Adherence to Staphylococcus aureus Bacteremia Management Recommendations Before, During, and After the COVID-19 Pandemic: Prognostic Implications
Abstract
1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Study Design
4.2. Participants
4.3. Definitions
4.4. Microbiological Identification Techniques
4.5. Main Study Variables
4.6. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
ASP | Antibiotics Stewardship Program |
FMEA | Failure Modes and Effects Analysis |
ID | Infectious disease |
MRSA | Methicillin-resistant S. aureus |
PCR | Polymerase chain reaction |
SAB | S. aureus bacteremia |
References
- Arientová, S.; Jícha, Z.; Beran, O.; Holub, M. Decreased quality of care for Staphylococcus aureus bacteremia during the COVID-19 pandemic. BMC Infect. Dis. 2022, 22, 631. [Google Scholar] [CrossRef]
- López-Cortés, L.E.; del Toro, M.D.; Gálvez-Acebal, J.; Bereciartua-Bastarrica, E.; Fariñas, M.C.; Sanz-Franco, M.; Natera, C.; Corzo, J.E.; Lomas, J.M.; Pasquau, J.; et al. Impact of an Evidence-Based Bundle Intervention in the Quality-of-Care Management and Outcome of Staphylococcus aureus Bacteremia. Clin. Infect. Dis. 2013, 57, 1225–1233. [Google Scholar] [CrossRef]
- Brotherton, A.L.; Rab, S.; Kandiah, S.; Kriengkauykiat, J.; Wong, J.R. The impact of an automated antibiotic stewardship intervention for the management of Staphylococcus aureus bacteraemia utilizing the electronic health record. J. Antimicrob. Chemother. 2020, 75, 1054–1060. [Google Scholar] [CrossRef]
- Böing, C.W.; Froböse, N.J.; Schaumburg, F.; Kampmeier, S. Impact of the COVID-19 Pandemic on the Management of Staphylococcus aureus Bloodstream Infections in a Tertiary Care Hospital. Pathogens 2023, 12, 611. [Google Scholar] [CrossRef]
- Gudiol, F.; Aguado, J.M.; Almirante, B.; Bouza, E.; Cercenado, E.; Domínguez, M.Á.; Gasch, O.; Lora-Tamayo, J.; Miró, J.M.; Palomar, M.; et al. Diagnosis and treatment of bacteremia and endocarditis due to Staphylococcus aureus. A clinical guideline from the Spanish Society of Clinical Microbiology and Infectious Diseases (SEIMC). Enfermedades Infect. Microbiol. Clín. 2015, 33, e1–e625. [Google Scholar]
- Escrihuela-Vidal, F.; Kaasch, A.J.; Von Cube, M.; Rieg, S.; Kern, W.V.; Seifert, H.; Song, K.-H.; Liao, C.-H.; Tilley, R.; Gott, H.; et al. Impact of adherence to individual quality-of-care indicators on the prognosis of bloodstream infection due to Staphylococcus aureus: A prospective observational multicentre cohort. Clin. Microbiol. Infect. 2023, 29, 498–505. [Google Scholar] [CrossRef]
- Kufel, W.D.; Mastro, K.A.; Steele, J.M.; Wang, D.; Riddell, S.W.; Paolino, K.M.; Thomas, S.J. Impact of a pharmacist-facilitated, evidence-based bundle initiative on Staphylococcus aureus bacteremia management. Diagn. Microbiol. Infect. Dis. 2021, 101, 115535. [Google Scholar] [CrossRef]
- Nguyen, D.T.; Graviss, E.A. Development and validation of a prognostic score to predict tuberculosis mortality. J. Infect. 2018, 77, 283–290. [Google Scholar] [CrossRef]
