The antimicrobial susceptibility and contribution of Staphylococcus aureus to surgical site infections in patients hospitalized in the West Pomeranian region (Poland) during the COVID-19 pandemic period – a 3-year follow-up

Helena Masiuk, Piotr Ostrowski, Marek Masiuk, Agata Pruss, Paweł Kwiatkowski, Iwona Bilska, Klaudia Rusińska, Anastasiia Skoryk, Joanna Jursa-Kulesza


Introduction: Surgical site infections (SSIs) are at the forefront of healthcare-associated infections and the second most common cause of hospital readmission. The etiology of these infections is generally monobacterial with a predominance of Staphylococcus aureus. Although it is a preventable infection it significantly increases the cost of hospitalization and doubles the mortality rate.
The aim of the present study was to evaluate the prevalence of SSIs and antimicrobial susceptibility of S. aureus isolated from SSIs in patients hospitalized at the Clinical Hospital No. 1 of the Pomeranian Medical University in Szczecin (Poland) – CH-1 – during the period 2019–2021, in the course of the COVID-19 pandemic.
Materials and methods: Analysed specimens were collected from patients with diagnosed skin and soft tissue infections (SSTIs) caused by S. aureus, collected in 2019–2021, and then examined during routine microbiological diagnostics. The collection included specimens from patients hospitalized at CH-1, as well as consulted at the Emergency Department (ED) of CH-1, patients from healthcare facility of the Ministry of Internal Affairs and Administration in Szczecin, and from detainees of the Szczecin Detention Centre (Poland). Out of the total of 1140 results, 232 were classified as SSIs caused by S. aureus and then analysed. All the data were systemically entered into a spreadsheet (Excel 2019) and later subjected to several statistical tests (using StatSoft Statistica 13 package).
Results: From the collection of results, 20.4% (232/1140) were considered as SSIs of S. aureus etiology. In the following years 2019, 2020, and 2021, the SSIs of S. aureus etiology were 17.1% (72/421), 19.5% (66/339), and 24.7% (94/380), respectively. Methicillin- -resistant S. aureus (MRSA) was the cause of 7% of analysed SSIs. The highest incidence of SSIs was observed mainly in patients admitted to the trauma and orthopaedic wards and in patients seen in the ED. The majority of SSIs were mono-etiologic, caused by S. aureus only (93%). Mixed etiology was determined in 7% of SSIs with a significant share of beta hemolytic streptococci, enterobacteria, and non-fermentative Gram-negative rods. A slight increase in the prevalence of SSIs was observed during the analysed period. The overall antimicrobial susceptibility of all examined strains was noted, with a low rate of MRSA. The obtained results demonstrate the good practice of both strategies of hospital infection control, as well as the coherent and rational antibiotic policy in the CH-1 in the West Pomeranian region in Poland. The 2017–2018 data on the incidence of SSTIs and the percentage of SSIs among patients hospitalized in CH-1 show that in 2017, SSIs represented 17.9% of all cases classified as SSTIs (57/318), followed by SSIs in 2018, which represented 19.5% of all SSTIs analysed in CH-1 (68/348). The percentage of SSIs among the total SSTIs confirmed during the 2-year pre-pandemic period did not indicate significant changes in the number of SSIs among CH-1 patients hospitalized during the period of analysis. Therefore, it can be concluded that pandemic restrictions did not significantly affect the trend in the predominant proportion of S. aureus among SSIs during the study period.


skin and soft tissue infections; methicillin-resistant S. aureus (MRSA); osteomyelitis; hospital-acquired infections

Full Text:



Sakr A, Brégeon F, Mège JL, Rolain JM, Blin O. Staphylococcus aureus nasal colonization: an update on mechanisms, epidemiology, risk fac-tors, and subsequent infections. Front Microbiol 2018;9:2419.

Yüksel YT, Edslev SM, Janstrup AK, Goldeman MS, Nørreslet LB, Andersen PS, et al. Colonization with Staphylococcus aureus in healthcare workers: consequences of hand eczema. Br J Dermatol 2022;187(4):609-11.

Garoy EY, Gebreab YB, Achila OO, Tekeste DG, Kesete R, Ghirmay R, et al. Methicillin-resistant Staphylococcus aureus (MRSA): prevalence and antimicrobial sensitivity pattern among patients – a multicenter study in Asmara, Eritrea. Can J Infect Dis Med Microbiol 2019;2019:8321834. doi: 10.1155/2019/8321834.

