Healthcare-associated Staphylococcus aureus infections in children in Turkey: A six-year retrospective, single-center study

Abstract

Objective: To describe clinical and epidemiological characteristics, antimicrobial susceptibility and mortality-associated factors of healthcare-associated infections (HCAIs) caused by Staphylococcus (S.) aureus in children. Methods: We conducted a retrospective, single-centre study of pediatric HCAIs caused by S. aureus from a tertiary care hospital in Turkey between February 2014 and December 2019. The clinical and epidemiological characteristics and antimicrobial susceptibility of the methicillin-susceptible and methicillin-resistant S. aureus (MSSA and MRSA) isolates was evaluated. Results: A total of 310 pediatric patients were examined. Overall, 225 (72.6%) isolates were MSSA and 85 (27.4%) were MRSA. All S. aureus isolates were susceptible to teicoplanin, vancomycin, linezolid, tigecycline, mupirocin, and daptomycin. Penicillin resistance rates were high (89.0%), while fosfomycin, gentamicin, and clindamycin resistance rates were low (1.3%, 1.0%, and 2.3%, respectively). Except susceptibility to fosfomycin, which was significantly lower in 2014 compared to 2018 and 2019, no significant difference was found in the antimicrobial susceptibility ofS. aureus isolates between the years. Baseline characteristics and mortality rate were similar comparing MRSA and MSSA causing HCAIs. The mortality rate of HCAIs caused by S. aureus was 6.5% (20 patients). Malignancy was an independent risk factor associated with mortality in the multivariate analysis (OR 5.446, 95% CI 1.573-18.849). Conclusions: Our findings demonstrate that MSSA remained the most causative agent of HCAIs caused byS. aureus. The mortality rate was 6.5%, the antibiotic resistance rate was quite high for penicillin and diagnosis of malignancy was the main risk factor for increasing mortality in children. These findings could help improve the management of HCAIs caused by S. aureus in children.

Keywords

Healthcare-associated infections / Staphylococcus aureus / Children / Antimicrobial susceptibility / Mortality

References

[1] Rasigade JP, Vandenesch F. Staphylococcus aureus: A pathogen with still unresolved issues. Infect Genet Evol 2014; 21:510-514.

[2] Tong SYC, Davis JS, Eichenberger E, Holland TL, Fowler VG. Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015; 28(3):603-661.

[3] Zervou FN, Zacharioudakis IM, Ziakas PD, Mylonakis E. MRSA colonization and risk of infection in the neonatal and pediatric ICU: A meta-analysis. Pediatrics 2014; 133(4):e1015-e1023.

[4] Koeck M, Como-Sabetti K, Boxrud D, Dobbins G, Glennen A, Anacker M, et al. Burdens of invasive methicillin-susceptible and methicillin-resistant Staphylococcus aureus disease, Minnesota, USA. Emerg Infect Dis 2019; 25(1):171-174.

[5] Jokinen E, Laine J, Huttunen R, Lyytikäinen O, Vuento R, Vuopio J, et al. Trends in incidence and resistance patterns of Staphylococcus aureus bacteremia. Infect Dis 2018; 50(1):52-58.

[6] Jokinen E, Laine J, Huttunen R, Rahikka P, Huhtala H, Vuento R, et al. Comparison of outcome and clinical characteristics of bacteremia caused by methicillin-resistant, penicillin-resistant and penicillin-susceptible Staphylococcus aureus strains. Infect Dis 2017; 49(7):493-500.

[7] Lyles RD, Trick WE, Hayden MK, Lolans K, Fogg L, Logan LK, et al. Regional epidemiology of methicillin-resistant Staphylococcus aureus among critically ill children in a state with mandated active surveillance. J Pediatr Infect Dis Soc 2016; 5(4):409-416.

[8] Waitayangkoon P, Thongkam A, Benjamungkalarak T, Rachayon M, Thongthaisin A, Chatsuwan T, et al. Hospital epidemiology and antimicrobial susceptibility of isolated methicillin-resistant Staphylococcus aureus: A one-year retrospective study at a tertiary care center in Thailand. Pathog Glob Health 2020; 114(4):212-217.

[9] McMullan BJ, Bowen A, Blyth CC, Van Hal S, Korman TM, Buttery J, et al. Epidemiology and mortality of Staphylococcus aureus bacteremia in Australian and New Zealand children. JAMA Pediatr 2016; 170(10):979-986.

