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Surgical management of chronic pulmonary embolism Surgical treatment and late results
J THORAC
CARDIOV ASC SURG
79:523-531, 1980
Surgical management of chronic pulmonary embolism Surgical treatment and late results Failure of pulmonary emboli to undergo fibrinolytic resolution generates a small but significant patient population progressively disabled by hypoxemia, chronic pulmonary hypertension, and eventual right heart failure. Medical management of these patients has not been effective. In the few patients treated surgically, no clear picture has emerged regarding the most effective surgical approach or the late results. Four male patients with chronic pulmonary embolism were managed operatively. Extrapericardial dissection, cardiopulmonary bypass, deep hypothermia, and intermittent circulatory arrest were utilized to perform pulmonary thromboendarterectomy. All patients, ages 30 to 65 years, had had severe dyspnea with minimal exertion for I to 20 years. Angiograms showed 50% to 75% of the pulmonary vasculature to be occluded, with frequent involvement of the segmental arteries. Preoperative pulmonary pressures varied from 60/33 to 74/24 mm Hg. Pulmonary vascular resistance values ranged from 450 to 750 dynes-sec-em:". All patients survived the operative procedure. The eldest patient died 3 weeks postoperatively following an acute posteroseptal myocardial infarction. The remaining patients had a 20 to 50 mm Hg decrease in pulmonary systolic pressure with a 50% to 75% reduction in pulmonary vascular resistance. Neither static nor dynamic lung volumes were changed appreciably. Follow-up angiograms in all patients confirmed significant increase in pulmonary perfusion. Each patient had improvement in functional capacity; one is completely asymptomatic. The primary advantage of the surgical approach described is the more complete removal of distally located thrombofibrotic material. The late results suggest that this surgical approach should be considered in the management of patients disabled by chronic pulmonary embolism.
Pat O. Daily, M.D.,* G. Gilbert Johnston, M.D.,* Cecile J. Simmons,* and Kenneth M. Moser, M.D., ** San Diego, Calif.
Chronic pulmonary hypertension subsequent to massive and repeated pulmonary embolism is infrequently observed. Attempts to relieve chronic pulmonary artery obstruction surgically have been reported even less frequently. Even so, a variety of surgical approaches have been described with variable results. However, no single surgical approach previously reported has allowed reasonable access to most major pulmonary arteries. This report describes a surgical procedure which affords exposure of the main pulmonary artery, both right Read at the Fifth Annual Meeting of The Samson Thoracic Surgical Society, Sun Valley, Idaho, June 5 to 8, 1979. Address for reprints: Pat O. Daily, M.D., 7930 Frost St., Suite 305, San Diego, Calif. 92123. *Donald N. Sharp Memorial Community Hospital, San Diego, Calif. **Professor and Head, Pulmonary Division, University Hospital, San Diego, Calif.
and left pulmonary arteries, and the lobar branches of each. Its applicability and results are described in four patients. Methods and patients Four male patients, ages 40, 32, 65, and 33 years, underwent pulmonary thromboendarterectomy between Feb. 1, 1975, and May 4, 1978. All procedures were performed through a median sternotomy with standard cardiopulmonary bypass. After the pericardium was suspended, the superior and inferior venae cavae were encircled with umbilical tapes passed through lengths of soft rubber tubing. The superior and inferior venae cavae were cannulated with 7 mm Polystan cannulas inserted through the right atrium, and the ascending aorta was cannulated with a 6.5 mm Sams cannula. On both the right and left sides, the pericardium was divided down to the pulmonary arteries. The phrenic
0022-5223/80/040523+09$00.90/0 © 1980 The C. V. Mosby Co.
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Table I
Pa02 (mm Hg)* Case No.
1 2
3 4
Age (yr)
Preop.
40 32 65
42 46 53 65
33
I
Pulmonary artery pressure (mm Hg)
Postop .
Preop.
66 71 58 74
60/33 74/25 70/36 65/29
I
Pulmonary vascular resistance (dynessec-cm-O)
Postop.
Preop.
37/7 24/6 88/48 43/22
450 756 620 480
I
Postop.
136 124 743 248
*Systemic arterial blood was analyzed. Flo, = 0.20.
nerves were identified and retracted anteriorly with umbilical tapes. On the right side, the superior vena cava was dissected superiorly to the azygos vein and then retracted anteriorly to increase exposure of the right pulmonary artery (Fig. 1). On that side, a pulmonary arteriotomy was performed in the right upper lobe (RUL) artery and also in the pulmonary artery distal to the RUL branch. The superior pulmonary vein was retracted inferiorly to improve exposure of the right upper and intermediate pulmonary arteries (Fig. 1). On the left, a single arteriotomy was utilized, beginning just outside the pericardium and extending distally (Fig. 1). Once exposed, the occluding material was removed with an endarterectomy spatula. In the last three cases it was necessary to utilize deep hypothermia with circulatory arrest to control severe back bleeding from the endarterectomized arteries.
Case reports and results CASE 1. A 40-year-old laborer sustained a spinal injury at the level of the seventh cervical vertebra in January of 1974, which resulted in a mild Brown-Sequard syndrome. He was first admitted to University Hospital the following December complaining of severe shortness of breath. He was dyspneic at rest, had great difficulty dressing himself, and could ambulate less than one half block. There was no history of chest pain, hemoptysis, or cough and there were no symptoms of lower extremity edema or pain. Physical examination revealed a thin, afebrile, normotensive, dyspneic black man. Marked jugulovenous distention, a prominent P2 accentuation with a loud S3 gallop, and a soft holosystolic tricuspid murmur were observed. The liver spanned 15 em and a hepatojugular reflex was present. A moderate right hemiparesis with atrophy and patchy left hemihyperesthesia was noted. P0 2 was 40 mm Hg with the patient breathing room air, and ventilation-perfusion scans were indicative of multiple, bilateral pulmonary emboli. Venograms demonstrated thrombosis of the right iliac and femoral veins. The patient was treated for 6 weeks with a constant intravenous infusion of heparin without appreciable improvement. Results of subsequent right heart catheterization are presented in Table I. Pulmonary angiograms revealed large, organized thromboemboli in both the right and left pulmonary artery
bifurcations with near-total occlusion of flow to both lower lobes. Operation was performed on Feb. I, 1975. Opening the right pulmonary artery exposed a large, densely adherent thrombus just distal to the RUL branch. This thrombus was successfully extracted by endarterectomy. The left pulmonary artery was obstructed by a similar fibrinous mass at the junction of the left upper lobe (LUL) artery, with inferior extension into the lower lobe segmental branches which could not be adequately cleared. Hypothermia with circulatory arrest was not utilized. A Moretz clip was applied to the vena cava. By the third postoperative week the P0 2 was 65 mm Hg with the patient breating room air, and he experienced progressive subjective improvement as well as increased strength and stamina. Results of catheterization are summarized in Table 1. Repeat pulmonary arteriograms performed in January of 1976 revealed significantly increased pulmonary blood flow, particularly to the right lower lobe (RLL) and left upper lobe (LUL). Additionally, the heart size was significantly smaller postoperatively as compared to preoperatively (Figs. 2 and 3). He has remained asymptomatic from a cardiovascular standpoint. CASE 2. A 32-year-old architectural engineer apparently first developed deep venous thrombosis early in 1974 following a skiing injury. No treatment was initiated. In October, 1974, he had an acute episode of severe substernal discomfort, weakness, diaphoresis, and dyspnea, which was diagnosed as asthma. He remained markedly disabled through late 1974, when extensive pulmonary occlusion was documented and anticoagulation was begun. He noted modest improvement and warfarin sodium (Coumadin) therapy was continued through June, 1975. The man experienced no further symptoms of deep venous thrombosis but remained disabled, being unable to walk more than 50 feet without having to rest. He was unable to maintain a normal work schedule and was referred to the University of California Medical Center, San Diego, California, in June of 1976. Physical examination revealed a thin, normotensive, afebrile white man who became dyspneic from disrobing. There was no cyanosis, clubbing, or edema. Three separate murmurs, which increased with inspiration and decreased with expiration, were audible in the peripheral lung fields. A palpable right ventricular heave was present, and pulmonic closure with a prominent systolic ejection murmur along the left sternal border and a fixed-split S2 was observed. The liver's edge was palpable and nontender and spanned 11 em. There were no stigmata of lower extremity venous disease. Pertinent laboratory and catheterization data are presented
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Fig. 2. Case I. Chest x-ray film taken 4 week s preoperatively .
