Published ahead of print on June 12, 2008, doi:10.1164/rccm.200801-101OC
American Journal of Respiratory and Critical Care Medicine Vol 178. pp. 419-424, (2008)
© 2008 American Thoracic Society
doi: 10.1164/rccm.200801-101OC
Long-term Outcome after Pulmonary Endarterectomy
Angelo G. Corsico1,
Andrea M. D'Armini2,
Isa Cerveri1,
Catherine Klersy3,
Elena Ansaldo1,
Rosanna Niniano1,
Elena Gatto1,
Cristian Monterosso2,
Marco Morsolini2,
Salvatore Nicolardi2,
Corrado Tramontin2,
Ernesto Pozzi1 and
Mario Viganò2
1 Division of Respiratory Diseases, 2 Division of Cardiac Surgery, and 3 Service of Biometry and Clinical Epidemiology, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy
Correspondence and requests for reprints should be addressed to Isa Cerveri, M.D., Clinica di Malattie dell'Apparato Respiratorio, Fondazione IRCCS Policlinico San Matteo, via Taramelli 5, 27100 Pavia, Italy. E-mail: icerveri{at}smatteo.pv.it
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ABSTRACT
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Rationale: There are few follow-up studies on long-term cardiopulmonary function after pulmonary endarterectomy (PEA), the operation of choice for chronic thromboembolic pulmonary hypertension (CTEPH).
Objectives: To prospectively evaluate long-term outcome of patients with CTEPH treated with PEA.
Methods: Between 1994 and 2006, 157 patients (mean age 55 yr) were treated with PEA at Pavia University Hospital. The patients were evaluated before PEA and at 3 months (n = 132), 1 year (n = 110), 2 years (n = 86), 3 years (n = 69), and 4 years (n = 49) afterward by NYHA class, right heart hemodynamic, spirometry, carbon monoxide transfer factor (TLCO), arterial blood gas, and treadmill incremental exercise test.
Measurements and Main Results: Cumulative survival was 84%. Within 3 months, 18 patients died in-hospital and 2 had lung transplantation; during long-term follow-up, 6 died, 1 had lung transplantation, and 3 had a second PEA (2.5 events per 100 person-years). NYHA class III–IV was the most important predictor of late death, lung transplant, or PEA redo (hazard ratio, 3.94). Extraordinary improvement in NYHA class, hemodynamic, and PaO2 were achieved in the first 3 months (P < 0.001) and persisted during follow-up; exercise tolerance progressively increased over time (P < 0.001). At 4 years, although 74% of the patients were in NYHA class I and none was in class IV, 24% had pulmonary vascular resistance greater than 500 dyne.s/cm5 or PaO2 less than 60 mm Hg; they were significantly older and were more frequently in NYHA class III–IV 3 months after surgery than the others.
Conclusions: After PEA, long-term survival and cardiopulmonary function recovery is excellent in most patients.
Key Words: chronic thromboembolic pulmonary hypertension • surgery • survival • lung function • hemodynamic
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AT A GLANCE COMMENTARY
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Scientific Knowledge on the Subject
There is substantial agreement on short-term favorable outcome after pulmonary endarterectomy, but there are few follow-up studies on long-term cardiopulmonary function after the operation.
What This Study Adds to the Field
This study provides evidence that long-term survival after pulmonary endarterectomy is excellent and cardiopulmonary function can be almost normalized in most patients.
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Pulmonary endarterectomy (PEA), a conservative surgery for chronic thromboembolic pulmonary hypertension (CTEPH), is the operation of choice because it is considered curative and therefore greatly superior to medical treatment or transplantation for this condition. Current techniques of operation lead this complex procedure to an acceptably low risk of death (1, 2).
At present, there is substantial agreement on favorable outcomes early after PEA with regard to survival, functional status, quality of life, hemodynamics, right ventricular function, and gas exchange (3–9).
There is scant information on long-term effects of PEA on survival, clinical and cardiopulmonary function status, and exercise tolerance. Long-term follow-up studies are challenging both for the largest international referral center (University of California, San Diego [UCSD] Medical Center, San Diego, CA), since patients referred for surgical intervention are from many countries and are difficult to follow subsequently, and for the national centers because of the small number of patients included per year in single institutions. Most of the available follow-up studies have a retrospective design and a small sample size (7, 10–14).
