Banerjee, Ritu

Brogan, Thomas V

Courter, Joshua D

Gerber, Jeffrey S

Hersh, Adam L

Kronman, Matthew P

Lee, Brian R

Newland, Jason G

Parker, Sarah K

Patel, Sameer J

Shah, Samir S

Smith, Michael J

Spaulding, Alicen B

Thurm, Cary

English

Digital Commons@Becker

Washington University School of MedicineDigital Commons@BeckerOpen Access Publications2018Epidemiology of Staphylococcus aureus infectionsin patients admitted to freestanding pediatrichospitals, 2009-2016Alicen B. SpauldingChildren’s Minnesota Research InstituteCary ThurmChildren’s Hospital Association, Lenexa, KansasJoshua D. CourterDivision of Pharmacy, Cincinnati Children’s Hospital Medical CenterRitu BanerjeeVanderbilt University School of MedicineJeffrey S. GerberChildren’s Hospital of PhiladelphiaSee next page for additional authorsFollow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubsThis Open Access Publication is brought to you for free and open access by Digital Commons@Becker. It has been accepted for inclusion in OpenAccess Publications by an authorized administrator of Digital Commons@Becker. For more information, please contact engeszer@wustl.edu.Recommended CitationSpaulding, Alicen B.; Thurm, Cary; Courter, Joshua D.; Banerjee, Ritu; Gerber, Jeffrey S.; Newland, Jason G.; Parker, Sarah K.; Brogan,Thomas V.; Kronman, Matthew P.; Shah, Samir S.; Smith, Michael J.; Patel, Sameer J.; Lee, Brian R.; and Hersh, Adam L.,,"Epidemiology of Staphylococcus aureus infections in patients admitted to freestanding pediatric hospitals, 2009-2016." InfectionControl & Hospital Epidemiology.39,12. 1487-1490. (2018).https://digitalcommons.wustl.edu/open_access_pubs/7401AuthorsAlicen B. Spaulding, Cary Thurm, Joshua D. Courter, Ritu Banerjee, Jeffrey S. Gerber, Jason G. Newland,Sarah K. Parker, Thomas V. Brogan, Matthew P. Kronman, Samir S. Shah, Michael J. Smith, Sameer J. Patel,Brian R. Lee, and Adam L. HershThis open access publication is available at Digital Commons@Becker: https://digitalcommons.wustl.edu/open_access_pubs/7401Infection Control & Hospital Epidemiology (2018), 39, 1487–1490doi:10.1017/ice.2018.259Concise CommunicationEpidemiology of Staphylococcus aureus infections in patientsadmitted to freestanding pediatric hospitals, 2009–2016Alicen B. Spaulding PhD, MPH1, Cary Thurm PhD2, Joshua D. Courter PharmD3, Ritu Banerjee MD, PhD4,Jeffrey S. Gerber MD5, Jason G. Newland MD6, Sarah K. Parker MD7, Thomas V. Brogan MD8, Matthew P. KronmanMD9, Samir S. Shah MD, MSCE10, Michael J. Smith MD11, Sameer J. Patel MD, MPH12, Brian R. Lee PhD13 andAdam L. Hersh MD PhD141Children’s Minnesota Research Institute, Minneapolis, Minnesota, 2Children’s Hospital Association, Lenexa, Kansas, 3Division of Pharmacy, Cincinnati Children’sHospital Medical Center, Cincinnati, Ohio, 4Division of Pediatrics Infectious Diseases, Vanderbilt University School of Medicine, Nashville, Tennessee, 5Division ofInfectious Diseases, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania, 6Division of Pediatric Infectious Diseases, School of Medicine, WashingtonUniversity, St Louis, Missouri, 7Division of Pediatric Infectious Diseases, Children’s Hospital Colorado and University of Colorado, Aurora, Colorado, 8PediatricCritical Care Medicine, Seattle Children’s Hospital, School of Medicine, University of Washington, Seattle, Washington, 9Division of Infectious Diseases, SeattleChildren’s Hospital, School of Medicine, University of Washington, Seattle, Washington, 10Division of Hospital Medicine, Cincinnati Children’s Hospital MedicalCenter and University of Cincinnati College of Medicine, Cincinnati, Ohio, 11Division of Pediatric Infectious Diseases, Duke University, Durham, North Carolina,12Division of Pediatric Infectious Diseases, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, Illinois, 