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(Chest. 2003;123:504-509.)
© 2003 American College of Chest Physicians

Respiratory Failure and Sepsis Are the Major Causes of ICU Admissions and Mortality in Survivors of Lung Transplants*

Celestino Pietrantoni, DO; Omar A. Minai, MD; Nelson C. Yu, MD; Janet R. Maurer, MD, FCCP; Marcus T. Haug, III, PharmD; Atul C. Mehta, MD, FCCP and Alejandro C. Arroliga, MD, FCCP

* From the Cleveland Clinic Foundation, Cleveland, OH.

Correspondence to: Omar A. Minai, MD, Department of Pulmonary and Crit Care Med, A-90, Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH 44195; e-mail: minaio{at}ccf.org


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: To identify outcome predictors and prognostic factors in long-term survivors (> 30 days post-transplant) of single-lung and double-lung transplants on readmission to the medical ICU (MICU).

Design: Retrospective study.

Setting: MICU of the Cleveland Clinic Foundation, a lung transplantation center.

Patients: As of August 2000, 210 lung transplantations have been performed at our institution. The records of 33 lung transplant recipients who required readmission to the MICU after the initial 30-day post-transplant period over a 4-year period from August 16, 1996 to August 15, 2000 were reviewed.

Results: Thirty-three patients had a total of 46 MICU readmissions. Twenty-seven MICU admissions (59%) were due to respiratory deterioration with mechanical ventilation (10 deaths), and 16 MICU admissions (35%) were due to the systemic inflammatory response syndrome (SIRS; 8 deaths). The MICU mortality rate was 37% per admission in our group of patients. A preadmission diagnosis of bronchiolitis obliterans syndrome was observed in 7 of 14 nonsurvivors (50%) and in 5 of 25 patients (20%) surviving to hospital discharge.

Conclusions: Respiratory failure and SIRS are the predominant causes of MICU readmissions and are frequent causes of death. APACHE (acute physiology and chronic health evaluation) III scores, nonpulmonary organ system dysfunction, initial serum albumin level, and duration of mechanical ventilation are important prognostic factors.

Key Words: ARDS • intensive care • lung transplant • respiratory failure • sepsis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Lung transplantation offers an improved quality of life and prolonged survival in patients with a variety of advanced lung diseases.1 Lung transplantation is associated with substantial risks and complications, with primary graft failure, infection, hemorrhage, and airway complications accounting for the vast majority of early deaths.2 Hemorrhage and airway dehiscence have been significantly reduced or eliminated by advances in surgical techniques and by the experience of the surgeons performing transplantations. Long-term survival is limited primarily by the development of bronchiolitis obliterans syndrome (BOS), the effects of which may be manifested as progressive respiratory failure or by an increased risk of infection.3 4

Most of the attention to date has focused on the immediate peritransplant period. Factors influencing the readmission of lung transplant recipients to the ICU after the early post-transplant period have not been described previously. This subgroup of immunosuppressed patients is unique in that the transplanted organ is constantly exposed to the environment and deprived of its lymphatic drainage and nerve supply, rendering it uniquely susceptible to infection. Other features that separate this group of patients from other immunosuppressed groups of patients include a propensity for airway complications and variations on the immunosuppressive regimens utilized. Significant prognostic data regarding bone marrow transplant recipients has led to criteria that may be used as predictors of ICU outcome in these unique populations.5 6 7 We analyzed several clinical factors that may be predictors of mortality in lung transplant recipients. The objective of this study was to identify these outcome predictors and the prognostic factors that are associated with long-term survivors (ie, > 30 days post-transplant) of single-lung and double-lung transplants on readmission to the medical ICU (MICU) at our institution.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
As of August 2000, 210 lung transplants have been performed at our institution. We retrospectively reviewed the records of single-lung and double-lung transplant recipients who subsequently required readmission to the MICU > 30 days post-transplantation over a 4-year period between August 16, 1996, and August 15, 2000. The MICU admissions were categorized into the following two groups: those leading to survival; and those resulting in death during the hospitalization that encompassed the MICU admission.

Data collection included age, gender, reason for and type of lung transplantation (single or double), donor and recipient organ typing by ABO blood groupings, cytomegalovirus serology, previous episodes of acute rejection on a pathologic and/or clinical basis, and a prior history of BOS. Variables specific to individual MICU admissions included admission diagnosis, length of stay, duration of mechanical ventilation, major clinical procedures and operative interventions performed, blood product utilization, interval time from transplantation, acute physiology and chronic health evaluation (APACHE) III score8 on MICU admission, initial serum albumin level, and the identification of additional nonpulmonary systemic organ dysfunction.

