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doi:10.1378/chest.06-2783
(Chest. 2007; 132:829-835)
© 2007 American College of Chest Physicians
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Nonpulmonary Organ Dysfunction and Its Impact on Outcome in Patients With Acute Respiratory Failure*

Ashutosh N. Aggarwal, MD, FCCP; Ritesh Agarwal, MD; Dheeraj Gupta, MD, FCCP and Surinder K. Jindal, MD, FCCP

* From the Department of Pulmonary Medicine, Postgraduate Institute of Medical Education and Research, Chandigarh, India.

Correspondence to: Surinder K. Jindal, MD, FCCP, Department of Pulmonary Medicine, Postgraduate Institute of Medical Education and Research, Chandigarh 160012 India; e-mail: skjindal{at}indiachest.org

Abstract

Purpose: This study aimed to define the prevalence, severity, and progression of nonpulmonary organ dysfunction, and its impact on outcome in patients with acute respiratory failure (ARF) at a respiratory ICU of a tertiary referral hospital in northern India.

Methods: Daily patient data were collected on 711 adult patients with ARF to calculate component and total nonpulmonary sequential organ failure assessment (SOFA) scores. Hospital survival was the main outcome measure. Multiple logistic regression modeling was conducted to assess contribution of incremental dysfunction of various nonpulmonary organ systems to mortality. Kaplan-Meier curves were drawn to assess temporal trends in survival, and group comparisons were based on log-rank test. Cox proportional hazard modeling was performed to define hazards of earlier mortality. Discrimination was evaluated using receiver operating characteristic (ROC) curves.

Results: Four hundred seventy-five patients (66.8%) had one or more nonpulmonary organ dysfunctions at hospital admission. The overall hospital mortality rate was 33.9%. Hospital survival rates and median survival declined steadily as the number of organs involved increased. Admission, maximum, and {Delta}SOFA scores were significantly higher in nonsurvivors. Increasing baseline cardiovascular and neurologic SOFA scores, and corresponding {Delta}SOFA scores, were associated with progressively higher odds of hospital mortality, as well as increasing hazard for earlier mortality after adjustment for etiology of respiratory failure. Maximum nonpulmonary SOFA score was the best discriminator in predicting mortality (area under ROC curve, 0.767).

Conclusion: Baseline and new-onset nonpulmonary organ dysfunction significantly influences hospital survival in patients with ARF.

Key Words: hospital mortality • multiple organ failure • multivariate analysis • respiratory insufficiency • severity of illness

The traditional outcome of critically ill patients admitted to the ICU has always remained hospital mortality. Indeed, standard severity scoring systems such as the acute physiology and chronic health evaluation and the simplified acute physiology score use values obtained within the first 24 h of ICU stay to predict hospital outcome. However, these scores ignore the many factors that influence patient outcome during ICU stay beyond the initial 24 h. Thus, there is a need for severity indexes that monitor and quantify disease process and organ dysfunction in a continuous and dynamic fashion.

A few scores have been developed to assess organ dysfunction/failure.123 One of the most widely used such scores, the sepsis-related organ failure assessment score, was developed to evaluate organ dysfunction in patients with sepsis.3 Later, it was renamed the sequential organ failure assessment (SOFA) score because its utility was not restricted merely to patients with sepsis. Although primarily developed to describe organ dysfunction, and not predict mortality risk, correlation between organ dysfunction/failure and outcome has been demonstrated in both prospective and retrospective analyses.345

We are actively involved in managing patients with acute respiratory failure (ARF) at our specialized respiratory ICU (RICU). We have earlier shown that failure of extrapulmonary organs was a predictor of mortality in patients of ARDS.6 Other investigators789101112131415 have also shown that outcome of patients with ARF is influenced by nonpulmonary organ dysfunction. We found that standard severity scoring systems developed in the West, based on physiologic assessment in the first 24 h of RICU stay, perform poorly in describing hospital outcome in our patients.16 One factor for such discrepancy could be a difference in the patient spectrum.17 Additionally, progression of nonpulmonary organ dysfunction, either manifest at hospital admission or developing later, may have greater influence on outcome. We therefore planned this study to do the following: (1) describe prevalence, severity, and progression of nonpulmonary organ dysfunction; and (2) assess the contribution of such dysfunction at hospital admission and subsequently to patient outcome in patients with ARF.