[10] Campbell AJ, Al Yazidi LS, Phuong LK, Leung C, Best EJ, Webb RH, et al. Pediatric Staphylococcus aureus bacteremia: Clinical spectrum and predictors of poor outcome. Clin Infect Dis 2022; 74(4):604-613.

[11] Gordon O, Cohen MJ, Gross I, Amit S, Averbuch D, Engelhard D, et al. Staphylococcus aureus bacteremia in children: Antibiotic resistance and mortality. Pediatr Infect Dis J 2019; 38(5):459-463.

[12] The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 11.0. 2021. [Online]. Available from:http://www.eucast.org. [Accessed on 21 May 2023].

[13] Roediger JC, Outhred AC, Shadbolt B, Britton PN. Paediatric Staphylococcus aureus bacteraemia: A single-centre retrospective cohort. Paediatr Child Health 2017; 53(2):180-186.

[14] Arikan K, Karadag-Oncel E, Aycan AE, Yuksekkaya S, Sancak B, Ceyhan M. Epidemiologic and molecular characteristics of Staphylococcus aureus strains isolated from hospitalized pediatric patients. Pediatr Infect Dis J 2020; 39(11):1002-1006.

[15] Cay U, Celik U, Barutcu A, Ozdemir U, Unal N. Clinical characteristics and resistance patterns of Staphylococcus aureus infections in children at a tertiary care hospital in southern Turkey. Cukurova Med J 2022; 47(2):580-588.

[16] Naves KS, Vaz da Trindade N, Gontijo Filho PP. Methicillin-resistant Staphylococcus aureus bloodstream infection: Risk factors and clinical outcome in non-intensive-care units. Rev Soc Bras Med Trop 2012; 45(2):189-193.

[17] Davis WT, Gilbert SR. Comparison of methicillin-resistant versus susceptible Staphylococcus aureus pediatric osteomyelitis. J Pediatr Orthop 2018; 38(5):e285-e291.

[18] Baranovich T, Zaraket H, Shabana II, Nevzorova V, Turcutyuicov V, Suzuki H. Molecular characterization and susceptibility of methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from hospitals and the community in Vladivostok, Russia. Clin Microbiol Infect 2010; 16(6):575-582.

[19] Sutter DE, Milburn E, Chukwuma U, Dzialowy N, Maranich AM, Hospenthal DR. Changing susceptibility of Staphylococcus aureus in a US pediatric population. Pediatrics 2016; 137(4):e20153099.

[20] Junaidi NSSA, Shakrin NNSM, Huri MFD, Kamarudin AZ, Desa MNM, Yunus WMZW. Antibiotic resistance and molecular typing of clinical Staphylococcus aureus isolates from Malaysian military hospital. Asian Pac J Trop Med 2023; 16(5):220-231.

[21] Ramarathnam V, De Marco B, Ortegon A, Kemp D, Luby J, Sreeramoju P. Risk factors for development of methicillin-resistant Staphylococcus aureus infection among colonized patients. Am J Infect Control 2013; 41(7):625-628.

[22] Gomes RT, Lyra TG, Alves NN, Caldas RM, Barberino MG, Nascimento-Carvalho CM. Methicillin-resistant and methicillin-susceptible community-acquired Staphylococcus aureus infection among children. Braz J Infect Dis 2013; 17(5):573-578.

[23] La Vecchia A, Ippolito G, Taccani V, Gatti E, Bono P, Bettocchi S, et al. Epidemiology and antimicrobial susceptibility of Staphylococcus aureus in children in a tertiary care pediatric hospital in Milan, Italy, 2017-2021. Ital J Pediatr 2022; 48(1):67.

[24] Naimi HM, Rasekh H, Noori AZ, Bahaduri MA. Determination of antimicrobial susceptibility patterns in Staphylococcus aureus strains recovered from patients at two main health facilities in Kabul, Afghanistan. BMC Infect Dis 2017; 17(1):737.

[25] Pignataro D, Foglia F, Della Rocca MT, Melardo C, Santella B, Folliero V, et al. Methicillin-resistant Staphylococcus aureus: Epidemiology and antimicrobial susceptibility experiences from the University Hospital 'Luigi Vanvitelli' of Naples. Pathog Glob Health 2020; 114(8):451-456.

[26] Li Z, Zhuang H, Wang G, Wang H, Dong Y. Prevalence, predictors, and mortality of bloodstream infections due to methicillin-resistant Staphylococcus aureus in patients with malignancy: Review and meta-analysis. BMC Infect Dis 2021; 21(1):74.