Fig. 1. Surgic al approach showing incisions in pericardium with retraction of phrenic nerves and incision s in pulmonary arteries. in Table I. Preoperative pulmonary arteriograms are illustrated in Fig . 4. The patient was subjected to pulmonary endarterectomy in July. 1976, by means of the technique described previou sly . No residual thrombus was present within the right pulmonary artery , but the wall was markedly thickened and fibrotic material was removed from the almost completely occluded origin of the right middle lobe (RML) artery . A large, well-organized , den sely adherent thrombus wasdissected from the left main pulmonary artery as well as itslobar and several segmental branches (Fig . 5). Circulatory arrest was performed for 61f2 and 81f2 minutes . The patient made a rapid and uncomplicated recovery and was discharged on a regimen of 5,000 U of heparin administered subcutaneously twice a day. He obtained dramatic improvement in his functional capacity . The results of follow-up pulmonary angiograms with right heart catheterization obtained 4 months postoperatively are presented in Table I and Fig. 6. The man elected to discontinue his subcutaneous heparin 1herapy after 6 months, and shortly thereafter exten sive deep venous thrombosis redeveloped in the right leg with extension into the inferior vena cava . Therapeutic anticoagulation was .Jministered and the inferior cava was clipped . No evidence
Fig. 3. Case I . Chest x-ray film taken 47 months postoperatively showing significant decrease in heart size. of recurrent embolization was found, and at present he is essentially asymptomatic except for mild residual swelling of the right leg . C A S E 3 . A 65-year-old retired contractor was admitted in September of 1976, following 20 years of respiratory illness. He remembered multiple bout s of pneumonia in adolescence, and after World War II he had several episodes of respiratory infection with associated hemoptysis . Five years before admission he began to experience intermittent chest pain ,
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Fig. 4. Case 2. Preoperative pulmonary arteriogram. There is marked reduction in pulmonary blood flow with minimal perfusion of the upper and lower lobes bilaterally . hemoptysis , and increasing dyspnea and had two myocardial infarctions. At the time of admission he led a bed-to-chair existence requiring constant oxygen supplementation . Physical examination revealed an afebrile extremely tachypneic, cyanotic white man with clubbed fingers and toes. There were diminished respiratory excursions and scattered rales throughout both lung fields. A systolic outflow murmur was present along the left sternal border without gallops , thrills, or increased P2. There was no organomegaly , but 1+ ankle edema was present bilaterally. Chest films demonstrated huge pulmonary arteries with scattered zones of parenchymal fibrosis . P0 2 with the patient breathing room air was less than 50 mm Hg. Pulmonary angiograrns showed numerous mural irregularities, occlusion of the RML artery, but no acute proximal thromb i. Results of right-sided catheterization are shown in Table 1. Left heart catheterization revealed a left ventricular end-diastolic pressure of 15 mm Hg, reduced ejection fraction, a high-grade stenos is of the right coronary artery , and total occlusion of the circumflex coronary artery beyond the first marg inal branch with no visualization of the distal artery . At operation the right side of the heart appeared to be twice the size of the left. A large amount of free thrombu s was found within the lumen of the right pulmonary artery . It extended into and occluded the lower lobe arter ies, with a fibrinous membrane obstructing those of the RML. A similar combination of old and recent thrombus was evacuated from the left pulmonary system , after which a saphenous vein graft was placed from the aorta to the distal right coronary artery . Circulatory arrest occurred for 30 minutes and 13 minutes. The patient required pharmacologic support to be weaned from cardiopulmonary bypass , and he exhibited a low cardiac output in the initial postoperative period although there was no electrocardiographic or enzymatic evidence of perioperative infarction .
Fig. 5. Case 2. Surgical specimen removed from left lower lobe pulmonary artery . Note extensions from main thrombus corre sponding to segmental arterial branches. He was extubated on the fourth postoperati ve day with a P0 2 greater than 50 mm Hg while breathing room air. However , I week postoperatively he developed left lower lobe (LLL ) Klebsiella pneumonia , sepsis, and respiratory failure necessitating prolonged ventilatory support and eventual tracheostomy. Postoperative anticoagulation was discontinued owing to gastrointestinal bleeding. By the third postoperative week he no longer required mechan ical ventilation , and antibiotic s were discontinued . His stools were Hematest negative and he was beginning ambulation when he suddenly became hypotensive and developed atrioventricular dissociation and subsequent anuria. Resuscitative efforts over the next 24 hours were unsuccessful and he died on postoperati ve day 25. Postmortem examination revealed recent , recurrent , nonobstructing pulmonary thrombi compromising the chronic obliteration of the peripheral pulmonary arteries . The cause of death was a large , acute , posteroseptal myocardial infarction. The aorta-coronary artery vein graft was patent and the anastomosis was unremarkable. CASE 4. A 33-year-old black man first complained of easy fatigability and progressive shortness of breath at the age of 23 years. In 1970 he was hospitalized elsewhere where he exhibited dyspnea after walking half a block and was unable to climb stairs. Right heart catheterization revealed a pulmo-
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nary pressure of 95/45 mm Hg , and an angiographic diagnosis of recurrent pulmonary embolism was made . A Moretz clip was placed across the inferior vena cava in February, 1970. The patient was maintained on anticoagulation, which produced a modest improvement. Through late 1973, he was admitted on multiple occasions for recurrent painless hemop tysis , increasing dyspnea, and progressive decrease in exercise tolerance. After 1974 he remained clinically stable but had to limit his activity severely and could not find employment. He was referred for pulmonary thromboendarterectomy in January of 1978. Preoperative angiograms showed an old thromboembolic mass beginning in the left main pulmonary artery and extending downward into the lower lobe branches. There were mural irregularities on the right side but no filling defects. On physical examination he was afebrile, normotensive, acyanotic , and comfortable at rest without digital clubbing. There were loud, distinct, peripheral pulmonary bruits over the LLL and RUL with a right ventricular heave , a palpable P2, but no significant cardiac murmurs, and no evidence of lower extremity venous disease. Results of repeat catheterization are shown in Table I. Thromboendarterectomy was performed on May 4 , 1978. Minimal material was removed from the right side , but both recent and old thrombotic material was encountered on the left, totally occluding the distal left pulmonary artery, and its extraction opened multiple branches to both lobes. Circulatory arrest was performed for 5 minutes, 19 minutes, and 29 minutes . The postoperative convalescence was uncomplicated , and at I year his ergometrically measured exercise tolerance had increased from a preoperative value of less than 7 minutes to 27 minutes. Results of catheterization 1 year postoperatively are given in Table I. Postoperative angiography revealed modest improvement in perfusion of the right lung, with the most significant return of flow to the LLL.
Pathology Surgical specimens were quite heterogeneous, varying from pigmented, fibrogelatinous material to large, well-organized, fibrous "casts" with pseudocapsules. Much of the material was freed by sharp dissection and was somewhat friable. It consisted of fibroconnective tissue , which contained recanalized, hyaline connective tissue, scattered foci of inflammatory cells, and the intimal layer of the vessel wall. The total amount of material recovered ranged from 47 gm (Case 1) to 280 gm (Case 2).
Discussion Rapid and essentially complete resolution of pulmonary emboli, after even massive pulmonary embolism, is the usual natural history. This has been reported experimentally by Moser and associates! and clinically by Fred ," Dalen ," and their colleagues. However, rarely, persistent emboli and recurrent emboli may lead to significant clinical disability including cor pulmonale. Although the exact incidence of this aspect of pulmonary embolism is unknown, Paraskos and associates"
Fig. 6. Case 2. Postoperative pulmonary arteriogram. There is significantly increased perfusion of the right pulmonary arter ies and markedly increased perfu sion of the left lower lobe artery .