Materials and Methods

We prospectively recorded demographic, clinical, laboratory, and therapeutic data from hospital admission to discharge on all adult patients (aged ≥ 15 years) with ARF managed at our RICU over a 5-year period. The study was approved by our hospital ethics committee. Data were registered on hospital admission and every 24 h thereafter, using the worst daily values for all variables of interest. Day 0 was defined as the interval from time of RICU admission to 8:00 AM the next day; data from this time period were used to calculate admission SOFA scores. All remaining days were calendar days from 8:00 AM to 8:00 AM. In accordance with available description of the SOFA, initial missing laboratory results were recorded as normal. Subsequently, missing values for investigations not performed earlier were considered normal, and those for tests done previously were recorded by carrying the last available value forward. The primary outcome variable was hospital mortality. Patients dying within 3 days of RICU admission were arbitrarily categorized as having early mortality. SOFA scores were not calculated after RICU discharge.

Nonpulmonary (cardiovascular, neurologic, renal, hepatic, and coagulation) organ dysfunctions were assessed using the SOFA.3 In sedated patients, the assumed Glasgow coma scale (recorded prior to sedation) was used to evaluate neurologic status. An aggregate score (total nonpulmonary SOFA score) was calculated summing the worst scores for each nonpulmonary component for each day of RICU stay. Organ dysfunction was defined as SOFA score of 1 to 2 points, and organ failure as score higher than that. The quantum of organ dysfunction/failure appearing after RICU admission ({Delta}SOFA) was computed by subtracting the admission SOFA score from the maximum SOFA score during RICU stay.

Daily SOFA scores for all nonpulmonary organ systems were compared between survivors and nonsurvivors using the Mann-Whitney U test. The discriminative power of baseline and maximum aggregate scores, and their difference, in predicting hospital mortality was defined as area under the receiver operating characteristic (ROC) curve.18 Survival probabilities and median survivals were calculated by Kaplan-Meier method, and comparison between different groups was performed using the log-rank test.19 A Cox proportional hazards model was constructed to study association between admission SOFA and {Delta}SOFA scores, and time to death in hospital, after adjusting for age, gender, and diagnosis. We also fitted a logistic regression model to evaluate relative contributions of {Delta}SOFA and admission SOFA scores to hospital outcome.20

Results

Data from 711 RICU admissions (428 men [60.2%] and 283 women [39.8%]) were analyzed. More than half (53.7%) required respiratory support for either ARDS or acute exacerbation of bronchial asthma or COPD (Table 1 ). The overall hospital mortality rate was 33.9%, with highest rates for patients with ARDS (Table 1). Of these, 14 deaths occurred in wards after patients had been transferred out of the RICU. On initial evaluation, 475 patients (66.8%) had at least one nonpulmonary organ dysfunction, and 281 patients (39.5%) had at least one nonpulmonary organ failure. The most common organ dysfunction or failure at hospital admission was neurologic (290 patients [40.8%] and 154 patients [21.7%], respectively), followed by renal (246 patients [34.6%] and 104 patients [14.6%]).


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  		Table 1.. Etiology and Outcome of Respiratory Failure in the Study Population

 
While more than three fourths of patients without any baseline nonpulmonary organ dysfunction or failure survived, 69.4% patients with dysfunction of three or more such organs, and 76.0% patients with two or more such organ failures died (Table 2 ). Hospital survival rates declined as number of organs involved increased (Table 2). Most patients with four or more organ dysfunctions (11 of 18 patients, 61.1%) or three or more organ failures (12 of 18 patients, 66.7%) had early mortality (Table 2). Total admission nonpulmonary SOFA scores were higher in those who died than in those who survived (median, 4.0 vs 2.0; p < 0.001) [Fig 1 ]. Mean daily component organ SOFA scores in nonsurvivors were also uniformly higher than survivors for all nonpulmonary organ systems during the first week of RICU stay (Fig 2 ). Maximum total nonpulmonary SOFA scores during hospital stay were significantly higher in those who died than those who survived (median, 6.0 vs 2.0; p < 0.001) [Fig 1]. Similarly, {Delta}SOFA scores were significantly higher in those who died than those who survived (median, 1.0 vs 0.0; p < 0.001) [Fig 1]. As a result, median hospital stay progressively decreased as the number of organs failing at RICU admission increased (Fig 3 ). These differences were significant on formal log-rank test (p < 0.001).


