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Combined Pulmonary Artery and Bronchial Sleeve Resection

      The basic technique and the principles of bronchial and pulmonary artery (PA) reconstruction were established in the late 1940s and early 1950s.
      • Prince-Thomas C.
      Conservative resection of the bronchial tree.
      • Johnson J.B.
      • Jones P.H.
      The treatment of bronchial carcinoma by lobectomy and sleeve resection of the main bronchus.
      • Kittle F.C.
      Atypical resections of the lung: brochoplasties, sleeve resections and segmentectomies; their evolution and present status.
      Only recently, however, has interest in these techniques grown with the publication of extensive reports on technical variations, pitfalls, and complications.
      • Rendina E.A.
      • Venuta F.
      • De Giacomo T.
      • et al.
      Parenchymal sparing operations for bronchogenic carcinoma.
      • Venuta F.
      • Ciccone A.M.
      Reconstruction of the pulmonary artery.
      After 40 years of alternating enthusiasm and doubt, these procedures remain technically demanding; however, they now have a definite role in the management of lung cancer. We can now achieve complete resection while preserving viable functioning lung parenchyma and respecting the principles of surgical oncology.
      A sleeve resection for lung cancer is indicated in the case of a tumor arising at the origin of a lobar bronchus, a situation that precludes simple lobectomy but does not require pneumonectomy. The bulk of the tumor or the satellite lymph nodes may invade the PA, requiring reconstruction of the vessel. The artery can be involved to various degrees, from partial infiltration to a more extensive and even circumferential involvement. In the former case, a simple tangential resection with direct suture is indicated
      • Shrager J.B.
      • Lambright E.S.
      • McGrath C.M.
      • et al.
      Lobectomy with tangential pulmonary artery reconstruction without regard to pulmonary function.
      ; however, this procedure should not be considered as vascular reconstruction but rather as a simple variation of standard lobectomy. Extensive defects in the arterial wall usually require patch reconstruction, end-to-end anastomosis, or interposition of a prosthetic conduit. Invasion of the main PA requires proximal reconstruction with the use of cardiopulmonary bypass.
      • Rendina E.A.
      • De Giacomo T.
      • Venuta F.
      • et al.
      Sleeve resection and prosthetic reconstruction of the pulmonary artery for lung cancer.
      A sleeve lobectomy avoids pneumonectomy and preserves lung function, with no effect on oncologic results. This issue has been fully debated: recent studies demonstrate not only that functional performance, associated morbidity, and quality-of-life outcomes are superior but also that the oncologic outcome with sleeve lobectomy is equivalent to that with pneumonectomy.
      • Okada M.
      • Yamagashi H.
      • Stake S.
      • et al.
      Survival related to lymph node involvement in lung cancer after sleeve lobectomy compared with pneumonectomy.
      • Suen H.C.
      • Meyers B.F.
      • Gutrie T.
      • et al.
      Favourable results after sleeve lobectomy or bronchoplasty for bronchial malignancies.
      • Yoshino I.
      • Yokoyama H.
      • Yano T.
      • et al.
      Comparison of the surgical results of lobectomy with bronchoplasty and pneumonectomy for lung cancer.
      These findings support the conclusion that sleeve resection should be performed whenever anatomically feasible, regardless of the cardiopulmonary status of the patient. Most of the oncologic debate concerns N1 disease; the argument in favor of a more extended resection is that tumor cells may progress along the bronchial tree through the lymphatic network. However, evidence shows that N1 disease does not mandate pneumonectomy as an alternative to sleeve resection just as hilar nodal involvement does not require pneumonectomy when simple lobectomy is feasible.
      • Okada M.
      • Yamagashi H.
      • Stake S.
      • et al.
      Survival related to lymph node involvement in lung cancer after sleeve lobectomy compared with pneumonectomy.
      • Ferguson M.K.
      • Karrison T.
      Does pneumonectomy for lung cancer adversely influence long term survival?.
      • Van Schil P.E.
      • Vankeirsbilck J.
      • Brutel de la Riviere A.
      • et al.
      Long term survival after bronchial sleeve resection: univariate and multivariate analysis.
      This concept has also been extended to the segmental bronchus, and atypical bronchoplasty at this level, although less common, has been described extensively.
      • Tsubota N.
      Bronchoplasty at the level of the segmental bronchus.
      They can be performed especially in pathologic conditions other than lung cancer, including low-grade malignant tumors, metastatic lesions, and strictures caused by tuberculosis.
      • Hsu H.S.
      • Hsu W.H.
      • Huang B.S.
      • et al.
      Surgical treatment of endobronchial tuberculosis.
      Advantages include less tension on the distal stump, more efficient blood supply to the airway, and placement of the anastomosis inside the lung parenchyma, such that the pull is outside the suture line with its negative pressure. In these cases, the fissure should not be entered. The intersegmentary plane should be isolated as for a standard segmentectomy, and the bronchus should be reimplanted with the anastomotic technique previously described. Development of bare surface of the lung after isolating the segment to be removed rarely causes problems during the postoperative course.
      • Tsubota N.
      Bronchoplasty at the level of the segmental bronchus.
      After induction therapy, the bronchus and PA can be infiltrated not only by residual tumor but also by desmoplastic reaction, scarring tissue, or fibrosis; bronchovascular reconstruction can also be performed safely in this subset of patients.
      • Rendina E.A.
      • Venuta F.
      • De Giacomo T.
      • et al.
      Safety and efficacy of bronchovascular reconstruction after induction chemotherapy.
      Preoperative evaluation and screening always include computed tomographic (CT) scans and fiberoptic bronchoscopy. The infiltration of the origin of a lobar bronchus can be easily ascertained by these two exams. It may, however, be difficult to establish preoperatively an indication for PA reconstruction. Angiographic, CT, and magnetic resonance imaging scans may contribute to the assessment of the extent of infiltration, but the decision is usually made intraoperatively.