13Division of Infectious Diseases, Children’s MercyHospital, Kansas City, Missouri and 14Division of Pediatric Infectious Diseases, Department of Pediatrics, School of Medicine, University of Utah, Salt Lake City, Utah.AbstractWe observed pediatric S. aureus hospitalizations decreased 36% from 26.3 to 16.8 infections per 1,000 admissions from 2009 to 2016, withmethicillin-resistant S. aureus (MRSA) decreasing by 52% and methicillin-susceptible S. aureus decreasing by 17%, among 39 pediatrichospitals. Similar decreases were observed for days of therapy of anti-MRSA antibiotics.(Received 14 May 2018; accepted 9 September 2018; electronically published October 29, 2018)Staphylococcus aureus (S. aureus) causes a substantial number ofpediatric infections each year in the United States, with potentialfor severe complications including death.1–4 Although the emer-gence of methicillin-resistant S. aureus (MRSA) led to a rapidincrease in the number of S. aureus infections in children,5 recentdata suggest that S. aureus infections are declining in adults,driven primarily by decreases in MRSA.6,7 Similar findings havebeen reported in pediatric populations, but these studies werelimited to single centers and unique populations, such as militarymembers or infants.4,5,8–10 A nationally representative and con-temporary characterization of epidemiologic trends in S. aureusinfections has not been conducted. The objective of this study wasto describe recent trends in pediatric S. aureus hospitalizationsand associated antibiotic prescribing patterns.Patients and MethodsData source and qualityWe conducted a retrospective cohort study using the PediatricHealth Information Systems (PHIS) administrative database,maintained by the Children’s Hospital Association (OverlandPark, KS). PHIS includes clinical and resource utilization datafrom inpatient, emergency, ambulatory surgery, and observationunits at more than 45 tertiary-care freestanding children’s hos-pitals in the United States. The data are subject to numerousvalidity and reliability checks before incorporation into thedatabase. The data warehouse function was provided by TruvenHealth Analytics (Ann Arbor, MI).Study populationAll inpatient encounters for patients <18 years of age hospitalizedbetween January 1, 2009, and December 31, 2016, at a PHIShospital with continuous reporting were included. The studypopulation was limited to patients with an S. aureus infectionindicated in the electronic medical record, defined as (1) having≥1 International Classification of Disease, Clinical Modificationsversion 9 or version 10 discharge code for MRSA (038.12, 041.12,482.42, A41.02, A49.02, B95.62, J152.12, V02.54) or methicillin-susceptible S. aureus (MSSA) (038.11, 041.11, 482.41, A41.01,A49.01, B95.61, J152.11, V02.53) present on admission oroccurring during the admission; and (2) receiving ≥1 anti-staphylococcal antibiotic (list available upon request). Usingadditional discharge codes when present, S. aureus infectionswere further stratified into 4 infection categories: (1) skin or soft-tissue infection (SSTI); (2) myositis/osteomyelitis/septic arthritis;Cite this article: Spaulding AB, et al. (2018). Epidemiology of Staphylococcus aureusinfections in patients admitted to freestanding pediatric hospitals, 2009–2016. InfectionControl & Hospital Epidemiology 2018, 39, 1487–1490. doi: 10.1017/ice.2018.259Author for correspondence: Alicen Burns Spaulding, PhD, MPH, Children’s Min-nesota Research Institute, 2525 Chicago Ave. S. MS 40–460, Minneapolis, MN 55404.E-mail: Alicen.Spaulding@childrensmn.org© 2018 by The Society for Healthcare Epidemiology of America. All rights reserved.