found only one instance of angiographically proved pulmonary embolism progressing to chronic cor pulmonale in 60 cases. The causes of this manifestation of pulmonary embolism are uncertain, but Dalen and Alpert" have suggested that recurrent pulmonary embolism represents a more likely explanation than failure of resolution after a single , massive episode of pulmonary embolism. It is conceivable that the pathological nature of the embolic material with respect to the degree of fibrosis may be of importance in affecting resolution. While performing pulmonary embolectomies, one of us (P. O. D.) has encountered pulmonary emboli ranging from recent, relatively fresh thrombi to extremely fibrotic, highly organized ones. In any event, mechanical obstruction of the pulmonary vasculature rather than reflex vasoconstriction is the predominant mechanism." The feasibility of embolectomy or endarterectomy for chronic pulmonary embolism was suggested in 1956 by Hollister and CulJ.7 Although Hurwitt and associates" reported the attempted removal of chronic pulmonary emboli in 1958, the first successful pulmonary endarterectomy was described in 1963 by Snyder, Kent, and Baisch." In the same year Houk and associates" related a similar case . By 1970 Moor and Sabiston!' had tabulated only 11 instances l l - ! 8of removal of chronic pulmonary emboli, seven of the patients surviving. (The case of Allison and associates" was excluded, since only 13 days elapsed from the onset of symptoms until pulmonary embolectomy was performed .) An additional successful case was reported by Moser and Braunwald'" in 1973. Consequently, in 1976 Tilkian, Schroeder, and
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Robin;" basing their recommendation in part on the previous surgical experience, advocated anticoagulation therapy for chronic pulmonary thromboembolic disease. In 1977 Sabiston and associates'" updated their report of 1970 10 with an additional five patients, all of whom survived, with only one obtaining a poor result; this result was related to occlusion of the smaller pulmonary arteries as evidenced by a lack of "back bleeding" from the distal pulmonary arteries at operation. In a recent report, Cabrol and associates'" described 16 additional cases of operations for chronic postembolic obstruction of the pulmonary arteries. Six operative deaths occurred. Nine of the ten survivors had a good result. In the discussion of that paper, Hammon>' added two cases to the Duke University experience and Chiu'" described another. Thus it appears that to date the English literature contains 36 case reports of surgical procedures for removal of chronic pulmonary emboli. No single surgical approach has emerged as the preferable one. Median sternotomy has been utilized only five times. 14. 21. 23 Cabrol and associates.P after using median sternotomy and cardiopulmonary bypass, stated, "It was impossible by that route to free the peripheral pulmonary trunks, and both patients died postoperatively. " Consequently, in their next 14 cases they approached the most severely affected side through a lateral thoracotomy, using cardiopulmonary bypass when needed for circulatory support. This experience caused them to state, "It is as illogical to attempt to remove chronic thrombi from the pulmonary artery through a central approach as it is to free the femoral arteries through an approach at the aortic bifurcation. " Our experience has shown that division of the pericardium, bilaterally, to the pulmonary arteries with retraction of the phrenic nerves permits direct exposure of all lobar arteries as well as some of the segmental arteries of the lower lobes. On the right side, exposure is facilitated by dissection of the superior vena cava with anterior retraction and retraction of the superior pulmonary vein inferiorly. With this approach, incisions in the pulmonary arteries may be placed where necessary. Advantages of this surgical approach are as follows: Equal access is provided to either side with a single surgical procedure. More complete removal of the chronically obstructing material can be accomplished, so that the postoperative result is optimized. Extensive dissection of frequently vascular pleural adhesions is minimized. Other cardiac procedures can be performed if necessary, such as coronary artery bypass grafting as
The Journal of Thoracic and Cardiovascular Surgery
in Case 3. Finally, this method can be used for removal of acute pulmonary emboli and should result in the more complete removal of distally impacted emboli. In all four cases presented the emboli were markedly adherent, so that endarterectomy procedures were necessary. Also, frequently the occluding thrombi were found to extend distally into the segmental branches. Significant back bleeding occurred when these branches were freed, as described by Sabiston. H • 22 Hypothermia to 20° C with brief periods of circulatory arrest, as described in Cases 2, 3, and 4, greatly facilitated removal of the adherent, distally located emboli. No complications related to hypothermia occurred. The primary indications for operation in this series have been severe dyspnea at rest or with minimal exertion and pulmonary hypertension (i.e., greater than 50 mm Hg systolic). The definitive diagnosis is based upon the pulmonary arteriograms which, in order to indicate operation, should reveal proximal obstruction at least at the lobar level. Bronchial arteriography, as suggested by Sabiston.P Cabrol.P and their colleagues, was not performed because we thought that failure to visualize the distal pulmonary arteries would not represent an absolute contraindication to operation in severely disabled patients. On the basis of the present experience, providing the indications are met, we suggest the only contraindication is serious concomitant cardiopulmonary disease, as in Case 3. Of the long-term survivors reported to date, including those of this report, all but two (25 of 27) have obtained significant symptomatic improvement and several have become asymptomatic. It is not necessary to remove all of the occluding material in order to afford considerable relief of symptoms. However, Case 3 illustrates that careful selection is important, particularly with respect to associated cardiopulmonary disease. As mentioned, the patient described in Case 3 had had two previous myocardial infarctions. Coronary arteriography revealed high-grade right coronary artery stenosis and total occlusion of the circumflex coronary artery, with no distal artery visualized. The cause of death on the Postoperative day 25 was acute posteroseptal myocardial infarction, the area supplied by the nongrafted circumflex coronary artery. The right coronary artery graft was patent. An additional significant finding was that of recent thrombi in the pulmonary arteries. This correlates with an increase in the pulmonary artery pressure from 70/36 mm Hg preoperatively to 88/48 mm Hg postoperatively. (All other patients experienced a significant drop in pulmonary artery pressure postoperatively.) While it was not possible to
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distinguish postoperative in situ thrombosis from repeated pulmonary embolism, it seems logical to strongly endorse vena caval clipping or ligation at the time of thromboendarterectomy, as suggested by Sabiston,22 Cabrol.f" and their co-workers. This is further emphasized by the necessity to clip the inferior vena cava postoperatively in Case 2.
13 14
15
Conclusion A small but significantly disabled group of patients has pulmonary hypertension resulting from chronic thromboembolic occlusion of the pulmonary arteries. A surgical approach is described which, at a single operation, allows exploration and removal of thromboembolic material from all of the lobar arteries. The late results suggest that increased effort should be directed toward identification and surgical management of these patients. REFERENCES Moser KM, Guisan M, Bartimmo EE: In vivo and post mortem dissolution rates of pulmonary emboli and venous thrombi in the leg. Circulation 48: 170-178, 1973 2 Fred HL, Axelrad MA, Lewis JM, Alexander JK: Rapid resolution of pulmonary thromboemboli in man. JAMA 196:121-123, 1966 3 Dalen JE, Banas JS, Brooks HL, Evans GL, Paraskos JA, Dexter L: Resolution rate of acute pulmonary embolism in man. N Engl J Med 280:1194-1199,1969 4 Paraskos JA, Adelstein SJ, Smith RE, Rickman FD, Grossman WG, Dexter L, Dalen JE: Late prognosis of acute pulmonary embolism. N Engl J Med 289:55-58, 1973 5 Dalen JE, Alpert JS: Natural history of pulmonary embolism. Prog Cardiovasc Dis 17:259-270,1975 6 Daily PO, Lancaster JR, Moulder PV: The mechanism of pulmonary hypertension following miliary pulmonary embolism. Surg Gynecol Obstet 120:1009-1018, 1965 7 Hollister LE, Cull VL: The syndrome of chronic thrombosis of the major pulmonary arteries. Am J Med 21:312-320, 1956 8 Hurwitt ES, Schein CJ, Rifkin H, Lebendiger A: A surgical approach to the problem of chronic pulmonary artery obstruction due to thrombosis or stenosis. Am Surg 147:157-165, 1958 9 Snyder WA, Kent DC, Baisch BF: Successful endarterectomy of chronically occluded pulmonary artery. J THORAC CARDIOVASC SURG 45:482-489, 1963 10 Houk VN, Hufnagel CA, McClenathan JE, Moser KM: Chronic thrombosis obstruction of major pulmonary arteries. Am J Med 35:269-282, 1963 11 Moor GF, Sabiston DC: Embolectomy for chronic pulmonary embolism and hypertension. Circulation 41:701708, 1970 12 Moser KM, Rhodes PG, Hufnagel CA: Chronic unilateral
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pulmonary artery thrombosis. N Engl J Med 272: 11951199, 1965 Castleman B: Case records of the Massachusetts General Hospital. N Engl J Med 271:40-50, 1964 Moser KM, Houk VN, Jones RC, Hufnagel CA: Chronic massive obstruction of the pulmonary arteries. Circulation 32:377-385, 1965 Jones RC, Jones CB, Jahnke EJ: Chronic thrombotic pulmonary artery obstruction due to recurrent embolization. Milit Med 130: 1110-1121, 1965 Frater RWM, Beck W, Schrire V: The syndrome of pulmonary artery aneurysms, pulmonary artery thrombi and peripheral venous thrombi. J THORAC CARDIOVASC SURG 49:330-336, 1965 Makey AR, Bliss BP: Pulmonary embolectomy. Lancet 2:1155-1158,1966 Nash ES, Shapiro S, Landau A, Bamard CN: Successful thrombo-embolectomy in longstanding thrombo-embolic pulmonary hypertension. Thorax 23: 121-130, 1968 Allison PR, Dunnill MS, Marshall R: Pulmonary embolism. Thorax 15:273-283, 1960 Moser KM, Braunwald NS: Successful surgical intervention in severe chronic thromboembolic pulmonary hypertension. Chest 64:29-35, 1973 Tilkian AG, Schroeder JS, Robin ED: Chronic thromboembolic occlusion of main pulmonary artery or primary branches. Am J Med 60:563-573, 1976 Sabiston DC, Wolfe WG, Oldham HN, Wechsler AS, Crawford FA, Jones KW, Jones RH: Surgical management of chronic pulmonary embolism. Ann Surg 185: 699-712,1977 Cabrol C, Cabrol A, Acar J, Gandjbakhch I, Guiraudon G, Laughlin L, Mattei MF, Godeau P: Surgical correction of chronic postembolic obstructions of the pulmonary arteries. J THoRAc CARDIOVASC SURG 76:620-628, 1978 Hammon JW Jr: Discussion of Cabrol et aJ23 Chiu RCJ: Discussion of Cabrol et aJ23
Discussion DR. RICHARD C. SHAW 51. Louis. Mo.
