Impact of health care–associated community-onset cellulitis in Korea: a multicenter study
Abstract
We conducted a multicenter study to determine the clinical and microbiological characteristics of health care–associated (HCA) cellulitis in Korea. We retrospectively reviewed the medical records of patients who had been diagnosed with community-onset cellulitis. Of the 2208 cellulitis patients, 232 (10.5%) had HCA cellulitis, 1243 (56.3%) patients were hospitalized, and 15 (0.7%) died in hospital. Compared with community-acquired (CA) cellulitis, patients with HCA cellulitis were older and more frequently presented with comorbidity and septic shock. A total of 355 microorganisms were isolated from 314 patients (14.2%). Staphylococcus aureus (134 isolates) was the most common organism, followed by Streptococcus spp. (86 isolates) and Gram-negative fermenters (58 isolates). Methicillin-resistant S. aureus (MRSA) accounted for 29.1% (39/134) of S. aureus infections. None of the Gram-negative fermenters were resistant to carbapenem. The antibiotic susceptibility pattern of isolated microorganisms was not different between HCA and CA cellulitis. In patients with HCA cellulitis, S. aureus (11.2% [26/232] vs. 5.5% [108/1976], p = 0.001), including MRSA (4.3% [10/232] vs. 1.5% [29/1976], p = 0.003) and Gram-negative fermenters (6.0% [14/232] vs. 2.3% [44/1976], p = 0.002), were more common causative organisms than in CA-cellulitis patients. Age ≥ 65 years, septic shock, and HCA infection were statistically significant factors associated with in-hospital mortality.
Keywords
Cellulitis Health care–associated infection Staphylococcus aureusNotes
Authors’ contributions
PSY contributed to the study design, data gathering, analyses, and interpretation and wrote the first draft of the manuscript. KT, JJ, CSH, YSN, HHL, KYK, PSY, SHE, PKH, COH, and CSH contributed to data analyses and data interpretation, and critiqued the report. KYG contributed to the study design, data interpretation, and review and critiqued the report. KYG had full access to all data and made the final decision to submit for publication.
Compliance with ethical standards
Conflict of interest
The author declare that they have no conflict of interest.
Ethical approval
This work was approved by the Institutional Review Board of each hospital, and informed consent was waived since this was a retrospective study without intervention that did not involve extra clinical specimens.
References
- 1.Cox NH, Colver GB, Paterson WD (1998) Management and morbidity of cellulitis of the leg. J R Soc Med 91:634–637CrossRefGoogle Scholar
- 2.Ginsberg MB (1981) Cellulitis: analysis of 101 cases and review of the literature. South Med J 74:530–533CrossRefGoogle Scholar
- 3.Jeng A, Beheshti M, Li J et al (2010) The role of beta-hemolytic streptococci in causing diffuse, nonculturable cellulitis: a prospective investigation. Medicine (Baltimore) 89:217–226. https://doi.org/10.1097/MD.0b013e3181e8d635 CrossRefGoogle Scholar
- 4.Friedman ND, Kaye KS, Stout JE et al (2002) Health care--associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med 137:791–797CrossRefGoogle Scholar
- 5.Kollef MH, Shorr A, Tabak YP et al (2005) Epidemiology and outcomes of health-care-associated pneumonia: results from a large US database of culture-positive pneumonia. Chest 128:3854–3862. https://doi.org/10.1378/chest.128.6.3854 CrossRefGoogle Scholar
- 6.Shorr AF, Tabak YP, Killian AD et al (2006) Healthcare-associated bloodstream infection: a distinct entity? Insights from a large U.S. database. Crit Care Med 34:2588–2595. https://doi.org/10.1097/01.ccm.0000239121.09533.09 CrossRefGoogle Scholar
- 7.Zilberberg MD, Shorr AF, Micek ST et al (2009) Epidemiology and outcomes of hospitalizations with complicated skin and skin-structure infections: implications of healthcare-associated infection risk factors. Infect Control Hosp Epidemiol 30:1203–1210. https://doi.org/10.1086/648083 CrossRefGoogle Scholar
