Antibiotic Usage and Healthcare-Associated Clostridioides difficile in Patients with and Without COVID-19: A Tertiary Hospital Experience
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Data Collection
4.2. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
BMI | Body mass index |
CDI | Clostridioides difficile infections |
COVID-19 | Coronavirus disease 2019 |
DDD | Defined daily dose |
ECDC | European Centre for Disease Prevention and Control |
ELISA | Enzyme-linked immunosorbent assay |
GDH | Glutamate dehydrogenase |
HA-CDI | Healthcare-associated C. difficile infection |
IPC | Infection prevention and control |
PCR | Polymerase chain reaction |
PY | Person-year |
SD | Standard deviation |
WHO | World Health Organization |
References
- Feuerstadt, P.; Nelson, W.W.; Drozd, E.M.; Dreyfus, J.; Dahdal, D.N.; Wong, A.C.; Mohammadi, I.; Teigland, C.; Amin, A. Mortality, health care use, and costs of Clostridioides difficile infections in older adults. J. Am. Med. Dir. Assoc. 2022, 23, 1721–1728.e19. [Google Scholar] [CrossRef] [PubMed]
- Lessa, F.C.; Mu, Y.; Bamberg, W.M.; Beldavs, Z.G.; Dumyati, G.K.; Dunn, J.R.; Farley, M.M.; Holzbauer, S.M.; Meek, J.I.; Phipps, E.C.; et al. Burden of Clostridium difficile infection in the United States. N. Engl. J. Med. 2015, 372, 825–834. [Google Scholar] [CrossRef]
- European Centre for Disease Prevention and Control. Clostridioides difficile Infections—Annual Epidemiological Report for 2018–2020; European Centre for Disease Prevention and Control: Stockholm, Sweden, 2024. Available online: https://www.ecdc.europa.eu/en/publications-data/clostridioides-difficile-infections-annual-epidemiological-report-2018-2020 (accessed on 12 August 2024).
- Forrester, J.D.; Cai, L.Z.; Mbanje, C.; Rinderknecht, T.N.; Wren, S.M. Clostridium difficile infection in low- and middle-human development index countries: A systematic review. Trop. Med. Int. Health 2017, 22, 1223–1232. [Google Scholar] [CrossRef] [PubMed]
- Heymann, D.L.; Shindo, N.; WHO Scientific and Technical Advisory Group for Infectious Hazards. COVID-19: What is next for public health? Lancet 2020, 395, 542–545. [Google Scholar] [CrossRef] [PubMed]
- Abubakar, U.; Awaisu, A.; Khan, A.H.; Alam, K. Impact of COVID-19 Pandemic on Healthcare-Associated Infections: A Systematic Review and Meta-Analysis. Antibiotics 2023, 12, 1600. [Google Scholar] [CrossRef]
- Advani, S.D.; Sickbert-Bennett, E.; Moehring, R.; Cromer, A.; Lokhnygina, Y.; Dodds-Ashley, E.; Kalu, I.C.; DiBiase, L.; Weber, D.J.; Anderson, D.J.; et al. The Disproportionate Impact of Coronavirus Disease 2019 (COVID-19) Pandemic on Healthcare-Associated Infections in Community Hospitals: Need for Expanding the Infectious Disease Workforce. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2023, 76, e34–e41. [Google Scholar] [CrossRef]
- Granata, G.; Petrosillo, N.; Al Moghazi, S.; Caraffa, E.; Puro, V.; Tillotson, G.; Cataldo, M.A. The burden of Clostridioides difficile infection in COVID-19 patients: A systematic review and meta-analysis. Anaerobe 2022, 74, 102484. [Google Scholar] [CrossRef]
- Khan, S.; Hasan, S.S.; Bond, S.E.; Conway, B.R.; Aldeyab, M.A. Antimicrobial consumption in patients with COVID-19: A systematic review and meta-analysis. Expert Rev. Anti-Infect. Ther. 2022, 20, 749–772. [Google Scholar] [CrossRef]
- Satria, Y.A.A.; Utami, M.S.; Prasudi, A. Prevalence of antibiotics prescription amongst patients with and without COVID-19 in low- and middle-income countries: A systematic review and meta-analysis. Pathog. Glob. Health 2023, 117, 437–449. [Google Scholar] [CrossRef]