I would like to congratulate Dr. Daily on the development of this surgical technique and on his excellent clinical results. Also I want to express my gratitude to Dr. Daily for his invaluable advice and assistance to me in treating two patients with chronic pulmonary embolism. The clinical histories of my two patients were quite similar to those presented in this report. One is a 30-year-old man who had a history of documented thrombophlebitis and recurrent pulmonary embolization proven by angiography and complicated by unremitting pulmonary hypertension. The second is a 23-year-old woman who was taking oral contraceptives and had well-documented pulmonary embolization resulting in severe pulmonary hypertension. Each underwent pulmonary thromboendarterectomy as described in this report. The patients have now been followed for 3 and 2
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months, respectively, since their embolectomies and are showing the kind of clinical improvement that was described in this paper. I would like to make two comments. First, regarding the incidence of this disease, accurate statistics regarding pulmonary thromboembolism are not readily available. In one series, it was estimated that hundreds of thousands of cases per year occur in the United States. There is a good chance for survival following the initial embolization. If the diagnosis is made and proper treatment instituted, there is an excellent chance for long-term survival. The important point is that there are many patients who have undergone this clinical event and are still alive. From the urokinase intervention study, the time course of resolution of pulmonary thromboemboli is relatively rapid. Most of the thrombi dissolve within the first 2 weeks. However, on follow-up, 23% of these patients will have unresolved emboli at 1 year. Long-term follow-up by autopsy and by lung scan has shown unresolved clots in the pulmonary vasculature in approximately 12% of these patients. This, combined with the number of patients who have pulmonary thromboembolic phenomena, would indicate that a significantly larger number of patients are candidates for this operation than has been recognized previously. Some patients who have been given a diagnosis of primary pulmonary hypertension might be found to have this reversible form of the disease on further investigation. My second comment concerns the histologic appearance of the lung. Biopsy specimens of peripheral lung tissue were obtained in both cases at the time of embolectomy in order to examine the vasculature distal to the emboli. [Slide] This slide demonstrates a pulmonary vessel. It is a pulmonary artery rather than a bronchial artery because it has both an internal and external elastic layer. The vessel is almost completely occluded. [Slide] This slide demonstrates another occluded, very distal vessel. When we initially looked at these findings with our pathologists, our impression was that the occlusion represented intimal hyperplasia as a reaction to long-standing pulmonary hypertension. On further examination using special stains, we have concluded that these represent organized microemboli in the very distal pulmonary vasculature. Evidence for this conclusion included the fact that these changes were found both in lung fields that were perfused under higher pressures and in those areas of the lung that should have been protected by proximal major vessel occlusion. Peripheral microembolization could account for the failure of the pulmonary artery pressure to decrease early in the postoperative course, since there still is significant obstruction of the pulmonary vasculature on the microcirculation level. I believe that this operation and the postoperative clinical Course raise a few questions. As Dr. Daily mentioned, the failure to resolve pulmonary emboli may represent a coagulopathy. In the thrombosis-thrombolysis continuum, there may be a deficiency in thrombolysis, and it would seem that further investigation is indicated. Finally, what is the future for these patients? What mechanism accounts for clinical
improvement in the face of an obstructed microcirculation? Follow-up histologic data at a time remote from the operation would be very valuable. DR. DANIEL SMITH Denver, Colo.
I wish to compliment the authors on their results in a group of patients who are doomed without surgical intervention. I would like to support their paper with a single, welldocumented, and successfully treated case with a 4\12 year follow-up and use this case to highlight a couple of points which we feel are important in the disease process. The patient was a 29-year-old white man who was transferred to the Veterans Administration Hospital in San Francisco, California, under the care of Dr. Daniel Ullyot and me in October of 1974 for treatment of right heart failure. The patient had been in good health until he was involved in an automobile accident in April, 1969, in which he incurred a T 12 , L1 vertebral fracture with concomitant lower extremity partial paresis. Elimination difficulty secondary to his neurologic deficit led to an end sigmoid colostomy and a suprapubic cystostomy in June of 1972. Twenty-two days after his discharge from the hospital, which was 30 days after his operative procedure, he returned to that hospital because of pleuritic pain. A lung scan showed no perfusion to the right middle (RML) and right lower lobes (RLL). Over the next several months, he had two more episodes of chest pain, and lung scans showed small defects in the left lung in addition to persistent absence of perfusion to the RML and RLL. In October of 1973, a Miles clip was placed across the inferior vena cava, and he had no further episode of chest pain. However, in March of 1974, he was beginning to show evidence of pulmonary hypertension on chest roentgenogram and electrocardiogram. By October, he was hypoxic, confused, and in frank right ventricular failure. He was transferred to our case where he underwent right heart catheterization and pulmonary angiography. The pulmonary angiogram showed the absence of perfusion to the RLL and RML. Other projections showed that there was also no perfusion of a segment of the RUL, and there were some irregular filling defects in the left lung. A right pulmonary artery thromboendarterectomy was performed with the aid of cardiopulmonary bypass. The right main pulmonary artery was exposed intrapleurally, as described by the authors. An intact cast of the primary and secondary pulmonary arteries was removed, and brisk arterial back bleeding resulted. The postoperative course was complicated by hemorrhagic pneumonitis of the RML and RLL, which is a very common occurrence following this procedure, but this resolved over a 2 week period. Two months postoperatively we restudied the patient. [Slide] The lung scan shows reperfusion on the right side. [Slide] The arteriogram shows perfusion of the RML and RLL. [Slide] This slide compares the pre- and postoperative catheterization data. The systolic pulmonary artery pressure had decreased from 110 torr preoperatively to 45 torr, 2 months postoperatively. The cardiac output had almost dou-
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bled, and the total pulmonary resistance had dropped from 29 to 5.8 Wood units. The patient is presently alive, clinically in Class II by the New York Heart Classification, 4V2 years postoperatively. Dr. Ullyot has informed me that he restudied the patient at 46 months and the postoperative data remained as they were at 2 months. I would like to make several points: First, in regard to the cause of this disease process (something that Dr. Daily alluded to), Dr. Sabiston has hypothesized and shown experimentally that it is the age of the thrombus, that is, its organized, fibrotic character when embolized, that prevents the "older emboli" from being handled by the normal fibrinolytic process. Our case supports this concept. If you accept the hypothesis that the plebothrombosis occurred in the perioperative period, the first and most significant pulmonary embolus occurred 30 days following the colostomy and cystostomy. My second point concerns the progressive nature of the clinical course, and I guess this is somewhat at variance with what Dr. Shaw has just said. The major hemodynamic effect of a pulmonary embolus is mechanical. Fifty to 60 percent of the pulmonary arterial vascular tree must be obstructed acutely in an otherwise normal cardiovascular system before serious hemodynamic effects occur. With less than this critical mass effect, another process analogous to the left-to-right shunt in congenital heart disease probably occurs. The arterioles of the unobstructed pulmonary vascular tree are exposed to increased flow which, in tum, causes arteriole con-
53 1
stncnon, further increasing pulmonary artery pressure and leading eventually to right ventricular strain. Although our patient stopped having emboli 12 months prior to his thromboendarterectomy, his right ventricular failure was progressive over the following year. Similarly, when the major portion of the obstruction was surgically relieved, the process was reversed. The pre-endarterectomy pulmonary artery pressure of 95 torr at the time of operation dropped to 75 torr immediately after the operation. Two months later it had dropped to 45 torr. My third point is somewhat technical. We used a coronary artery endarterectomy spatula through which carbon dioxide was flowing at a rate of 10 Llmin. We found this to be very helpful in developing the endarterectomy plane and extracting an intact core.
DR. 0 A I L Y (Closing) I would like to thank both discussers for their comments. I am afraid Dr. Shaw's question, "What causes this disease?, " will have to go unanswered. Obviously, there is no answer for that. That is, why should most patients have rapid resolution of their emboli while a small minority do not. Finally, as to the future course of these patients, so few have been operated upon that we have not had the opportunity to follow them longitudinally to see what the long-term results will be. That, of course, will be of interest, but their clinical status at the time of operation usually is such that there really is no alternative to thromboendarterectomy. We will simply have to observe the late surgical results.
