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Historical Perspective: Surgery for Chronic Thromboembolic Disease
Historical Perspective: Surgery for Chronic Thromboembolic Disease Stuart W. Jamieson, MB, FRCS This article provides a historical perspective for our current understanding of chronic thromboembolic pulmonary hypertension and surgery for this disease. It chronicles the developments in surgical techniques that have made pulmonary endarterectomy the procedure of choice for obstruction of pulmonary vessels by organized thromboemboli and secondary vessel wall thickening. Semin Thorac Cardiovasc Surg 18:218-222 © 2006 Elsevier Inc. All rights reserved. KEYWORDS PTE, surgical history, chronic thromboembolism
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he entity of acute pulmonary embolism was described by Laennec in 1819,1 who also recognized its relation to deep venous thrombosis. That deep venous thrombosis was related to stasis, hypercoagulability, and vessel wall injury was recognized by Virchow2 in 1846. The first to describe an operative approach for acute pulmonary embolism was Trendelenberg in 1908.3 In a moribund patient, and without anesthesia, he exposed the heart and great vessels through a vertical incision to the left of the sternum and a horizontal extension over the second rib. He passed a rubber tape beneath the aorta and pulmonary artery through the transverse sinus, and after snaring the tape, he incised the pulmonary artery, removed the clot, and closed the pulmonary arteriotomy with a clamp, all within 45 seconds. The pulmonary arteriotomy was then repaired. The patient survived the operation but died of heart failure 15 hours later, probably as a result of inadequate removal of thrombus. A second patient he described also had immediate survival but died of hemorrhage from the internal mammary artery 37 hours after operation. It was 19244 before long-term survival after acute embolectomy with complete functional recovery was described by Kirschner, and several other reports later followed. When Steenberg and coworkers5 reported the first survivor of the “Trendelenburg operation” in the United States in 1958, there had been 12 other reports of successful embolectomy in the European literature. Pulmonary embolectomy remained a very hazardous procedure, however, until a more careful Division of Cardiothoracic Surgery, University of California, San Diego, San Diego, CA. Address reprint requests to Stuart W. Jamieson MB, FRCS, Division of Cardiothoracic Surgery, University of California, San Diego, 200 West Arbor Drive, San Diego, CA 92103-8892. E-mail: [email protected].
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and thorough approach by using cardiopulmonary bypass was described by Cooley and colleagues in 19616 and Sharp in 1962.7 The use of cardiopulmonary bypass, when available, remains the standard for acute pulmonary endarterectomy, though controversy remains regarding the place of the operation. The recognition of chronic thrombotic obstruction of the pulmonary arteries came more than 100 years after that of acute pulmonary embolism. In 1928 Lungdahl8 described two women, one aged 38 and one aged 51, who had suffered for several years from dyspnea, cyanosis, and palpitations. Ultimately, both died of right heart failure, and at autopsy chronic pulmonary arterial obstruction was found. There was marked dilation of the proximal main pulmonary artery, with increased vascularity of the bronchial circulation. The fact that the lungs were free of infarction was observed. Lungdahl thought that it was likely that the obstruction was due to pulmonary emboli—a variation from the previously held concept that, in patients with cor pulmonale where occlusion of the pulmonary arteries was found, the process was one of primary thrombosis. A review of chronic thrombotic occlusion of the pulmonary arteries by Means and Mallory9 in 1931 found only 6 cases, and a new description and further review in 1934 by Kampmeier10 yielded 24 case reports. By 1956 Hollister and Cull11 found only 100 case reports published before 1941, including one group of 14 cases derived from a single study of 706 autopsies.12 Another series of 14 cases in this review came from admissions to a single 335-bed teaching hospital over a 10-year period.13 They found a comparable number of case reports from 1941 to 1955, and stated (in 1956): “it is probable that no more than 200 cases of the syndrome have been reported in the medical literature to date.”11
Surgery for chronic thromboembolic disease Fifty years ago, then, the finding of chronic thrombosis within the pulmonary arteries was still considered a reportable rarity, and there remained uncertainty as to whether this entity represented spontaneous thrombosis “in situ” (the etiology favored at the time) or embolization. It was, however, widely held that chronic thrombotic occlusion was not amenable to surgical correction.11,14-16 Houk and colleagues, in 1963,17 found approximately 250 reported cases of chronic thromboembolic obstruction of the major pulmonary arteries. In only six of these was the diagnosis established before death, and in only three was direct surgical therapy attempted. The first exploration for thrombotic occlusion of the pulmonary arteries was probably by Dr. Alfred Blalock at Johns Hopkins hospital in January 1948, in an operation described by Carroll in 1950.18 The left pulmonary artery was exposed through a thoracotomy incision and found to be small, with proximal occlusion, though aspiration with a needle produced red blood. The artery was divided and found to contain organized thrombus. Dr. Blalock thought the case to be inoperable and made no attempt to relieve the obstruction. The patient was discharged from the hospital unimproved. In 1951 Boucher and coworkers performed a pneumonectomy in a patient suspected of a pulmonary aneurysm.19 The pathology showed chronic thrombotic obstruction of the pulmonary arteries. A possible surgical approach to the condition by endarterectomy was suggested in 195611 and the first planned pulmonary endarterectomy was performed in 1957 by Hurwitt and colleagues on a patient operated on with inflow occlusion and systemic hypothermia through a transverse sternotomy. Although the period of inflow occlusion was only 2½ minutes, the patient arrested and could not be resuscitated.20 Allison and coworkers21 performed a right lower lobectomy in a 59-year-old man in June 1957 in Oxford—this patient was subsequently found to have chronic thrombotic occlusion of this lobe. Many bloody adhesions were encountered with the thoracotomy approach (an additional reason that the midline approach is better and is now the favored standard). The patient recovered, but was admitted to hospital again 3 months later with left-sided chest pain and heart failure. He died that month, and autopsy revealed massive thromboembolic obstruction of the left main pulmonary artery and adherent emboli. However, the same author performed the first successful embolectomy for recurrent emboli—again with the technique of inflow occlusion, in March 1958.21 In this operation the patient was cooled to 29°C in a waterbath, and the chest was then opened with a trans-sternal approach. An embolectomy (not a true endarterectomy) was performed using suction and forceps. However “a mass of tough thrombus was removed from the right pulmonary artery. After this, suction was effective in drawing out many lengths of softer “tailed” thrombus, the tails representing branches of the artery.” The patient survived and was improved. In July 1961 Snyder and coworkers operated on a 71-yearold man initially suspected of having a tumor, at the San