Respiratory failure requiring mechanical ventilation was differentiated by adapting the criteria for the diagnosis of acute lung injury (ALI) and ARDS as set by the North American/European Consensus Conference.9 The criteria were as follows: acute onset of lung injury; diffuse bilateral infiltrates seen on chest radiography; PaO2/fraction of inspired oxygen ratio of < 200 mm Hg for ARDS and PaO2/fraction of inspired oxygen ratio < 300 mm Hg for ALI; pulmonary artery occlusion pressure of < 19 mm Hg; or no clinical evidence of congestive heart failure.9 The criteria for systemic inflammatory response syndrome (SIRS) were adapted from the American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference and included at least two of the following conditions: temperature, < 36°C or > 38°C; heart rate, > 90 beats/min; respiratory rate, > 20 breaths/min; PaCO2, < 32 mm Hg; and WBC count, > 12,000 cells/µL, or < 4,000 cells/µL, or > 10% immature (band) forms.10 We defined shock as hypotension with a systolic BP < 90 mm Hg or a reduction of > 40 mm Hg from baseline, despite adequate resuscitation with fluids.

Nonpulmonary organ systemic dysfunction developing after admission to the ICU was defined by any single derangement of the following parameters: cardiovascular dysfunction (ie, hypotension [systolic BP, < 90 mm Hg; or mean arterial BP, < 65 mm Hg]; bradycardia or tachycardia [ie, heart rate, < 60 or > 120 beats/min, respectively]; cardiac arrest; or a requirement for inotropic support); renal dysfunction (ie, BUN, > 100 mg/dL; serum creatinine level, > 2 mg/dL; or a requirement for hemodialysis); hepatobiliary dysfunction (ie, total bilirubin level, > 2.5 mg/dL without hemolysis; aspartate serine transaminase or lactate dehydrogenase level greater than twice the upper limit of normal; or at least grade 2 encephalopathy); gastroenterologic dysfunction (ie, alimentary tract bleed requiring blood transfusion); hematologic dysfunction (ie, anemia [hemoglobin level, < 12 g/dL]; leukopenia [WBC count, < 4,000 cells/µL]; or thrombocytopenia [platelet level, < 20,000 cells/µL]); and Glasgow coma scale-defined neurologic dysfunction (ie, score < 15 without sedation or any clinically apparent CNS infarction).

In those patients with multiple admissions to the MICU within a single hospitalization, individual MICU admissions were independently evaluated in our study. The Fisher exact test compared survivors and nonsurvivors for various demographic, clinical, and laboratory parameters. p Values were compared as none vs others. Continuous variables and hospital survival were compared using the Wilcoxon rank sum test.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
During the study period, 188 of 210 lung transplant recipients (89.5%) survived for > 30 days after undergoing transplantation at our institution. Thirty-three of these patients (17.6%) had a total of 46 MICU readmissions between August 16, 1996, and August 15, 2000. The demographics of this population are presented in Table 1 . The MICU mortality rate was 37%. Of the 46 MICU admissions, 6 were deemed "elective" for planned major surgical procedures requiring postoperative MICU monitoring, and none of these admissions led to death. The nonelective MICU admission mortality rate was 43%. The overall MICU mortality rate for all admissions during the period of our study was 22%.


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  		Table 1.. Characteristics of ICU Admissions*

 
Nine patients accounted for 22 MICU admissions, and 24 patients accounted for the remainder of the total 46 MICU admissions. Among those in the group requiring multiple MICU admissions, four occurred within 15 days of the prior admission, and the remaining MICU admissions occurred within a range of 25 to 547 days. Two of the nine patients requiring multiple MICU admissions survived the study period

Twenty-seven MICU admissions (59%) were due to respiratory failure, and all of those patients eventually required mechanical ventilation, resulting in 10 deaths. ARDS accounted for 18 MICU admissions (39%), while ALI accounted for 9 MICU admissions (20%) [Table 2 ]. The second most common cause for MICU admission was SIRS with 16 MICU admissions (35%). Thirteen of these patients had "severe SIRS" (ie, multi-organ system dysfunction and SIRS), and all eight deaths occurred in this subgroup. Seven MICU admissions were for surgical procedures, of which six were elective and one was for small bowel obstruction requiring open laparotomy and lysis of adhesions.


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  		Table 2.. Admission Diagnoses and Survivors

 
A diagnosis of ARDS, SIRS, or shock at MICU admission was an especially poor prognostic sign. Fifty percent of patients with SIRS, 44% of patients with ARDS, and 40% of patients with shock survived the MICU admission.

The underlying reason for transplantation was not a significant independent predictor of mortality. However, a history of acute rejection or BOS (p = 0.088 and p = 0.075, respectively; Table 3 ) was associated with increased mortality, although this comparison did not reach statistical significance.