      Operative Technique

      Bronchial Sleeve Resection

      Most bronchial sleeve resections can be planned preoperatively. An intercostal pedicle flap should be prepared before opening the chest; we routinely use this flap to wrap the anastomosis: it favors protection and revascularization and separates the bronchial from the arterial side when a combined bronchovascular reconstruction is performed, avoiding broncho-arterial fistulas
      • Rendina E.A.
      • Venuta F.
      • De Giacomo T.
      • et al.
      Intercostal pedicle flap in tracheobronchial surgery.
      • Rendina E.A.
      • Venuta F.
      • Ricci P.
      • et al.
      Protection and revascularization of bronchial anastomosis by the intercostal pedicle flap.
      ; a small dehiscence can be “contained” by the wrap. Alternatively, the anastomosis can be encircled by thymic or mediastinal tissue.
      Figure thumbnail gr1
      Figure 1Most of the bronchial sleeve resections are performed by removing the right and left upper lobes along with a sleeve of main bronchus. Frozen sections should always be performed to confirm complete resection. Radical hilar and mediastinal lymphadenectomy may be easily performed after the lobe has been removed and the bronchial stumps lie open in the operative field. (Reprinted with permission from Ashiku and DeCamp.
      • Ashiku S.
      • DeCamp Jr, M.M.
      Parencymal-sparing procedures in lung cancer: sleeve resection of the lung for proximal lesions.
      )
      Figure thumbnail gr2
      Figure 2Bronchial end-to-end anastomosis (right upper sleeve lobectomy). The bronchial anastomosis is performed with interrupted polydioxanone (PDS) 4-0 sutures. (A) The first two sutures are placed outside the mucosal layer of the far end of the cartilaginous ring and tied extraluminally by the operator and the first assistant. (B) Interrupted sutures are placed on the remaining cartilaginous ring and the membranous portion and are left untied. The stitches are usually placed submucosally on the cartilaginous portion. Placing the sutures in this order helps prevent caliber discrepancies and torsion of the anastomosis. (C) The sutures are tied starting from the mediastinal side where the first stitches were closed. The anastomosis should be tension-free; this is done by dividing the pulmonary ligament. On the right side, the pericardium can be incised around the inferior pulmonary vein to help upward mobilization of the lobe. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      • De Giacomo T.
      • et al.
      Parenchymal sparing operations for bronchogenic carcinoma.
      )
      Figure thumbnail gr3
      Figure 3Y-sleeve resection on the right side: this type of reconstruction is required when a tumor arising in the intermediate bronchus involves the spur with the upper lobe bronchus. The middle and lower bronchi are removed along with the intermediate bronchus; the bronchus for the upper lobe is reimplanted with an end-to-end anastomosis. A few technical details should be kept in mind in the case of Y-sleeve resection with reimplantation of the upper lobe bronchus. This bronchus is usually short and minute, especially on the right side; the PA and lung parenchyma are extremely close to the bronchus, worsening the exposure on the mediastinal side of the anastomosis. Size discrepancies with the right main bronchus are not rare and in extreme cases the smaller side can be intussuscepted. However, more often, the larger bronchial stump works as a stent, increasing the caliber of the anastomosis and helping to keep the distal part open. This type of resection and reconstruction can obviously be performed also on the left side with the same technical details. (Reprinted with permission from Ashiku and DeCamp.
      • Ashiku S.
      • DeCamp Jr, M.M.
      Parencymal-sparing procedures in lung cancer: sleeve resection of the lung for proximal lesions.
      )