219 Diego Naval Hospital.22 A right thoracotomy was made, through the fifth intercostal space. There were upper lobe adhesions. No tumor was found, but a thickened pulmonary artery was encountered. No pulsations were palpable below the right upper lobe pulmonary artery, and a longitudinal incision was made in the pulmonary artery. A thrombotic mass was removed with endarterectomy spoons. An angiogram performed in August 1961 showed a patent pulmonary artery. Snyder made an important observation: “The findings in the present case unequivocally demonstrate that the pulmonary artery, after occlusion for a considerable number of years, continues to maintain a relatively normal relationship to the pulmonary veins at the capillary level, that the pulmonary alveolar membrane is not irreparably damaged by prolonged pulmonary artery occlusion, and that functional return of the affected lung may be expected after pulmonary endarterectomy.” Another important concept was expressed in 1963 by Houk and colleagues,17 describing a case operated on at Georgetown in November 1961. A bilateral anterior thoracotomy incision was made, and though it was not used, cardiopulmonary bypass standby was available. They referenced the success with cardiopulmonary bypass in acute embolectomy and suggested that perhaps cardiopulmonary bypass should be used electively for operation on chronic thrombotic occlusion. The progress of this patient was updated in two reports in 196523,24 and he was said to be alive and asymptomatic now more than 3 years after surgery. A further successful case, of a 42-year-old man, was now also presented.24 Operation was performed through a median sternotomy incision on May 18, 1962. Cardiopulmonary bypass was on standby. A true endarterectomy was again performed here, and a large thrombotic mass was freed by blunt dissection medially and sharp dissection distally. The patient was discharged on June 9th. Moser and colleagues reemphasized that the same technical advances that had made emergency pulmonary embolectomy and openheart surgery possible had now made pulmonary endarterectomy feasible in selected patients with massive thromboembolic pulmonary artery occlusion. He stated that “our present consensus is that bypass should be available on a standby basis in all cases and is required if extensive bilateral obstruction is to be corrected. Perhaps bypass should be used in all cases to permit more detailed exploration of the pulmonary arterial tree, but the problems associated with bypass must be balanced against the advantages of its use in each case.” The May 1962 patient, operated at Georgetown University by Dr. Charles Hufnagel,24 was probably the first with this disorder in whom the diagnosis was made before operation and successful correction achieved. The operation demonstrated that extensive well-organized thrombi, having obstructed major pulmonary vessels from months to years, could be removed successfully. Furthermore, the reclaimed lung areas were shown to be able to safely accept the sudden return of blood flow and to resume adequate respiratory function.
220 In his subsequent analysis of four operated cases,23 in addition to the above two successful cases, Moser described two in whom surgical correction could not be achieved, with the patients dying postoperatively. The first of these was operated on in April 1964. Hypotension developed during induction of anesthesia, accentuated by temporary occlusion of the right main pulmonary artery, and the procedure was abandoned. Hypotension persisted and the patient died 2 hours later. The other case was the same described in more detail by Jones and coworkers in 1965.25 This was a 37-year-old man with a previous fractured right arm and a separate injury to the right leg, who also had varicose veins. He was operated on on 1 April 1964. The chest was entered through a bilateral anterior thoracotomy with cardiopulmonary bypass standby, but without the use of bypass. Dense vascular adhesions were found diffusely between the lungs, chest wall, and pericardium throughout both hemithoraces. The right lung was freed by sharp dissection and the right main pulmonary artery was isolated. An incision was made in the right pulmonary artery and extended into the branches of the upper lobe. “These vessels were entirely patent proximally; however, at the segmental and subsegmental level they were relatively bloodless and were occluded by fibrous webs of material having a peculiar moth-eaten appearance. There was no identifiable lumen.” Similar changes were found in the lower lobe, and it was concluded that “there was no proximal block amenable to endarterectomy, and the more distal lesions were inoperable.” 7500 mL of blood were required to replace that lost during dissection of vascular adhesions on the right. The patient became hypotensive and died 24 hours later. Jones concluded “it is patently clear that we were dealing with a patient with inoperable chronic obstructive disease of the pulmonary arteries.” Frater and colleagues,26 in 1965, discussed the case of a 23-year-old farm worker operated upon on September 4, 1963. This patient presented with a pulmonary artery aneurysm originally thought to be mycotic. Subsequent angiography demonstrated pulmonary artery occlusion. A left anterolateral thoracotomy was made, with cardiopulmonary bypass standby, though bypass was not used. The pulmonary artery pressures were unchanged postoperatively, and the patient was not benefited. The first operation using cardiopulmonary bypass was probably performed by Dr. Scannell in 196427 at the Massachusetts General Hospital. The patient was a 39-year-old physician with dyspnea and chest pain. At cardiac catheterization his pulmonary artery pressures were 100/30 with a mean of 55. A bilateral anterior thoracotomy was performed. The patient had a cardiac arrest on opening the chest, and he was placed on cardiopulmonary bypass. Though this was a case of chronic thrombotic occlusion, an embolectomy was performed with forceps and by squeezing the lung. Postoperatively the patient developed severe pulmonary edema with a “high degree of residual pulmonary hypertension,” and died 2 hours after operation. Autopsy showed residual clot and fibrous bands, adherent to the intima, which “couldn’t merely be picked off.”
