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Ann Thorac Surg 2006;82:2080-2087
© 2006 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Long-Term Outcome of Survivors of Prolonged Intensive Care Treatment After Cardiac Surgery

Maurizio Mazzoni, MDa,*, Renata De Maria, MDb, Franco Bortone, MDa, Marina Parolini, BStatb, Roberto Ceriani, MDa, Costantino Solinas, MDa, Vincenzo Arena, MDc, Oberdan Parodi, MDb

a Department of Anesthesia and Intensive Care, Bergamo
c Department of Cardiac Surgery Humanitas Gavazzeni, Bergamo
b CNR Clinical Physiology Institute, Cardiology Department Niguarda Ca' Granda Hospital, Milan, Italy

Accepted for publication July 13, 2006.

* Address correspondence to Dr Mazzoni, Department of Anesthesia and Intensive Care, Humanitas Gavazzeni, Via Mauro Gavazzeni 21, 24125 Bergamo, Italy. (Email: maurizio.mazzoni{at}gavazzeni.it).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: The relative impact of perioperative risk profile and postoperative complications on long-term outcome in cardiac surgical patients is currently unclear. The aim of this work was to assess the relative predictive value of the European System for Cardiac Operative Risk Evaluation (EuroSCORE) and Sequential Organ Failure Assessment (SOFA) on long-term event-free survival in this patient population.

METHODS: Preoperative and postoperative variables, EuroSCORE and SOFA, 30-day mortality, and long-term mortality or hospital admission for cardiovascular events were assessed in 115 consecutive cardiac surgical patients in whom multiorgan dysfunction syndrome developed postoperatively.

RESULTS: Mean age was 70 ± 8 years, 41% were women, EuroSCORE averaged 7.87 ± 3.99, and postoperative stay in the intensive care unit was 10.3 ± 8.2 days. In-hospital 30-day mortality was 10.4% (n = 12). During 1998 person-months follow-up, 12 (11.6%) of 103 patients discharged alive died, and 46 (44.7%) met the combined end point of all-cause death or cardiovascular admission. By Cox multivariate analysis, maximum SOFA (hazard ratio [HR], 2.17; 95% confidence interval [CI], 1.34 to 3.51) and maximum cardiovascular score (HR, 2.35; 95% CI, 1.22 to 4.51) independently predicted all-cause mortality. EuroSCORE (HR, 1.33; 95% CI, 1.01 to 1.76), maximum cardiovascular score (HR 2.09; 95% CI 1.41 to 3.10), and maximum liver score (HR 2.67; 95% CI, 1.46 to 4.86) were independently associated with the combined end point.

CONCLUSIONS: High-risk cardiac surgical patients with postoperative multiorgan dysfunction syndrome show excess mortality and cardiovascular morbidity after hospital discharge. Combined preoperative and postoperative risk stratification identifies patients with the highest likelihood of death or early readmission.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Cardiac surgery may be associated with complications and in-hospital mortality. After hospital discharge, patients who have significant postoperative morbidity and need prolonged treatment in the intensive care unit (ICU) may experience a high rate of events leading to hospital admission and reduced survival. Accordingly, long-term outcome is a more appropriate measure of procedural benefit for the cardiac surgical patient [1–6].

Risk stratification has gained widespread acceptance by the application of specifically designed scoring systems. The European System for Cardiac Operative Risk Evaluation (EuroSCORE), a validated model for preoperative risk stratification and prediction of in-hospital mortality [7], has shown good predictive power for long-term events and mortality in cardiac surgical patients [6–8] in both European and North American cohorts [9]. Most patients at low preoperative risk will have an uncomplicated postoperative course and a long-term event-free survival, but early surgery-related complications have long been recognized to additively impact on outcome of high-risk patients [6, 10–12].

Length of intensive care unit (ICU) and in-hospital postoperative stay have been used as surrogate markers of postsurgical morbidity. Prolonged postoperative ICU stay predicts both early and late mortality in cardiac surgical patients [6, 13–14], and patients with extracardiac complications and multiorgan dysfunction syndrome (MODS) are at greatest risk [12–15]. The impact of MODS on the risk of in-hospital mortality after cardiac surgery [15–16] has been described by the use of models purposely developed to measure its dynamic pattern, such as the Sequential Organ Failure Assessment (SOFA) scoring system [17]. However, the available prognostic models do not take into account long-term results in critically ill patients. Furthermore, studies on the factors that influence long-term morbidity and mortality in survivors of prolonged intensive care are scanty.