      Pulmonary Artery Reconstruction

      Figure thumbnail gr4
      Figure 4Full circumference infiltration of the pulmonary artery requiring sleeve resection. (A) Surgical anatomy of the left interlobar artery from a posterolateral view. (B) A schematic drawing of the infiltrated pulmonary artery from a lateral view. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )
      Figure thumbnail gr5
      Figure 5Infiltration of the pulmonary artery by a left lower lobe tumor. The tumor involves the distal pulmonary artery before its lower lobe branching; the lingular artery is free of disease. The defect can be repaired with a patch of autologous pericardium or polytetrafluoroethylene (PTFE). The main pulmonary artery is usually clamped after administration of 5000 U heparin. The pulmonary vein of the residual lobe is usually clamped to avoid back bleeding. Heparin is not reversed at the end of the operation. No heparin is administered during the postoperative course but the standard antithrombotic protocol is employed. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )
      The techniques of pulmonary artery reconstruction include different options, as follows:
      • Patch reconstruction after partial resection
      • Sleeve resection with end-to-end-anastomosis
      • Sleeve resection followed by reconstruction with a prosthetic conduit
      • Reconstruction of the main PA at its origin under cardiopulmonary bypass

      Partial Resection and Patch Reconstruction

      Figure thumbnail gr6
      Figure 6Partial tumor infiltration of the right pulmonary artery requiring patch reconstruction of the vessel. It is usually indicated to repair the vessel in a variety of circumstances from limited infiltration on the convex side of the artery to larger longitudinal defects. The wall of the vessel on the opposite side should be free of tumor. It can be associated with a standard lobectomy or a lobectomy with a sleeve resection of the bronchus. (A) The right upper lobe tumor partially infiltrates the artery. (B) After the resection, the defect can be reconstructed by a patch. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )
      Figure thumbnail gr7
      Figure 7Left upper lobectomy: patch reconstruction of the pulmonary artery. (A) After upper lobectomy and partial resection of the pulmonary artery, an oval defect ensues, caused by the tension applied to the vessel by the lower lobe. (B) The patch is held in place by two stay sutures. Some degree of tension on the patch is desirable at this stage; it shows that the patch is not too long. Tension will disappear after declamping. (C) The lower stay suture is not tied but simply keeps the patch in the correct place. (D) Completed patch reconstruction of the pulmonary artery. The pericardial defect is left open. The closed stump of the lingular artery can also be seen. The size and shape of the patch should be tailored to the resected portion of the vessel. Our choice for reconstruction is autologous pericardium
      • Rendina E.A.
      • De Giacomo T.
      • Venuta F.
      • et al.
      Sleeve resection and prosthetic reconstruction of the pulmonary artery for lung cancer.
      • Ricci C.
      • Rendina E.A.
      • Venuta F.
      • et al.
      Reconstruction of the pulmonary artery in patients with lung cancer.
      ; it is fresh, unpreserved, cost-free, and biocompatible. It is usually harvested anteriorly to the phrenic nerve; the defect is small and can be left open with no fear of cardiac herniation. After adequately trimming the patch (this can be further completed during suturing), it is sutured with a 5-0 nonabsorbable monofilament. Autologous pericardium may be fixed in dilute glutaraldehyde to let it stiffen and facilitate manipulation during the reconstruction phase. Bovine pericardium may also be used; this material helps overcome pitfalls related to harvesting and trimming and shows even and stiff edges; however, it is more expensive than the autologous material. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )

      End-to-End Anastomosis After Sleeve Resection

      Figure thumbnail gr8
      Figure 8Sleeve resection of the artery is usually required when the circumference of the vessel is extensively invaded; it is required also when vascular and bronchial reconstructions are performed simultaneously, with a marked shortening of the bronchial axis. (A) The right upper lobe tumor involves the pulmonary artery. (B) After the resection the ensuing defect can be reconstructed by end-to-end anastomosis after bronchial reconstruction. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )
      Figure thumbnail gr9
      Figure 9Sleeve resection of the pulmonary artery with end-to-end anastomosis. (A) The involved arterial segment has been removed along with the lobe. (B) Avoiding irregular and uneven edges of the transacted pulmonary artery facilitates proper placement of the stitches. (C) The anastomosis is completed; caliber discrepancy is compensated by the elasticity of the wall of the vessel. Sectioning the vessel improves exposure of the bronchial side. In this situation, the vascular anastomosis should be completed after performing the bronchial reconstruction. It is accomplished with a 5-0 or 6-0 nonabsorbable monofilament. Caliber discrepancy between the two sides of the anastomosis is never a problem and matching is greatly helped by the elasticity of the vessel. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )

      Reconstruction by a Prosthetic Conduit

      Figure thumbnail gr10
      Figure 10Sleeve resection and reconstruction by a prosthetic conduit. This reconstruction is performed in the very unusual case of extended defects in which end-to-end anastomosis is not feasible. It can be used when a left upper lobe tumor extensively infiltrates the PA and the lobar bronchus is not involved, keeping the vascular edges far away after a bronchial sleeve resection. (A) The long bronchial segment separates the two pulmonary artery stumps, so that end-to-end anastomosis is not feasible. (B) The proximal anastomosis between the pulmonary artery and the conduit is performed first. (C) The distal anastomosis is performed last, overlapping the suture margins to create tension, which will be relieved by declamping. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )
      Figure thumbnail gr11
      Figure 11The autologous pericardial tube is trimmed and sewed over a syringe or a 28-F chest drain.
      • Rendina E.A.
      • Venuta F.
      • de Giacomo T.
      • et al.
      Reconstruction of the pulmonary artery by a conduit of autologous pericardium.
      The size and length of the tube should be tailored for the resected vascular segment. The use of PTFE has also been reported.
      • Solli P.
      • Spaggiari L.
      • Grazia F.
      • et al.
      Double prosthetic replacement of pulmonary artery and superior vena cava and sleeve lobectomy for lung cancer.