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CARDIOV ASC SURG
79:523-531, 1980
Surgical management of chronic pulmonary embolism Surgical treatment and late results Failure of pulmonary emboli to undergo fibrinolytic resolution generates a small but significant patient population progressively disabled by hypoxemia, chronic pulmonary hypertension, and eventual right heart failure. Medical management of these patients has not been effective. In the few patients treated surgically, no clear picture has emerged regarding the most effective surgical approach or the late results. Four male patients with chronic pulmonary embolism were managed operatively. Extrapericardial dissection, cardiopulmonary bypass, deep hypothermia, and intermittent circulatory arrest were utilized to perform pulmonary thromboendarterectomy. All patients, ages 30 to 65 years, had had severe dyspnea with minimal exertion for I to 20 years. Angiograms showed 50% to 75% of the pulmonary vasculature to be occluded, with frequent involvement of the segmental arteries. Preoperative pulmonary pressures varied from 60/33 to 74/24 mm Hg. Pulmonary vascular resistance values ranged from 450 to 750 dynes-sec-em:". All patients survived the operative procedure. The eldest patient died 3 weeks postoperatively following an acute posteroseptal myocardial infarction. The remaining patients had a 20 to 50 mm Hg decrease in pulmonary systolic pressure with a 50% to 75% reduction in pulmonary vascular resistance. Neither static nor dynamic lung volumes were changed appreciably. Follow-up angiograms in all patients confirmed significant increase in pulmonary perfusion. Each patient had improvement in functional capacity; one is completely asymptomatic. The primary advantage of the surgical approach described is the more complete removal of distally located thrombofibrotic material. The late results suggest that this surgical approach should be considered in the management of patients disabled by chronic pulmonary embolism.
Pat O. Daily, M.D.,* G. Gilbert Johnston, M.D.,* Cecile J. Simmons,* and Kenneth M. Moser, M.D., ** San Diego, Calif.
Chronic pulmonary hypertension subsequent to massive and repeated pulmonary embolism is infrequently observed. Attempts to relieve chronic pulmonary artery obstruction surgically have been reported even less frequently. Even so, a variety of surgical approaches have been described with variable results. However, no single surgical approach previously reported has allowed reasonable access to most major pulmonary arteries. This report describes a surgical procedure which affords exposure of the main pulmonary artery, both right Read at the Fifth Annual Meeting of The Samson Thoracic Surgical Society, Sun Valley, Idaho, June 5 to 8, 1979. Address for reprints: Pat O. Daily, M.D., 7930 Frost St., Suite 305, San Diego, Calif. 92123. *Donald N. Sharp Memorial Community Hospital, San Diego, Calif. **Professor and Head, Pulmonary Division, University Hospital, San Diego, Calif.
and left pulmonary arteries, and the lobar branches of each. Its applicability and results are described in four patients. Methods and patients Four male patients, ages 40, 32, 65, and 33 years, underwent pulmonary thromboendarterectomy between Feb. 1, 1975, and May 4, 1978. All procedures were performed through a median sternotomy with standard cardiopulmonary bypass. After the pericardium was suspended, the superior and inferior venae cavae were encircled with umbilical tapes passed through lengths of soft rubber tubing. The superior and inferior venae cavae were cannulated with 7 mm Polystan cannulas inserted through the right atrium, and the ascending aorta was cannulated with a 6.5 mm Sams cannula. On both the right and left sides, the pericardium was divided down to the pulmonary arteries. The phrenic
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Table I
Pa02 (mm Hg)* Case No.
1 2
3 4
Age (yr)
Preop.
40 32 65
42 46 53 65
33
I
Pulmonary artery pressure (mm Hg)
Postop .
Preop.
66 71 58 74
60/33 74/25 70/36 65/29
I
Pulmonary vascular resistance (dynessec-cm-O)
Postop.
Preop.
37/7 24/6 88/48 43/22
450 756 620 480
I
Postop.
136 124 743 248
*Systemic arterial blood was analyzed. Flo, = 0.20.
nerves were identified and retracted anteriorly with umbilical tapes. On the right side, the superior vena cava was dissected superiorly to the azygos vein and then retracted anteriorly to increase exposure of the right pulmonary artery (Fig. 1). On that side, a pulmonary arteriotomy was performed in the right upper lobe (RUL) artery and also in the pulmonary artery distal to the RUL branch. The superior pulmonary vein was retracted inferiorly to improve exposure of the right upper and intermediate pulmonary arteries (Fig. 1). On the left, a single arteriotomy was utilized, beginning just outside the pericardium and extending distally (Fig. 1). Once exposed, the occluding material was removed with an endarterectomy spatula. In the last three cases it was necessary to utilize deep hypothermia with circulatory arrest to control severe back bleeding from the endarterectomized arteries.
Case reports and results CASE 1. A 40-year-old laborer sustained a spinal injury at the level of the seventh cervical vertebra in January of 1974, which resulted in a mild Brown-Sequard syndrome. He was first admitted to University Hospital the following December complaining of severe shortness of breath. He was dyspneic at rest, had great difficulty dressing himself, and could ambulate less than one half block. There was no history of chest pain, hemoptysis, or cough and there were no symptoms of lower extremity edema or pain. Physical examination revealed a thin, afebrile, normotensive, dyspneic black man. Marked jugulovenous distention, a prominent P2 accentuation with a loud S3 gallop, and a soft holosystolic tricuspid murmur were observed. The liver spanned 15 em and a hepatojugular reflex was present. A moderate right hemiparesis with atrophy and patchy left hemihyperesthesia was noted. P0 2 was 40 mm Hg with the patient breathing room air, and ventilation-perfusion scans were indicative of multiple, bilateral pulmonary emboli. Venograms demonstrated thrombosis of the right iliac and femoral veins. The patient was treated for 6 weeks with a constant intravenous infusion of heparin without appreciable improvement. Results of subsequent right heart catheterization are presented in Table I. Pulmonary angiograms revealed large, organized thromboemboli in both the right and left pulmonary artery
bifurcations with near-total occlusion of flow to both lower lobes. Operation was performed on Feb. I, 1975. Opening the right pulmonary artery exposed a large, densely adherent thrombus just distal to the RUL branch. This thrombus was successfully extracted by endarterectomy. The left pulmonary artery was obstructed by a similar fibrinous mass at the junction of the left upper lobe (LUL) artery, with inferior extension into the lower lobe segmental branches which could not be adequately cleared. Hypothermia with circulatory arrest was not utilized. A Moretz clip was applied to the vena cava. By the third postoperative week the P0 2 was 65 mm Hg with the patient breating room air, and he experienced progressive subjective improvement as well as increased strength and stamina. Results of catheterization are summarized in Table 1. Repeat pulmonary arteriograms performed in January of 1976 revealed significantly increased pulmonary blood flow, particularly to the right lower lobe (RLL) and left upper lobe (LUL). Additionally, the heart size was significantly smaller postoperatively as compared to preoperatively (Figs. 2 and 3). He has remained asymptomatic from a cardiovascular standpoint. CASE 2. A 32-year-old architectural engineer apparently first developed deep venous thrombosis early in 1974 following a skiing injury. No treatment was initiated. In October, 1974, he had an acute episode of severe substernal discomfort, weakness, diaphoresis, and dyspnea, which was diagnosed as asthma. He remained markedly disabled through late 1974, when extensive pulmonary occlusion was documented and anticoagulation was begun. He noted modest improvement and warfarin sodium (Coumadin) therapy was continued through June, 1975. The man experienced no further symptoms of deep venous thrombosis but remained disabled, being unable to walk more than 50 feet without having to rest. He was unable to maintain a normal work schedule and was referred to the University of California Medical Center, San Diego, California, in June of 1976. Physical examination revealed a thin, normotensive, afebrile white man who became dyspneic from disrobing. There was no cyanosis, clubbing, or edema. Three separate murmurs, which increased with inspiration and decreased with expiration, were audible in the peripheral lung fields. A palpable right ventricular heave was present, and pulmonic closure with a prominent systolic ejection murmur along the left sternal border and a fixed-split S2 was observed. The liver's edge was palpable and nontender and spanned 11 em. There were no stigmata of lower extremity venous disease. Pertinent laboratory and catheterization data are presented
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Fig. 2. Case I. Chest x-ray film taken 4 week s preoperatively .