The aim of this study was to ascertain the long-term outcome of cardiac surgical patients with postoperative MODS and to test the relative predictive potential of EuroSCORE and SOFA score for fatal and nonfatal cardiovascular events.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Study Population
We studied 115 consecutive cardiac surgical patients, operated on between January 2000 and August 2002 at a tertiary care hospital, who required uninterrupted ICU stay exceeding 96 hours for postoperative complications. Because this was an epidemiologic study without intervention, the Institutional Ethics Committee waived the informed consent and approved the project.

At our institution, all cardiac surgery patients are transferred from the operating room to the ICU for routine surveillance and care. A period exceeding 96 hours spent in the ICU, corresponding to the 90th percentile in the frequency distribution analysis of ICU length of stay, was selected as the threshold for a prolonged ICU stay [18–19]. Patients were not discharged from the ICU if any of the following was present: hemoglobin oxygen saturation less than 90% on spontaneous breathing, with fraction of inspired oxygen 0.4; respiratory rate exceeding 30 per minute, or need for mechanical ventilation; serum creatinine level exceeding 120 µmol/L; urea exceeding 8 mmol/L; urine output of less than 800 mL per 24 hours; in the presence of chronic renal insufficiency, postoperative increase in serum creatinine level exceeding 60 µmol/L, urea exceeding 4 mmol/L, and urine output of less than 800 mL per 24 hours, or need for renal replacement therapy; infusion of a vasoactive/inotropic agent, either dopamine or dobutamine exceeding 2 µg/(kg · min); or need of monitoring or treating newly acquired dysrhythmias. No patient was transferred to another ICU, to an intermediate care unit within the hospital, or to a different institution.

Study Design
Detailed data were collected on the index admission, when cardiac surgery was performed, including EuroSCORE, calculated according to the standard additive method (Appendix 1) [20] and to the logistic method [21], and time spent in ICU. In-hospital mortality was defined as death within 30 days of operation or within the same hospital admission.


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  		Appendix 1. The EuroSCORE
 
During ICU stay, MODS severity was graded according to the SOFA system, in which a daily score from 0 to 4 is assigned according to the severity of functional deterioration, if any, for each of six individual organ systems (Appendix 2) [17]. The SOFA score was computed starting on the first postoperative day and for the entire duration of ICU stay. The worst value for each organ system in each 24-hour period was considered. In sedated patients, the neurologic score was computed retrospectively when sedatives were stopped or alternatively, after their temporary discontinuation [22]. The aggregate total maximum SOFA score was calculated by adding the worst scores for each of the organ systems, and the maximum SOFA was defined as the highest total SOFA score recorded during the observation period. We also calculated the number of days when at least two organ systems had a failure, as defined by a score of 3 or more. No patient received a mechanical cardiac assist device.


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  		Appendix 2. The SOFA Score
 
Follow-up data were derived from the Regional Health Database, which includes all hospital discharges, using the Regional Health System number for record linkage. Subsequent hospital admissions were coded according to the principal or additional International Classification of Disease (9th version) diagnoses and procedures. Out-of-hospital deaths were identified through the National Death Index.

To assess the impact of a complicated postoperative course on outcome, each of the 115 patients was cross-matched by age, gender, and EuroSCORE (in a 1:2 proportion whenever possible) with controls with a postoperative ICU stay of 96 hours or less selected among consecutive patients who had undergone cardiac surgery at our institution during the same period.

Statistical Analysis
Continuous variables were expressed as mean ± standard deviation or median and interquartile range (I, III). Proportionality of hazards was checked using the Grambsch-Therneau test and diagnostic plots based on Schoenfeld residuals. Time to death and time to first event for the combined end point (all-cause death or first cardiovascular admission) were studied as a function of covariates selected by univariate analysis and entered in a Cox multivariate model by backward selection using the Akaike Information Criterion. Estimated hazard ratios (HRs) with 95% confidence interval (CI) are presented.

