Multiple organ system failure was first described in the mid-1970s in adult patients as a complication after repair of ruptured abdominal aortic aneurysms (1) and represents the most severe form of organ dysfunction. As such, the term Multiple Organ Dysfunction Syndrome (MODS) was adopted to focus on the process of organ dysfunction rather than failure. MODS has been described in connection with a variety of disease processes stemming from both systemic and localized insults and is recognized as a leading contributor to death and disability in the PICU (2–4).
Mortality rates in the PICU have fallen markedly in the last 10 years, to as low as 1.3% (35–9) as best-practice care guidelines have been implemented, PICUs have been routinely compared with national benchmarks (9–11), and use of organ support technology, such as extracorporeal membrane oxygenation (ECMO) and continuous renal replacement therapy (CRRT), has increased (1213). In addition, average severity of illness has decreased in many ICUs due to earlier transfer of patients to the PICU prompted by early warning system scores and rapid response teams (1415). Nonetheless, the prevalence of chronic illness in patients who use PICU services continues to rise as more children survive previously fatal neonatal and pediatric diseases, potentially driving an increase in baseline PICU mortality risk (16–18).
We previously reported outcomes of pediatric MODS present on the day of ICU admission in the 2004–2005 Virtual Pediatric Systems (VPS, LLC) dataset using International Pediatric Sepsis Consensus Conference (IPSCC) organ dysfunction criteria (161920). Given the improvement in overall PICU mortality, the increase in utilization of organ support technology, and changes in case-mix over the last decade, we sought to describe the current epidemiology and outcomes of day 1 MODS in the 2014–2015 VPS dataset. This project was deemed exempt from institutional review board review by the Human Subjects Protection Program at the University of Arizona.
MATERIALS AND METHODS
The VPS database is a prospective observational cohort of consecutive PICU admissions from diverse PICUs (721). Data are entered by trained individuals, and data quality and completeness are continually assessed by VPS. Several risk-of-mortality scores and their raw data variables are mandatory elements of data collection, in addition to patient demographics, diagnoses, and interventions. We obtained the VPS data for consecutive patient admissions from January 1, 2014, to December 31, 2015, for the purposes of this study. Because VPS guidelines state that systolic blood pressure (SBP) should be collected for each patient, we excluded hospitals with greater than 10% missing values for SBP. We excluded patients less than 1 month or greater than 18 years old, if they were pregnant, had continuous cardiopulmonary resuscitation from time of PICU admission, less than 2-hour duration of PICU admission, or were admitted to the PICU after surgery to repair congenital heart disease (Fig. 1).
Day 1 MODS was defined as greater than or equal to 2 organs with dysfunction, present on day of admission to the PICU. We coded organ dysfunction based on age-specific IPSCC organ dysfunction criteria, using vital sign and laboratory values collected in the VPS dataset in a method previously described by our group (Fig. A, Supplemental Digital Content 1, http://links.lww.com/PCC/B23; legend, Supplemental Digital Content 2, http://links.lww.com/PCC/B24) (19), with two exceptions related to changes in VPS data collection. First, we were able to classify hematologic dysfunction by international normalized ratio values (in addition to platelet values). Second, we improved classification of IPSCC respiratory dysfunction by excluding patients with Pao2/Fio2 ratios less than 300 who had a diagnosis of cyanotic congenital heart disease or chronic lung disease (because these diagnoses are now reliably recorded). Primary outcomes for this study were death or a combined morbidity/mortality metric of death or poor neurologic outcome. Our study is designed as a retrospective observational cohort to describe the current epidemiology and outcomes of day 1 MODS by IPSCC organ dysfunction criteria.
Pediatric Overall Performance Category and Pediatric Cerebral Performance Category Scores
Sites participating in VPS can choose to collect Pediatric Overall Performance Category (POPC) and Pediatric Cerebral Performance Category (PCPC) scores, which are validated global and cognitive function scores, respectively (22). Both are graded on a 6-point scale with 1 indicating normal function and 6 indicating death. Scores obtained at time of admission reflect a “baseline” functional and cognitive status and “discharge” scores are reflective of patients’ status at time of discharge from the PICU (22). Poor neurologic outcome in this study was defined as a discharge POPC or PCPC score of greater than or equal to 3 with at least a 1 point worsening of POPC or PCPC score, to indicate at least a moderate disability at discharge that is a worsening from baseline.