Laupland KB, Lyytikäinen O, Søgaard M, Kennedy KJ, Knudsen JD, Ostergaard C, et al. The changing epidemiology of Staphylococcus aureus bloodstream infection: a multinational population-based surveillance study. Clin Microbiol Infect 2013;19(5):465-71.

Shoaib M, Aqib AI, Muzammil I, Majeed N, Bhutta ZA, Kulyar MF, et al. MRSA compendium of epidemiology, transmission, pathophysiology, treatment, and prevention within one health framework. Front Microbiol 2022;13:1067284.

European Centre for Disease Prevention and Control. Antimicrobial resistance (EARS-Net). In: ECDC. Annual epidemiological report for 2014. Stockholm: ECDC; 2018.

Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical man-ifestations, and management. Clin Microbiol Rev 2015;28(3):603-61.

Laux C, Peschel A, Krismer B. Staphylococcus aureus colonization of the human nose and interaction with other microbiome members. Mi-crobiol Spectr 2019;7(2).

Dana AN, Bauman WA. Bacteriology of pressure ulcers in individuals with spinal cord injury: what we know and what we should know. J Spinal Cord Med 2015;38(2):147-60.

Olaniyi R, Pozzi C, Grimaldi L, Bagnoli F. Staphylococcus aureus – associated skin and soft tissue infections: anatomical localization, epide-miology, therapy and potential prophylaxis. Curr Top Microbiol Immunol 2017;409:199-227.

Coates M, Blanchard S, MacLeod AS. Innate antimicrobial immunity in the skin: a protective barrier against bacteria, viruses, and fungi. PLoS Pathog 2018;14(12):e1007353.

Mertz PM, Cardenas TC, Snyder RV, Kinney MA, Davis SC, Plano LR. Staphylococcus aureus virulence factors associated with infected skin lesions: influence on the local immune response. Arch Dermatol 2007;143(10):1259-63.

Shettigar K, Murali TS. Virulence factors and clonal diversity of Staphylococcus aureus in colonization and wound infection with emphasis on diabetic foot infection. Eur J Clin Microbiol Infect Dis 2020;39(12):2235-46.

Pérez-Montarelo D, Viedma E, Larrosa N, Gómez-González C, Ruiz de Gopegui E, Muñoz-Gallego I, et al. Molecular epidemiology of Staphy-lococcus aureus bacteremia: association of molecular factors with the source of infection. Front Microbiol 2018;9:2210.

Vella V, Galgani I, Polito L, Arora AK, Creech CB, David MZ, et al. Staphylococcus aureus skin and soft tissue infection recurrence rates in out-patients: a retrospective database study at 3 US Medical Centers. Clin Infect Dis 2021;73(5):e1045-53.

De Rose DU, Pugnaloni F, Martini L, Bersani I, Ronchetti MP, Diociaiuti A, et al. Staphylococcal infections and neonatal skin: data from litera-ture and suggestions for the clinical management from four challenging patients. Antibiotics (Basel) 2023;12(4):632.

Del Giudice P. Skin infections caused by Staphylococcus aureus. Acta Derm Venereol 2020;100(9):adv00110.

Sabbagh P, Riahi SM, Gamble HR, Rostami A. The global and regional prevalence, burden, and risk factors for methicillin-resistant Staphy-lococcus aureus colonization in HIV-infected people: a systematic review and meta-analysis. Am J Infect Control 2019;47(3):323-33.

McCaig LF, McDonald LC, Mandal S, Jernigan DB. Staphylococcus aureus--associated skin and soft tissue infections in ambulatory care. Emerg Infect Dis 2006;12(11):1715-23.

Creech CB, Al-Zubeidi DN, Fritz SA. Prevention of Recurrent Staphylococcal Skin Infections. Infect Dis Clin North Am 2015;29(3):429-64.

Zagólski O, Stręk P, Kasprowicz A, Białecka A. Effectiveness of polyvalent bacterial lysate and autovaccines against upper respiratory tract bacterial colonization by potential pathogens: a randomized study. Med Sci Monit 2015;21:2997-3002.