S.W. Jamieson Nash and coworkers28 in 1968 described a case, operated on in June 1966, where a large thrombus was removed from the left pulmonary artery using cardiopulmonary bypass. A left thoracotomy was performed at the level of the fourth rib. After cardiopulmonary bypass was established he developed a line of cleavage between the thrombus and the left pulmonary artery wall and the entire thrombus was removed. This again was a true endarterectomy with a typical cast specimen. The patient recovered fully and went back to normal activity. Subsequent arteriogram was performed showing a patent left main pulmonary artery. By the end of the 1960s then, a true appreciation of this disorder was appearing. It had become clear that a formal endarterectomy needed to be performed to remove all parts of the chronic thrombotic mass, and that for this to be done completely, cardiopulmonary bypass was required. The condition was often associated with extensive adhesions of the lung to the chest wall, and a lateral thoracotomy was often associated with extensive blood loss. Dr. Kenneth Moser, who was a pulmonary physician with an abiding interest in pulmonary hypertension from thrombotic occlusion of the pulmonary arteries, and had previously been a colleague of Dr. Hufnagel, moved from Georgetown to San Diego in the late 1960s. In 1973 he and Nina Braunwald presented the first case that was operated on at the University of California, San Diego (UCSD).29 The patient was a 67-yearold man who underwent surgery on July 14, 1970. Through a right lateral thoracotomy, a pulmonary “thromboendarterectomy” was performed using cardiopulmonary bypass. The thrombus was removed with forceps and embolectomy spoons. In addition, gallstone forceps and also a balloon catheter were passed into both lungs and good back-bleeding was obtained. The patient was discharged from the hospital and returned to full activity. Moser and Braunwald observed that the patient had a “two compartment pulmonary vascular bed.” The open pulmonary arteries probably had advanced changes of pulmonary hypertension, but the “closed” vascular bed, which had never been subjected to high pressures, had retained normal structure. In this patient the thromboembolism was known to have been present for 10 years or more, and this was the first documentation of the ability to remove such material and to achieve long-term patency at operation. The pulmonary vascular resistance fell from 1208 to 640, and the patient was discharged well. Sabiston and coworkers30 in 1977 described six patients whom they had operated on at Duke University and published a summary article of the published surgical experience to date. They found a total of 12 patients previously reported in the world literature in which pulmonary “embolectomy” was performed, which together with their patients of six brought the total to 18. In the six patients, five improved postoperatively. In three of the patients bypass was used, and in two a median sternotomy was performed. Sabiston pointed out that the lung receives two sources of blood: that from the pulmonary artery and that from the bronchial arteries (as first described by Trendelenberg). The latter maintains patency of the pulmonary arteriolar circulation distal to a
Surgery for chronic thromboembolic disease proximal occlusion by a chronic embolus and provides the ability for later endarterectomy to recruit once more the pulmonary parenchyma in the role of oxygenation of the blood. This observation was the rationale for pulmonary endarterectomy; the lung does not infarct after embolization. Cabrol and colleagues in 197831 reported on a series of 16 patients operated on in Paris. In the first two operations, the main pulmonary artery was approached through a median sternotomy, using cardiopulmonary bypass. In the other patients a lateral thoracotomy was used. In his series of 16 patients there were six deaths, and 10 were alive six months to 10 years after operation. Three patients had an excellent result; six patients had good results and 1 of the 10 survivors was only moderately improved. In 1980 Daily and coworkers32 described a further four patients undergoing operation at UCSD, with three survivors. A median sternotomy and cardiopulmonary bypass were used, and in three, circulatory arrest was used. Daily at this time reviewed the English literature and found a total of 36 patients that had been treated operatively. A median sternotomy had been used only five times. Dor and colleagues33 reported on a further 12 patients in 1981, and Utley and coworkers updated the UCSD series in 1982,34 discussing a further 10 patients who were operated on between July 1977 and June 1981. Five patients had complete obstruction of a pulmonary artery. Again, a median sternotomy was performed, and the heart–lung machine was used to cool the patients’ temperature to 16°C or less. The endarterectomy was performed with circulatory arrest. The importance of not dividing the azygos vein or mobilizing it because of its significance as a collateral venous channel in patients with inferior vena caval interruption was emphasized. Only 1 of the 10 patients died, and all survivors showed improvement in hemodynamic function. Utley pointed out the importance of using fiberoptic headlights, long dissecting instruments, and fine-tipped long suction devices. No neurological deficits were encountered from the circulatory arrest, though one patient had transient bilateral phrenic nerve dysfunction. Dr. Utley, in his closing statements, emphasized that “the technique of circulatory arrest is absolutely essential for this distal “thromboendarterectomy” because the bronchial circulation is increased so greatly in these patients that one really cannot see distally in pulmonary circulation to locate the segmental vessels unless the circulation is totally arrested.” In 1984 Chitwood and colleagues35 reviewed the world’s literature to date and found a total of 85 cases managed surgically, with a mortality of 22%. Although several centers have lately started pulmonary endarterectomy programs, the majority of the subsequent surgical experience in pulmonary endarterectomy has been reported from the UCSD Medical Center, and it is this experience that forms the basis for this report. Dr. Braunwald commenced the UCSD experience with this operation in 1970. Drs. Braunwald, Utley, Daily, and Dembitsky together performed 189 cases in the 20 years between 1970 and 1989. More than 2000 operations have been done since that time by
221 Drs. Jamieson, Kapelanski (now no longer practicing), and Madani. The operation continues to be refined. The basic principles remain that the operation must be bilateral, the pleural spaces are avoided, bypass is used for hemodynamic control and cooling, and circulatory arrest is essential. The focus is on removing completely all occluding material— complications and mortality after operation are related only to residual pulmonary hypertension.36 As experience continues to be gained with the procedure, we have established that there is no thrombotic occlusion that is inaccessible at operation and no degree of pulmonary hypertension or right ventricular failure that contraindicates surgery. Although our cases are largely unselected, and we operate on many patients referred from other hospitals that do this procedure, the mortality remains at about 5%—testimony to the value of the operation. By far the majority of patients return to normal activity. It is likely that thromboembolic pulmonary hypertension will be more and more recognized as a significant cause of dyspnea and heart failure, and the surgical remedy for this condition increasingly applied. Many other surgeons now perform this operation, though not with the numbers of the UCSD group, and the future will hopefully see this therapy become available to larger numbers of patients.