We used previously published methods developed by our research group to classify 14 chronic illnesses categories in the VPS dataset (16): respiratory, cardiovascular, neurologic, endocrine, gastrointestinal, hematologic, rheumatologic, transplant, metabolic, genetic, renal, genitourinary, immune, and oncologic. Hematologic and oncologic categories were collapsed into a single category due to small frequencies. Chronic illness categories were mutually exclusive.
We report median (25–75th percentiles) for variables with skewed distributions and mean, sem, for variables with normal distributions. We assessed group differences in categorical and ordinal nonnormal continuous variables with chi-square and Mann-Whitney rank-sum tests, respectively. We assessed the effect of MODS and individual dysfunctional organ systems on mortality with chi-square test. We assessed the effect of MODS on log-transformed PICU length of stay with Student t test. We used multilevel mixed-effects logistic regression with patients clustered by hospital of origin to assess the independent effect of MODS, the number of dysfunctional organ systems, each type of organ dysfunction, and the presence of chronic illness on mortality, poor functional outcome or a combined poor outcome of death OR poor functional outcome. For logistic regression models, we controlled for patient age, race/ethnicity, sex, postoperative status, trauma status, limitations of care decisions, and preexisting chronic illness. Kaplan-Meier survival analysis was used to describe the effect of day 1 MODS or the number of dysfunctional organ systems on death over a 90-day observation time. Hazard ratios (HRs) were reported from Cox regression mixed-effects model, clustered by hospital of origin, and covariates of age, sex, race/ethnicity, presence of preexisting chronic illness, operative status, trauma status, and limitation of care decisions. Statistical analysis was accomplished using Statistical Analysis Systems, Version 9.4 (SAS Institute Inc. Cary, NC) and STATA/SE 14.1 software (StataCorp LLC, College Station, TX).
From 208,598 consecutive patient admissions, we identified 194,017 meeting inclusion and exclusion criteria in the 2014–2015 VPS dataset (Fig. 1). Operative admissions accounted for 26.7%, and 7.1% were following trauma. At least one preexisting chronic illness was present in 64.3% of admissions (Table 1). Overall unadjusted PICU mortality was 2.1%. Only 43,358 (22.3%) had baseline and discharge PCPC scores recorded, and 42,781(22.1%) had baseline and discharge POPC scores recorded (Table 1). Pediatric Index of Mortality 2 score risk-adjusted mortality was not different for patient admissions with POPC and/or PCPC scores recorded, as compared with patient admissions without these scores recorded, p value equals to 0.235 (odds ratio [OR], 1.09; 95% CI, 0.94–1.3).
Multiple Organ Dysfunction Syndrome
We identified MODS on day 1 of PICU admission in 14.4% of patient admissions (Fig. 1). Consistent with the categorization of day 1 organ dysfunction, patients with day 1 MODS had higher median Pediatric Risk of Mortality (PRISM) 3 scores with median PRISM 3 score of 3 versus 0 (p < 0.0001) (Table 1). Age was associated with the prevalence of day 1 MODS, with older children more likely to meet criteria for day 1 MODS (p < 0.0001) (Table 1). In multivariate analysis, there was no association between race/ethnicity and MODS, or sex and MODS. Preexisting chronic illness was associated with MODS (p < 0.0001) (Table 1). Patients with day 1 MODS were more likely to have baseline POPC (49.7% vs 29.3%) and PCPC (35.1% vs 16.5%) scores greater than or equal to 3 (p < 0.0001), indicating at least a moderate overall or cognitive disability.