(3) bacteremia/endocarditis; or (4) pneumonia.10 Patients couldbe assigned >1 category.Data analysisThe annual rates for S. aureus overall, MRSA, and MSSA werecalculated per 1,000 hospital admissions. Trends in hospitalizationrates over time were analyzed using the Cochran-Armitage trendtest, with 2-sided P values reported and statistical significance setat P< .05. Median and interquartile ranges (IQR) are reported forcontinuous variables. Antibiotic days of therapy (DOT) per 1,000patient days were evaluated, where the DOT numerator is theaggregate sum of anti-staphylococcal antibiotics used per patientwith S. aureus infections per day and the denominator is the totalhospital inpatient days for all hospitalized patients, analyzedseparately for antibiotics with activity against MRSA. Data ana-lyses were performed with SAS version 9.4 software (SAS Insti-tute, Cary, NC). The Institutional Review Board of Children’sMinnesota Hospital deemed this study exempt from review.ResultsAmong 39 hospitals with continuous reporting to PHIS from2009 to 2016, we identified 116,152 S. aureus hospitalizations.Among patients with S. aureus hospitalizations, the median agewas 3 years (IQR, 0–11 years), 53.7% were male, 52.5% werewhite, and 18.8% were African American. The median length ofhospital stay was 5 days (IQR, 2–13 days), with intensive care unitadmissions occurring in 26.3% of MSSA hospitalizations com-pared with 22.3% of MRSA hospitalizations (Table 1).From 2009 to 2016, pediatric S. aureus hospitalizationsdecreased 36% from 26.3 to 16.8 infections per 1,000 admissions(P< .001) (Fig. 1A). Overall, there was a 52% decrease in MRSAinfections (14.4 to 6.9 infections per 1,000 admissions; P< .001)and a 17% decrease in MSSA infections (11.9 to 9.9 infections per1,000 admissions; P< .001). In 2009, 55% of all S. aureus infec-tions were MRSA, and this rate decreased to 41% in 2016.MRSA infections were most often categorized as SSTIs(44.7%), followed by myositis/osteomyelitis/septic arthritis(7.1%), bacteremia/endocarditis (4.5%), and pneumonia (4.8%);44.3% of MRSA infections were not categorized. Although rates inall MRSA categories decreased over time, the decrease was mostnotable among SSTIs, which decreased from 7.3 in 2009 to 2.9infections per 1,000 admissions in 2016 (P< .001); other MRSAcategories remained relatively unchanged. Notably the proportionof MRSA infections decreased among non-Hispanic AfricanAmericans (22.9% to 19.1% from 2009 to 2016; P< .001), 1–5-year-olds (39% to 32.1% from 2009 to 2016; P< .001), and amongpatients from the South (47.2% to 43.8%; P< .001).MSSA infection categories were similar to MSRA in distribu-tion. Over time, these decreases were most notable among SSTIs(from 4.1 in 2009 to 2.9 in 2016; P< .001) and bacteremia/endocarditis infections (from 1.2 in 2009 to 0.6 in 2016; P< .001).The antibiotics most commonly used to treat S. aureusinfections were vancomycin (14.9% of DOT per 1,000 patientdays), clindamycin (11.3%), cefazolin (4.1%), trimethoprim/sul-famethoxazole (TMP/SMX) (4.1%), and ceftriaxone (2.4%).Vancomycin and clindamycin remained the 2 most commonlyprescribed antibiotics over the study period. Days of therapy per1,000 patient days among antibiotics with activity against MRSAspecifically decreased from 38.0 to 24.5, with the most notableTable 1. Demographics of Pediatric Patients With Staphylococcus aureusInfections in 39 PHIS Hospitals With Continuous Reporting, 2009–2016.aVariableAll S. aureus(n= 116,152)No. (%)bMRSA(n= 59,762)No. (%)bMSSA(n= 56,390)No. (%)bDemographic variablesGenderFemale 53,773 (46.3) 28,582 (47.8) 25,191 (44.7)Male 62,379 (53.7) 31,180 (52.2) 31,199 (55.3)AgeMedian (IQR), y 3 (0–11) 3 (1–11) 4 (0–11)<1 y 29,336 (25.3) 14,453 (24.2) 14,883 (26.4)1–5 y 37,509 (32.3) 21,446 (35.9) 16,063 (28.5)6–12 y 26,092 (22.5) 12,462 (20.9) 13,630 (24.2)13–17 y 23,215 (20) 11,401 (19.1) 11,814 (21)Race and ethnicityWhite 61,020 (52.5) 31,823 (53.2) 29,197 (51.8)African American 21,855 (18.8) 12,316 (20.6) 9,539 (16.9)Hispanic 20,366 (17.5) 9,738 (16.3) 10,628 (18.8)Asian American 2,387 (2.1) 839 (1.4) 1,548 (2.7)Other 10,524 (9.1) 5,046 (8.4) 5,478 (9.7)Census regionMidwest 31,285 (26.9) 16,166 (27.1) 15,119 (26.8)Northeast 13,818 (11.9) 6,122 (10.2) 7,696 (13.6)South 46,462 (40) 26,446 (44.3) 20,016 (35.5)West 24,587 (21.2) 11,028 (18.5) 13,559 (24.0)Health insurance payerPrivate 37,297 (32.1) 17,041 (28.5) 20,256 (35.9)Government 72,619 (62.5) 39,370 (65.9) 33,249 (59)Other payer 6,236 (5.4) 3,351 (5.6) 2,885 (5.1)Hospital-encountervariablesLength of hospital stayMedian (IQR), d 5 (2–13) 4 (2–12) 5 (3–14)ICU or NICU stay 28,137 (24.2) 13,321 (22.3) 14,816 (26.3)Primary reason for visitMedical 85,895 (74) 45,466 (76.1) 40,429 (71.7)Surgical 30,257 (26) 14,296 (23.9) 15,961 (28.3)Any complex chroniccondition54,517 (46.9) 26,569 (44.5) 27,948 (49.6)Crude mortality 1,850 (1.6) 754 (1.3) 1,096 (1.9)30-day all-causereadmission rate13,858 (11.9) 6,604 (11.1) 7,254 (12.9)1488 Alicen B. Spaulding et aldecreases for clindamycin (14.32 to 7.5) and vancomycin (16.6 to10.8) (Fig. 1B).DiscussionIn this study, we observed a 36% decrease for S. aureus hospi-talizations between 2009 and 2016. Notably, MRSA hospitaliza-tions decreased 52%, including a corresponding decrease in DOTfor anti-MRSA antibiotics during the same period.Decreases in S. aureus hospitalizations detected in this studywere similar to findings from studies performed in other adultand pediatric inpatient populations.6,7 A number of factors maycontribute to these decreases: (1) earlier recognition of S. aureusinfections (especially SSTIs) and initiation of appropriatetherapy in outpatient settings, such as incision and drainageand/or targeted antibiotic therapy which might prevent hospi-talization and/or recurrences; (2) changes in the tendency tohospitalize patients with suspected staphylococcal infectionssuch as SSTIs presenting to emergency departments; (3)increased provider confidence to manage infections in theoutpatient settings, and (4) the possibility of reductions intransmission of MRSA due to better infection control strategiesespecially in community settings or due to changes in circu-lating MRSA clones or lower prevalence in the community.Future studies are warranted to determine whether MRSAinfections at the community-level are also decreasing, how tobest measure the impact of infection control practices, and howSSTI visits in the emergency department might have alsochanged over time.This study has several limitations. First, we identified cases ofS. aureus using administrative coding and, though this methodhas been used in other studies, it has not been validated. Toenhance specificity, we included an additional requirement ofreceipt of an antibiotic with activity against S. aureus during thehospitalization. Second, PHIS only includes hospitalized patientsand therefore does not allow us to distinguish between hospital-onset versus community-onset infections or to addressconcurrent trends in outpatient care settings that might havecontributed to our findings. When we looked at our “present onadmission” flag, we found only 9.3% of all S. aureus infectionswere marked as “no.” Third, the generalizability of our findings topediatric hospitalizations outside of freestanding children’s hos-pitals is uncertain including the possibility that some S. aureushospitalizations may have shifted to hospitals not capturedby PHIS.Despite these limitations, these results provide evidence ofsubstantial and sustained decreases in pediatric S. aureus hospi-talizations, driven by declining MRSA hospitalizations. FurtherTable 1. (Continued )VariableAll S. aureus(n= 116,152)No. (%)bMRSA(n= 59,762)No. (%)bMSSA(n= 56,390)No. (%)bS. aureus infection categorySSTI 