References 1. Laennec RTH. Traite de l’auscultation mediate et des maladies des poumons et du coeur (thesis). Paris, 1819 2. Virchow R: Uber die Verstopfung der Lungenarterie. Reue Notizen Geb Natur Heilk 37:26, 1846 3. Trendelenburg F: Uber die operative behandlung der embolie derlungarterie. Arch Klin Chir 86:686-700, 1908 4. Kirschner M: Ein durch die Trendelenburgsche Operation genheilter Fall von Embolie der Arterien pulmonalis. Arch Klin Chir 133:312, 1924 5. Steenberg RW, Warren R, Wilson RE, et al: New look at pulmonary embolectomy. Surg Gynecol Obstet 107:214, 1958 6. Cooley DA, Beall AC, Alexander JK: Acute massive pulmonary embolism: successful surgical treatment using temporary cardiopulmonary bypass. JAMA 177:283, 1961 7. Sharp EH: Pulmonary embolectomy: successful removal of a massive pulmonary embolus with the support of cardiopulmonary bypass: a case report. Ann Surg 156:1, 1962 8. Lungdahl M: Gibt es eine chroniche embolisierg der lungenarterie? Deutsches Archiv Klin Med 160:1, 1928 9. Means JH, Mallory TB: Total occlusion of the right branch of pulmonary artery by organized thrombus. Ann Intern Med 5:417, 1931 10. Kampmeier RH: Thrombosis of main branches of the pulmonary artery with a case report and review of the literature. J Thorac Surg 3:513, 1934 11. Hollister LE, Cull VL: The syndrome of chronic thromboembolism of the major pulmonary arteries. Am J Med 21:312-320, 1956 12. Lenegre J, Gerbaux A: Le coeur pulmonaire par thrombose arterielle pulmonaire. Arch D mal Coeur 45:289, 1952 13. Kyser FA: Pulmonary artery thrombosis. Q Bull Northwestern Univ Med Sch 25:206, 1951 14. Carroll D: Chronic obstruction of major pulmonary arteries. Am J Med 9:175-15, 1950 15. Ball KP, Goodwin JF, Harrison CV: Massive thrombotic occlusion of major pulmonary arteries. Circulation 14:766-73, 1956 16. Owen WR, Thomas WA, Castleman B, et al: Unrecognized emboli to lungs with subsequent cor pulmonale. New Engl J Med 249:919-926, 1953
222 17. Houk VN, Hufnagel CA, McClenathan JE, et al: Chronic thrombosis obstruction of major pulmonary arteries. Report of a case successfully treated by thromboendarterectomy and review of the literature. Am J Med 35:269-282, 1963 18. Carroll D: Chronic obstruction of major pulmonary arteries. Am J Med 9:175-185, 1950 19. Boucher H, Protar M, Bertein J: Aneurysme de la branche droite de l’artere pulmonaire par embol latent post-phlebitique. J Franc Med Chir Thorac 5:421-427, 1951 20. Hurwitt ES, Schein CJ, Rifkin H, et al: A surgical approach to the problem of chronic pulmonary artery obstruction due to thrombosis or stenosis. Ann Surg 147:157-165, 1958 21. Allison PR, Dunnill MS, Marshall R: Pulmonary embolism. Thorax 15:273-283, 1960 22. Snyder WA, Kent DC, Baish BF: Successful endarterectomy of chronically occluded pulmonary artery. J Thorac Cardiovasc Surg 45:482489, 1963 23. Moser KM, Houk VN, Jones RC, et al: Chronic, massive thrombotic obstruction of the pulmonary arteries—analysis of four operated cases. Circulation 32:377-385, 1965 24. Moser KM, Rhodes PG, Hufnagel CC: Chronic unilateral pulmonary artery thrombosis. New Engl J Med 272:1195-1199, 1965 25. Jones RC, Jones CB, Jahnke EJ: Chronic thrombotic pulmonary artery obstruction due to recurrent embolization. Report of attempt of thromboendarterectomy. Mil Med 1110-1121, 1965 26. Frater RWM, Beck W, Schrire V: The syndrome of pulmonary artery aneurysms, pulmonary artery thrombi, and peripheral venous thrombi. J Thorac Cardiovasc Surg 49:330-338, 1965
S.W. Jamieson 27. Castleman B, McNeely BU, Scannell G: Case records of the Massachusetts General Hospital. Case 32-1964. New Engl J Med 271:40-50, 1964 28. Nash ES, Shapiro S, Landau A, et al: Successful thrombo-embolectomy in long-standing thrombo-embolic pulmonary hypertension. Thorax 23:121-130, 1968 29. Moser KM, Braunwald NS: Successful surgical intervention in severe chronic thromboembolic pulmonary hypertension. Chest 64:29-35, 1973 30. Sabiston DC, Wolfe WG, Oldham HN, et al: Surgical management of chronic pulmonary embolism. Ann Surg 185:699-712, 1977 31. Cabrol C, Cabrol A, Acar J, et al. Surgical correction of chronic postembolic obstructions of the pulmonary arteries. J Thorac Cardiovasc Surg 76:620-628, 1978 32. Daily PO, Johnston GG, Simmons CJ, et al: Surgical management of chronic pulmonary embolism. Surgical treatment and late results. J Thorac Cardiovasc Surg 79:523-531, 1980 33. Dor V, Jourdan J, Schmitt R, et al: Delayed pulmonary thrombectomy fire a peripheral approach in the treatment of pulmonary embolism and sequelae. Thorac Cardiovasc Surg 29:227-232, 1981 34. Utley JR, Spragg RG, Long WB, et al: Pulmonary endarterectomy for chronic thromboembolic obstruction: recent surgical experience. Surgery 92:1096-1102, 1982 35. Chitwood WR, Sabiston DC, Wechsler AS: Surgical treatment of chronic unresolved pulmonary embolism. Clin Chest Med 5:507-536, 1984 36. Jamieson SW, Kapelanski DP, Sakakibara N, et al: Pulmonary endarterectomy: experience and lessons learned in 1,500 cases. Ann Thorac Surg 76(5):1457-64, 2003
T
he entity of acute pulmonary embolism was described by Laennec in 1819,1 who also recognized its relation to deep venous thrombosis. That deep venous thrombosis was related to stasis, hypercoagulability, and vessel wall injury was recognized by Virchow2 in 1846. The first to describe an operative approach for acute pulmonary embolism was Trendelenberg in 1908.3 In a moribund patient, and without anesthesia, he exposed the heart and great vessels through a vertical incision to the left of the sternum and a horizontal extension over the second rib. He passed a rubber tape beneath the aorta and pulmonary artery through the transverse sinus, and after snaring the tape, he incised the pulmonary artery, removed the clot, and closed the pulmonary arteriotomy with a clamp, all within 45 seconds. The pulmonary arteriotomy was then repaired. The patient survived the operation but died of heart failure 15 hours later, probably as a result of inadequate removal of thrombus. A second patient he described also had immediate survival but died of hemorrhage from the internal mammary artery 37 hours after operation. It was 19244 before long-term survival after acute embolectomy with complete functional recovery was described by Kirschner, and several other reports later followed. When Steenberg and coworkers5 reported the first survivor of the “Trendelenburg operation” in the United States in 1958, there had been 12 other reports of successful embolectomy in the European literature. Pulmonary embolectomy remained a very hazardous procedure, however, until a more careful Division of Cardiothoracic Surgery, University of California, San Diego, San Diego, CA. Address reprint requests to Stuart W. Jamieson MB, FRCS, Division of Cardiothoracic Surgery, University of California, San Diego, 200 West Arbor Drive, San Diego, CA 92103-8892. E-mail: [email protected].