PICU mortality was significantly higher for patients with day 1 MODS (10.3% vs 0.7%; p < 0.0001), and in multivariate analysis day 1 MODS was associated with an odds of death of 14.3 (95% CI, 13.0–15.7) (Table 2). Although infants had the lowest prevalence of MODS compared with other age groups, they had the highest hospital mortality (13.7%; p < 0.0001) when day 1 MODS was present. In multivariate analysis, infant age (OR, 2.0; 95% CI, 1.7–2.4) and age of 1–2 years (OR, 2.2 yr; 95% CI, 1.9–2.6 yr) were associated with increased odds of death as compared with children 15–18 years old. Operative patients had a lower prevalence of day 1 MODS than medical patients (12.5% vs 15.1%; p < 0.0001), and a lower mortality when day 1 MODS was present (5.5% vs 11.8%; p < 0.0001). Patients with day 1 MODS had longer median length of PICU stay (3.5 vs 1.4 d; p < 0.0001).
In hospitals where the presence or absence of limitation of support decisions and withdrawal of support decisions were routinely recorded within our analysis dataset, 5.8% of 148,188 eligible patients with MODS had limitation of support decisions in place during their PICU stay, compared with 0.8% of patients without MODS (p < 0.0001) (Table 1). Of patients with day 1 MODS, 4.7% had withdrawal of life-sustaining therapies. Of day 1 MODS patients who died, 43.1% had limitation of support decisions in place, and 41.6% had withdrawal of life-sustaining therapies.
MODS was associated with greater (worse) change in POPC and PCPC scores at PICU discharge. Of patients with day 1 MODS, 16.4% had at least 1 category higher, and 6.0% had at least 2 category higher, POPC score (vs 11.3% and 1.8% of patients without day 1 MODS; p < 0.0001). For PCPC scores, 8.8% had at least 1 category higher, and 3.5% had at least a 2 category higher score (vs 2.4% and 0.5% of patients without MODS; p < 0.0001) (Table 2). Patients with day 1 MODS had higher rates of death or poor neurologic outcome (15.3% vs 2.6%; p < 0.0001) (Table 2). In multivariate analysis, day 1 MODS was associated with an odds of death or discharge alive with poor neurologic outcome of 6.7 (95% CI, 6.0–7.4) (Table 2).
Number of Dysfunctional Organ Systems
The number of dysfunctional organ systems present on day 1 of PICU admission was associated with death and with death or poor neurologic outcome. Mortality for dysfunction of 2, 3, and greater than or equal to 4 organ systems was 6.1%, 22.5%, and 47.8%, respectively (Table 3). Each additional dysfunctional organ system present on day 1 was associated with higher odds of death or odds of a combined outcome of death or discharge alive with poor neurologic outcome (Table 3). In 90-day Kaplan-Meier survival analysis, MODS present on day 1 was associated with higher hazard of mortality (HR, 4.5; 95% CI, 4.2–4.9) (Fig. 2). There was a dose-response effect of each additional organ dysfunction on the odds of death over the 90-day observation period (Fig. 2). The HRs for number of dysfunctional organ systems present on day 1 of PICU admission on 90-day survival were as follows: (1 HR = 3.5 [3.0–4.2], p < 0.0001; 2 HR = 8.2 [7.0–9.7], p ≤ 0.0001; 3 HR = 20.5 [17.2–24.4], p < 0.0001; and ≥ 4 HR = 32.3 [26.6–39.2], p ≤ 0.0001).
Impact of Individual Dysfunctional Organ Systems
Respiratory dysfunction was most common, present on day 1 in 29.6% of patient admissions (Table 4), followed by cardiovascular and neurologic dysfunction, occurring in 21.1% and 7.5% of patient admissions, respectively. Day 1 respiratory, neurologic, and hematologic dysfunction had the highest independent odds of death with OR of 10.7, 5.5, and 4.9, respectively (Table 4). With regard to functional outcomes, day 1 hematologic (OR, 3.0) and respiratory (OR, 2.4) dysfunction had the highest odds of change in POPC score greater than or equal to 2, while respiratory (OR, 4.9) and neurologic (OR, 4.5) dysfunction had the highest odds of change in PCPC score greater than or equal to 2 (Table 4).