- Kuehn, B.M. Antibiotic Use in UK’s COVID-19 Patients Often Unnecessary. JAMA 2021, 326, 214. [Google Scholar] [CrossRef]
- Langford, B.J.; So, M.; Raybardhan, S.; Leung, V.; Soucy, J.R.; Westwood, D.; Daneman, N.; MacFadden, D.R. Antibiotic prescribing in patients with COVID-19: Rapid review and meta-analysis. Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 2021, 27, 520–531. [Google Scholar] [CrossRef]
- Zouridis, S.; Sangha, M.; Feustel, P.; Richter, S. Clostridium difficile Infection Rates During the Pandemic in New York Capital Area: A Single-Center Study. Cureus 2023, 15, e37576. [Google Scholar] [CrossRef] [PubMed]
- Karampatakis, T.; Tsergouli, K.; Kandilioti, E.; Nikopoulou, A.; Katsifa, H.; Kachrimanidou, M. Implication of COVID-19 pandemic on the incidence of Clostridioides difficile infection in a Greek tertiary hospital. J. Med. Microbiol. 2023, 72, 001689. [Google Scholar] [CrossRef] [PubMed]
- Markovic-Denic, L.; Nikolic, V.; Toskovic, B.; Brankovic, M.; Crnokrak, B.; Popadic, V.; Radojevic, A.; Radovanovic, D.; Zdravkovic, M. Incidence and Risk Factors for Clostridioides difficile Infections in Non-COVID and COVID-19 Patients: Experience from a Tertiary Care Hospital. Microorganisms 2023, 11, 435. [Google Scholar] [CrossRef] [PubMed]
- Slimings, C.; Riley, T.V. Antibiotics and hospital-acquired Clostridium difficile infection: Update of systematic review and meta-analysis. J. Antimicrob. Chemother. 2014, 69, 881–891. [Google Scholar] [CrossRef]
- Slimings, C.; Riley, T.V. Antibiotics and healthcare facility-associated Clostridioides difficile infection: Systematic review and meta-analysis 2020 update. J. Antimicrob. Chemother. 2021, 76, 1676–1688. [Google Scholar] [CrossRef]
- World Health Organization. WHO Reports Widespread Overuse of Antibiotics in Patients Hospitalized with COVID-19; WHO: Geneva, Switzerland, 2024; Available online: https://www.who.int/news/item/26-04-2024-who-reports-widespread-overuse-of-antibiotics-in-patients--hospitalized-with-covid-19 (accessed on 10 January 2025).
- Bignardi, G.E. Risk factors for Clostridium difficile infection. J. Hosp. Infect. 1998, 40, 1–15. [Google Scholar] [CrossRef]
- Tabak, Y.P.; Srinivasan, A.; Yu, K.C.; Kurtz, S.G.; Gupta, V.; Gelone, S.; Scoble, P.J.; McDonald, L.C. Hospital-level high-risk antibiotic use in relation to hospital-associated Clostridioides difficile infections: Retrospective analysis of 2016–2017 data from US hospitals. Infect. Control Hosp. Epidemiol. 2019, 40, 1229–1235. [Google Scholar] [CrossRef]
- Ma, H.; Zhang, L.; Zhang, Y.; Liu, Y.; He, Y.; Guo, L. Combined administration of antibiotics increases the incidence of antibiotic-associated diarrhea in critically ill patients. Infect. Drug Resist. 2019, 12, 1047–1054. [Google Scholar] [CrossRef]
- Czepiel, J.; Dróżdż, M.; Pituch, H. Clostridium difficile infection: Review. Eur. J. Clin. Microbiol. Infect. Dis. 2019, 38, 1211. [Google Scholar] [CrossRef]
- Huang, H.; Wu, S.; Chen, R.; Xu, S.; Fang, H.; Weintraub, A.; Nord, C.E. Risk factors of Clostridium difficile infections among patients in a university hospital in Shanghai, China. Anaerobe 2014, 30, 65–69. [Google Scholar] [CrossRef] [PubMed]
- European Center for Disease Prevention and Control. Antimicrobial Consumption in the EU/EEA (ESAC-Net). Annual Epidemiological Report for 2023; ECDC: Stockholm, Sweden, 2024.
- European Center for Disease Prevention and Control. Antimicrobial Consumption in the EU/EEA (ESAC-Net). Annual Epidemiological Report for 2022; ECDC: Stockholm, Sweden, 2023.