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and thorough approach by using cardiopulmonary bypass was described by Cooley and colleagues in 19616 and Sharp in 1962.7 The use of cardiopulmonary bypass, when available, remains the standard for acute pulmonary endarterectomy, though controversy remains regarding the place of the operation. The recognition of chronic thrombotic obstruction of the pulmonary arteries came more than 100 years after that of acute pulmonary embolism. In 1928 Lungdahl8 described two women, one aged 38 and one aged 51, who had suffered for several years from dyspnea, cyanosis, and palpitations. Ultimately, both died of right heart failure, and at autopsy chronic pulmonary arterial obstruction was found. There was marked dilation of the proximal main pulmonary artery, with increased vascularity of the bronchial circulation. The fact that the lungs were free of infarction was observed. Lungdahl thought that it was likely that the obstruction was due to pulmonary emboli—a variation from the previously held concept that, in patients with cor pulmonale where occlusion of the pulmonary arteries was found, the process was one of primary thrombosis. A review of chronic thrombotic occlusion of the pulmonary arteries by Means and Mallory9 in 1931 found only 6 cases, and a new description and further review in 1934 by Kampmeier10 yielded 24 case reports. By 1956 Hollister and Cull11 found only 100 case reports published before 1941, including one group of 14 cases derived from a single study of 706 autopsies.12 Another series of 14 cases in this review came from admissions to a single 335-bed teaching hospital over a 10-year period.13 They found a comparable number of case reports from 1941 to 1955, and stated (in 1956): “it is probable that no more than 200 cases of the syndrome have been reported in the medical literature to date.”11
Surgery for chronic thromboembolic disease Fifty years ago, then, the finding of chronic thrombosis within the pulmonary arteries was still considered a reportable rarity, and there remained uncertainty as to whether this entity represented spontaneous thrombosis “in situ” (the etiology favored at the time) or embolization. It was, however, widely held that chronic thrombotic occlusion was not amenable to surgical correction.11,14-16 Houk and colleagues, in 1963,17 found approximately 250 reported cases of chronic thromboembolic obstruction of the major pulmonary arteries. In only six of these was the diagnosis established before death, and in only three was direct surgical therapy attempted. The first exploration for thrombotic occlusion of the pulmonary arteries was probably by Dr. Alfred Blalock at Johns Hopkins hospital in January 1948, in an operation described by Carroll in 1950.18 The left pulmonary artery was exposed through a thoracotomy incision and found to be small, with proximal occlusion, though aspiration with a needle produced red blood. The artery was divided and found to contain organized thrombus. Dr. Blalock thought the case to be inoperable and made no attempt to relieve the obstruction. The patient was discharged from the hospital unimproved. In 1951 Boucher and coworkers performed a pneumonectomy in a patient suspected of a pulmonary aneurysm.19 The pathology showed chronic thrombotic obstruction of the pulmonary arteries. A possible surgical approach to the condition by endarterectomy was suggested in 195611 and the first planned pulmonary endarterectomy was performed in 1957 by Hurwitt and colleagues on a patient operated on with inflow occlusion and systemic hypothermia through a transverse sternotomy. Although the period of inflow occlusion was only 2½ minutes, the patient arrested and could not be resuscitated.20 Allison and coworkers21 performed a right lower lobectomy in a 59-year-old man in June 1957 in Oxford—this patient was subsequently found to have chronic thrombotic occlusion of this lobe. Many bloody adhesions were encountered with the thoracotomy approach (an additional reason that the midline approach is better and is now the favored standard). The patient recovered, but was admitted to hospital again 3 months later with left-sided chest pain and heart failure. He died that month, and autopsy revealed massive thromboembolic obstruction of the left main pulmonary artery and adherent emboli. However, the same author performed the first successful embolectomy for recurrent emboli—again with the technique of inflow occlusion, in March 1958.21 In this operation the patient was cooled to 29°C in a waterbath, and the chest was then opened with a trans-sternal approach. An embolectomy (not a true endarterectomy) was performed using suction and forceps. However “a mass of tough thrombus was removed from the right pulmonary artery. After this, suction was effective in drawing out many lengths of softer “tailed” thrombus, the tails representing branches of the artery.” The patient survived and was improved. In July 1961 Snyder and coworkers operated on a 71-yearold man initially suspected of having a tumor, at the San