      Reconstruction of the Main Pulmonary Artery via Cardiopulmonary Bypass

      Figure thumbnail gr12
      Figure 12Resection and reconstruction of the main pulmonary artery via cardiopulmonary bypass. This is a complex reconstruction associated with left pneumonectomy; it is required when the origin of the left PA is invaded by hilar tumors. It is performed via median sternotomy with the use of cardiopulmonary bypass. The right PA is temporarily clamped between the ascending aorta and superior vena cava. (A) The tumor infiltrates the left and main pulmonary artery. Cardiopulmonary bypass is instituted and the main pulmonary artery is clamped. (B) After left pneumonectomy and en bloc resection of the main pulmonary artery, the defect is reconstructed by a patch of autologous pericardium or PTFE. During this procedure, the left recurrent nerve may be injured. (Reprinted with permission from Rendina et al.
      • Rendina E.A.
      • Venuta F.
      Pulmonary artery reconstruction.
      )

      Results

      The recent international literature reports results with sleeve resection of the bronchus and reconstruction of the PA with a favorable outcome in terms of reduced complications and mortality, preserved cardiopulmonary function, and survival rates; this strongly supports the use of these procedures compared with pneumonectomy.
      • Van Schil P.E.
      • Vankeirsbilck J.
      • Brutel de la Riviere A.
      • et al.
      Long term survival after bronchial sleeve resection: univariate and multivariate analysis.
      • Tedder M.
      • Anstadt M.P.
      • Tedder S.T.
      • et al.
      Current morbidity, mortality and survival after bronchoplastic procedures for malignancies.
      • Tronc F.
      • Gregoire J.
      • Rouleau J.
      • et al.
      Long term results of sleeve lobectomy for lung cancer.
      When the main bronchus is partially or completely obstructed by the abutting tumor, preoperative laser recanalization may be helpful. It contributes to improved morphological and functional evaluation of the distal airway and lung parenchyma, helps to prevent infectious complications during induction chemotherapy, does not affect the adjacent mucosa, and does not increase postoperative complications.
      • Venuta F.
      • Rendina E.A.
      • de Giacomo T.
      • et al.
      Nd:YAG laser resection of lung cancer invading the airway as a bridge to surgery and palliative treatment.
      Protection of the bronchial anastomosis is still a subject of debate
      • Rendina E.A.
      • Venuta F.
      • De Giacomo T.
      • et al.
      Parenchymal sparing operations for bronchogenic carcinoma.
      • Rendina E.A.
      • Venuta F.
      • De Giacomo T.
      • et al.
      Safety and efficacy of bronchovascular reconstruction after induction chemotherapy.
      • Kutlu C.A.
      • Goldstraw P.
      Tracheobronchial sleeve resection with the use of a continuous anastomosis: results of one hundred consecutive cases.
      ; we strongly encourage the protection of the bronchial anastomosis, especially when PA reconstruction is involved.
      Specific vascular complications include thrombosis and leakage and are observed in fewer than 5% of cases. Bronchoarterial fistula may occur with bronchial and vascular reconstruction, but the interposition of the intercostal muscle between the two structures helps prevent it.
      • Rendina E.A.
      • Venuta F.
      • De Giacomo T.
      • et al.
      Safety and efficacy of bronchovascular reconstruction after induction chemotherapy.
      Kinking and rotation of the axis may occur after lung re-expansion; anastomotic stricture is extremely rare.
      Results of vascular reconstruction should be evaluated in terms of patency of the vessel, function of the right compartments of the heart, and rates of survival. Patency problems are observed in fewer than 2% of cases.
      • Venuta F.
      • Ciccone A.M.
      Reconstruction of the pulmonary artery.
      In such cases, CT is a versatile diagnostic tool; magnetic resonance provides improved imaging for diagnosing this complication during the immediate postoperative period. These noninvasive techniques have completely replaced standard angiography.
      In terms of heart function, lobectomy associated with PA reconstruction behaves like standard lobectomy.
      • Rendina E.A.
      • De Giacomo T.
      • Venuta F.
      • et al.
      Sleeve resection and prosthetic reconstruction of the pulmonary artery for lung cancer.
      • Lausberg H.F.
      • Grater T.P.
      • Tscholl D.
      • et al.
      Bronchovascular versus bronchial sleeve resection for central lung tumors.
      • Deslauriers J.
      • Gaulin P.
      • Beaulieu M.
      • et al.
