate mesh flexibility to adapt to the transition of main and interlobar arteries. Sharp ends, as with the Wallstent (8), are considered to be risky, particularly in cases with concomitant thrombolysis, where wall penetration would be a likely cause of hemorrhage. Our dedicated stent is tulip-like, with rounded ends. It has a larger proximal end and a relatively wide mesh to support inflow. Stent placement and removal was fast and straightforward. In all cases, the stent was successfully deployed alongside the thrombus so that its upper and lower ends lay in the patent artery. However, there were some limitations to the present preliminary study. Whereas bilateral PE is very likely, a model of unilateral PE was used. Additionally, the clot model applied may not fully resemble fresh acute PE. A major limitation of the promoted recanalization technique may be a lack of efficacy in case of distal pulmonary artery occlusion by fresh thrombi. Furthermore, the stents were removed approximately 30 to 60 min after placement. For the desired clinical application in acute massive PE, the stent is intended to stay in place for hours up to days, as long as is necessary for circulatory stabilization. Conclusions. Our experimental study in 9 sheep proves a first decisive step of the concept and the technical feasibility
4 JACC Vol. 48, No. 4, 2006 August 15, 2006:812 6 Schmitz-Rode et al. 815 Figure 2. Pulmonary angiograms obtained in the frontal (A to D) and oblique (E) views in 1 sheep. (A) Normal baseline pulmonary angiogram. (B) Angiogram obtained after thrombus injection shows massive pulmonary embolism of the left main pulmonary artery with complete occlusion of the depending left pulmonary arteries (arrows). (C) Fluoroscopy image after placement of the pulmonary stent (arrows) attached to the wire. (D, E) Frontal and left anterior oblique angiograms obtained by contrast injection through the stent delivery sheath after left-sided stent deployment shows considerable recanalization and improved perfusion of the left upper and lower lobes. Residual stenosis due to compressed embolus (arrow in E).
5 816 Schmitz-Rode et al. JACC Vol. 48, No. 4, 2006 August 15, 2006:812 6 of temporary placement and removal of a newly designed dedicated pulmonary stent to recanalize centrally located embolic occlusions in severe PE. Our experimental results show that this is a very predictable, reproducible, and rapid technique that achieved significant circulatory improvement. Its possible role as an adjunctive emergency treatment option in patients with severe PE needs to be addressed in subsequent clinical trials. Reprint requests and correspondence: Prof. Dr. Thomas Schmitz-Rode, Managing Director, Helmholtz Institute Aachen, Chairman, Department of Applied Medical Engineering, RWTH Aachen University and University Hospital, Aachen, Pauwelsstrasse 20, D Aachen, Germany. smiro@hia.rwthaachen.de. REFERENCES 1. Goldhaber SZ. Pulmonary embolism. Lancet 2004;363: Task Force on Pulmonary Embolism, European Society of Cardiology. Guidelines on diagnosis and management of acute pulmonary embolism. Eur Heart J 2000;21: Uflacker R. Interventional therapy for pulmonary embolism. J Vasc Interv Radiol 2001;12: Schmitz-Rode T, Janssens U, Duda SH, Erley CM, Gunther RW. Massive pulmonary embolism: percutaneous emergency treatment by pigtail rotation catheter. J Am Coll Cardiol 2000;36: Schmitz-Rode T, Gunther RW, Pfeffer JG, Neuerburg JM, Geuting B, Biesterfeld S. Acute massive pulmonary embolism: use of a rotatable pigtail catheter for diagnosis and fragmentation therapy. Radiology 1995;197: Kucher N, Windecker S, Banz Y, Schmitz-Rode T, Mettler D, Meier B, Hess OM. Percutaneous catheter thrombectomy device for acute pulmonary embolism: in vitro and in vivo testing. Radiology 2005;236: Leacche M, Unic D, Goldhaber SZ, et al. Modern surgical treatment of massive pulmonary embolism: results in 47 consecutive patients after rapid diagnosis and aggressive surgical approach. J Thorac Cardiovasc Surg 2005;129: Haskal ZJ, Soulen MC, Huettl EA, Palevsky HI, Cope C. Lifethreatening pulmonary emboli and cor pulmonale: treatment with percutaneous pulmonary artery stent placement. Radiology 1994;191: Koizumi J, Kusano S, Akima T, et al. Emergent Z stent placement for treatment of cor pulmonale due to pulmonary emboli after failed lytic treatment: technical considerations. Cardiovasc Intervent Radiol 1998; 21: Figure 3. Graphs show (A) heart rate, (B) mean pulmonary artery pressure, and (C) mean aortic pressure at baseline, after embolus injection, and after stent placement in 7 sheep. The average of the parameters improved significantly after stent placement.
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