The prognostic risk index for each patient, calculated by adding up the coefficient estimates of those predictors that were present in the patient, was exponentiated and tested by receiver operating characteristic (ROC) analysis against the probability of death or cardiovascular events. The results are expressed in terms of the area under the curve (AUC) and its 95% confidence interval. Kaplan-Meier curves between the study cohort and the matched control group were compared by the log-rank test. A value of p < 0.05 was considered statistically significant. Analyses were performed with SPSS 10.0 (SPSS Inc, Chicago, IL) for Windows (Microsoft Corp, Redmond, WA) and S-PLUS (S-PLUS 2000 Guide to Statistics, Volume 2, Data Analysis Products Division, MathSoft, Seattle, WA).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Perioperative Characteristics
Clinical characteristics of the 115 study patients are shown in Tables 1 and 2. Go ICU bed-occupancy for these 115 patients was 1189 days, or 38.9% of 3056 total ICU days for all 1231 cardiac surgical patients admitted to the ICU during the same period.


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  		Table 1. Main Preoperative Characteristics of the Study Population
 

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  		Table 2. Perioperative Variables and Postoperative Complications of the Study Population
 
Outcome
During the index admission, 12 of the 115 patients died (total in-hospital or 30-day mortality, 10.4%). During 1998 person-months, 12 (11.6%) of 103 patients discharged alive died. Thus, total mortality rate of the study cohort at 17 ± 11 months was 20.9%.

The combined end point (all-cause death or cardiovascular admission) occurred in 46 patients (44.7%), and 57 were alive and free of events at the end of the study. There were 55 unplanned admissions for cardiovascular causes in 39 patients (37.9%) that were due to heart failure in 29 (53%), acute coronary syndromes in 7 (13%), cerebrovascular events (transient ischemic attack, stroke) in 5 (9%), arrhythmias in 7 (13%), peripheral vascular complications in 3 (5%), and other causes in 4 (7%).

Predictors of Prognosis
Significant univariate predictors of death and of the combined end point in the 115 patients (Table 3) were entered in a Cox multivariate model to analyze their independent impact on outcome.


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  		Table 3. Main Characteristics of the Study Population With Hazard Ratio of Death or Death and Cardiovascular Events by Univariate Analysis
 
Maximum SOFA score (HR, 2.17; 95% CI, 1.34 to 3.51) and maximum cardiovascular score (HR, 2.35; 95% CI, 1.22 to 4.51) were the best independent predictors of all-cause mortality. The area under the ROC curve was 0.82 (95% CI, 0.73 to 0.91). The cumulative hazard function according to a maximum SOFA of 10 or less and more than 10, adjusted by maximum cardiovascular score, is presented in Figure 1.


Figure 1
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  		Fig 1. The cumulative hazard function of all-cause death, adjusted by the maximum cardiovascular score, was significantly higher in patients with a maximum sequential organ failure (SOFA) score >10 (thick line) than in those with a score ≤10 (thin hatched line).

 
The independent predictors of the combined end point of death or unplanned cardiovascular admission were the additive EuroSCORE (HR, 1.33; 95% CI, 1.01 to 1.76), maximum cardiovascular score (HR, 2.09; 95% CI, 1.41 to 3.10), and maximum liver score (HR, 2.67; 95% CI, 1.46 to 4.86). The area under the ROC curve was 0.76 (95% CI, 0.67 to 0.84). The cumulative hazard function according to a maximum cardiovascular score less than 3 and 3 or more, adjusted by EuroSCORE and maximum liver score, is shown in Figure 2.


Figure 2
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  		Fig 2. The cumulative hazard function of death or hospitalization for a cardiovascular event, adjusted by the European System for Cardiac Operative Risk Evaluation (EuroSCORE) and maximum liver score, was significantly higher in patients with a maximum cardiovascular score (CV) ≥3 (thick line) than in those with a score of <3 (thin hatched line).