Since 1994 we have collected and organized in a registry prospectively filled information on patients with CTEPH treated with PEA at the Fondazione IRCCS Policlinico San Matteo, University of Pavia, Italy. Our follow-up protocol required examinations before PEA, 3 months after the operation and then yearly for up to 4 years. The program has grown steadily, indicating an increased awareness of the disease and the effectiveness of the treatment. The aims of our prospective study were: (1) to evaluate event-free survival in the short term and in the long term up to 5 years after PEA; (2) to evaluate the clinical and functional changes from surgery to 4 years in survivors; and (3) to evaluate the determinants of the long-term functional outcome in survivors.
Some of the results of this study have been previously reported in the form of abstracts (15–17).
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METHODS
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Pulmonary Endarterectomy
Patients were selected for PEA on the basis of combined clinical, anatomical, and hemodynamic (pulmonary vascular resistance [PVR] > 300 dyne · s/cm5) characteristics. No patient was excluded from our PEA program because of the severity of hemodynamic disease. The standardized protocol for the operation was previously published (18, 19).
Surgical specimens have been classified into four types: (1) fresh thrombus in main-lobar pulmonary arteries; (2) intimal thickening and fibrosis proximal to the segmental arteries; (3) disease within distal segmental arteries only; and (4) distal arteriolar vasculopathy without visible thromboembolic disease (20).
Three months after the operation, PEA was considered to be unsuccessful when PVR was greater than 500 dyne · s/cm5 or there was a drop less than or equal to 50%; otherwise it was considered to be successful. Details on the selection criteria and on the definition of unsuccessful PEA are reported in the online repository.
Definitions of the Endpoints
The endpoints were defined as follows. Short-term event: death, lung transplant, or PEA redo occurring within 3 months from the procedure. Long-term event: death related to CTEPH or PEA, lung transplant or PEA redo occurring between 3 months and 5 years after PEA. Poor long-term functional outcome: PVR greater than 500 dyne · s/cm5 or PaO2 less than 60 mm Hg at 48 months.
Preoperative and Postoperative Measurements
Preoperatively and at each follow-up after PEA, the patients underwent the following (see also the online supplement): (1) determination of the New York Heart Association (NYHA) class of physical activity; (2) right heart hemodynamics; (3) spirometry and single breath CO transfer factor (TLCO) (21–23); (4) arterial blood gas analyses; and (5) treadmill exercise (modified Bruce protocol) (24). TLCO was considered moderately to severely impaired when less than 60% predicted and severely impaired when less than 40% (25). Patients were defined as hypoxemic when PaO2was less than 80 mm Hg and with respiratory failure when PaO2 was less than 60 mm Hg; to evaluate changes over time, the measured arterial oxygen tension was standardized (PaO2st) to an arterial CO2 tension (PaCO2) of 40 mm Hg (26). Good or poor tolerance to exercise was defined as the ability to cover at least 400 m or not; this threshold was the median distance covered at 1 year. Before PEA 45 patients and at 3 months 8 patients did not perform the treadmill exercise testing because of respiratory failure at rest.
Statistical Analysis
The median survival time and its 25th to 75th percentiles (interquartile range [IQR]) were computed according to the inverse Kaplan Meier method. Predictors of late events were identified by Cox models. Hazard ratios (HR) with 95% confidence intervals (95% CI) were reported. Changes over time were assessed by mixed regression or with general estimating equations (GEE) models. The association of patients' characteristics with the distance walked was assessed by a general linear regression model; a multivariable model with backward selection was performed. Finally, logistic regression models were fitted to identify predictors of long-term functional failure. A two-sided P value less than 0.05 was considered statistically significant (Stata 9.2; Stata Corporation, College Station, TX). Additional detail is provided in the online supplement.
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RESULTS
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The study was conducted from April 1994 to December 2006. In this period, 157 patients (85 men and 72 women) with CTEPH were treated with PEA; according to the UCSD protocol, 151 of them had had an inferior vena cava filter placed. The age at surgery ranged from 11 to 84 years (mean age 55, SD 16 yr). Our follow-up protocol yielded detailed data on 132 patients at 3 months, 110 at 1 year, 86 at 2 years, 69 at 3 years, and 49 at 4 years; no patient was lost to the event-free survival follow-up.
Before surgery, 5 of the 157 patients (3%) enrolled were in NYHA class II, while 62 (40%) were in NYHA class III and 90 (57%) in class NYHA IV. The mean value of mean pulmonary artery pressure ( ) was 47.6 mm Hg (SD 12.9) and the mean PVR 1,140 dyne · s/cm5 (SD 517). The mean PaO2 was 65.4 mm Hg (SD 10.4) with a PaO2st of 50.3 mm Hg (SD 12.3).
Eighteen patients died within 3 months, and two were transplanted. Thirteen additional patients died within 5 years (six of CTEPH related causes, six of neoplasm, and 1 of vascular accident); one patient was transplanted and three underwent a second PEA.