- Morris, D.E.; Cleary, D.W.; Clarke, S.C. Secondary bacterial infections associated with influenza pandemics. Front. Microbiol. 2017, 8, 1041. [Google Scholar] [CrossRef]
- Huttner, B.D.; Catho, G.; Pano-Pardo, J.R.; Pulcini, C.; Schouten, J. COVID-19: Don’t neglect antimicrobial stewardship principles! Clin. Microbiol. Infect. 2020, 26, 808–810. [Google Scholar] [CrossRef] [PubMed]
- Shetty, Y.C.; Manjesh, P.S.; Churiwala, W.; Jain, S.M.; Singh, V.K. Drug use evaluation of cephalosporins in a tertiary care hospital. Perspect. Clin. Res. 2022, 13, 38–42. [Google Scholar] [CrossRef]
- Perić, A.; Rančić, N.; Dragojević-Simić, V.; Milenković, B.; Ljubenović, N.; Rakonjac, B.; Begović-Kuprešanin, V.; Šuljagić, V. Association between antibiotic use and hospital-onset Clostridioides difficile infection in university tertiary hospital in Serbia, 2011–2021: An ecological analysis. Antibiotics 2022, 11, 1178. [Google Scholar] [CrossRef] [PubMed]
- Webb, B.J.; Subramanian, A.; Lopansri, B.; Goodman, B.; Jones, P.B.; Ferraro, J.; Stenehjem, E.; Brown, S.M. Antibiotic exposure and risk for hospital-associated Clostridioides difficile infection. Antimicrob. Agents Chemother. 2020, 64, AAC.02169-19. [Google Scholar] [CrossRef]
- Kovačević, N.; Petrić, V.; Pete, M.; Popović, M.; Plećaš-Đurić, A.; Pejaković, S.; Tomić, S.; Damjanov, D.; Kosijer, D.; Lekin, M. Clostridioides difficile infection before and during Coronavirus Disease 2019 pandemic—Similarities and differences. Microorganisms 2022, 10, 2284. [Google Scholar] [CrossRef]
- Marinescu, A.R.; Laza, R.; Musta, V.F.; Cut, T.G.; Dumache, R.; Tudor, A.; Porosnicu, M.; Lazureanu, V.E.; Licker, M. Clostridium difficile and COVID-19: General data, ribotype, clinical form, treatment—Our experience from the largest infectious diseases hospital in Western Romania. Medicina 2021, 57, 1099. [Google Scholar] [CrossRef]
- Chen, Y.; Xie, X.; Ge, Q.; He, X.; Sun, Z.; Li, Y.; Guo, Y.; Geng, C.; Li, X.; Wang, C. The global burden and trend of Clostridioides difficile and its association with world antibiotic consumption, 1990–2019. J. Glob. Health 2024, 14, 04135. [Google Scholar] [CrossRef]
- Skjøt-Arkil, H.; Rune Nanthan, K.; Chen, M.; Rosenvinge, F.S. Carrier prevalence of Clostridioides difficile in emergency departments and the association of prior antibiotic consumption: A combined cross-sectional and nested case-control study. J. Antimicrob. Chemother. 2023, 78, 2089–2096. [Google Scholar] [CrossRef]
- Merchante, N.; Chico, P.; Márquez-Saavedra, E.; Riera, G.; Herrero, R.; González-de-la-Aleja, P.; Aller, A.I.; Rodríguez, J.C.; Rodríguez-Fernández, M.; Ramos, J.M.; et al. Impact of COVID19 pandemic on the incidence of health-care associated Clostridioides difficile infection. Anaerobe 2022, 75, 102579. [Google Scholar] [CrossRef] [PubMed]
- Ponce-Alonso, M.; Sáez de la Fuente, J.; Rincón-Carlavilla, A.; Moreno-Nunez, P.; Martínez-García, L.; Escudero-Sánchez, R.; Pintor, R.; García-Fernández, S.; Cobo, J. Impact of the coronavirus disease 2019 (COVID-19) pandemic on nosocomial Clostridioides difficile infection. Infect. Control. Hosp. Epidemiol. 2021, 42, 406–410. [Google Scholar] [CrossRef] [PubMed]
- Lewandowski, K.; Rosokowski, M.; Kanievska, M.; Kucha, P.; Melen, A.; Wietzba, W.; Rydzewska, G. Clostridioides difficile infection in coronavirus disease 2019 (COVID-19): An underestimated problem? Pol. Arch. Intern. Med. 2021, 13, 121–127. [Google Scholar]
- Maldonado-Barrueco, A.; Moreno-Ramos, F.; Díaz-Pollán, B.; Loeches-Yagüe, B.; Rico-Nieto, A.; García-Rodríguez, J.; Ruiz-Carrascoso, G. Increase of healthcare-onset Clostridioides difficile infection in adult population since SARS-CoV-2 pandemic: A retrospective cohort study in a tertiary care hospital from 2019 to 2022. Anaerobe 2024, 86, 102836. [Google Scholar] [CrossRef]