45,148 (38.9) 26,709 (44.7) 18,439 (32.7)Myositis/osteomyelitis/septic arthritis11,750 (10.1) 4,231 (7.1) 7,519 (13.3)Bacteremia/endocarditis 8,140 (7) 2,717 (4.5) 5,423 (9.6)Pneumonia 9,174 (7.9) 2,861 (4.8) 6,313 (11.2)Not specified 49,971 (43) 26,450 (44.3) 23,521 (41.7)Treatment-related variablesMRSA treatment coverage,DOT/1,000 patient days36.9 20.1 16.8Top 5 antibiotics prescribedduring hospital admissionClindamycin 64,059 (55.2) 35,874 (60) 28,185 (50)Vancomycin 51,047 (43.9) 26,967 (45.1) 24,080 (42.7)Cefazolin 25,131 (21.6) 7,111 (11.9) 18,020 (32)Ceftriaxone 17,732 (15.3) 7,846 (13.1) 9,886 (17.5)TMP/SMX 15,856 (13.7) 9,712 (16.3) 6,144 (10.9)Note. IQR, interquartile range; ICU, intensive care unit; NICU, neonatal intensive care unit;SSTI, skin and soft-tissue infection; DOT, days of therapy; TMP/SMX, trimethoprim/sulfa-methoxazole.aAll differences between groups were statistically significant.bUnless otherwise specified.Fig. 1. (A) S. aureus hospitalization rate per 1,000 hospital admissions in 39 PHIShospitals with continuous reporting, 2009–2016. (B) Days of therapy for the mostcommonly used antibiotics per patient day among S. aureus hospital admissions.Infection Control & Hospital Epidemiology 1489research is necessary to better understand the factors drivingthese epidemiologic changes.Acknowledgments.Financial support. No financial support was provided relevant to this article.Conflicts of interest. All authors report no conflicts of interest relevant tothis article.References1. Klein EY, Mojica N, Jiang W, et al. Trends in methicillin-resistantStaphylococcus aureus hospitalizations in the United States, 2010–2014.Clin Infect Dis 2017;65:1921–1923.2. Hamdy RF, Hsu AJ, Stockmann C, et al. Epidemiology of methicillin-resistant Staphylococcus aureus bacteremia in children. Pediatrics2017;139.3. Klieger SB, Vendetti ND, Fisher BT, Gerber JS. Staphylococcus aureusbacteremia in hospitalized children: incidence and outcomes. InfectControl Hosp Epidemiol 2015;36:603–605.4. Sutter DE, Milburn E, Chukwuma U, Dzialowy N, Maranich AM,Hospenthal DR. Changing susceptibility of Staphylococcus aureus in a USpediatric population. Pediatrics 2016;137.5. Le J, Dam Q, Tran T, et al. Epidemiology and hospital readmissionassociated with complications of Staphylococcus aureus bacteremia inpediatrics over a 25-year period. Epidemiol Infect 2017;145:2631–2639.6. Landrum ML, Neumann C, Cook C, et al. Epidemiology of Staphylococcusaureus blood and skin and soft tissue infections in the US military healthsystem, 2005–2010. JAMA 2012;308:50–59.7. Dantes R, Mu Y, Belflower R, et al. National burden of invasivemethicillin-resistant Staphylococcus aureus infections, United States, 2011.JAMA Intern Med 2013;173:1970–1978.8. Ericson JE, Popoola VO, Smith PB, et al. Burden of invasiveStaphylococcus aureus infections in hospitalized infants. JAMA Pediatr2015;169:1105–1111.9. Hulten KG, Mason EO, Lamberth LB, Forbes AR, Revell PA, Kaplan SL.Analysis of invasive community-acquired methicillin-susceptible Staphy-lococcus aureus infections during a period of declining CA-MRSAinfections at a large children’s hospital. Pediatr Infect Dis J2018;37:235–241.10. Herigon JC, Hersh AL, Gerber JS, Zaoutis TE, Newland JG. Antibioticmanagement of Staphylococcus aureus infections in US children’shospitals, 1999–2008. Pediatrics 2010;125:e1294–e1300.1490 Alicen B. Spaulding et al

Epidemiology of Staphylococcus aureus infections in patients admitted to freestanding pediatric hospitals, 2009-2016

https://digitalcommons.wustl.edu/cgi/viewcontent.cgi?article=8409&amp;context=open_access_pubs

Epidemiology of Staphylococcus aureus infections in patients admitted to freestanding pediatric hospitals, 2009-2016

Abstract

Similar works

Full text

Available Versions

Digital Commons@Becker