219 Diego Naval Hospital.22 A right thoracotomy was made, through the fifth intercostal space. There were upper lobe adhesions. No tumor was found, but a thickened pulmonary artery was encountered. No pulsations were palpable below the right upper lobe pulmonary artery, and a longitudinal incision was made in the pulmonary artery. A thrombotic mass was removed with endarterectomy spoons. An angiogram performed in August 1961 showed a patent pulmonary artery. Snyder made an important observation: “The findings in the present case unequivocally demonstrate that the pulmonary artery, after occlusion for a considerable number of years, continues to maintain a relatively normal relationship to the pulmonary veins at the capillary level, that the pulmonary alveolar membrane is not irreparably damaged by prolonged pulmonary artery occlusion, and that functional return of the affected lung may be expected after pulmonary endarterectomy.” Another important concept was expressed in 1963 by Houk and colleagues,17 describing a case operated on at Georgetown in November 1961. A bilateral anterior thoracotomy incision was made, and though it was not used, cardiopulmonary bypass standby was available. They referenced the success with cardiopulmonary bypass in acute embolectomy and suggested that perhaps cardiopulmonary bypass should be used electively for operation on chronic thrombotic occlusion. The progress of this patient was updated in two reports in 196523,24 and he was said to be alive and asymptomatic now more than 3 years after surgery. A further successful case, of a 42-year-old man, was now also presented.24 Operation was performed through a median sternotomy incision on May 18, 1962. Cardiopulmonary bypass was on standby. A true endarterectomy was again performed here, and a large thrombotic mass was freed by blunt dissection medially and sharp dissection distally. The patient was discharged on June 9th. Moser and colleagues reemphasized that the same technical advances that had made emergency pulmonary embolectomy and openheart surgery possible had now made pulmonary endarterectomy feasible in selected patients with massive thromboembolic pulmonary artery occlusion. He stated that “our present consensus is that bypass should be available on a standby basis in all cases and is required if extensive bilateral obstruction is to be corrected. Perhaps bypass should be used in all cases to permit more detailed exploration of the pulmonary arterial tree, but the problems associated with bypass must be balanced against the advantages of its use in each case.” The May 1962 patient, operated at Georgetown University by Dr. Charles Hufnagel,24 was probably the first with this disorder in whom the diagnosis was made before operation and successful correction achieved. The operation demonstrated that extensive well-organized thrombi, having obstructed major pulmonary vessels from months to years, could be removed successfully. Furthermore, the reclaimed lung areas were shown to be able to safely accept the sudden return of blood flow and to resume adequate respiratory function.
220 In his subsequent analysis of four operated cases,23 in addition to the above two successful cases, Moser described two in whom surgical correction could not be achieved, with the patients dying postoperatively. The first of these was operated on in April 1964. Hypotension developed during induction of anesthesia, accentuated by temporary occlusion of the right main pulmonary artery, and the procedure was abandoned. Hypotension persisted and the patient died 2 hours later. The other case was the same described in more detail by Jones and coworkers in 1965.25 This was a 37-year-old man with a previous fractured right arm and a separate injury to the right leg, who also had varicose veins. He was operated on on 1 April 1964. The chest was entered through a bilateral anterior thoracotomy with cardiopulmonary bypass standby, but without the use of bypass. Dense vascular adhesions were found diffusely between the lungs, chest wall, and pericardium throughout both hemithoraces. The right lung was freed by sharp dissection and the right main pulmonary artery was isolated. An incision was made in the right pulmonary artery and extended into the branches of the upper lobe. “These vessels were entirely patent proximally; however, at the segmental and subsegmental level they were relatively bloodless and were occluded by fibrous webs of material having a peculiar moth-eaten appearance. There was no identifiable lumen.” Similar changes were found in the lower lobe, and it was concluded that “there was no proximal block amenable to endarterectomy, and the more distal lesions were inoperable.” 7500 mL of blood were required to replace that lost during dissection of vascular adhesions on the right. The patient became hypotensive and died 24 hours later. Jones concluded “it is patently clear that we were dealing with a patient with inoperable chronic obstructive disease of the pulmonary arteries.” Frater and colleagues,26 in 1965, discussed the case of a 23-year-old farm worker operated upon on September 4, 1963. This patient presented with a pulmonary artery aneurysm originally thought to be mycotic. Subsequent angiography demonstrated pulmonary artery occlusion. A left anterolateral thoracotomy was made, with cardiopulmonary bypass standby, though bypass was not used. The pulmonary artery pressures were unchanged postoperatively, and the patient was not benefited. The first operation using cardiopulmonary bypass was probably performed by Dr. Scannell in 196427 at the Massachusetts General Hospital. The patient was a 39-year-old physician with dyspnea and chest pain. At cardiac catheterization his pulmonary artery pressures were 100/30 with a mean of 55. A bilateral anterior thoracotomy was performed. The patient had a cardiac arrest on opening the chest, and he was placed on cardiopulmonary bypass. Though this was a case of chronic thrombotic occlusion, an embolectomy was performed with forceps and by squeezing the lung. Postoperatively the patient developed severe pulmonary edema with a “high degree of residual pulmonary hypertension,” and died 2 hours after operation. Autopsy showed residual clot and fibrous bands, adherent to the intima, which “couldn’t merely be picked off.”
