Sepsis, an acute, life-threatening dysregulated response to infection, affects millions of patients within the United States annually and 30 million worldwide (1 , 2). Studies indicate that the incidence of sepsis, known prior to 2016 as severe sepsis, is increasing at the national level (3–5). At the same time, sepsis-related in-hospital mortality appears to be decreasing (5–8).
Sepsis survivors frequently experience 30-day hospital readmissions (9–19). The costs of hospital readmissions after sepsis have been estimated at 3 billion dollars (19), reinforcing sepsis as the most expensive inpatient medical condition (20). As part of the Affordable Care Act, passed in March of 2010, a Hospital Readmissions Reduction Program (HRRP) was developed. Starting in October 2012, financial penalties for hospitals with higher than expected 30-day readmission rates were implemented for targeted conditions (e.g., pneumonia). Despite being the most costly cause of readmission, sepsis is not a targeted condition of the HRRP.
Little is known about the relationship between sepsis incidence, in-hospital mortality, and postdischarge outcomes among sepsis survivors over time. Specific to sepsis survivorship, it is unclear whether the rate of hospital-based acute care use after sepsis, including 30-day hospital readmissions and emergency department (ED) treat-and-release visits, has changed over time. To examine these aspects of sepsis, which matter to patients and families (21), we conducted a retrospective cohort study within an integrated academic medical center between 2010 and 2015. As a nontargeted condition of the HRRP, we hypothesized that the rate of hospital-based acute care use after sepsis, and 30-day readmission rate and ED treat-and-release visits specifically, would remain stable (i.e., readmission rates would not decrease over time), leading to a rising number of readmissions that follow a recent sepsis hospitalization. Further, we hypothesized that readmission rates after pneumonia—a diagnosis targeted by the HRPP—would decrease over time.
The University of Pennsylvania Institutional Review Board approved the study (Protocol no. 818852) with an informed consent exemption.
We conducted a multicenter retrospective cohort study within the University of Pennsylvania Health System (UPHS), an integrated academic healthcare system consisting of three acute care hospitals in Philadelphia, PA: The Hospital of the University of Pennsylvania, Penn Presbyterian, and Pennsylvania Hospital.
We evaluated adult medical and surgical admissions to UPHS hospitals between July 1, 2010, and June 30, 2015. Given the outcomes of interest, and based on prior work (9 , 10 , 22), we excluded observation stays, admissions with a disposition of left against medical advice (AMA), transfer to another hospital, or when disposition was missing. In accord with the Agency for Healthcare Research and Quality approach to readmissions (23), and prior work (9 , 10), an admission could serve as an index admission and a hospital readmission. For analyses pertaining to rehospitalization, we limited our analyses to patients discharged alive and not transitioned to hospice, hereafter known as discharges at-risk for hospital readmission. In accordance with our Institutional Review Board, admissions discharged to a correctional facility were excluded from our readmissions analyses.
To examine the incidence, mortality, and readmission rates associated with sepsis hospitalizations, we merged administrative and electronic health record datasets. The quality of the administrative dataset using this approach had been previously validated (24) and subsequent quality assurance performed (9 , 10). As in prior studies (9 , 10), we collected information on sociodemographics, comorbid conditions, and hospitalizations in the prior year, in addition to hospitalization details.
We identified sepsis using International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) codes, using previously validated approaches (1 , 9 , 10 , 24 , 25). As the study period predated the 2016 definitions (26), we used administrative codes that align with the categories of sepsis, severe sepsis, and septic shock in accord with the 2001 definitions (27). We identified sepsis hospitalizations using three approaches: (1) explicit diagnosis codes for sepsis (ICD-9-CM code 995.91), referred to hereafter as explicit sepsis, (2) explicit diagnoses codes for severe sepsis and septic shock (995.92, 785.52), referred to hereafter as explicit severe sepsis, and (3) modified Angus approach of concurrent ICD-9-CM codes for infection (including codes for septicemia) and organ dysfunction (1 , 24 , 25), referred to hereafter as implicit severe sepsis.
For comparison, we examined 30-day readmission rates after hospitalizations for acute myocardial infarction, congestive heart failure, and pneumonia (independent of sepsis status) over the study period using established ICD-9-CM codes (22). These conditions were selected as they are the high-risk conditions targeted by the HRRP at its inception. Because coding for pneumonia has varied over time (28), and given our hypotheses, we also used the pneumonia and sepsis codes to identify three discrete admission categories: (1) pneumonia, nonsepsis admissions, (2) sepsis related to pneumonia admissions, and (3) nonpneumonia sepsis admissions.