- Rose, A.N.; Baggs, J.; Kazakova, S.V.; Guh, A.Y.; Yi, S.H.; McCarthy, N.L.; Jernigan, J.A.; Reddy, S.C. Trends in facility-level rates of Clostridioides difficile infections in US hospitals, 2019–2020. Infect. Control. Hosp. Epidemiol. 2023, 44, 238–245. [Google Scholar] [CrossRef]
- Tsankof, A.; Protopapas, A.A.; Mantzana, P.; Protonotariou, E.; Skoura, L.; Protopapas, A.N.; Savopoulos, C.; Mimidis, K. Clostridioides difficile infection in patients with and without COVID-19 during the pandemic: A retrospective cohort study from a tertiary referral hospital. Anaerobe 2024, 88, 102864. [Google Scholar] [CrossRef]
- Courjon, J.; Contenti, J.; Demonchy, E.; Levraut, J.; Barbry, P.; Rios, G.; Dellamonica, J.; Chirio, D.; Bonnefoy, C.; Giordanengo, V.; et al. COVID-19 patients age, comorbidity profiles and clinical presentation related to the SARS-CoV-2 UK-variant spread in the Southeast of France. Sci. Rep. 2021, 11, 18456. [Google Scholar] [CrossRef]
- Lang, K.; Atchison, T.J.; Singh, P.; Kline, D.M.; Odei, J.B.; Martin, J.L.; Smyer, J.F.; Day, S.R.; Hebert, C.L. Describing the monthly variability of hospital-onset Clostridioides difficile during early coronavirus disease 2019 (COVID-19) using electronic health record data. Infect. Control. Hosp. Epidemiol. 2024, 45, 329–334. [Google Scholar] [CrossRef]
- Arsenovic, D. Excess mortality and COVID-19 deaths: Preliminary data from Serbia and comparison with European experience. Geogr. Pannonica 2023, 27, 1–9. [Google Scholar] [CrossRef]
- Crobach, M.J.; Planche, T.; Eckert, C.; Barbut, F.; Terveer, E.M.; Dekkers, O.M.; Wilcox, M.H.; Kuijper, E.J. European Society of Clinical Microbiology and Infectious Diseases: Update of the diagnostic guidance document for Clostridium difficile infection. Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 2016, 22 (Suppl. 4), S63–S81. [Google Scholar] [CrossRef]
- Shane, A.L.; Mody, R.K.; Crump, J.A.; Tarr, P.I.; Steiner, T.S.; Kotloff, K.; Langley, J.M.; Wanke, C.; Warren, C.A.; Cheng, A.C.; et al. 2017 Infectious Diseases Society of America Clinical Practice Guidelines for the Diagnosis and Management of Infectious Diarrhea. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2017, 65, e45–e80. [Google Scholar] [CrossRef]
- Kelly, C.R.; Fischer, M.; Allegretti, J.R.; LaPlante, K.; Stewart, D.B.; Limketkai, B.N.; Stollman, N.H. ACG clinical guidelines: Prevention, diagnosis, and treatment of Clostridioides difficile infections. Am. J. Gastroenterol. 2021, 116, 1124–1147. [Google Scholar] [CrossRef]
- European Centre for Disease Prevention and Control (ECDC). COVID-19: ECDC Updates Case Definition for EU Surveillance. Available online: https://www.ecdc.europa.eu/en/news-events/covid-19-ecdc-updates-case-definition-eu-surveillance (accessed on 10 January 2025).
- World Health Organization (WHO). Laboratory Testing for 2019 Novel Coronavirus (2019-nCoV) in Suspected Human Cases: Interim Guidance, 17 January 2020. Available online: https://iris.who.int/bitstream/handle/10665/330676/9789240000971-eng.pdf?sequence=1 (accessed on 10 January 2025).
- Institute of Public Health of Serbia. Healthcare-Associated Infections Definitions; Institute of Public Health of Serbia: Belgrade, Serbia, 2017. (In Serbian) [Google Scholar]
- World Health Organization (WHO). Defined Daily Dose (DDD): Definition and General Considerations; WHO: Geneva, Switzerland; Available online: https://www.who.int/tools/atc-ddd-toolkit/about-ddd (accessed on 10 January 2025).
- Ministry of Health. National Guide to Good Clinical Practice. Rational Use of Antibiotics. Belgrade, 2018. Available online: https://www.zdravlje.gov.rs/view_file.php?file_id=527&cache=sr (accessed on 9 January 2025).