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  		Table 3.. Relationship of Rejection Episodes and BOS to Survival in Lung Recipients

 
As a group, these patients required a number of clinical procedures and operative interventions per MICU admission, with central venous catheterization being performed most commonly among 41 of 46 patients who were admitted to the MICU (Table 4 ). All 27 patients who were admitted to the MICU for respiratory failure eventually underwent intubation. Thirty-nine intubations were performed among the 46 patients admitted to the MICU. The other causes for intubation included elective surgical procedures and the need for airway protection. Two patients underwent open lung biopsies. The pathology report on the left lower lobe biopsy specimen taken from the first patient indicated culture-negative, exudative bronchopneumonia, without evidence of rejection. The patient expired 3 months after the referenced hospitalization from an unrelated complication of lung transplantation. The pathology report on the left lower lobe biopsy specimen of the other patient indicated culture-negative, acute, and early organizing diffuse alveolar damage with atypical, reactive, type II, pneumocyte hyperplasia. The second patient died 5 days after undergoing the lung biopsy, after medical treatment had been withdrawn because of the futility of medical care.


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  		Table 4.. ICU Clinical Variables in Lung Transplant Recipients*

 
The documented absence of infection during the MICU stay indicated a trend toward significance for survival (p = 0.059). Table 4 demonstrates the causes of infection in nonsurvivors in descending order (bacterial, eight patients; fungal [Candida and Aspergillus species], six patients; and viral [cytomegalovirus] four patients). Fungal infection was uniformly fatal in the MICU setting. All patients were treated, at the discretion of the clinician, with antibiotics directed at the likely pathogens. A review of autopsy data for nonsurvivors did not reveal unforeseen infections such as occult abscesses or Aspergillus.

Table 5 demonstrates the relationship between survival and MICU variables. Nonsurvivors had a significantly longer mean (± SD) duration of mechanical ventilation (12.53 ± 9.95 vs 6.14 ± 5.90 days, respectively; p = 0.024), more organ system dysfunction (4 ± 1 vs 2 ± 1 organs, respectively; p = 0.0005), and higher APACHE III scores (99.6 ± 30.2 vs 77.3 ± 24.5, respectively; p = 0.030). A low serum albumin level also indicated a trend toward significance for nonsurvivors vs survivors (2.54 ± 0.79 vs 3.09 ± 0.77 g/dL, respectively; p = 0.025).


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  		Table 5.. ICU Variables in Lung Recipients*

 
The intervals of time from lung transplantation to ICU admission (mean duration, 866.82 ± 714.26 vs 636.00 ± 518.70 days, respectively; p = 0.212) and ICU length of stay (mean length of stay, 12.94 ± 10.17 vs 8.90 ± 7.80 days, respectively; p = 0.137) were not statistically significant comparing survivors and nonsurvivors.

Five of 33 patients had designated a do-not-resuscitate (DNR) order > 24 h prior to the referenced MICU admission. Of the five nonsurviving patients admitted to the MICU with designated DNR orders, the average time between ascertainment of the DNR to death was 7.6 days. Ten of the 17 nonsurviving patients who were admitted to the MICU had DNR orders designated within 1 day of their death. The other two nonsurviving patients who were admitted to the MICU died after cardiopulmonary arrest with unsuccessful resuscitation had occurred.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
To our knowledge, this is the first study focusing on ICU outcomes and predictors of mortality in lung transplant patients beyond the immediate peritransplant period. Our study showed that ARDS was the leading cause of ICU readmission, accounting for 39% of total ICU admissions, and that only 44% of these patients survived to ICU discharge. ALI seemed to convey a relatively better prognosis than ARDS. Among patients admitted to the MICU who had received a diagnosis of SIRS, 50% survived to ICU discharge. When admissions for SIRS and shock were combined, these two diagnoses accounted for 46% of total admissions, with 48% of those patients surviving to ICU discharge. The vast majority of our patients were admitted to the MICU for various degrees of respiratory difficulty. Despite aggressive medical interventions, the outcomes of patients with bilateral pulmonary infiltrates and hypoxia were dismal.

Pneumonia, sepsis, and gastric aspiration are the most prevalent predisposing conditions for ALI and ARDS among MICU patients.11 One observational study of 100 MICU patients who were admitted to the MICU for ALI/ARDS by Zilberberg and Epstein,11 concluded that the principal independent predictors of hospital mortality were age > 65 years and the presence of sepsis syndrome, while other important comorbid conditions included cirrhosis, HIV infection, active malignancy, and organ transplantation. Lung transplant patients were not among those in the study group. Although we did not further differentiate the predisposing condition for the cause of ALI/ARDS in our study, as a group our patients manifested at least one of these predictors for poor outcome related to ALI/ARDS, mainly due to organ transplantation.

SIRS is not a diagnosis or a good indicator of outcome, but its presence in individual patients must be explained adequately. The American College of Chest Physicians/Society of Critical Care Medicine12 concept of SIRS is a common response to many initiating circumstances such as infection, bacteremia, trauma, burns, and pancreatitis. A large prospective survey13 identified a proven infection in only one half of all ICU patients, while the other patients had culture-negative SIRS. In our study population, culture-proven infections developed in 11 of 16 patients admitted for SIRS to the ICU. Six of these patients died. Bacterial infections acquired during the ICU admission clearly indicated a trend toward a worse outcome. The rate of infection among lung transplant recipients is several times higher than that among recipients of other organs and is most likely related to the constant exposure of the allograft to the external environment, the immunocompromised state, and the ineffective clearance of secretions.3 Chaparro et al14 concluded that infection is the primary cause of early and late death after patients undergo unilateral and bilateral lung transplantations. Bacterial infections that cause death occur primarily in the perioperative setting or late in the presence of underlying complications such as BOS. Overall, BOS with bacterial infection is the second most common cause of death in lung transplant recipients and is the most common cause of death in those patients who die > 6 months after undergoing transplantation.14 Five of 16 patients with SIRS had negative cultures. Given the inherently unique population and our relatively small sample size, we can only speculate that either the culture-negative SIRS patients had infections that did not grow or that the symptoms were related to medications or to other unidentified causes.

We also identified variables that were associated with a favorable outcome. In our study, the absence of prior rejection or the absence of BOS were associated with better outcomes on ICU readmission, although they did not reach statistical significance. BOS is a major factor limiting long-term survival in patients undergoing lung transplantation. The mean survival rate after the diagnosis of BOS is 66%, 44%, 37%, and 10% after 1, 3, 5, and 10 years, respectively.15 BOS also may lead to substantial disability and morbidity through infection.16 17

When patients decide to proceed with transplantation, they are usually well-informed about potentially lethal complications. The level of care that patients would like to have continued in light of potential medical catastrophes should be spelled out clearly beforehand. However, physicians need guidance when counseling patients regarding which clinical variables have prognostic significance and when it may be time to proceed with or withdraw intensive life support. The relatively small size of this unique population limited our efforts at proving a definitive group of risk factors influencing MICU readmission. Our data suggested both positive and negative predictors of MICU outcome.

Lung transplant recipients requiring MICU treatment represent a unique group of patients who may typically request aggressive medical care until their death. This is demonstrated in our study by the lack of predesignated directives regarding resuscitation efforts in those MICU admissions that eventually lead to death. We speculate that these patients may perceive themselves and be perceived by their physicians to be near a relatively "healthy" baseline after undergoing a transplantation procedure, and thus end-of-life issues may not have been discussed. In addition, the health of these patients may deteriorate rapidly, thereby precluding adequate discussion about resuscitation status before admission to an ICU. This phenomenon also may be explained by physician bias toward the selection of patients who lack a specified resuscitation status for admission to the MICU. Previous studies18 19 20 have shown that physicians are less likely to transfer patients with DNR status to the ICU for aggressive intervention. Further investigation of prognostic factors for lung transplant recipients requiring ICU admission eventually may improve our ability to inform patients or surrogate decision-makers about end-of-life decisions in this group of patients, thus avoiding futile or heroic medical care if it is not indicated.

Although this study is the first of its kind in this population, it remains a small study, and as such certain factors such as resistant organisms and antibiotic resistance patterns could not be analyzed sufficiently. Other limitations include its retrospective design, which made it difficult to analyze certain data such as the impact of immunosuppressive regimens on patient outcome.

In conclusion, survival was associated with shorter duration of mechanical ventilation, lower APACHE III scores, higher admission albumin levels, and less organ system dysfunction. Overall, survivors were less severely ill, as demonstrated by lower APACHE scores and fewer organ systems involved. However, those survivors who were admitted to the hospital for elective surgical procedures introduce a potential source of bias. The factors described should be considered when counseling patients and families regarding life support in long-term lung recipients. Although the prognosis associated with MICU admission is poor, most patients present with acute or subacute precipitating factors that are potentially treatable if an aggressive posture is adopted for earlier diagnosis and therapy. Our study supports the concept of providing aggressive life support to these patients. New modalities for the prompt diagnosis and treatment of infection or rejection within patient populations are on the horizon and can potentially impact on ICU and long-term outcomes.


   Footnotes
 
Abbreviations: ALI = acute lung injury; APACHE = acute physiology and chronic health evaluation; BOS = bronchiolitis obliterans syndrome; DNR = do not resuscitate; MICU = medical ICU; SIRS = systemic inflammatory response syndrome

Received for publication July 2, 2001. Accepted for publication May 29, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Maurer, JR, Frost, AE, Estenne, M, et al (1998) International guidelines for the selection of lung transplant candidates: the International Society for Heart and Lung Transplantation, the American Thoracic Society, the American Society of Transplant Physicians, the European Respiratory Society. J Heart Lung Transplant 17,703-709[ISI][Medline]
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