      Long term clinical and functional results of sleeve lobectomy for primary lung cancer.
      In the absence of complications like kinking or thrombosis, right ventricle morphology and function and PA pressure are equally related to standard lobectomy. The advantages of sleeve resection over pneumonectomy in the presence of a well-perfused residual lung have been extensively described.
      From the oncologic point of view, comparison between the different series is difficult because of the differences in size of the groups, demographics, selection criteria, and length of follow-up. It was recently reported that survival after lobectomy associated with PA reconstruction is comparable, stage by stage, to that reported in the major reviews on lung cancer surgery and sleeve resection.
      • Shrager J.B.
      • Lambright E.S.
      • McGrath C.M.
      • et al.
      Lobectomy with tangential pulmonary artery reconstruction without regard to pulmonary function.
      • Rendina E.A.
      • De Giacomo T.
      • Venuta F.
      • et al.
      Sleeve resection and prosthetic reconstruction of the pulmonary artery for lung cancer.
      • Okada M.
      • Yamagashi H.
      • Stake S.
      • et al.
      Survival related to lymph node involvement in lung cancer after sleeve lobectomy compared with pneumonectomy.
      • Lausberg H.F.
      • Grater T.P.
      • Tscholl D.
      • et al.
      Bronchovascular versus bronchial sleeve resection for central lung tumors.
      • Lausberg H.F.
      • Graeter T.P.
      • Wendler O.
      • et al.
      Bronchial and bronchovascular sleeve resection for treatment of central lung tumors.
      • Chunwei F.
      • Weiji W.
      • Xinguan Z.
      • et al.
      Evaluation of bronchoplasty and pulmonary artery reconstruction for bronchogenic carcinoma.
      • Nagayasu T.
      • Matsumoto T.
      • Tagawa T.
      • et al.
      Factors affecting survival after bronchoplasty and broncho-angioplasty for lung cancer: single institutional review of 147 patients.
      • Icard P.
      • Regnard J.F.
      • Guibert L.
      • et al.
      Survival and prognostic factors in patients undergoing parenchymal saving bronchoplastic operations for primary lung cancer: a series of 110 consecutive cases.
      • Fadel E.
      • Yildizeli B.
      • Chapelier A.R.
      • et al.
      Sleeve lobectomy for bronchogenic cancers: factors affecting survival.
      The impact of the nodal status on survival is also comparable with that reported for bronchial sleeve and standard resection. When N1 and N2 are involved, PA reconstruction can safely be performed when anatomically required, although some surgeons still advocate pneumonectomy. No statistically significant difference has been observed between PA reconstruction alone or PA reconstruction combined with bronchial sleeve resection. This finding strongly suggests that these complex lung-sparing procedures can be performed with curative intent as long as complete resection is obtained.
      In conclusion, morbidity, mortality, functional results, and long-term survival rates support parenchyma-sparing operations not only as a viable option in the treatment of lung cancer invading the airway and the PA but as the gold standard.

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        Conservative resection of the bronchial tree.
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        Current morbidity, mortality and survival after bronchoplastic procedures for malignancies.
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        Long term results of sleeve lobectomy for lung cancer.
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        Nd:YAG laser resection of lung cancer invading the airway as a bridge to surgery and palliative treatment.
        Ann Thorac Surg. 2002; 74: 995-998
        • Kutlu C.A.
        • Goldstraw P.
        Tracheobronchial sleeve resection with the use of a continuous anastomosis: results of one hundred consecutive cases.
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        • Lausberg H.F.
        • Grater T.P.
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        Bronchovascular versus bronchial sleeve resection for central lung tumors.
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        Long term clinical and functional results of sleeve lobectomy for primary lung cancer.
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        Bronchial and bronchovascular sleeve resection for treatment of central lung tumors.
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        Evaluation of bronchoplasty and pulmonary artery reconstruction for bronchogenic carcinoma.
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