Fig. 1. Surgic al approach showing incisions in pericardium with retraction of phrenic nerves and incision s in pulmonary arteries. in Table I. Preoperative pulmonary arteriograms are illustrated in Fig . 4. The patient was subjected to pulmonary endarterectomy in July. 1976, by means of the technique described previou sly . No residual thrombus was present within the right pulmonary artery , but the wall was markedly thickened and fibrotic material was removed from the almost completely occluded origin of the right middle lobe (RML) artery . A large, well-organized , den sely adherent thrombus wasdissected from the left main pulmonary artery as well as itslobar and several segmental branches (Fig . 5). Circulatory arrest was performed for 61f2 and 81f2 minutes . The patient made a rapid and uncomplicated recovery and was discharged on a regimen of 5,000 U of heparin administered subcutaneously twice a day. He obtained dramatic improvement in his functional capacity . The results of follow-up pulmonary angiograms with right heart catheterization obtained 4 months postoperatively are presented in Table I and Fig. 6. The man elected to discontinue his subcutaneous heparin 1herapy after 6 months, and shortly thereafter exten sive deep venous thrombosis redeveloped in the right leg with extension into the inferior vena cava . Therapeutic anticoagulation was .Jministered and the inferior cava was clipped . No evidence
Fig. 3. Case I . Chest x-ray film taken 47 months postoperatively showing significant decrease in heart size. of recurrent embolization was found, and at present he is essentially asymptomatic except for mild residual swelling of the right leg . C A S E 3 . A 65-year-old retired contractor was admitted in September of 1976, following 20 years of respiratory illness. He remembered multiple bout s of pneumonia in adolescence, and after World War II he had several episodes of respiratory infection with associated hemoptysis . Five years before admission he began to experience intermittent chest pain ,
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Fig. 4. Case 2. Preoperative pulmonary arteriogram. There is marked reduction in pulmonary blood flow with minimal perfusion of the upper and lower lobes bilaterally . hemoptysis , and increasing dyspnea and had two myocardial infarctions. At the time of admission he led a bed-to-chair existence requiring constant oxygen supplementation . Physical examination revealed an afebrile extremely tachypneic, cyanotic white man with clubbed fingers and toes. There were diminished respiratory excursions and scattered rales throughout both lung fields. A systolic outflow murmur was present along the left sternal border without gallops , thrills, or increased P2. There was no organomegaly , but 1+ ankle edema was present bilaterally. Chest films demonstrated huge pulmonary arteries with scattered zones of parenchymal fibrosis . P0 2 with the patient breathing room air was less than 50 mm Hg. Pulmonary angiograrns showed numerous mural irregularities, occlusion of the RML artery, but no acute proximal thromb i. Results of right-sided catheterization are shown in Table 1. Left heart catheterization revealed a left ventricular end-diastolic pressure of 15 mm Hg, reduced ejection fraction, a high-grade stenos is of the right coronary artery , and total occlusion of the circumflex coronary artery beyond the first marg inal branch with no visualization of the distal artery . At operation the right side of the heart appeared to be twice the size of the left. A large amount of free thrombu s was found within the lumen of the right pulmonary artery . It extended into and occluded the lower lobe arter ies, with a fibrinous membrane obstructing those of the RML. A similar combination of old and recent thrombus was evacuated from the left pulmonary system , after which a saphenous vein graft was placed from the aorta to the distal right coronary artery . Circulatory arrest occurred for 30 minutes and 13 minutes. The patient required pharmacologic support to be weaned from cardiopulmonary bypass , and he exhibited a low cardiac output in the initial postoperative period although there was no electrocardiographic or enzymatic evidence of perioperative infarction .
Fig. 5. Case 2. Surgical specimen removed from left lower lobe pulmonary artery . Note extensions from main thrombus corre sponding to segmental arterial branches. He was extubated on the fourth postoperati ve day with a P0 2 greater than 50 mm Hg while breathing room air. However , I week postoperatively he developed left lower lobe (LLL ) Klebsiella pneumonia , sepsis, and respiratory failure necessitating prolonged ventilatory support and eventual tracheostomy. Postoperative anticoagulation was discontinued owing to gastrointestinal bleeding. By the third postoperative week he no longer required mechan ical ventilation , and antibiotic s were discontinued . His stools were Hematest negative and he was beginning ambulation when he suddenly became hypotensive and developed atrioventricular dissociation and subsequent anuria. Resuscitative efforts over the next 24 hours were unsuccessful and he died on postoperati ve day 25. Postmortem examination revealed recent , recurrent , nonobstructing pulmonary thrombi compromising the chronic obliteration of the peripheral pulmonary arteries . The cause of death was a large , acute , posteroseptal myocardial infarction. The aorta-coronary artery vein graft was patent and the anastomosis was unremarkable. CASE 4. A 33-year-old black man first complained of easy fatigability and progressive shortness of breath at the age of 23 years. In 1970 he was hospitalized elsewhere where he exhibited dyspnea after walking half a block and was unable to climb stairs. Right heart catheterization revealed a pulmo-
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nary pressure of 95/45 mm Hg , and an angiographic diagnosis of recurrent pulmonary embolism was made . A Moretz clip was placed across the inferior vena cava in February, 1970. The patient was maintained on anticoagulation, which produced a modest improvement. Through late 1973, he was admitted on multiple occasions for recurrent painless hemop tysis , increasing dyspnea, and progressive decrease in exercise tolerance. After 1974 he remained clinically stable but had to limit his activity severely and could not find employment. He was referred for pulmonary thromboendarterectomy in January of 1978. Preoperative angiograms showed an old thromboembolic mass beginning in the left main pulmonary artery and extending downward into the lower lobe branches. There were mural irregularities on the right side but no filling defects. On physical examination he was afebrile, normotensive, acyanotic , and comfortable at rest without digital clubbing. There were loud, distinct, peripheral pulmonary bruits over the LLL and RUL with a right ventricular heave , a palpable P2, but no significant cardiac murmurs, and no evidence of lower extremity venous disease. Results of repeat catheterization are shown in Table I. Thromboendarterectomy was performed on May 4 , 1978. Minimal material was removed from the right side , but both recent and old thrombotic material was encountered on the left, totally occluding the distal left pulmonary artery, and its extraction opened multiple branches to both lobes. Circulatory arrest was performed for 5 minutes, 19 minutes, and 29 minutes . The postoperative convalescence was uncomplicated , and at I year his ergometrically measured exercise tolerance had increased from a preoperative value of less than 7 minutes to 27 minutes. Results of catheterization 1 year postoperatively are given in Table I. Postoperative angiography revealed modest improvement in perfusion of the right lung, with the most significant return of flow to the LLL.
Pathology Surgical specimens were quite heterogeneous, varying from pigmented, fibrogelatinous material to large, well-organized, fibrous "casts" with pseudocapsules. Much of the material was freed by sharp dissection and was somewhat friable. It consisted of fibroconnective tissue , which contained recanalized, hyaline connective tissue, scattered foci of inflammatory cells, and the intimal layer of the vessel wall. The total amount of material recovered ranged from 47 gm (Case 1) to 280 gm (Case 2).
Discussion Rapid and essentially complete resolution of pulmonary emboli, after even massive pulmonary embolism, is the usual natural history. This has been reported experimentally by Moser and associates! and clinically by Fred ," Dalen ," and their colleagues. However, rarely, persistent emboli and recurrent emboli may lead to significant clinical disability including cor pulmonale. Although the exact incidence of this aspect of pulmonary embolism is unknown, Paraskos and associates"
Fig. 6. Case 2. Postoperative pulmonary arteriogram. There is significantly increased perfusion of the right pulmonary arter ies and markedly increased perfu sion of the left lower lobe artery .