 
Comparison of High-Risk Cohorts According to Length of ICU Stay
To adjust for the impact of preoperative risk profile, each of the 115 study patients was cross-matched in a 1:2 proportion, whenever feasible, to controls (n = 218) with an ICU stay of 96 hours or less selected among patients who had undergone cardiac surgery during the same period. Matched controls were comparable with study patients for age (71 ± 8 years, p = 0.44), gender distribution (42% women, p = 0.91), preoperative left ventricular ejection fraction (0.51 ± 0.12, p= 0.22), and EuroSCORE (7.04 ± 3.31, p = 0.057). In patients with an ICU stay exceeding 96 hours, survival (78% versus 89%, p = 0.001; Fig 3) and event-free survival (46% versus 70%, p = 0.001; Fig 4) were significantly lower than in matched controls.


Figure 3
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  		Fig 3. Kaplan-Meier survival curves in 115 patents with a prolonged intensive care unit (ICU) stay (continuous line) and in the matched control group with an ICU stay of ≤96 hours (hatched line). Numbers below the x axis are patients exposed at risk at different time intervals.

 

Figure 4
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  		Fig 4. Kaplan-Meier event-free survival curves in 115 patients with a prolonged intensive care unit (ICU) stay (continuous line) and in the matched control group with an ICU stay ≤96 hours (hatched line). Numbers below the x axis are patients exposed at risk at different time intervals.

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
This study underscores the impact of severity of postoperative morbidity, together with preoperative risk stratification, on the postdischarge outcome of cardiac surgical patients. In patients with a complicated postoperative course requiring prolonged ICU stay, severity of postoperative MODS and cardiac failure after surgery were associated with long-term mortality, whereas preoperative risk stratification by the additive EuroSCORE, and postoperative occurrence of cardiac and hepatic failure by SOFA score predicted the combined end point of mortality and cardiovascular admissions.

In the continuum of care for the cardiac patient, information on long-term survival and incidence of late cardiovascular events after cardiac surgery is needed to provide a framework for decisions regarding both individual patients’ needs and prospective resource allocation. The patients with significant postoperative morbidity described in this series had a high-risk preoperative profile as summarized by their median EuroSCORE: they were older, more often female and had a lower left ventricular ejection fraction than the unselected cohort of cardiac surgical patients [6].

Although the interaction between the high-risk preoperative profile and postoperative MODS may partially account for the lack of independent predictive value of EuroSCORE on long-term mortality in this group, survival rates in the 115 study patients were significantly worse than in matched controls with comparable EuroSCORE values and a ICU stay of less than 96 hours. Therefore, a favorable outcome in patients with severe complications after cardiac surgery remains elusive, and the long-term impact of postoperative morbidity needs to be considered.

The logistic EuroSCORE has been suggested as a better model than the additive one for individual mortality prediction in high-risk patients [23], whereas for group analysis, the logistic and additive EuroSCOREs seem to have similar prognostic value [24]. In our relatively small series of complicated patients, the logistic EuroSCORE was not predictive of either mortality or the combined end point. This finding may be explained by the widely skewed distribution of preoperative logistic scores in this cohort, and it further underscores the onerous impact of perioperative adverse events on patients’ outcome, not only in the short term but also in the long term. In addition, the system’s relevance for this purpose may be limited because it was not designed for prediction of postoperative morbidity.

Discrepancy exists on the threshold value used to define the period spent in ICU after cardiac surgery as "prolonged." In addition to clinical factors, the impact of institutional characteristics and type of ICU organization on length of stay must be taken into account [25–26]. ICU stays ranging from more than 24 hours to longer than 14 days have been reported as prolonged [1, 12, 14, 27]. The 96-hour threshold value allowed us to exclude patients with minor complications and those with extremely severe conditions leading to early mortality. This relatively small group of patients imposed a greater demand on ICU resources and used almost 40% of the total ICU days for all cardiac surgical patients during the study period.

The SOFA score was designed to objectively evaluate the severity of functional deterioration of each of six different organ systems, daily. It has shown consistent prognostic value for the description of MODS severity and evolution in both medical and surgical cardiac ICU patients [15–16, 28]. Other systems developed for use in ICU patient groups with various diseases, with the exclusion of cardiac surgical patients, are exclusively based on data obtained during the first 24 hours after ICU admission and incorporate information about physiologic derangement, admitting diagnosis, age, and comorbidity, but do not take into account complications that may develop during treatment [29–32]. The strong independent predictive value of a maximum SOFA score exceeding 10 for in-hospital and long-term all-cause mortality in our patients underscores the importance of multiorgan dysfunction for the ultimate outcome. Nonetheless, severity of cardiac impairment, defined by the maximum cardiovascular score, showed an even greater prognostic impact, which was also apparent for cardiovascular events.