- Fukushima, S.; Hagiya, H.; Kuninaga, N.; Haruki, Y.; Yamada, H.; Iwamoto, Y.; Yoshida, M.; Sato, K.; Hanayama, Y.; Tanaka, S.; et al. Adherence to and clinical utility of “quality indicators” for Staphylococcus aureus bacteremia: A retrospective, multicenter study. Infection 2024, 52, 1527–1538. [Google Scholar] [CrossRef]
- Nagao, M.; Yamamoto, M.; Matsumura, Y.; Yokota, I.; Takakura, S.; Teramukai, S.; Ichiyama, S. Complete adherence to evidence-based quality-of-care indicators for Staphylococcus aureus bacteremia resulted in better prognosis. Infection 2017, 45, 83–91. [Google Scholar] [CrossRef]
- Liu, C.; Bayer, A.; Cosgrove, S.E.; Daum, R.S.; Fridkin, S.K.; Gorwitz, R.J.; Kaplan, S.L.; Karchmer, A.W.; Levine, D.P.; Murray, B.E.; et al. Clinical Practice Guidelines by the Infectious Diseases Society of America for the Treatment of Methicillin-Resistant Staphylococcus aureus Infections in Adults and Children. Clin. Infect. Dis. 2011, 52, e18–e55. [Google Scholar] [CrossRef]
- Lorenzo-Hernández, E.; Rivas-Ruiz, F.; Del Arco-Jiménez, A. Consequences of the COVID-19 Pandemic on the Incidence, Management and Outcomes of Staphylococcus aureus Bacteraemia: Experience in a Spanish Hospital. Pathogens 2024, 13, 847. [Google Scholar] [CrossRef]
- Casalini, G.; Pagani, C.; Giacomelli, A.; Galimberti, L.; Milazzo, L.; Coen, M.; Reato, S.; Caloni, B.; Caronni, S.; Pagano, S.; et al. Impact of a Bundle of Interventions on Quality-of-Care Indicators for Staphylococcus aureus Bacteraemia: A Single-Centre, Quasi-Experimental, Before–After Study. Antibiotics 2024, 13, 646. [Google Scholar] [CrossRef] [PubMed]
- Green, J.; Howard, J.; Shankar, A.; Clinghan, R.; Luff, T.; Birch, M.; Pithie, A.; Werno, A.; Metcalf, S.; Chambers, S. Assessing the impact of a ‘bundle of care’ approach to Staphylococcus aureus bacteraemia in a tertiary hospital. Infect. Prev. Pr. 2020, 2, 100096. [Google Scholar] [CrossRef]
- Pérez-Rodríguez, M.T.; Sousa, A.; López-Cortés, L.E.; Martínez-Lamas, L.; Val, N.; Baroja, A.; Nodar, A.; Vasallo, F.; Álvarez-Fernández, M.; Crespo, M.; et al. Moving beyond unsolicited consultation: Additional impact of a structured intervention on mortality in Staphylococcus aureus bacteraemia. J. Antimicrob. Chemother. 2019, 74, 1101–1107. [Google Scholar] [CrossRef]
- Ministerio de Sanidad—Ciudadanos—Prestaciones y Centro Sanitarios—Centros y Servicios del SNS—Instituto de Informacion Sanitaria—Centros y Servicios del SNS—Centros [Internet]. Available online: https://www.sanidad.gob.es/fr/ciudadanos/centros.do?metodo=realizarDetalle&tipo=hospital&numero=290287 (accessed on 25 March 2025).
- Kuehl, R.; Morata, L.; Boeing, C.; Subirana, I.; Seifert, H.; Rieg, S.; Bin Kim, H.; Kim, E.S.; Liao, C.-H.; Tilley, R.; et al. Defining persistent Staphylococcus aureus bacteraemia: Secondary analysis of a prospective cohort study. Lancet Infect. Dis. 2020, 20, 1409–1417. [Google Scholar] [CrossRef]
- Goto, M.; Schweizer, M.L.; Vaughan-Sarrazin, M.S.; Perencevich, E.N.; Livorsi, D.J.; Diekema, D.J.; Richardson, K.K.; Beck, B.F.; Alexander, B.; Ohl, M.E. Association of Evidence-Based Care Processes With Mortality in Staphylococcus aureus Bacteremia at Veterans Health Administration Hospitals, 2003–2014. JAMA Intern. Med. 2017, 177, 1489. [Google Scholar] [CrossRef]