found only one instance of angiographically proved pulmonary embolism progressing to chronic cor pulmonale in 60 cases. The causes of this manifestation of pulmonary embolism are uncertain, but Dalen and Alpert" have suggested that recurrent pulmonary embolism represents a more likely explanation than failure of resolution after a single , massive episode of pulmonary embolism. It is conceivable that the pathological nature of the embolic material with respect to the degree of fibrosis may be of importance in affecting resolution. While performing pulmonary embolectomies, one of us (P. O. D.) has encountered pulmonary emboli ranging from recent, relatively fresh thrombi to extremely fibrotic, highly organized ones. In any event, mechanical obstruction of the pulmonary vasculature rather than reflex vasoconstriction is the predominant mechanism." The feasibility of embolectomy or endarterectomy for chronic pulmonary embolism was suggested in 1956 by Hollister and CulJ.7 Although Hurwitt and associates" reported the attempted removal of chronic pulmonary emboli in 1958, the first successful pulmonary endarterectomy was described in 1963 by Snyder, Kent, and Baisch." In the same year Houk and associates" related a similar case . By 1970 Moor and Sabiston!' had tabulated only 11 instances l l - ! 8of removal of chronic pulmonary emboli, seven of the patients surviving. (The case of Allison and associates" was excluded, since only 13 days elapsed from the onset of symptoms until pulmonary embolectomy was performed .) An additional successful case was reported by Moser and Braunwald'" in 1973. Consequently, in 1976 Tilkian, Schroeder, and
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Robin;" basing their recommendation in part on the previous surgical experience, advocated anticoagulation therapy for chronic pulmonary thromboembolic disease. In 1977 Sabiston and associates'" updated their report of 1970 10 with an additional five patients, all of whom survived, with only one obtaining a poor result; this result was related to occlusion of the smaller pulmonary arteries as evidenced by a lack of "back bleeding" from the distal pulmonary arteries at operation. In a recent report, Cabrol and associates'" described 16 additional cases of operations for chronic postembolic obstruction of the pulmonary arteries. Six operative deaths occurred. Nine of the ten survivors had a good result. In the discussion of that paper, Hammon>' added two cases to the Duke University experience and Chiu'" described another. Thus it appears that to date the English literature contains 36 case reports of surgical procedures for removal of chronic pulmonary emboli. No single surgical approach has emerged as the preferable one. Median sternotomy has been utilized only five times. 14. 21. 23 Cabrol and associates.P after using median sternotomy and cardiopulmonary bypass, stated, "It was impossible by that route to free the peripheral pulmonary trunks, and both patients died postoperatively. " Consequently, in their next 14 cases they approached the most severely affected side through a lateral thoracotomy, using cardiopulmonary bypass when needed for circulatory support. This experience caused them to state, "It is as illogical to attempt to remove chronic thrombi from the pulmonary artery through a central approach as it is to free the femoral arteries through an approach at the aortic bifurcation. " Our experience has shown that division of the pericardium, bilaterally, to the pulmonary arteries with retraction of the phrenic nerves permits direct exposure of all lobar arteries as well as some of the segmental arteries of the lower lobes. On the right side, exposure is facilitated by dissection of the superior vena cava with anterior retraction and retraction of the superior pulmonary vein inferiorly. With this approach, incisions in the pulmonary arteries may be placed where necessary. Advantages of this surgical approach are as follows: Equal access is provided to either side with a single surgical procedure. More complete removal of the chronically obstructing material can be accomplished, so that the postoperative result is optimized. Extensive dissection of frequently vascular pleural adhesions is minimized. Other cardiac procedures can be performed if necessary, such as coronary artery bypass grafting as
The Journal of Thoracic and Cardiovascular Surgery
in Case 3. Finally, this method can be used for removal of acute pulmonary emboli and should result in the more complete removal of distally impacted emboli. In all four cases presented the emboli were markedly adherent, so that endarterectomy procedures were necessary. Also, frequently the occluding thrombi were found to extend distally into the segmental branches. Significant back bleeding occurred when these branches were freed, as described by Sabiston. H • 22 Hypothermia to 20° C with brief periods of circulatory arrest, as described in Cases 2, 3, and 4, greatly facilitated removal of the adherent, distally located emboli. No complications related to hypothermia occurred. The primary indications for operation in this series have been severe dyspnea at rest or with minimal exertion and pulmonary hypertension (i.e., greater than 50 mm Hg systolic). The definitive diagnosis is based upon the pulmonary arteriograms which, in order to indicate operation, should reveal proximal obstruction at least at the lobar level. Bronchial arteriography, as suggested by Sabiston.P Cabrol.P and their colleagues, was not performed because we thought that failure to visualize the distal pulmonary arteries would not represent an absolute contraindication to operation in severely disabled patients. On the basis of the present experience, providing the indications are met, we suggest the only contraindication is serious concomitant cardiopulmonary disease, as in Case 3. Of the long-term survivors reported to date, including those of this report, all but two (25 of 27) have obtained significant symptomatic improvement and several have become asymptomatic. It is not necessary to remove all of the occluding material in order to afford considerable relief of symptoms. However, Case 3 illustrates that careful selection is important, particularly with respect to associated cardiopulmonary disease. As mentioned, the patient described in Case 3 had had two previous myocardial infarctions. Coronary arteriography revealed high-grade right coronary artery stenosis and total occlusion of the circumflex coronary artery, with no distal artery visualized. The cause of death on the Postoperative day 25 was acute posteroseptal myocardial infarction, the area supplied by the nongrafted circumflex coronary artery. The right coronary artery graft was patent. An additional significant finding was that of recent thrombi in the pulmonary arteries. This correlates with an increase in the pulmonary artery pressure from 70/36 mm Hg preoperatively to 88/48 mm Hg postoperatively. (All other patients experienced a significant drop in pulmonary artery pressure postoperatively.) While it was not possible to
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distinguish postoperative in situ thrombosis from repeated pulmonary embolism, it seems logical to strongly endorse vena caval clipping or ligation at the time of thromboendarterectomy, as suggested by Sabiston,22 Cabrol.f" and their co-workers. This is further emphasized by the necessity to clip the inferior vena cava postoperatively in Case 2.
13 14
15
Conclusion A small but significantly disabled group of patients has pulmonary hypertension resulting from chronic thromboembolic occlusion of the pulmonary arteries. A surgical approach is described which, at a single operation, allows exploration and removal of thromboembolic material from all of the lobar arteries. The late results suggest that increased effort should be directed toward identification and surgical management of these patients. REFERENCES Moser KM, Guisan M, Bartimmo EE: In vivo and post mortem dissolution rates of pulmonary emboli and venous thrombi in the leg. Circulation 48: 170-178, 1973 2 Fred HL, Axelrad MA, Lewis JM, Alexander JK: Rapid resolution of pulmonary thromboemboli in man. JAMA 196:121-123, 1966 3 Dalen JE, Banas JS, Brooks HL, Evans GL, Paraskos JA, Dexter L: Resolution rate of acute pulmonary embolism in man. N Engl J Med 280:1194-1199,1969 4 Paraskos JA, Adelstein SJ, Smith RE, Rickman FD, Grossman WG, Dexter L, Dalen JE: Late prognosis of acute pulmonary embolism. N Engl J Med 289:55-58, 1973 5 Dalen JE, Alpert JS: Natural history of pulmonary embolism. Prog Cardiovasc Dis 17:259-270,1975 6 Daily PO, Lancaster JR, Moulder PV: The mechanism of pulmonary hypertension following miliary pulmonary embolism. Surg Gynecol Obstet 120:1009-1018, 1965 7 Hollister LE, Cull VL: The syndrome of chronic thrombosis of the major pulmonary arteries. Am J Med 21:312-320, 1956 8 Hurwitt ES, Schein CJ, Rifkin H, Lebendiger A: A surgical approach to the problem of chronic pulmonary artery obstruction due to thrombosis or stenosis. Am Surg 147:157-165, 1958 9 Snyder WA, Kent DC, Baisch BF: Successful endarterectomy of chronically occluded pulmonary artery. J THORAC CARDIOVASC SURG 45:482-489, 1963 10 Houk VN, Hufnagel CA, McClenathan JE, Moser KM: Chronic thrombosis obstruction of major pulmonary arteries. Am J Med 35:269-282, 1963 11 Moor GF, Sabiston DC: Embolectomy for chronic pulmonary embolism and hypertension. Circulation 41:701708, 1970 12 Moser KM, Rhodes PG, Hufnagel CA: Chronic unilateral
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17 18
19 20
21
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23
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pulmonary artery thrombosis. N Engl J Med 272: 11951199, 1965 Castleman B: Case records of the Massachusetts General Hospital. N Engl J Med 271:40-50, 1964 Moser KM, Houk VN, Jones RC, Hufnagel CA: Chronic massive obstruction of the pulmonary arteries. Circulation 32:377-385, 1965 Jones RC, Jones CB, Jahnke EJ: Chronic thrombotic pulmonary artery obstruction due to recurrent embolization. Milit Med 130: 1110-1121, 1965 Frater RWM, Beck W, Schrire V: The syndrome of pulmonary artery aneurysms, pulmonary artery thrombi and peripheral venous thrombi. J THORAC CARDIOVASC SURG 49:330-336, 1965 Makey AR, Bliss BP: Pulmonary embolectomy. Lancet 2:1155-1158,1966 Nash ES, Shapiro S, Landau A, Bamard CN: Successful thrombo-embolectomy in longstanding thrombo-embolic pulmonary hypertension. Thorax 23: 121-130, 1968 Allison PR, Dunnill MS, Marshall R: Pulmonary embolism. Thorax 15:273-283, 1960 Moser KM, Braunwald NS: Successful surgical intervention in severe chronic thromboembolic pulmonary hypertension. Chest 64:29-35, 1973 Tilkian AG, Schroeder JS, Robin ED: Chronic thromboembolic occlusion of main pulmonary artery or primary branches. Am J Med 60:563-573, 1976 Sabiston DC, Wolfe WG, Oldham HN, Wechsler AS, Crawford FA, Jones KW, Jones RH: Surgical management of chronic pulmonary embolism. Ann Surg 185: 699-712,1977 Cabrol C, Cabrol A, Acar J, Gandjbakhch I, Guiraudon G, Laughlin L, Mattei MF, Godeau P: Surgical correction of chronic postembolic obstructions of the pulmonary arteries. J THoRAc CARDIOVASC SURG 76:620-628, 1978 Hammon JW Jr: Discussion of Cabrol et aJ23 Chiu RCJ: Discussion of Cabrol et aJ23
Discussion DR. RICHARD C. SHAW 51. Louis. Mo.