- 8.Zilberberg MD, Shorr AF, Micek ST et al (2010) Hospitalizations with healthcare-associated complicated skin and skin structure infections: impact of inappropriate empiric therapy on outcomes. J Hosp Med 5:535–540. https://doi.org/10.1002/jhm.713 CrossRefGoogle Scholar
- 9.Christensen KL, Holman RC, Steiner CA et al (2009) Infectious disease hospitalizations in the United States. Clin Infect Dis 49:1025–1035. https://doi.org/10.1086/605562 CrossRefGoogle Scholar
- 10.Fridkin SK, Hageman JC, Morrison M et al (2005) Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med 352:1436–1444. https://doi.org/10.1056/NEJMoa043252 CrossRefGoogle Scholar
- 11.Moran GJ, Krishnadasan A, Gorwitz RJ et al (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355:666–674. https://doi.org/10.1056/NEJMoa055356 CrossRefGoogle Scholar
- 12.King MD, Humphrey BJ, Wang YF et al (2006) Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann Intern Med 144:309–317CrossRefGoogle Scholar
- 13.Chira S, Miller LG (2010) Staphylococcus aureus is the most common identified cause of cellulitis: a systematic review. Epidemiol Infect 138:313–317. https://doi.org/10.1017/s0950268809990483 CrossRefGoogle Scholar
- 14.Levy MM, Fink MP, Marshall JC et al (2003) 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 31:1250–1256. https://doi.org/10.1097/01.ccm.0000050454.01978.3b CrossRefGoogle Scholar
- 15.Clinical and Laboratory Standards Institute (2011) Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement. CLSI document M100-S21. Clinical and laboratory Standards Institiue, WayneGoogle Scholar
- 16.Perelló-Alzamora M-R, Santos-Duran J-C, Sánchez-Barba M et al (2012) Clinical and epidemiological characteristics of adult patients hospitalized for erysipelas and cellulitis. Eur J Clin Microbiol Infect Dis 31:2147–2152. https://doi.org/10.1007/s10096-012-1549-2 CrossRefGoogle Scholar
- 17.Carratalà J, Rosón B, Fernández-Sabé N et al (2003) Factors associated with complications and mortality in adult patients hospitalized for infectious cellulitis. Eur J Clin Microbiol Infect Dis 22:151–157. https://doi.org/10.1007/s10096-003-0902-x Google Scholar
- 18.Kwak YG, Kim NJ, Choi S-H et al (2012) Clinical characteristics and organisms causing erysipelas and cellulitis. Infect Chemother 44:45–50CrossRefGoogle Scholar
- 19.Kwak YG, Choi SH, Kim T et al (2017) Clinical guidelines for the antibiotic treatment for community-acquired skin and soft tissue infection. Infect Chemother 49:301–325. https://doi.org/10.3947/ic.2017.49.4.301 CrossRefGoogle Scholar
- 20.Leppard BJ, Seal DV, Colman G et al (1985) The value of bacteriology and serology in the diagnosis of cellulitis and erysipelas. Br J Dermatol 112:559–567CrossRefGoogle Scholar
- 21.Ruef C (2008) Complicated skin and soft-tissue infections--consider gram-negative pathogens. Infection 36:295. https://doi.org/10.1007/s15010-008-3408-8 CrossRefGoogle Scholar
- 22.Kang CI, Chung DR, Peck KR et al (2010) Hematologic malignancy as a risk factor for bacteremic skin and soft tissue infection caused by gram-negative bacilli. Ann Hematol 89:1171–1173. https://doi.org/10.1007/s00277-010-0914-4 CrossRefGoogle Scholar
- 23.Corredoira JM, Ariza J, Pallarés R et al (1994) Gram-negative bacillary cellulitis in patients with hepatic cirrhosis. Eur J Clin Microbiol Infect Dis 13:19–24. https://doi.org/10.1007/bf02026118 CrossRefGoogle Scholar
- 24.Stevens DL, Bisno AL, Chambers HF et al (2014) Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the Infectious Diseases Society of America. Clin Infect Dis 59:e10–e52. https://doi.org/10.1093/cid/ciu444 CrossRefGoogle Scholar
- 25.Gunderson CG, Cherry BM, Fisher A (2018) Do patients with cellulitis need to be hospitalized? A systematic review and meta-analysis of mortality rates of inpatients with cellulitis. J Gen Intern Med 33:1553–1560. https://doi.org/10.1007/s11606-018-4546-z CrossRefGoogle Scholar