- Mason, C.Y.; Sobti, A.; Goodman, A.L. Staphylococcus aureus bacteriuria: Implications and management. JAC Antimicrob. Resist. 2023, 5, dlac123. [Google Scholar] [CrossRef]
- Cauhapé, V.; Lamy, B.; Lotte, R.; Touitou, I.; Boyer, L.; Contenti, J.; Parisot, F.; Ruimy, R.; Carles, M.; Courjon, J. Lesson from the COVID-19 pandemic lockdown: A major change of hospital-diagnosed bacteremia epidemiology. Infect. Dis. Now 2023, 53, 104709. [Google Scholar] [CrossRef]
- Bauer, K.A.; Puzniak, L.A.; Yu, K.C.; Finelli, L.; Moise, P.; Ai, C.; Watts, J.A.; Gupta, V. Epidemiology and outcomes of culture-positive bloodstream pathogens prior to and during the SARS-CoV-2 pandemic: A multicenter evaluation. BMC Infect Dis. 2022, 22, 841. [Google Scholar] [CrossRef]
- Falces-Romero, I.; Bloise, I.; García-Rodríguez, J.; Cendejas-Bueno, E. Staphylococcus aureus bacteremia in patients with SARS-CoV-2 infection. Med. Clin. (Engl. Ed.) 2023, 160, 495–498. [Google Scholar]
- Baker, M.A.; Sands, K.E.; Huang, S.S.; Kleinman, K.; Septimus, E.J.; Varma, N.; Blanchard, J.; Poland, R.E.; Coady, M.H.; Yokoe, D.S.; et al. The Impact of Coronavirus Disease 2019 (COVID-19) on Healthcare-Associated Infections. Clin. Infect. Dis. 2022, 74, 1748–1754. [Google Scholar] [CrossRef] [PubMed]
- Weiner-Lastinger, L.M.; Pattabiraman, V.; Konnor, R.Y.; Patel, P.R.; Wong, E.; Xu, S.Y.; Smith, B.; Edwards, J.R.; Dudeck, M.A. The impact of coronavirus disease 2019 (COVID-19) on healthcare-associated infections in 2020: A summary of data reported to the National Healthcare Safety Network. Infect. Control. Hosp. Epidemiol. 2022, 43, 12–25. [Google Scholar] [CrossRef] [PubMed]
- Parriott, A.M.; Kazerouni, N.N.; Epson, E.E. Association of the coronavirus disease 2019 (COVID-19) pandemic with the incidence of healthcare-associated infections in California hospitals. Infect. Control Hosp. Epidemiol. 2023, 44, 1429–1436. [Google Scholar] [CrossRef]
- Tong, S.Y.C.; Fowler VGJr Skalla, L.; Holland, T.L. Management of Staphylococcus aureus Bacteremia: A Review. JAMA 2025. [Google Scholar] [CrossRef]
- Willekens, R.; Puig-Asensio, M.; Suanzes, P.; Fernández-Hidalgo, N.; Larrosa, M.N.; González-López, J.J.; Rodríguez-Pardo, D.; Pigrau, C.; Almirante, B. Mortality in Staphylococcus aureus bacteraemia remains high despite adherence to quality indicators: Secondary analysis of a prospective cohort study. J. Infect. 2021, 83, 656–663. [Google Scholar] [CrossRef]
- Lyall, M.J.; Lone, N.I. Higher clinical acuity and 7-day hospital mortality in non-COVID-19 acute medical admissions: Prospective observational study. Emerg. Med. J. 2021, 38, 366–370. [Google Scholar] [CrossRef] [PubMed]
- Jakoby, L.; Molitor, E.; Mutters, N.T.; Weppler, R.; Rauschning, D.; Döhla, M. Quality Management Outweighs Pandemic: Retrospective Analysis Shows Improved Quality of Care for Staphylococcus aureus Bacteremia Despite SARS-CoV-2. Diseases 2025, 13, 104. [Google Scholar] [CrossRef]