S.W. Jamieson Nash and coworkers28 in 1968 described a case, operated on in June 1966, where a large thrombus was removed from the left pulmonary artery using cardiopulmonary bypass. A left thoracotomy was performed at the level of the fourth rib. After cardiopulmonary bypass was established he developed a line of cleavage between the thrombus and the left pulmonary artery wall and the entire thrombus was removed. This again was a true endarterectomy with a typical cast specimen. The patient recovered fully and went back to normal activity. Subsequent arteriogram was performed showing a patent left main pulmonary artery. By the end of the 1960s then, a true appreciation of this disorder was appearing. It had become clear that a formal endarterectomy needed to be performed to remove all parts of the chronic thrombotic mass, and that for this to be done completely, cardiopulmonary bypass was required. The condition was often associated with extensive adhesions of the lung to the chest wall, and a lateral thoracotomy was often associated with extensive blood loss. Dr. Kenneth Moser, who was a pulmonary physician with an abiding interest in pulmonary hypertension from thrombotic occlusion of the pulmonary arteries, and had previously been a colleague of Dr. Hufnagel, moved from Georgetown to San Diego in the late 1960s. In 1973 he and Nina Braunwald presented the first case that was operated on at the University of California, San Diego (UCSD).29 The patient was a 67-yearold man who underwent surgery on July 14, 1970. Through a right lateral thoracotomy, a pulmonary “thromboendarterectomy” was performed using cardiopulmonary bypass. The thrombus was removed with forceps and embolectomy spoons. In addition, gallstone forceps and also a balloon catheter were passed into both lungs and good back-bleeding was obtained. The patient was discharged from the hospital and returned to full activity. Moser and Braunwald observed that the patient had a “two compartment pulmonary vascular bed.” The open pulmonary arteries probably had advanced changes of pulmonary hypertension, but the “closed” vascular bed, which had never been subjected to high pressures, had retained normal structure. In this patient the thromboembolism was known to have been present for 10 years or more, and this was the first documentation of the ability to remove such material and to achieve long-term patency at operation. The pulmonary vascular resistance fell from 1208 to 640, and the patient was discharged well. Sabiston and coworkers30 in 1977 described six patients whom they had operated on at Duke University and published a summary article of the published surgical experience to date. They found a total of 12 patients previously reported in the world literature in which pulmonary “embolectomy” was performed, which together with their patients of six brought the total to 18. In the six patients, five improved postoperatively. In three of the patients bypass was used, and in two a median sternotomy was performed. Sabiston pointed out that the lung receives two sources of blood: that from the pulmonary artery and that from the bronchial arteries (as first described by Trendelenberg). The latter maintains patency of the pulmonary arteriolar circulation distal to a
Surgery for chronic thromboembolic disease proximal occlusion by a chronic embolus and provides the ability for later endarterectomy to recruit once more the pulmonary parenchyma in the role of oxygenation of the blood. This observation was the rationale for pulmonary endarterectomy; the lung does not infarct after embolization. Cabrol and colleagues in 197831 reported on a series of 16 patients operated on in Paris. In the first two operations, the main pulmonary artery was approached through a median sternotomy, using cardiopulmonary bypass. In the other patients a lateral thoracotomy was used. In his series of 16 patients there were six deaths, and 10 were alive six months to 10 years after operation. Three patients had an excellent result; six patients had good results and 1 of the 10 survivors was only moderately improved. In 1980 Daily and coworkers32 described a further four patients undergoing operation at UCSD, with three survivors. A median sternotomy and cardiopulmonary bypass were used, and in three, circulatory arrest was used. Daily at this time reviewed the English literature and found a total of 36 patients that had been treated operatively. A median sternotomy had been used only five times. Dor and colleagues33 reported on a further 12 patients in 1981, and Utley and coworkers updated the UCSD series in 1982,34 discussing a further 10 patients who were operated on between July 1977 and June 1981. Five patients had complete obstruction of a pulmonary artery. Again, a median sternotomy was performed, and the heart–lung machine was used to cool the patients’ temperature to 16°C or less. The endarterectomy was performed with circulatory arrest. The importance of not dividing the azygos vein or mobilizing it because of its significance as a collateral venous channel in patients with inferior vena caval interruption was emphasized. Only 1 of the 10 patients died, and all survivors showed improvement in hemodynamic function. Utley pointed out the importance of using fiberoptic headlights, long dissecting instruments, and fine-tipped long suction devices. No neurological deficits were encountered from the circulatory arrest, though one patient had transient bilateral phrenic nerve dysfunction. Dr. Utley, in his closing statements, emphasized that “the technique of circulatory arrest is absolutely essential for this distal “thromboendarterectomy” because the bronchial circulation is increased so greatly in these patients that one really cannot see distally in pulmonary circulation to locate the segmental vessels unless the circulation is totally arrested.” In 1984 Chitwood and colleagues35 reviewed the world’s literature to date and found a total of 85 cases managed surgically, with a mortality of 22%. Although several centers have lately started pulmonary endarterectomy programs, the majority of the subsequent surgical experience in pulmonary endarterectomy has been reported from the UCSD Medical Center, and it is this experience that forms the basis for this report. Dr. Braunwald commenced the UCSD experience with this operation in 1970. Drs. Braunwald, Utley, Daily, and Dembitsky together performed 189 cases in the 20 years between 1970 and 1989. More than 2000 operations have been done since that time by
221 Drs. Jamieson, Kapelanski (now no longer practicing), and Madani. The operation continues to be refined. The basic principles remain that the operation must be bilateral, the pleural spaces are avoided, bypass is used for hemodynamic control and cooling, and circulatory arrest is essential. The focus is on removing completely all occluding material— complications and mortality after operation are related only to residual pulmonary hypertension.36 As experience continues to be gained with the procedure, we have established that there is no thrombotic occlusion that is inaccessible at operation and no degree of pulmonary hypertension or right ventricular failure that contraindicates surgery. Although our cases are largely unselected, and we operate on many patients referred from other hospitals that do this procedure, the mortality remains at about 5%—testimony to the value of the operation. By far the majority of patients return to normal activity. It is likely that thromboembolic pulmonary hypertension will be more and more recognized as a significant cause of dyspnea and heart failure, and the surgical remedy for this condition increasingly applied. Many other surgeons now perform this operation, though not with the numbers of the UCSD group, and the future will hopefully see this therapy become available to larger numbers of patients.