I would like to congratulate Dr. Daily on the development of this surgical technique and on his excellent clinical results. Also I want to express my gratitude to Dr. Daily for his invaluable advice and assistance to me in treating two patients with chronic pulmonary embolism. The clinical histories of my two patients were quite similar to those presented in this report. One is a 30-year-old man who had a history of documented thrombophlebitis and recurrent pulmonary embolization proven by angiography and complicated by unremitting pulmonary hypertension. The second is a 23-year-old woman who was taking oral contraceptives and had well-documented pulmonary embolization resulting in severe pulmonary hypertension. Each underwent pulmonary thromboendarterectomy as described in this report. The patients have now been followed for 3 and 2
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months, respectively, since their embolectomies and are showing the kind of clinical improvement that was described in this paper. I would like to make two comments. First, regarding the incidence of this disease, accurate statistics regarding pulmonary thromboembolism are not readily available. In one series, it was estimated that hundreds of thousands of cases per year occur in the United States. There is a good chance for survival following the initial embolization. If the diagnosis is made and proper treatment instituted, there is an excellent chance for long-term survival. The important point is that there are many patients who have undergone this clinical event and are still alive. From the urokinase intervention study, the time course of resolution of pulmonary thromboemboli is relatively rapid. Most of the thrombi dissolve within the first 2 weeks. However, on follow-up, 23% of these patients will have unresolved emboli at 1 year. Long-term follow-up by autopsy and by lung scan has shown unresolved clots in the pulmonary vasculature in approximately 12% of these patients. This, combined with the number of patients who have pulmonary thromboembolic phenomena, would indicate that a significantly larger number of patients are candidates for this operation than has been recognized previously. Some patients who have been given a diagnosis of primary pulmonary hypertension might be found to have this reversible form of the disease on further investigation. My second comment concerns the histologic appearance of the lung. Biopsy specimens of peripheral lung tissue were obtained in both cases at the time of embolectomy in order to examine the vasculature distal to the emboli. [Slide] This slide demonstrates a pulmonary vessel. It is a pulmonary artery rather than a bronchial artery because it has both an internal and external elastic layer. The vessel is almost completely occluded. [Slide] This slide demonstrates another occluded, very distal vessel. When we initially looked at these findings with our pathologists, our impression was that the occlusion represented intimal hyperplasia as a reaction to long-standing pulmonary hypertension. On further examination using special stains, we have concluded that these represent organized microemboli in the very distal pulmonary vasculature. Evidence for this conclusion included the fact that these changes were found both in lung fields that were perfused under higher pressures and in those areas of the lung that should have been protected by proximal major vessel occlusion. Peripheral microembolization could account for the failure of the pulmonary artery pressure to decrease early in the postoperative course, since there still is significant obstruction of the pulmonary vasculature on the microcirculation level. I believe that this operation and the postoperative clinical Course raise a few questions. As Dr. Daily mentioned, the failure to resolve pulmonary emboli may represent a coagulopathy. In the thrombosis-thrombolysis continuum, there may be a deficiency in thrombolysis, and it would seem that further investigation is indicated. Finally, what is the future for these patients? What mechanism accounts for clinical
improvement in the face of an obstructed microcirculation? Follow-up histologic data at a time remote from the operation would be very valuable. DR. DANIEL SMITH Denver, Colo.
I wish to compliment the authors on their results in a group of patients who are doomed without surgical intervention. I would like to support their paper with a single, welldocumented, and successfully treated case with a 4\12 year follow-up and use this case to highlight a couple of points which we feel are important in the disease process. The patient was a 29-year-old white man who was transferred to the Veterans Administration Hospital in San Francisco, California, under the care of Dr. Daniel Ullyot and me in October of 1974 for treatment of right heart failure. The patient had been in good health until he was involved in an automobile accident in April, 1969, in which he incurred a T 12 , L1 vertebral fracture with concomitant lower extremity partial paresis. Elimination difficulty secondary to his neurologic deficit led to an end sigmoid colostomy and a suprapubic cystostomy in June of 1972. Twenty-two days after his discharge from the hospital, which was 30 days after his operative procedure, he returned to that hospital because of pleuritic pain. A lung scan showed no perfusion to the right middle (RML) and right lower lobes (RLL). Over the next several months, he had two more episodes of chest pain, and lung scans showed small defects in the left lung in addition to persistent absence of perfusion to the RML and RLL. In October of 1973, a Miles clip was placed across the inferior vena cava, and he had no further episode of chest pain. However, in March of 1974, he was beginning to show evidence of pulmonary hypertension on chest roentgenogram and electrocardiogram. By October, he was hypoxic, confused, and in frank right ventricular failure. He was transferred to our case where he underwent right heart catheterization and pulmonary angiography. The pulmonary angiogram showed the absence of perfusion to the RLL and RML. Other projections showed that there was also no perfusion of a segment of the RUL, and there were some irregular filling defects in the left lung. A right pulmonary artery thromboendarterectomy was performed with the aid of cardiopulmonary bypass. The right main pulmonary artery was exposed intrapleurally, as described by the authors. An intact cast of the primary and secondary pulmonary arteries was removed, and brisk arterial back bleeding resulted. The postoperative course was complicated by hemorrhagic pneumonitis of the RML and RLL, which is a very common occurrence following this procedure, but this resolved over a 2 week period. Two months postoperatively we restudied the patient. [Slide] The lung scan shows reperfusion on the right side. [Slide] The arteriogram shows perfusion of the RML and RLL. [Slide] This slide compares the pre- and postoperative catheterization data. The systolic pulmonary artery pressure had decreased from 110 torr preoperatively to 45 torr, 2 months postoperatively. The cardiac output had almost dou-
Volume 79
Chronic pulmonary embolism
Number 4 April,1980
bled, and the total pulmonary resistance had dropped from 29 to 5.8 Wood units. The patient is presently alive, clinically in Class II by the New York Heart Classification, 4V2 years postoperatively. Dr. Ullyot has informed me that he restudied the patient at 46 months and the postoperative data remained as they were at 2 months. I would like to make several points: First, in regard to the cause of this disease process (something that Dr. Daily alluded to), Dr. Sabiston has hypothesized and shown experimentally that it is the age of the thrombus, that is, its organized, fibrotic character when embolized, that prevents the "older emboli" from being handled by the normal fibrinolytic process. Our case supports this concept. If you accept the hypothesis that the plebothrombosis occurred in the perioperative period, the first and most significant pulmonary embolus occurred 30 days following the colostomy and cystostomy. My second point concerns the progressive nature of the clinical course, and I guess this is somewhat at variance with what Dr. Shaw has just said. The major hemodynamic effect of a pulmonary embolus is mechanical. Fifty to 60 percent of the pulmonary arterial vascular tree must be obstructed acutely in an otherwise normal cardiovascular system before serious hemodynamic effects occur. With less than this critical mass effect, another process analogous to the left-to-right shunt in congenital heart disease probably occurs. The arterioles of the unobstructed pulmonary vascular tree are exposed to increased flow which, in tum, causes arteriole con-
53 1
stncnon, further increasing pulmonary artery pressure and leading eventually to right ventricular strain. Although our patient stopped having emboli 12 months prior to his thromboendarterectomy, his right ventricular failure was progressive over the following year. Similarly, when the major portion of the obstruction was surgically relieved, the process was reversed. The pre-endarterectomy pulmonary artery pressure of 95 torr at the time of operation dropped to 75 torr immediately after the operation. Two months later it had dropped to 45 torr. My third point is somewhat technical. We used a coronary artery endarterectomy spatula through which carbon dioxide was flowing at a rate of 10 Llmin. We found this to be very helpful in developing the endarterectomy plane and extracting an intact core.
DR. 0 A I L Y (Closing) I would like to thank both discussers for their comments. I am afraid Dr. Shaw's question, "What causes this disease?, " will have to go unanswered. Obviously, there is no answer for that. That is, why should most patients have rapid resolution of their emboli while a small minority do not. Finally, as to the future course of these patients, so few have been operated upon that we have not had the opportunity to follow them longitudinally to see what the long-term results will be. That, of course, will be of interest, but their clinical status at the time of operation usually is such that there really is no alternative to thromboendarterectomy. We will simply have to observe the late surgical results.
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