The cardiac component of SOFA may be subjectively biased because it is based on treatment criteria and not on a direct measure of function. As inotropic agents are frequently administered perioperatively, regardless of hypotension, their use is not an objective measure of cardiac dysfunction. However, because patients discharged early from the ICU were excluded from the analysis, high cardiovascular scores observed in our cohort are representative of a prolonged need for inotropic support.

The association of postoperative cardiac functional impairment with late adverse outcome is akin to the observation of a direct relationship between intraoperative measurement of low pH values in the myocardium and decreased long-term patient survival [33] and suggests that the combination of ischemia and reperfusion injury is the most likely mechanism of cardiac damage in these patients. The increased risk of poor outcome may originate from the loss of cardiac functional reserve due to the superimposition of perioperative myocardial injury on preoperative cardiac dysfunction.

In our series, postoperative cardiac dysfunction requiring prolonged inotropic support was associated with a very high risk of death or early readmission after discharge, and heart failure was the most common cardiovascular event. Patients with high cardiac SOFA scores may benefit from close follow-up so that timely treatment directed at prevention of development of overt heart failure can be instituted.

Postoperative hyperbilirubinemia, an index variable of the maximum liver score, may result from hemolysis due to long cardiopulmonary bypass time or the intraaortic balloon pump, independent from hepatic dysfunction. A late postoperative rise in serum bilirubin is associated with increased mortality [14–15, 34], however, and hyperbilirubinemia may be a reliable indicator of the severity of hepatic dysfunction in patients with persistent severe left or right ventricular failure.

Our results also underscore the value of SOFA as a global index of postoperative complications and long-term outcome. Bashour and colleagues [1] reported postdischarge mortality rates of 46.8% in 42 patients with prolonged ICU stay after cardiac surgery but did not analyze the specific pattern of postoperative morbidity. In 124 patients needing prolonged postoperative mechanical ventilation, Engoren and colleagues [2] reported 6-month mortality of 20%, which was associated with perioperative cerebrovascular accidents and renal insufficiency.

Although the optimal duration of follow-up after intensive care is unknown, the temporal trend of all-cause mortality in these severely ill patients indicates that 91% of all deaths occurred in the initial 4 months after surgery, whereas cardiovascular events were more evenly distributed across the whole observation period. This finding suggests that closer follow-up after hospital discharge may be justified in patients identified by preprocedural and postprocedural risk factors to ameliorate long-term survival.

Neurocognitive impairment after cardiac surgery or critical illness is a frequent event that may affect long-term outcome [35–36]. Because neurocognitive sequelae may not require hospitalization, they might have eluded evaluation by analysis of hospital discharge codes.

This is a single-center study with a relatively small sample size, and differences in institutional and clinical setting may limit the general applicability of these results. Patients were enrolled during a relatively short period of time, however, during which perioperative and critical care management may be considered standardized. Furthermore, studies of survivors of prolonged intensive care after cardiac surgery are necessarily limited to a small proportion of the ICU population. Cause-specific cardiovascular mortality could not be assessed, and the cause of out-of-hospital deaths was not ascertained. All-cause mortality may be a better index of the global morbidity burden facing these patients, however.

In conclusion, despite advances in operative techniques and critical care interventions, cardiac surgery in high-risk patients is associated with considerable morbidity and mortality. Postoperative risk profiling by objective scoring systems may be a useful tool to identify subjects with the highest likelihood of death or early readmission. Further investigations are needed to assess the value of close follow-up after hospital discharge in decreasing mortality and cardiovascular events in high-risk patients through prompt institution of aggressive treatment.


   Appendix
 


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
We gratefully acknowledge the secretarial assistance of Elisabetta Spagnolo and the ICU staff for their invaluable help in data collection.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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