Event-free Survival
Overall, 24 patients died because of CTEPH or PEA related causes during a median follow-up of 43 months (IQR, 25–65), corresponding to a mortality rate of 5.2 per 100 person-years (95% CI, 3.4–7.7). The cumulative survival was 84% (95% CI, 76–89) at 5 years. Thirty events, including death, transplant and PEA redo, were recorded overall, corresponding to a rate of 6.4 per 100 person-years (95% CI, 4.5–9.2).
Twenty events (13%) were observed (18 deaths and 2 transplants) within 3 months from PEA.
Ten events were observed during a follow-up ranging from 3 months to 5 years after PEA, with a corresponding rate of 2.5 events per 100 person-years (95% CI, 1.4–4.7). Six patients died, one was transplanted, and three underwent a second PEA. The cumulative event-free survival at 1 and 5 years was, respectively, 96% (95% CI, 91–99) and 88% (95% CI, 79–94).
To be in a postoperative NYHA class III–IV and having an unsuccessful PEA as well as having higher , PVR, and lower CO and PaO2st were the predictors of late events during the long- term follow-up (Table 1). Particularly, postoperative NYHA class III–IV was associated with the highest risk of late events (Figure 1).
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Figure 1. Long-term event-free survival according to New York Heart Association at 3 months. Time 0 corresponds to the third month assessment after surgery. Patients at risk are summarized in the following table:
| At Risk |
Start of follow-up (3 mo after surgery) |
1 yr |
2 yr |
4 yr |
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| NYHA I–II |
116 |
101 |
85 |
48 |
| NYHA III–IV |
15 |
11 |
8 |
5 |
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TABLE 1. PREDICTORS OF LATE (UP TO 48 MO) EVENTS (INCLUDING DEATH, TRANSPLANT, AND PULMONARY ENDERARTERECTOMY REDO)
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Clinical and Functional Changes Occurring over a 4-Year Follow-up in Survivors
Before PEA, 97% of the patients were in NYHA class III–IV. This prevalence dropped to 12% at 3 months (P < 0.001) and then remained fairly unchanged; at 4 years, the proportion of patients in class I increased to 74%, and none was in class IV (Figure 2).
Similarly, the major change for the hemodynamic variables was observed at 3 months, with no or little variation afterward (Table 2). When only survivors were included in the analysis, the time profile of hemodynamics did not change. At 3 months, PEA intervention was considered successful in 88.5% of the patients.
Among the respiratory measures (Figure 3), we observed a decrease of VC and TLC 3 months after intervention. That is consistent with the deterioration seen after major cardiothoracic surgery; at 1 year there was a significant increase with restoration of normal volumes. Before PEA, the impairment in TLCO was moderate to severe (< 60% predicted) only in 68 (43.3%) subjects, and the mean TLCO value was reduced, but not as profoundly as one may have expected. In the same way, TLCO did not improve at 3 months with respect to the preoperative mean value. TLCO significantly increased by 1 year with a subsequent plateau and no restoration at the end of follow-up. At 4 years, TLCO was still moderately to severely impaired (< 60% predicted) in 14 (29.2%) subjects (Table 3).
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Figure 3. Changes over time of respiratory measures; mean and 95% confidence intervals (whiskers) are displayed (in all cases overall significant change over time, P < 0.001).
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Before PEA the mean PaO2 was moderately to severely reduced (65.4 ± 10.4 mm Hg) and PaCO2 was slightly reduced (30.9 ± 3.9 mm Hg); 45 (29.4%) subjects had respiratory failure. After intervention, PaO2st showed a significant improvement, which was already achieved by 3 months without any further improvement over time (Figure 3, Table 3). At 4 years, 28 (56%) subjects were still hypoxemic. The mean total distance covered at treadmill exercise testing progressively increased during the follow-up period. The improvement was significant by 3 months with a further significant increase up to 4 years. At that time, 21 (45.7%) subjects were not able to cover 400 m (the median walked distance at 1 yr). Among all the respiratory and hemodynamic variables only the current PVR and the distance previously covered at 3 months appeared independent predictors of the distance walked at 4 years, at the multivariable analysis.
Long-term Functional Outcome in Survivors and Determinants
The functional outcome at 4 years was evaluated in 49 patients. Twelve of them (24%) had PVR greater than 500 dyne · s/cm5 or PaO2 less than 60 mm Hg; the proportion of these patients with poor outcome was fairly constant over time (P = 0.497). The pre- and postoperative (evaluated at 3 mo) potential determinants of poor outcome at 4 years are summarized in Table 4. Among the clinical and functional variables, a postoperative NYHA class III–IV was associated with the highest risk of poor outcome.