To understand temporal changes in sepsis survivorship, we focused on trends in sepsis hospitalizations, sepsis survivors at-risk for hospital readmission, and postacute care use after sepsis. For postacute care use, we examined 7- and 30-day all-cause hospital readmission and ED treat-and-release visits within 30 days (9 , 29). We used a nonparametric test for trend across ordered groups (i.e., year) using the “nptrend” package in the Stata statistical software (Stata/IC 13 software; StataCorp, College Station, TX) for the primary analysis (30). This method is an extension of the Wilcoxon rank-sum test but differs in that it examines the ranks for the variable of interest across ordered groups (30).
First, we measured the incidence of sepsis hospitalizations and tested for changes over time. We completed this analysis separately for each sepsis coding strategy (explicit sepsis, explicit severe sepsis, and implicit severe sepsis). Next, we measured in-hospital sepsis-related mortality and again tested for changes over time. Additionally, we evaluated the trends in a composite of in-hospital mortality and discharged to hospice to account for potential hospice discharge practice changes. We also measured whether the proportion of deaths related to sepsis changed over time. We then examined the characteristics of sepsis survivors at-risk for hospital readmission over time.
Next, we evaluated 7- and 30-day all-cause hospital readmissions among sepsis survivors over time. We examined 30-day hospital readmissions after sepsis, and by discrete sepsis coding strategy, by year, to determine whether changes in readmission rates were driven by explicit cases and/or illness severity.
To examine whether readmission rates differed over time according to pneumonia status, we examined readmission rates among the three aforementioned subgroups: pneumonia, nonsepsis admissions; sepsis related to pneumonia admissions; and nonpneumonia sepsis admissions. As 2010 data began July 1, and 2015 data ended June 30, annualized volume is presented for these years.
We present the temporal trends in incidence, in-hospital mortality, in-hospital mortality and discharge to hospice, and 30-day readmission, at the monthly level, using 95% CI in graphical format using a local polynomial smoothing function. For statistical analyses, we used Stata 13 (StataCorp, College Station, TX). We defined significance as an α less than 0.05.
After excluding 80,423 nonmedical, nonsurgical health system admissions (e.g., obstetrics), 2,286 admissions where the patient left AMA, 1,777 admissions transferred to an outside hospital, and 333 admissions missing a disposition status, there were 275,600 medical and surgical admissions over 5 years. Of these 275,600 hospitalizations, 17,256 were sepsis hospitalizations (6.3%; 95% CI, 6.2, 6.4), including 7,603 explicit sepsis, 9,709 explicit severe sepsis, and 11,618 implicit severe sepsis.
As shown in Table 1 and Figure 1A, from 2010 to 2015, the proportion of sepsis hospitalizations increased more than two-fold, from 3.9% to 9.4% (p < 0.001); the absolute number increased from 2,224 in 2010 to 4,928 in 2015. Sepsis hospitalizations increased more than two-fold over time and independent of sepsis coding strategy (p < 0.001 for explicit sepsis, explicit severe sepsis, and implicit severe sepsis).
The in-hospital mortality rate for sepsis hospitalizations declined from 24.1% to 14.8% (p < 0.001) (Fig. 1B). Mortality declined over time for all sepsis definitions (p < 0.001) (Supplemental Table 1, Supplemental Digital Content 1, http://links.lww.com/CCM/D69). Despite the decline in sepsis case-fatality rate, given the increase in sepsis incidence, the total number of sepsis-related deaths increased from 536 to 728 from 2010 to 2015, and sepsis contributed to a higher percentage of in-hospital deaths over time (43.4% in 2010 to 55.4% in 2015; Fig. 1C).
As a result of rising sepsis hospitalizations and declining in-hospital mortality, the proportion of medical and surgical discharges at-risk for hospital readmission after a sepsis hospitalization (i.e., sepsis survivors) increased 2.9-fold, from 2.7% in 2010 to 7.8% in 2015 (Fig. 1D). The overall number of sepsis survivors at-risk for readmission increased from 1,502 in 2010 to 3,900 in 2015. The proportion of discharges at-risk for hospital readmission after a pneumonia hospitalization, regardless of sepsis status, began at a higher volume of cases, yet increased just 1.2-fold (2,186 hospitalizations in 2010 to 2,684 in 2015).
As shown in Supplemental Table 2 (Supplemental Digital Content 2, http://links.lww.com/CCM/D70), the age of sepsis survivors did not differ significantly over time. Clinically important differences, over time, include a shift in demographics (e.g., more female survivors), a shift in comorbid conditions (e.g., less malignancy among survivors), lower illness severity during the hospitalization (e.g., less ICU admission, shock, use of mechanical ventilation, procedures, and shorter hospital length of stay), and survivors were more likely to be discharged to home health services (26.9–33.5% over 6 years) and less likely to be discharged to skilled care or long-term acute care facilities.
Over 6 years, the 7- and 30-day hospital readmission rate of sepsis survivors declined modestly from 8.9% to 8.3% and 26.4% to 23.1%, respectively (Table 2). As a contrast, the 30-day hospital readmission rates were 10.8%, 18.2%, and 21.1% after acute myocardial infarction, heart failure, and pneumonia hospitalizations, respectively, and rates did not decline for any of these conditions between 2010 and 2015 (p = 0.67, p = 0.14, and p = 0.84 for trend).
The decline in 30-day all-cause hospital readmission after sepsis was offset by an increase in the rate of ED treat-and-release visits (from 2.8% in 2010 to a peak of 5.4% in 2014; p = 0.001). Additionally, despite the modest decline in readmission rates after sepsis, the total number of 7- and 30-day hospital readmissions of sepsis survivors increased nearly three-fold from 134 to 324 and 396 to 900, respectively.
The modest decline in 30-day all-cause hospital readmission after sepsis was present among explicit sepsis cases (p = 0.005) but not among explicit or implicit severe sepsis cases (p = 0.49 and p = 0.77, respectively) (Table 3). After combining explicit and implicit severe sepsis coding strategies, 30-day hospital readmission rates declined from 27.6% in 2010 to 22.9% in 2015 after sepsis (p = 0.005) but not after severe sepsis (26.4% in 2010 to 24.4% in 2015; p = 0.58) (Supplemental Table 3, Supplemental Digital Content 3, http://links.lww.com/CCM/D71). Contrary to our hypothesis, the declining readmission rate after sepsis was not explained by pneumonia admissions. Rather, there was a modest reduction in readmission rates after nonpneumonia sepsis admissions (p = 0.01).
In this multicenter observational study within an academic health system, we examined trends in hospital-based acute care use after sepsis, including 30-day hospital readmissions and ED treat-and-release visits, over a 6-year period. Consistent with previous reports using national data (1 , 3–5 , 31–33), we found a rising volume of sepsis hospitalizations and declining in-hospital mortality rate. As a result, sepsis survivors at-risk for hospital readmission increased nearly three-fold over time, suggesting that the growing number of sepsis survivors is not limited to Medicare beneficiaries (5). Given the long-term consequences of sepsis, which include recurrent infections and cognitive and physical impairment (10 , 11 , 34 , 35), this is a significant public health threat.
We found that the characteristics of sepsis survivors changed over time (e.g., more female survivors, lesser illness severity). For example, in 2010, 57% of sepsis survivors required ICU admission, compared with 35% in 2015. These observations reinforce the Stage Migration Effect (i.e., with increased awareness comes increased identification, often of cases with milder stages of disease) (36). These temporal shifts also highlight the importance of raising awareness of sepsis survivorship across ICUs and wards, both for evaluating the past medical history of newly admitted patients (i.e., is this patient a sepsis survivor?) and for discharge planning and anticipatory guidance, as 42% of hospital-based care encounters after sepsis may be preventable with effective out-patient management (15).
Between 2010 and 2015, the rate of 7- and 30-day hospital readmission after sepsis remained high, with rates higher than the HRRP targeted conditions. While 30-day readmission rates declined, the improvements were modest, decreasing from 28% in 2010 to 23% in 2015 after explicit sepsis and from 26% in 2010 to 24% in 2015 after severe sepsis. We found that readmission rates were largely similar after sepsis and severe sepsis, and both exceeded nationally targeted conditions. These findings, which suggest that patients hospitalized with infection who exhibit a systemic inflammatory response without overt organ dysfunction (i.e., sepsis in Sepsis-2) incur a readmission risk similar to those with organ dysfunction, require confirmation.