- Lines, T.H.; Nesbitt, W.J.; Greene, M.H.; Nelson, G.E. Description of a pharmacist-driven safety algorithm in Staphylococcus aureus bacteremia: Compliance, interventions, and good saves. Infect. Control. Hosp. Epidemiol. 2020, 41, 921–925. [Google Scholar] [CrossRef]
- Berger, N.J.; Wright, M.E.; Pouliot, J.D.; Green, M.W.; Armstrong, D.K. The Impact of a Pharmacist-Driven Staphylococcus aureus Bacteremia Initiative in a Community Hospital: A Retrospective Cohort Analysis. Pharmacy 2021, 9, 191. [Google Scholar] [CrossRef]
- Weis, S.; Hagel, S.; Palm, J.; Scherag, A.; Kolanos, S.; Bahrs, C.; Löffler, B.; Schmitz, R.P.H.; Rißner, F.; Brunkhorst, F.M.; et al. Effect of Automated Telephone Infectious Disease Consultations to Nonacademic Hospitals on 30-Day Mortality Among Patients With Staphylococcus aureus Bacteremia: The SUPPORT Cluster Randomized Clinical Trial. JAMA Netw. Open 2022, 5, e2218515. [Google Scholar] [CrossRef] [PubMed]
- Cercenado, E.; Rodríguez-Baño, J.; Alfonso, J.L.; Calbo, E.; Escosa, L.; Fernández-Polo, A.; García-Rodríguez, J.; Garnacho, J.; Gil-Navarro, M.V.; Grau, S.; et al. Antimicrobial stewardship in hospitals: Expert recommendation guidance document for activities in specific populations, syndromes and other aspects (PROA-2) from SEIMC, SEFH, SEMPSPGS, SEMICYUC and SEIP. Enfermedades Infecc. Microbiol. Clín. 2023, 41, 238–242. [Google Scholar] [CrossRef]
Pre-Pandemic Period | Pandemic Period | Post-Pandemic Period | p | ||
---|---|---|---|---|---|
Total | 75 | 97 | 104 | - | |
Sex (male); N (%) | 57 (76) | 69 (71.1) | 78 (75) | 0.940 | |
Age; Mean years (SD) | 61.6 (17.4) | 66.1 (15.4) | 63.8 (16.9) | 0.210 | |
Charlson Comorbidity Index; Median (P25–P75, range) | 2 (1–4.0, 0–8) | 2 (0–3.5, 0–8) | 2 (1–4, 0–12) | 0.380 | |
Pitt score; Median (P25–P75, range) | 1 (0–2, 0–6) | 0 (0–2, 0–14) | 0 (0–1, 0–8) | 0.025 | |
Mccabe; n (%) | Not fatal | 32 (42.7) | 45 (46.4) | 33 (31.7) | 0.500 |
Quickly fatal | 20 (26.7) | 31 (32) | 44 (42.3) | ||
Ultimately fatal | 23 (30.7) | 21 (21.6) | 27 (26) | ||
Sepsis at diagnosis, n (%) | 21 (28.4) | 31 (32) | 37 (35.9) | 0.570 | |
Bacteria; n (%) | MSSA | 71 (94.7) | 90 (92.8) | 91 (87.5) | 0.190 |
MRSA | 4 (5.3) | 7 (7.2) | 13 (12.5) | ||
Acquisition; n (%) | Community | 26 (34.7) | 26 (26.8) | 30 (28.8) | 0.640 |
Related to healthcare | 19 (25.3) | 21 (21.6) | 23 (22.1) | ||
Nosocomial | 30 (40) | 50 (51.5) | 51 (49) | ||
Source of infection; n (%) | Catheter | 24 (32) | 21 (21.6) | 32 (30.8) | - |
SSTI | 18 (24) | 26 (26.8) | 18 (17.3) | ||
Respiratory | 12 (16) | 15 (15.5) | 13 (12.5) | ||
Endocarditis | 4 (5.3) | 8 (8.2) | 4 (3.8) | ||
Osteoarticular | 3 (4) | 5 (5.2) | 13 (12.5) | ||
Abdominal | 1 (1.3) | 6 (6.2) | 4 (3.8) | ||
Urinary | 3 (4) | 5 (5.2) | 12 (11.5) | ||
Others | 1 (1.3) | 1 (1) | 0 | ||
Primary | 9 (12) | 10 (10.3) | 8 (7.7) |
Pre-Pandemic Period | Pandemic Period | Post-Pandemic Period | p | ||
---|---|---|---|---|---|
Adequate empirical therapy, n/total (%) | 56/72 (77.8) | 81/94 (86.2) | 80/97 (82.5) | 0.370 | |
Adequate empirical dosage, n/total (%) | 51/71 (71.8) | 77/86 (89.5) | 83/97 (85.6) | 0.009 | |
Early empirical therapy (before 24 h), n/total (%) | 57/73 (78.1) | 90/97 (92.8) | 90/104 (86.5) | 0.020 | |