Holtfreter S, Jursa-Kulesza J, Masiuk H, Verkaik NJ, de Vogel C, Kolata J, et al. Antibody responses in furunculosis patients vaccinated with autologous formalin-killed Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 2011;30(6):707-17.

Tattevin P, Schwartz BS, Graber CJ, Volinski J, Bhukhen A, Bhukhen A, et al. Concurrent epidemics of skin and soft tissue infection and bloodstream infection due to community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis 2012;55(6):781-8.

Pal S, Sayana A, Joshi A, Juyal D. Staphylococcus aureus: a predominant cause of surgical site infections in a rural healthcare setup of Utta-rakhand. J Family Med Prim Care 2019;8(11):3600-6.

Nichols RL. Postoperative infections in the age of drug-resistant Gram-positive bacteria. Am J Med 1998;104(5A):11-6S.

Antibacterial sutures for wound closure after surgery: a review of clinical and cost-effectiveness and guidelines for use. Ottawa (ON): Ca-nadian Agency for Drugs and Technologies in Health; 2014.

Deptuła A, Trejnowska E, Dubiel G, Żukowski M, Misiewska-Kaczur A, Ozorowski T, et al. Prevalence of healthcare-associated infections in Polish adult intensive care units: summary data from the ECDC European Point Prevalence Survey of Hospital-associated Infections and antimicrobial use in Poland 2012–2014. J Hospital Infect 2017;96(2):145-50.

Bowler PG, Duerden BI, Armstrong DG. Wound microbiology and associated approaches to wound management. Clin Microbiol Rev 2001;14(2):244-69.

Khan AKA, Mirshad PV, Rashed MR, Banu G. A Study on the usage pattern of antimicrobial agents for the prevention of surgical site infec-tions (SSIs) in a Tertiary Care Teaching Hospital. J Clin Diagn Res 2013;7(4):671-4.

Kalmerijer MD, van Nieuwland-Bollen E, Bogaers-Hoffman D, de Baere GA. Nasal carriage of Staphylococcus aureus is a major risk factor for surgical site infections in orthopedic surgery. Infect Control Hosp Epidemiol 2000;21(5):319-23.

Steiner Z, Natan OB, Sukhotnik I, Coran AG, Keren G. Does Staphylococcus aureus nasal carriage require eradication prior to elective ambula-tory surgery in children? Pediatr Surg Int 2014;30(5):521-5.

Anderson DJ, Podgorny K, Berríos-Torres SI, Bratzler DW, Dellinger EP, Greene L, et al. Strategies to prevent surgical site infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol 2014;35(6):605-27.

Gompelman M, Wertheim HFL, Bleeker-Rovers CP, Wanten GJA. Eradication of Staphylococcus aureus colonization by chronic use of mupiro-cin in patients on home parenteral nutrition. Nutrition 2021;81:110985.

Dupeyron C, Campillo B, Bordes M, Faubert E, Richardet JP, Mangeney N. A clinical trial of mupirocin in the eradication of methicillin-resistant Staphylococcus aureus nasal carriage in a digestive disease unit. J Hosp Infect 2002;52(4):281-7.

Pianka F, Mihaljevic AL. Prevention of postoperative infections: evidence-based principles. Chirurg 2017;88(5):401-7.

Bratzler DW, Dellinger EP, Olsen KM, Perl TM, Auwaerter PG, Bolon MK, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Am J Health Syst Pharm 2013;70(3):195-283.

David MZ, Boyle-Vavra S, Zychowski DL, Daum RS. Methicillin-susceptible Staphylococcus aureus as a predominantly healthcare-associated pathogen: a possible reversal of roles? PLoS One 2011;6(4):e18217.

World Health Organization. WHO guidelines on hand hygiene in health care: first global patient safety challenge clean care is safer care. Geneva: World Health Organization; 2009.

Haque M, Sartelli M, McKimm J, Abu Bakar M. Health care-associated infections – an overview. Infect Drug Resist 2018;11:2321-33.

Owens CD, Stoessel K. Surgical site infections: epidemiology, microbiology and prevention. J Hosp Infect 2008;70(Suppl 2):3-10.

Jernigan JA. Is the burden of Staphylococcus aureus among patients with surgical-site infections growing? Infect Control Hosp Epidemiol 2004;25(6):457-60.