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  		Table 2.. Relationship of the Number of Nonpulmonary Organs (Cardiovascular, Neurologic, Renal, Hepatic, or Coagulation) Showing Dysfunction, or Failing, at RICU Admission With Hospital Outcome and Morbidity

 

Figure 1
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  		Figure 1.. Distribution of admission and maximum values, as well as the difference between the two, of total nonpulmonary SOFA scores. Boxes represent the interquartile range of values in survivors (clear boxes) and nonsurvivors (shaded boxes), with median in-between. Whiskers on either side represent the fifth and ninety-fifth percentile values.

 

Figure 2
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  		Figure 2.. Distribution of mean component nonpulmonary SOFA scores in the first week of hospital stay among survivors (clear bars) and nonsurvivors (shaded bars). Significant differences between the two are represented by dots on top.

 

Figure 3
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  		Figure 3.. Kaplan-Meier survival curves stratified based on number of nonpulmonary organs failing at admission to the RICU.

 
Few patients also had new nonpulmonary organ dysfunction during RICU stay. The most common systems involved were cardiovascular and neurologic (77 occurrences and 73 occurrences, respectively). More than 75% instances of new cardiovascular, neurologic, or renal dysfunction occurred in the first week after RICU admission.

After adjustment for gender, age, and etiology of respiratory failure (categorized as per six major heads outlined in Table 1), cardiovascular and neurologic dysfunction, as well as {Delta}SOFA values for cardiovascular system, independently increased the odds of both early and delayed (> 3 days) hospital mortality (Table 3 ). After similar adjustment, progressively increasing admission SOFA and {Delta}SOFA values for cardiovascular and neurologic dysfunction independently increased the hazard of hospital mortality (Table 3).


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  		Table 3.. Influence of Initial and New-Onset Nonpulmonary Organ Dysfunction Over the Odds of Early, Delayed, and Overall Hospital Mortality, and Hazards of Overall Hospital Mortality*

 
The discriminative ability of the baseline total nonpulmonary SOFA score incorrectly predicting hospital outcome was moderate (area under ROC curve, 0.767). Maximum nonpulmonary SOFA score during RICU stay was a slightly (though not significantly) better discriminator (Fig 4 ).


Figure 4
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  		Figure 4.. ROC curves to assess the discriminative ability of SOFA scores in identifying ultimate survival status. AUC = area under the ROC curve (± SE).

 
Discussion

Organ dysfunction is a continuum, from normal organ function, through varying degrees of organ dysfunction, to severe organ failure, and alters over the duration of patient’s ICU stay. While clinicians understand the need to describe and quantify organ dysfunction, there is no consensus on the exact modality to do so. The SOFA is one such widely used instrument that not only describes severity of organ dysfunction, but also provides an aggregate score as a measure of morbidity related to organ dysfunction/failure. It has earlier been applied to several groups of ICU patients (medical, cardiac, trauma, pancreatitis, acute renal failure, and hematologic malignancy).2122232425 When comparisons were made among organ dysfunction systems in the predictive ability of outcome, the SOFA system demonstrated the best performance.252627 We used this measure to study nonpulmonary organ dysfunction in a group of patients already having respiratory failure. A similar approach has been earlier used in neurocritical care to evaluate influence of nonneurologic organ dysfunction on patient outcome.28

With advancements in techniques of providing assisted respiratory support, outcome of respiratory failure is becoming more dependent on level of dysfunction of nonpulmonary organs. Most of this information is derived from ARDS patients, but the scenario appears largely similar for other causes of ARF.7891011121314 However, these data stem from ICUs in the developed world. No real data are available for developing countries like India, where spectrum of patients, as well as resources, are different from the West. Our analysis reveals that irrespective of nature of organ involvement, hospital outcome worsened, both in terms of increased mortality and earlier death, as number of nonpulmonary organs failing increased. This is consistent with earlier reports1315 that overall prognosis for ICU patients with ARF alone is good, and mortality rates are increased by dysfunction in other organs. In an international study29 of patients receiving mechanical ventilation, overall ICU mortality more than doubled when shock, renal failure, coagulopathy, hepatic failure, or ARDS were superimposed.