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DISCUSSION
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Our study documents that PEA is a long-term safe and effective procedure for chronic thromboembolic pulmonary hypertension. In almost 75% of patients, the long-term functional outcome was good and almost a half of the patients recovered good exercise tolerance.
Event-free Survival
In our patients, perioperative and early postoperative mortality were substantially similar to that reported in the studies conducted in the same years ( 10%) (4–6, 9–11). As in the UCSD series, we observed a learning curve for the operation with a progressive decline in mortality (see Table E1 in the online supplement).
There are few other reports on late events after PEA. The first study evaluating long-term outcome in a very large sample of patients (532) from 1970 to 1994 showed that 75% of patients survived beyond 6 years with up to 19 years of follow-up (13). In our study, the overall mortality rate was 16%, the same reported in the recent retrospective review of the clinical records of 102 patients operated in the same years in Japan (10).
Clinical and Functional Changes Occurring over 4 Years of Follow-up in Survivors
In agreement with the results of all the other studies, most of the improvement in clinical and hemodynamic recovery was achieved in the first 3 months as a result of the relief of central mechanical obstruction. While a delay in recovery of restrictive pulmonary impairment due to major surgery was generally observed, the time trend of TLCO was not the same in the different studies (10). In fact, patients with chronic thromboembolic pulmonary hypertension often have TLCO in the normal range (27, 28). This is postulated to be because of back-perfusion of the capillary bed by the extensive bronchial arterial collateral flow. This "luxury perfusion" plays a role in the maintenance of pulmonary parenchymal viability and in carbon monoxide exchange, although it does not improve the oxygen exchange (29). The preoperative overestimation of TLCO by the single breath method masks the effect of PEA on the time trend of this parameter. The persistence of a significant impairment of TLCO at the end of follow-up is probably due to the remodeling before surgery on vessels in the nonobstructed segments of the lungs.
There is little information about the chronic effect of PEA on exercise capacity. In the three studies focused on this topic, patients were followed up for no more than 1 year (10, 30, 31), showing a continuous improvement in exercise capacity over this relatively short time interval. In contrast to Matsuda and coworkers (10), who found a plateau at 1 year in a small sample size, we observed a progressive increase in exercise tolerance until 4 years. Our data confirm that there is a discrepancy in the time course of recovery between hemodynamic and exercise data. In almost a half of the patients a reduced exercise tolerance persisted at 4 years. We speculate that the recovery of exercise capacity is not only an immediate result of hemodynamic recovery. The peripheral adaptation and the recovery from the physical deconditioning due to the decreased level of physical activity in daily life might delay or need a long time to be restored. This finding underlines the importance of an early identification of the patients before physical deconditioning.
Long-term Outcome
Postoperative NYHA class III–IV was associated with the highest risk of late events. At the end of follow-up, although 74% of the survivors were in NYHA class I and none was in class IV, about 25% of survivors still had moderate to severe hypoxemia or persistent pulmonary hypertension; they were significantly older and were more frequently in NYHA class III–IV 3 months after the operation than the others. This findings do not suggest that PEA should be avoided in the most severe cases; at variance, they underline the importance of an early surgical treatment.
The strength of our study is the large sample size including patients with a very compromised hemodynamic status. They were followed up for enough time to evaluate the long-term effects of PEA on survival and clinical and cardiopulmonary function status. On the other hand, due to the (favorable) low number of events, we only could rely on the univariable analysis to identify factors predicting the long-term outcome. A multivariable analysis would have been preferred to identify the independent determinants, but was not feasible given the low event number. Moreover, other predictors could have been considered to ameliorate our ability in predicting the outcome (32). However, we chose to stratify the risk of negative events in the follow-up by the criteria commonly used in the selection of the patients.
In conclusion, our study shows that long-term survival after PEA is excellent and cardiopulmonary function can almost be normalized in the most patients, underlying the importance of the intervention in the treatment for chronic thromboembolic pulmonary hypertension.
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FOOTNOTES
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This article has an online supplement, which is accessible from this issue's table of contents at www.atsjournals.org
Originally Published in Press as DOI: 10.1164/rccm.200801-101OC on June 12, 2008
Conflict of Interest Statement: None of the authors has a financial relationship with a commercial entity that has an interest in the subject of this manuscript.
Received in original form January 15, 2008;
accepted in final form June 6, 2008
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Copyright © 2008 American Thoracic Society
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ABSTRACT
AT A GLANCE COMMENTARY