O’Donnell RL, Angelopoulos G, Beirne JP, Biliatis I, Bolton H, Bradbury M, et al. Impact of surgical site infection (SSI) following gynaecologi-cal cancer surgery in the UK: a trainee-led multicentre audit and service evaluation. BMJ Open 2019;9(1):e024853.

Otto M. Staphylococcus colonization of the skin and antimicrobial peptides. Expert Rev Dermatol 2010;5(2):183-95.

Ellis MW, Schlett CD, Millar EV, Crawford KB, Cui T, Lanier JB, et al. Prevalence of nasal colonization and strain concordance in patients with community-associated Staphylococcus aureus skin and soft-tissue infections. Infect Control Hosp Epidemiol 2014;35(10):1251-6.

Takesue Y, Kusachi S, Mikamo H, Sato J, Watanabe A, Kiyota H, et al. Antimicrobial susceptibility of pathogens isolated from surgical site in-fections in Japan: comparison of data from nationwide surveillance studies conducted in 2010 and 2014–2015. J Infect Chemother 2017;23(6):339-48.

Sganga G, Tascini C, Sozio E, Colizza S. Early recognition of methicillin-resistant Staphylococcus aureus surgical site infections using risk and protective factors identified by a group of Italian surgeons through Delphi method. World J Emerg Surg 2017;12:25.

Tinelli M, Monaco M, Vimercati M, Ceraminiello A, Pantosti A. Methicillin-susceptible Staphylococcus aureus in skin and soft tissue infec-tions, Northern Italy. Emerg Infect Dis 2009;15(2):250-7.

Hershow RC, Khayr WF, Smith NL. A comparison of clinical virulence of nosocomially acquired methicillin-resistant and methicillin-sensitive Staphylococcus aureus infections in a university hospital. Infect Control Hosp Epidemiol 1992;13(10):587-93.

Romaniszyn D, Różańska A, Wójkowska-Mach J, Chmielarczyk A, Pobiega M, Adamski P, et al. Epidemiology, antibiotic consumption and molecular characterisation of Staphylococcus aureus infections – data from the Polish Neonatology Surveillance Network, 2009–2012. BMC Infect Dis 2015;15:169.

Romaniszyn D, Pobiega M, Wójkowska-Mach J, Chmielarczyk A, Gryglewska B, Adamski P, et al. The general status of patients and limited physical activity as risk factors of methicillin-resistant Staphylococcus aureus occurrence in long-term care facilities residents in Krakow, Poland. BMC Infect Dis 2014;14:271.

Ilczyszyn WM, Sabat AJ, Akkerboom V, Szkarlat A, Klepacka J, Sowa-Sierant I, et al. Clonal sructure and characterization of Staphylococcus aureus strains from invasive infections in paediatric patients from South Poland: association between age, spa types, clonal complexes, and genetic markers. PLoS One 2016;11(3):e0151937.

Lee A, de Lencastre H, Garau J, Kulytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Pri-mers 2018;4:18033.

Antimicrobial resistance in the EU/EEA (EARS-Net). Annual Epidemiological Report for 2021. Stockholm: EDC; 2022. (2.06.2023).

Rasmussen G, Monecke S, Brus O, Ehricht R, Söderquist B. Long term molecular epidemiology of methicillin-susceptible Staphylococcus au-reus bacteremia isolates in Sweden. PLoS One 2014;9(12):e114276.

Sasirekha B, Usha MS, Amruta JA, Ankit S, Brinda N, Divya R. Incidence of constitutive and inducible clindamycin resistance among hospi-tal-associated Staphylococcus aureus. 3 Biotech 2014;4(1):85-9.

Schreckenberger PC, Ilendo E, Ristow KL. Incidence of constitutive and inducible clindamycin resistance in Staphylococcus aureus and co-agulase-negative staphylococci in a community and a tertiary care hospital. J Clin Microbiol 2004;42(6):2777-9.

Marangon FB, Miller D, Muallem MS, Romano AC, Alfonso EC. Ciprofloxacin and levofloxacin resistance among methicillin-sensitive Staphy-lococcus aureus isolates from keratitis and conjunctivitis. Am J Ophthalmol 2004;137(3):453-8.

Weber SG, Gold HS, Hooper DC, Karchmer AW, Carmeli Y. Fluoroquinolones and the risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg Infect Dis 2003;9(11):1415-22.