Patients with day 1 MODS in our cohort experienced higher mortality and morbidity than patients without day 1 MODS. Our results reconfirm the importance of organ dysfunction as an appropriate method to assign risk and resource utilization to patients. When compared with our report 1 decade ago from the 2004–2005 VPS database, current day 1 MODS prevalence is lower (14.4% vs 18.6%), the odds of mortality from day 1 MODS is higher (OR 14.3 vs OR 11.1), and the odds of death or poor neurologic outcome after day 1 MODS is lower (OR 6.7 vs OR 8.7) (1619). These comparisons should be made with the caution, however, as differences exist between these cohorts with regard to case-mix, prevalence of chronic illness, baseline cognitive and functional disability, and the size of the two cohorts, limiting the ability to form strong conclusions from these results. Nevertheless, our data suggest that current PICU practices may reduce the odds of poor neurologic outcome after a PICU admission with day 1 MODS and that further prospective research is needed to characterize long-term outcomes after MODS, and to study how decisions regarding limitation of support and withdrawal of support in children admitted with MODS are made.
MODS prevalence is reported as 6–57%, depending on the MODS definition used and population studied (23). Variability in definitions and populations studied makes direct comparison of trends in MODS outcomes between studies, and over time, difficult. A strength of our study is the use of a consistent database, methodology to classify organ dysfunction, and MODS definition, which allows for comparison to results in previously published work. Limitations exist for IPSCC organ dysfunction criteria. They were developed by expert, consensus opinion to identify organ dysfunction in sepsis, but have been used to characterize organ dysfunction in a variety of disease states (1620). Other organ dysfunction scores, such as the Pediatric Logistic Organ Dysfunction (PELOD and PELOD 2) score, were developed with a data-driven approach (2425). IPSCC criteria were not developed in an evidence-based fashion, and yet they do characterize a step-wise risk of mortality in the general PICU population, as demonstrated in our current and previous study. Future research to compare current epidemiology of organ dysfunction using a variety of organ dysfunction scores is a needed next step.
Day 1 MODS captures the majority of children who develop MODS during their PICU stay (26). In the prospective RESTORE study, Weiss et al (26) reported that only 10% of patients with MODS develop organ dysfunction on day 2 or later. PICU bed utilization in the United States has increased, at a rate higher than population growth (27–29). The drivers for this growth in PICU bed capacity is not clear. The increased prevalence of pediatric chronic illness, and use of early warning systems and rapid response teams designed to initiate earlier transfer of patients to the PICU, may have increased PICU utilization (1415). The increase in the number of U.S. PICU beds with higher patient volume and earlier PICU transfer may contribute to a lower prevalence of MODS (2829). Our 2014–2015 VPS database analysis also differs in the number of PICU’s participating in VPS. We analyzed patients from 124 PICUs, quite an increase from the 24 PICUs included in our analysis in the 2004–2005 cohort. This expansion of units within VPS may also impact measured outcomes of MODS due to changes in unit volume, provider staffing, and patient case-mix.
PICU care practices and outcomes for clinical trials have focused on improvement of neurologic and functional outcomes, with an emphasis on quality of life after PICU hospitalization (3031). Published studies focus on long-term outcomes to better target PICU care to meaningful results for survivors and their families (22303233). It is possible that this shift in the odds of mortality and morbidity in the setting of day 1 MODS reflects an increased in family discussions regarding limitation of support decisions and discharge quality of life.
Importantly, we were able to examine limitation of support decisions and withdrawal of support in patients who died. We found that 43.1% of day 1 MODS patients who died had limitation of support decisions in place during their ICU stay, and 41.6% were withdrawn from support. We are unable to evaluate limitation of support and withdrawal of support in the 2004–2005 VPS data. Our findings are consistent with published data in the PICU regarding withdrawal of support. In a secondary analysis of 10,078 children admitted to hospitals within the Collaborative Pediatric Critical Care Research Network, 2.5% of families discussed limitation or withdrawal of support with clinicians (34). Factors associated with increased likelihood of these discussions included reduced functional status and cancer diagnosis, while neurologic illness and postoperative status were associated with less likelihood of these discussions (34). In our retrospective cohort study, we cannot know if shifts in morbidity and mortality outcomes of day 1 MODS over the last decade reflect a focus on cognitive and functional outcomes and an increase in withdrawal of support decisions. Further research is needed to understand end of life decisions made by parents and the interaction between morbidity and mortality for children with MODS.
We identified differences in prevalence and outcomes for specific organ dysfunction types which could contribute to differences in morbidity and mortality. The prevalence of respiratory and neurologic dysfunction is lower in the 2014–2015 cohort than in the 2004–2005 cohort. Differences in organ dysfunction prevalence may impact morbidity and mortality. Mortality is lower in the current decade for cardiovascular, renal, and hepatic dysfunction and could relate to increased use of organ support technology such as ECMO, CRRT, and membrane absorbent recirculating system (MARS) to treat patients with cardiovascular, renal, and hepatic dysfunction (12133536). In a 2015 meta-analysis, He et al (36) reported that MARS significantly improved survival in patients with acute liver failure. Similarly, multiple studies report the use and improved organ function with use of ECMO and CRRT, alone or in combination (1337). Further research is needed to examine how use of individual organ support therapies might alter the cognitive and functional outcomes of specific types of organ dysfunction present at admission to the PICU.
In our analysis, we found that any chronic illness increased risk for MODS, and chronic illness was associated with an increased odds of death or poor neurologic outcome. Our findings from the VPS database are consistent with other reports. In a single-center study of 554 critically ill children in the United Kingdom, O’Brien et al (17) identified chronic illness in 67.1% of all PICU patients and found that any chronic illness was associated with longer length of stay and higher mortality. As children continue to survive after premature birth, after PICU hospitalization, and with chronic illnesses which were previously fatal, the prevalence of children with chronic illness is likely to continue to rise in the PICU. These patients have longer PICU length of stay and are at high risk of MODS, mortality, and worsening functional status after PICU discharge.
A limitation of our study is that we cannot identify every component of the IPSCC definition for organ dysfunction, although we can identify at least one element of organ dysfunction for each organ system in the IPSCC definition. This could result in a potential underestimate of MODS prevalence and either an over or underestimate of MODS related mortality. In addition, we rely on usual practice to capture laboratory values which reflect organ dysfunction. Due to this limitation, we may misclassify patients as not having organ dysfunction when in fact they do, if their clinician did not order a given laboratory value. In addition, POPC and PCPC scores offer limited insight into functional outcomes, and more granular functional outcome scores have been developed recently, although none are currently collected in the VPS database. More granular measures would better capture the change in functional status for children with MODS. Our findings suggest that comprehensive evaluation of long-term functional outcomes for children admitted with MODS is needed. We had the usual limitations of database investigations.
By excluding patients admitted after cardiac surgery, some patients included in the analysis 1 decade ago were absent from our current dataset. However, few cardiovascular ICUs were participating in VPS 1 decade ago. We anticipated the inclusion of cardiac surgical patients in the current analysis would more significantly alter the case-mix as compared to 2004–2005, than would exclusion of cardiac surgery patients.
Another limitation of our study is that we do not know the duration of illness prior to PICU admission, and ICU’s may use different admission criteria with regard to organ dysfunction. Earlier transfer to the PICU might artificially lower the prevalence of day 1 MODS (14). The large number of participating institutions is an asset in this regard, as not all institutions use early warning transfer protocols. As the VPS records consecutive patient admissions, we may also have duplicate patients who were readmitted after discharge back to the ICU.
MODS present on day 1 of PICU admission continues to be a major source of morbidity and mortality in the PICU, but risk of poor neurologic outcome may be improved with current PICU care. Prospective studies are needed to examine long-term outcomes after MODS and to better understand how limitation and withdrawal of support decisions are determined in patients admitted with MODS.
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functional outcome; intensive care; Multiple Organ Dysfunction Syndrome; organ dysfunction; pediatrics
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