Adequate targeted therapy, n/total (%) | 69/73 (94.5) | 91/96 (94.8) | 100/103 (97.1) | 0.640 | |
Adequate targeted dosage, n/total (%) | 66/74 (89.2) | 87/96 (90.6) | 101/103 (98.1) | 0.040 | |
Infection source search, n/total (%) | 69/75 (92.0) | 93/97 (95.9) | 99/103 (96.1) | 0.400 | |
Adequate duration, n/total (%) | 66/74 (89.2) | 87/96 (90.6) | 101/103 (98.1) | 0.038 | |
Echocardiogram, n/total (%) | 59/75 (78.7) | 76/97 (78.4) | 79/104 (76.0) | 0.890 | |
Control blood cultures, n/total (%) | 48/75 (64.0) | 58/97 (59.8) | 62/104 (59.6) | 0.810 | |
Compliance with all recommendations, n/total (%) | 40/75 (53.3) | 51/97 (52.6) | 49/104 (47.1) | 0.640 | |
Written recommendations | 34 (45.3) | 39 (40.2) | 58 (55.8) | 0.080 | |
Adherence to the expert recommendations, n/total (%) | No adherence | 7 (20.6) | 4 (10.3) | 7 (12.1) | 0.310 |
Partial | 4 (11.8) | 5 (12.8) | 14 (24.1) | ||
Total | 23 (67.6) | 30 (76.9) | 37 (63.8) |
Pre-Pandemic Period | Pandemic Period | Post-Pandemic Period | p | ||
---|---|---|---|---|---|
Complications at 30 days | Total | 72 | 91 | 103 | - |
None | 60 (83.3) | 79 (86.8) | 85 (82.5) | ||
Endocarditis | 5 (6.9) | 3 (3.3) | 6 (5.8) | ||
Osteoarticular | 0 | 1 (1.1) | 2 (1.9) | ||
Abscess | 2 (2.8) | 1 (1.1) | 6 (5.8) | ||
Pulmonary embolism | 3 (4.2) | 2 (2.2) | 2 (1.9) | ||
CNS embolism | 0 | 3 (3.3) | 1 (1) | ||
Complications/death at 30 days, n (%) | 17/74 (23.0) | 25/95 (26.3) | 35/104 (33.7) | 0.260 | |
Death at 14 days, n (%) | 6/75 (8.0) | 10/97 (10.3) | 6/104 (5.8) | 0.490 | |
Death at 30 days, n (%) | 9/75 (12.0) | 17/95 (17.9) | 13/103 (12.6) | 0.460 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Lorenzo-Hernández, E.; Rivas-Ruiz, F.; Fernández-Casañas, J.; Puerto-Romero, V.; Martín-Escalante, M.D.; Del Arco-Jiménez, A. Adherence to Staphylococcus aureus Bacteremia Management Recommendations Before, During, and After the COVID-19 Pandemic: Prognostic Implications. Antibiotics 2025, 14, 615. https://doi.org/10.3390/antibiotics14060615
Lorenzo-Hernández E, Rivas-Ruiz F, Fernández-Casañas J, Puerto-Romero V, Martín-Escalante MD, Del Arco-Jiménez A. Adherence to Staphylococcus aureus Bacteremia Management Recommendations Before, During, and After the COVID-19 Pandemic: Prognostic Implications. Antibiotics. 2025; 14(6):615. https://doi.org/10.3390/antibiotics14060615
Chicago/Turabian StyleLorenzo-Hernández, Elizabeth, Francisco Rivas-Ruiz, Jorge Fernández-Casañas, Vanesa Puerto-Romero, Maria Dolores Martín-Escalante, and Alfonso Del Arco-Jiménez. 2025. "Adherence to Staphylococcus aureus Bacteremia Management Recommendations Before, During, and After the COVID-19 Pandemic: Prognostic Implications" Antibiotics 14, no. 6: 615. https://doi.org/10.3390/antibiotics14060615
APA StyleLorenzo-Hernández, E., Rivas-Ruiz, F., Fernández-Casañas, J., Puerto-Romero, V., Martín-Escalante, M. D., & Del Arco-Jiménez, A. (2025). Adherence to Staphylococcus aureus Bacteremia Management Recommendations Before, During, and After the COVID-19 Pandemic: Prognostic Implications. Antibiotics, 14(6), 615. https://doi.org/10.3390/antibiotics14060615