Norvell MR, Porter M, Ricco MH, Koonce RC, Hogan CA, Basler E, et al. Cefazolin vs second-line antibiotics for surgical site infection preven-tion after total joint arthroplasty among patients with a beta-lactam allergy. Open Forum Infect Dis 2023;10(6):ofad224.

Saadatian-Elahi M, Teyssou R, Vanhems P. Staphylococcus aureus, the major pathogen in orthopaedic and cardiac surgical site infections: a literature review. Int J Surg 2008;6(3):238-45.

Levy PY, Ollivier M, Drancourt M, Raoult D, Argenson JN. Relation between nasal carriage of Staphylococcus aureus and surgical site infec-tion in orthopedic surgery: the role of nasal contamination. A systematic literature review and meta-analysis. Orthop Traumatol Surg Res 2013;99(6):645-51.

Al-Mulhim FA, Baragbah MA, Sadat-Ali M, Alomran AS, Azam MQ. Prevalence of surgical site infection in orthopedic surgery: a 5-year anal-ysis. Int Surg 2014;99(3):264-8.

Tucci G, Romanini E, Zanoli G, Pavan L, Fantoni M, Venditti M. Prevention of surgical site infections in orthopaedic surgery: a synthesis of current recommendations. Eur Rev Med Pharmacol Sci 2019;23(2 Suppl):224-39.

Janeczek K, Emeryk A, Zimmer Ł, Poleszak E, Ordak M. Nasal carriage of Staphylococcus aureus in children with grass pollen-induced aller-gic rhinitis and the effect of polyvalent mechanical bacterial lysate immunostimulation on carriage status: a randomized controlled trial. Immun Inflamm Dis 2022;10(3):e584.

Preoţescu LL, Streinu-Cercel O. Prevalence of nasal carriage of S. aureus in children. Germs 2013;3(2):49-51.

Mitchell P, Gottschalk M, Butts G, Xerogeanes J. Surgical site infection: a comparison of multispecialty and single specialty outpatient facili-ties. J Orthop 2013;10(3):111-4.

Shah R, Pavey E, Ju M, Merkow R, Rajaram R, Wandling MW, et al. Evaluation of readmissions due to surgical site infections: a potential tar-get for quality improvement. Am J Surg 2017;214(5):773-9.

Merkow RP, Ju MH, Chung JW, Hall BL, Cohen ME, Williams MV, et al. Underlying reasons associated with hospital readmission following surgery in the United States. JAMA 2015;313(5):483-95.

ElHawary H, Hintermayer MA, Alam P, Brunetti VC, Janis JE. Decreasing surgical site infections in plastic surgery: a systematic review and meta-analysis of level 1 evidence. Aesthet Surg J 2021;41(7):NP948-58.

Drapeau CM, D’Aniello C, Brafa A, Nicastri E, Silvestri A, Nisi G, et al. Surgical site infections in plastic surgery: an italian multicenter study. J Surg Res 2007;143(2):393-7.

Bandyk DF. Vascular surgical site infection: risk factors and preventive measures. Semin Vasc Surg 2008;21(3):119-23.

Hassan RSEE, Osman SOS, Aabdeen MAS, Mohamed WEA, Hassan RSEE, Mohamed SOO. Incidence and root causes of surgical site infections after gastrointestinal surgery at a public teaching hospital in Sudan. Patient Saf Surg 2020;14(1):45.

Muilwijk J, Walenkamp GH, Voss A, Wille JC, van den Hof S. Random effect modelling of patient-related risk factors in orthopaedic proce-dures: results from the Dutch nosocomial infection surveillance network ‘PREZIES’. J Hosp Infect 2006;62(3):319-26.

Wójkowska-Mach J, Jaje E, Romaniszyn D, Kasparek M, Frańczuk B, Bulanda M, et al. Comparison of SSI rates in endoarthroplasty of hip and knee in a Cracow patient population and the importance of postdischarge surveillance. Infection 2008;36(1):36-40.


Copyright (c) 2023 Helena Masiuk, Piotr Ostrowski, Marek Masiuk, Agata Pruss, Paweł Kwiatkowski, Iwona Bilska, Klaudia Rusińska, Anastasiia Skoryk, Joanna Jursa-Kulesza

License URL: