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Figure.  Outpatient Health Care Use by Quarter in the Year Before and After Severe Sepsis
Outpatient Health Care Use by Quarter in the Year Before and After Severe Sepsis

Middle lines indicate medians; boxes, interquartile ranges; whiskers, the upper and lower adjacent values.

Table.  Cohort Characteristics and Outpatient Health Care Use
Cohort Characteristics and Outpatient Health Care Use
1.
Carlton  EF, Barbaro  RP, Iwashyna  TJ, Prescott  HC.  Cost of pediatric severe sepsis hospitalizations.   JAMA Pediatr. 2019;173(10):986-987. doi:10.1001/jamapediatrics.2019.2570 PubMedGoogle Scholar
2.
Carlton  EF, Kohne  JG, Shankar-Hari  M, Prescott  HC.  Readmission diagnoses after pediatric severe sepsis hospitalization.   Crit Care Med. 2019;47(4):583-590. doi:10.1097/CCM.0000000000003646 PubMedGoogle Scholar
3.
Dombrovskiy  VY, Martin  AA, Sunderram  J, Paz  HL.  Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003.   Crit Care Med. 2007;35(5):1244-1250. doi:10.1097/01.CCM.0000261890.41311.E9 PubMedGoogle Scholar
4.
Feudtner  C, Feinstein  JA, Zhong  W, Hall  M, Dai  D.  Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation.   BMC Pediatr. 2014;14:199. doi:10.1186/1471-2431-14-199PubMedGoogle Scholar
5.
Rhee  C, Dantes  R, Epstein  L,  et al; CDC Prevention Epicenter Program.  Incidence and trends of sepsis in US hospitals using clinical vs claims data, 2009-2014.   JAMA. 2017;318(13):1241-1249. doi:10.1001/jama.2017.13836 PubMedGoogle Scholar
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    Research Letter
    Critical Care Medicine
    September 10, 2020

    Comparison of Outpatient Health Care Use Before and After Pediatric Severe Sepsis

    Author Affiliations
    • 1Division of Critical Care Medicine, Department of Pediatrics, University of Michigan, Ann Arbor
    • 2Susan B. Meister Child Health Evaluation and Research Center, Department of Pediatrics, University of Michigan, Ann Arbor
    • 3Division of Pulmonary, Allergy and Critical Care Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
    • 4Department of Internal Medicine, Division of Pulmonary and Critical Care Medicine, University of Michigan, Ann Arbor
    • 5US Department of Veterans Affairs Center for Clinical Management Research, Health Services Research and Development Center of Innovation, Ann Arbor, Michigan
    JAMA Netw Open. 2020;3(9):e2015214. doi:10.1001/jamanetworkopen.2020.15214
    Introduction

    Severe sepsis hospitalizes more than 70 000 children each year in the United States, with costs exceeding $7.3 billion.1 More than 90% of children who experience sepsis hospitalization survive. However, 1 in 6 children is rehospitalized within 30 days, a rate markedly higher than that for other common pediatric hospitalizations.2 We hypothesized that outpatient health care is similarly greater following pediatric sepsis hospitalization than before this hospitalization. To test this hypothesis, we measured the change in outpatient health care visits among patients who survived pediatric sepsis.

    Methods

    This cohort study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline. The University of Michigan determined that the study did not require institutional review board review and was exempt from informed consent because the database used is deidentified. We studied pediatric severe sepsis hospitalizations in Optum’s deidentified Clinformatics Data Mart database (2010-2015), which contains health care claims from commercial and Medicare Advantage members. Neonatal and pregnancy-related hospitalizations were excluded. We identified severe sepsis by either (1) an explicit diagnosis code (using International Classification of Diseases, Ninth Revision [ICD-9] and International Statistical Classification of Diseases and Related Health Problems, Tenth Revision [ICD-10] coding systems) for severe sepsis or septic shock or (2) concurrent codes for sepsis or bacteremia and acute organ dysfunction.3 Comorbidities were measured using the Complex Chronic Conditions Classification algorithm.4

    We compared the number of outpatient visits in the year before vs the year after a severe sepsis hospitalization using a t test, and we compared the type of outpatient visits in the year before and the year after a severe sepsis hospitalization using a χ2 test. Outpatient visits included all primary care and subspecialty visits. We determined the percentage of patients with new subspecialty visits as the proportion with a subspecialty visit in the 90 days after sepsis hospitalization and no visit to that subspecialty in the preceding year. In our primary analysis, we required that children be consecutively enrolled in insurance for 3 or more months prior to sepsis hospitalization, but we performed several sensitivity analyses (eAppendix in the Supplement).

    Analyses were performed from January 2020 to April 2020 using Stata/MP statistical software version 15 (StataCorp). P values were 2-sided, and statistical significance was set at P < .05.

    Results

    Of 167 497 pediatric hospitalizations, 952 were for severe sepsis (0.6%); of patients hospitalized for severe sepsis, 855 (89.8%) survived to discharge and were included in our analysis (Table). This cohort had a median (interquartile range [IQR]) age of 12 (3-16) years, with median (IQR) length of stay of 9 (5-20) days; 404 patients (47.3%) were girls.