References 1. Laennec RTH. Traite de l’auscultation mediate et des maladies des poumons et du coeur (thesis). Paris, 1819 2. Virchow R: Uber die Verstopfung der Lungenarterie. Reue Notizen Geb Natur Heilk 37:26, 1846 3. Trendelenburg F: Uber die operative behandlung der embolie derlungarterie. Arch Klin Chir 86:686-700, 1908 4. Kirschner M: Ein durch die Trendelenburgsche Operation genheilter Fall von Embolie der Arterien pulmonalis. Arch Klin Chir 133:312, 1924 5. Steenberg RW, Warren R, Wilson RE, et al: New look at pulmonary embolectomy. Surg Gynecol Obstet 107:214, 1958 6. Cooley DA, Beall AC, Alexander JK: Acute massive pulmonary embolism: successful surgical treatment using temporary cardiopulmonary bypass. JAMA 177:283, 1961 7. Sharp EH: Pulmonary embolectomy: successful removal of a massive pulmonary embolus with the support of cardiopulmonary bypass: a case report. Ann Surg 156:1, 1962 8. Lungdahl M: Gibt es eine chroniche embolisierg der lungenarterie? Deutsches Archiv Klin Med 160:1, 1928 9. Means JH, Mallory TB: Total occlusion of the right branch of pulmonary artery by organized thrombus. Ann Intern Med 5:417, 1931 10. Kampmeier RH: Thrombosis of main branches of the pulmonary artery with a case report and review of the literature. J Thorac Surg 3:513, 1934 11. Hollister LE, Cull VL: The syndrome of chronic thromboembolism of the major pulmonary arteries. Am J Med 21:312-320, 1956 12. Lenegre J, Gerbaux A: Le coeur pulmonaire par thrombose arterielle pulmonaire. Arch D mal Coeur 45:289, 1952 13. Kyser FA: Pulmonary artery thrombosis. Q Bull Northwestern Univ Med Sch 25:206, 1951 14. Carroll D: Chronic obstruction of major pulmonary arteries. Am J Med 9:175-15, 1950 15. Ball KP, Goodwin JF, Harrison CV: Massive thrombotic occlusion of major pulmonary arteries. Circulation 14:766-73, 1956 16. Owen WR, Thomas WA, Castleman B, et al: Unrecognized emboli to lungs with subsequent cor pulmonale. New Engl J Med 249:919-926, 1953
222 17. Houk VN, Hufnagel CA, McClenathan JE, et al: Chronic thrombosis obstruction of major pulmonary arteries. Report of a case successfully treated by thromboendarterectomy and review of the literature. Am J Med 35:269-282, 1963 18. Carroll D: Chronic obstruction of major pulmonary arteries. Am J Med 9:175-185, 1950 19. Boucher H, Protar M, Bertein J: Aneurysme de la branche droite de l’artere pulmonaire par embol latent post-phlebitique. J Franc Med Chir Thorac 5:421-427, 1951 20. Hurwitt ES, Schein CJ, Rifkin H, et al: A surgical approach to the problem of chronic pulmonary artery obstruction due to thrombosis or stenosis. Ann Surg 147:157-165, 1958 21. Allison PR, Dunnill MS, Marshall R: Pulmonary embolism. Thorax 15:273-283, 1960 22. Snyder WA, Kent DC, Baish BF: Successful endarterectomy of chronically occluded pulmonary artery. J Thorac Cardiovasc Surg 45:482489, 1963 23. Moser KM, Houk VN, Jones RC, et al: Chronic, massive thrombotic obstruction of the pulmonary arteries—analysis of four operated cases. Circulation 32:377-385, 1965 24. Moser KM, Rhodes PG, Hufnagel CC: Chronic unilateral pulmonary artery thrombosis. New Engl J Med 272:1195-1199, 1965 25. Jones RC, Jones CB, Jahnke EJ: Chronic thrombotic pulmonary artery obstruction due to recurrent embolization. Report of attempt of thromboendarterectomy. Mil Med 1110-1121, 1965 26. Frater RWM, Beck W, Schrire V: The syndrome of pulmonary artery aneurysms, pulmonary artery thrombi, and peripheral venous thrombi. J Thorac Cardiovasc Surg 49:330-338, 1965
S.W. Jamieson 27. Castleman B, McNeely BU, Scannell G: Case records of the Massachusetts General Hospital. Case 32-1964. New Engl J Med 271:40-50, 1964 28. Nash ES, Shapiro S, Landau A, et al: Successful thrombo-embolectomy in long-standing thrombo-embolic pulmonary hypertension. Thorax 23:121-130, 1968 29. Moser KM, Braunwald NS: Successful surgical intervention in severe chronic thromboembolic pulmonary hypertension. Chest 64:29-35, 1973 30. Sabiston DC, Wolfe WG, Oldham HN, et al: Surgical management of chronic pulmonary embolism. Ann Surg 185:699-712, 1977 31. Cabrol C, Cabrol A, Acar J, et al. Surgical correction of chronic postembolic obstructions of the pulmonary arteries. J Thorac Cardiovasc Surg 76:620-628, 1978 32. Daily PO, Johnston GG, Simmons CJ, et al: Surgical management of chronic pulmonary embolism. Surgical treatment and late results. J Thorac Cardiovasc Surg 79:523-531, 1980 33. Dor V, Jourdan J, Schmitt R, et al: Delayed pulmonary thrombectomy fire a peripheral approach in the treatment of pulmonary embolism and sequelae. Thorac Cardiovasc Surg 29:227-232, 1981 34. Utley JR, Spragg RG, Long WB, et al: Pulmonary endarterectomy for chronic thromboembolic obstruction: recent surgical experience. Surgery 92:1096-1102, 1982 35. Chitwood WR, Sabiston DC, Wechsler AS: Surgical treatment of chronic unresolved pulmonary embolism. Clin Chest Med 5:507-536, 1984 36. Jamieson SW, Kapelanski DP, Sakakibara N, et al: Pulmonary endarterectomy: experience and lessons learned in 1,500 cases. Ann Thorac Surg 76(5):1457-64, 2003