Further, the modest reduction in the 30-day hospital readmission rate was offset by an increase in the rate of ED treat-and-release visits. As a result, the rate of hospital-based acute care use after sepsis remained largely unchanged. Coupled with an expanding population of sepsis survivors, the total number of 30-day hospital readmissions after sepsis increased three-fold over 6 years.
Recent evaluations of the national impact of the HRRP demonstrated declines in hospital readmissions among targeted conditions and non-targeted conditions, with greater declines in the targeted conditions (37). Contrary to our hypothesis, we did not observe a decline in readmission rates after pneumonia. Rather, we found that readmission rates declined modestly among nonpulmonary sources of sepsis (e.g., urinary tract infection) and, potentially related, among those with less severe cases (e.g., explicit sepsis). While there is no clear signal that readmission rates differ by source of infection at the time of the index admission (10), additional studies examining the relationship between the index sepsis admission and infection-related readmission are needed.
Our findings support the growing recommendations that sepsis warrants national attention as a targeted condition for acute care and postacute care performance metrics (18 , 38 , 39). To date, there has been little evaluation of hospital discharge practices after sepsis. We previously reported a notable lack of timely postdischarge follow-up for septic shock survivors, as most survivors are readmitted within 14 days (11), leaving many readmitted prior to their scheduled appointments. Even less attention is placed on what should happen during primary care follow-up visits after sepsis. Notably, nearly 70% of unplanned hospital readmissions after sepsis are due to infections—about half of which are relapse or recrudesce of the initial infection and half are new (11 , 40). Such results suggest that sepsis survivors are particularly susceptible to reinfection and may benefit from careful monitoring for recrudescence of infections.
The required care coordination is specifically challenging among this patient population, as sepsis survivors are two times more likely to be discharged to skilled nursing facilities and 10 times more likely to require long-term acute care hospital placement compared with nonsepsis patients (9). To improve postdischarge outcomes after sepsis, comprehensive, coordinated multidisciplinary approaches to caring for sepsis survivors are needed. Given the growth in home health services that we observed after sepsis, and evidence that early and intense home health visits can reduce hospital readmission (41), novel interventions applied to home health services and focused on ambulatory care sensitive conditions (15) for sepsis survivors are warranted. A successful program will likely include a number of facets, including continuity between inpatient, postacute care services, and outpatient providers, antibiotic stewardship, management of sepsis specific impairments, and surveillance for new or recurrent infection. Provider education will be an essential component, but likely incomplete without engaging survivors and caregivers to facilitate self-care. Empowerment, potentially augmented by survivors supporting one another (42), could expedite realization of readmission reductions (43).
Our findings suggest a number of future directions. First, investigation is warranted to determine the role that readmissions, and infection-related readmissions in particular, play in the long-term mortality risk of sepsis survivors. Future studies should examine the timing and location of death and hospice use in the year after sepsis. Second, given the growth in ED treat-and-release visits, a greater understanding of the nature of treatment delivered during these encounters, and subsequent outcomes, is warranted. Third, postdischarge, novel surveillance strategies, leveraging mobile health technology, may prove useful to identify a new or recurrent infection. Last, although studies have examined risk factors associated with hospital readmission after sepsis, important questions (e.g., do outcomes differ between culture-positive and culture-negative sepsis cases) remain unanswered.
There are important limitations to this study. This study is limited to three hospitals within a single academic center; confirmatory studies are justified. Although we included hospital transfers to increase our readmission captures, we acknowledge that the rate is likely an underestimate as we were unable to identify readmissions outside of UPHS. However, we are not aware of any systematic changes over the study period that would bias the measurements of trend. There is no perfect method for identifying sepsis hospitalizations in claims data, and we acknowledge temporal trends in clinical documentation and coding practice. For this reason, we used multiple, validated methods to identify sepsis hospitalizations. As sepsis cohorts derived from administrative datasets tend to be more severely ill (24), changes in documentation likely reflect a more accurate picture of the overall disease burden of sepsis and its outcomes, while admittedly overestimating the increase in sepsis incidence and the decline in sepsis-related mortality. Future studies should use objective clinical data–based abstraction methods to confirm our findings related to hospital readmissions.
In a retrospective cohort study conducted within an academic center over 6 years, we observed a growing population of sepsis survivors who experienced a high rate of 7- and 30-day hospital readmissions. The modest decline in 30-day hospital readmission rates after sepsis was countered by a rise in ED treat-and-release visits, revealing a potential shift in hospital-based acute care after sepsis.
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