We studied three aspects of nonpulmonary organ dysfunction using admission SOFA, {Delta}SOFA, and maximum SOFA scores. All three indexes address complementary facets of a complex response, and are independently important in their own domains. The admission SOFA score measured the total magnitude of nonpulmonary organ dysfunction/failure already manifest at the time of transferring the patient to RICU. This measurement is useful to initially stratify patients according to severity of illness. At admission, nearly two thirds of patients had nonpulmonary organ dysfunction. This is partly attributed to the systemic nature of several disease processes resulting in respiratory failure. Further, many patients were initially managed in general wards or other health-care facilities before being transferred to RICU when they became "too sick." Such "lead-time bias" artificially inflates both prevalence and magnitude of organ dysfunction at initial evaluation. {Delta}SOFA reflected overall patient improvement or deterioration during RICU stay, and was potentially influenced both by disease progression and by treatment offered. We have shown that new organ dysfunction may appear early in the course of RICU stay, and a scoring system permitting regular surveillance of organ function is definitely needed.30 The fact that {Delta}SOFA influenced patient outcome even after adjusting for admission SOFA scores suggests that strategies directed at prevention and/or limitation of further organ dysfunction may influence prognosis.5 Lastly, maximum nonpulmonary SOFA score is a surrogate for cumulative morbidity related to dysfunction of all nonpulmonary organ systems. This index had the best discrimination in correctly predicting hospital outcome out of all three indexes studied in our study, similar to previous experience.530

Both cardiovascular and neurologic systems stand out in our analyses. These were the most common organs showing dysfunction/failure at initial evaluation, and had the maximum difference in mean values between survivors and nonsurvivors during the first week of RICU stay (Fig 2). They also had the highest odds for hospital mortality for each unit increment in baseline component scores. They were the only systems whose dysfunction at admission was significantly associated with early mortality, and whose worsening in RICU (determined by {Delta}SOFA values) was independently associated with delayed mortality (Table 3). They were also the only organs whose baseline and {Delta}SOFA values had significantly elevated adjusted hazards of earlier mortality (Table 3). In an earlier prospective multicenter database using SOFA, principal components analysis demonstrated existence of a two-factor structure, where the first factor comprised respiratory, cardiovascular and neurologic scores, and the second comprised coagulation, hepatic, and renal components.5 Our results strengthen a case for such a two-tier association because all patients had respiratory failure, and cardiovascular and neurologic dysfunction accounted for bulk of the association with hospital outcome. One tempting explanation for such observations is the presence of two targets in this complex syndrome, with the first association representing primary insult, and the second its late consequences appearing as a result of the host response to primary insult.5 Such a scenario could also partly explain our seemingly contradictory observation that dysfunction of hepatic and coagulation systems was associated with improved survival (Table 3) because subsequent recovery of these secondary disturbances may have reflected an overall resolution of the primary pathophysiologic processes necessitating ICU admission. Our results are also consistent with another international prospective study4 reporting ICU outcome for patients with individual organ failure alone and in combination with other organ failures. In this study,4 ARF was present in 16.6% of patients, with a mortality rate of 20.7%. The combination of respiratory with cardiovascular or neurologic failure was associated with significantly higher mortality rates of 55.4% and 48.1%, respectively. The high prevalence of neurologic dysfunction in our study is related to a high proportion of patients with exacerbations of obstructive airways disease (in which altered sensorium is an indication to institute ventilatory support), and the general practice of intubating patients of hypoxemic respiratory failure when they show altered mentation.

What do our results add to existing knowledge base? Firstly, we focused on ARF due to diverse medical etiologies. Most of available literature on this subject focuses heavily on ARDS, which accounted for less than a third of all patients studied by us. Secondly, we have shown that baseline organ dysfunction influences not only early, but also delayed, mortality in ARF. The relationship to an early adverse outcome appears logically clear. An influence on delayed mortality is more difficult to explain but may be partly related to different therapeutic interventions aimed at providing organ specific support, but not reversing basic pathophysiologic mechanisms. Lastly, our efforts prove that use of instruments measuring organ dysfunction can be successfully applied in Indian ICUs to provide additional information to treating clinicians.

Footnotes

Abbreviations: ARF = acute respiratory failure; RICU = respiratory ICU; ROC = receiver operating characteristic; SOFA = sequential organ failure assessment

The authors have no conflicts of interest to disclose.

Received for publication November 15, 2006. Accepted for publication May 25, 2007.

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P. S. Barie, L. J. Hydo, S. R. Eachempati, S. K. Jindal, A. N. Aggarwal, D. Gupta, and R. Agarwal
Nonpulmonary Organ Dysfunction and Mortality With Acute Respiratory Failure
Chest, August 1, 2008; 134(2): 467 - 468.
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