    Outpatient visits increased from a median (IQR) of 5 (2-11) visits per patient in the year prior to hospitalization for severe sepsis to 8 (3-15) visits in the year after hospitalization (P < .001) and from 2 (1-4) visits in the 90 days before hospitalization for severe sepsis to 3 (1-6) visits in the 90 days after hospitalization (P < .001) (Figure). Of 855 patients, 478 (55.9%) had more visits in the 90 days after hospitalization vs before hospitalization and 514 (60.1%) had more visits in the year after sepsis hospitalization vs the year before hospitalization. Similar to the primary analysis, the median number of outpatient visits increased in the year after sepsis in all sensitivity analyses.

    Of 855 patients, 137 (16.0%) had a new subspecialist visit in the 90 days after sepsis hospitalization, most often for hematology and oncology (31 patients [4.3%]) or pulmonology (33 patients [4.1%]). Of 493 previously healthy children, 285 (57.8%) had an increase in outpatient visits by 90 days after sepsis hospitalization, while of 362 children with complex chronic conditions, 193 (53.3%) had an increase in such visits (P = .19). Among 493 previously healthy children, 60 (12.2%) had a new subspecialist visit, while of 362 children with complex chronic conditions, 77 (21.3%) had a new subspecialist visit (P < .001).

    Discussion

    In this national cohort of pediatric sepsis survivors, the median number of outpatient visits following sepsis hospitalization increased by 60% in the year after hospitalization for sepsis compared with each patient’s own baseline. Nearly 1 in 6 children had a new subspecialist visit within 3 months of severe sepsis hospitalization. However, not all children had an increase in outpatient visits, highlighting the heterogeneity of postsepsis experiences among children.

    The study has some limitations. This cohort consisted of privately insured children, so the results may not extrapolate to children on Medicaid or other types of insurance. We were unable to measure referrals or the number of patients who missed scheduled appointments. We used a claims-based algorithm to identify hospitalizations for severe sepsis, and that method may have resulted in some misclassification.5 This cohort study found that severe sepsis hospitalization was associated with an increase in subsequent outpatient primary care and subspecialty visits for most children who experience such hospitalization. That association may have a significant impact on children and their families, including potentially contributing to a financial burden on families, a decrease in parental work, and increased school absenteeism for children.

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    Article Information

    Accepted for Publication: June 17, 2020.

    Published: September 10, 2020. doi:10.1001/jamanetworkopen.2020.15214

    Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2020 Carlton EF et al. JAMA Network Open.

    Corresponding Author: Erin F. Carlton, MD, MSc, Susan B. Meister Child Health Evaluation and Research Center, Department of Pediatrics, University of Michigan, 1500 E Medical Center Dr, Ann Arbor, MI 48109 (ecarlton@med.umich.edu).

    Author Contributions: Dr Carlton had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

    Concept and design: All authors.

    Acquisition, analysis, or interpretation of data: Carlton, Kohne.

    Drafting of the manuscript: Carlton.

    Critical revision of the manuscript for important intellectual content: All authors.

    Statistical analysis: Carlton.

    Supervision: Prescott.

    Conflict of Interest Disclosures: Dr Prescott reported receiving grants from the US Agency for Healthcare Research and Quality, US Department of Veterans Affairs (VA) Health Services Research and Development, and Blue Cross Blue Shield of Michigan and serving on the Surviving Sepsis Campaign guidelines committee outside the submitted work. No other disclosures were reported.

    Funding/Support: This material is the result of work supported with resources and use of facilities at the Ann Arbor VA Medical Center. This work was supported by grant No. K08 GM115859 [HCP] from the US National Institutes of Health.

    Role of the Funder/Sponsor: The funding organizations had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

    Disclaimer: The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of the US Department of Veterans Affairs or the US government.

    References
    1.
    Carlton  EF, Barbaro  RP, Iwashyna  TJ, Prescott  HC.  Cost of pediatric severe sepsis hospitalizations.   JAMA Pediatr. 2019;173(10):986-987. doi:10.1001/jamapediatrics.2019.2570 PubMedGoogle Scholar
    2.
    Carlton  EF, Kohne  JG, Shankar-Hari  M, Prescott  HC.  Readmission diagnoses after pediatric severe sepsis hospitalization.   Crit Care Med. 2019;47(4):583-590. doi:10.1097/CCM.0000000000003646 PubMedGoogle Scholar
    3.
    Dombrovskiy  VY, Martin  AA, Sunderram  J, Paz  HL.  Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003.   Crit Care Med. 2007;35(5):1244-1250. doi:10.1097/01.CCM.0000261890.41311.E9 PubMedGoogle Scholar
    4.
    Feudtner  C, Feinstein  JA, Zhong  W, Hall  M, Dai  D.  Pediatric complex chronic conditions classification system version 2: updated for ICD-10 and complex medical technology dependence and transplantation.   BMC Pediatr. 2014;14:199. doi:10.1186/1471-2431-14-199PubMedGoogle Scholar
    5.
    Rhee  C, Dantes  R, Epstein  L,  et al; CDC Prevention Epicenter Program.  Incidence and trends of sepsis in US hospitals using clinical vs claims data, 2009-2014.   JAMA. 2017;318(13):1241-1249. doi:10.1001/jama.2017.13836 PubMedGoogle Scholar
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