Total n (%) | Non-COVID-19 n (%) | COVID-19 n (%) | p Value | |
---|---|---|---|---|
Age | 70.9 ± 12.3 | 72.5 ± 11.6 | 69.9 ± 12.6 | |
Age under 65 years | 133 (24.3) | 38 (18.4) | 95 (27.9) | 0.017 |
Age 65 years and above | 414 (75.7) | 168 (81.6) | 246 (72.1) | |
Sex | ||||
Female | 283 (51.7) | 110 (53.4) | 173 (50.7) | 0.546 |
Male | 264 (48.3) | 96 (46.6) | 168 (49.3) | |
BMI | 27.5 ± 5.5 | 27.6 ± 6.9 | 27.5 ± 4.7 | 0.900 |
Comorbidity | ||||
Without | 97 (17.1) | 16 (7.8) | 81 (23.8) | <0.001 |
One comorbidity present | 177 (32.4) | 57 (27.7) | 120 (35.2) | |
Two comorbidities present | 184 (33.6) | 79 (38.3) | 105 (30.8) | |
Three or more comorbidities present | 89 (16.3) | 54 (26.2) | 35 (10.3) | |
Season during the medical examination | ||||
Spring | 117 (21.4) | 73 (35.4) | 44 (12.9) | <0.001 |
Summer | 92 (16.8) | 68 (33) | 24 (7) | |
Autumn | 246 (45) | 21 (10.2) | 225 (66) | |
Winter | 92 (16.8) | 44 (21.4) | 48 (14.1) | |
Outcome | ||||
Discharge | 427 (77.7) | 155 (72.5) | 270 (79.2) | 0.387 |
Death | 121 (22.1) | 81 (24.8) | 70 (20.5) | |
Admission to another hospital | 1 (0.2) | 1 (0.3) | 0 (0.0) | |
Duration of hospitalization | 20.5 ± 11.8 | 21.2 ± 12.8 | 20.1 ± 11.2 | 0.272 |
Antibiotics | Total | Non-COVID-19 | COVID-19 | p Value | |||
---|---|---|---|---|---|---|---|
n (%) | Duration Mean ± SD | n (%) | Duration Mean ± SD | n (%) | Duration Mean ± SD | ||
Cephalosporins 2nd gen | 6 (1.1) | 4.2 ± 2.5 | 4 (1.9) | 4.7 ± 2.5 | 2 (0.6) | 2.0 ± 0.0 | 0.205 *, 0.398 ** |
Cephalosporins 3rd gen | 378 (69.1) | 7.1 ± 4.8 | 119 (57.8) | 6.1 ± 3.7 | 259 (76.0) | 7.5 ± 5.1 | <0.001 *, 0.010 ** |
Cephalosporins 4th gen | 68 (12.4) | 5.6 ± 3.4 | 7 (3.4) | 7.7 ± 2.6 | 61 (17.9) | 5.7 ± 3.5 | <0.001 *, 0.472 ** |
Aminoglycosides | 33 (6.0) | 6.1 ± 4.4 | 23 (11.2) | 6.2 ± 4.2 | 10 (2.9) | 5.9 ± 5.2 | <0.001 *, 0.873 ** |
Fluoroquinolones | 208 (38) | 7.0 ± 4.4 | 49 (23.8) | 6.5 ± 3.6 | 159 (46.6) | 7.2 ± 4.6 | <0.001 *, 0.352 ** |
Sulfonamides and trimethoprim | 15 (2.7) | 6.1 ± 4.4 | 9 (4.4) | 6.1 ± 5.1 | 6 (1.8) | 6.1 ± 4.0 | 0.070 *, 0.994 ** |
Macrolides, lincosamines and streptogramins | 60 (11.0) | 5.7 ± 4.0 | 11 (5.3) | 6.2 ± 5.4 | 49 (14.4) | 5.5 ± 3.7 | 0.010 *, 0.642 ** |
Carbapenems | 92 (16.8) | 7.5 ± 5.5 | 31 (15.0) | 8.4 ± 5.2 | 61 (17.9) | 7.0 ± 5.7 | 0.390 *, 0.277 |
Tetracyclines and chloramphenicol | 6 (1.1) | 5.0 ± 1.9 | 1 (0.5) | NA | 5 (1.5) | 5.0 ± 1.9 | 0.286 *, NA ** |
Glycopeptides | 33 (6.0) | 6.9 ± 4.5 | 17 (7.3) | 7.9 ± 4.7 | 18 (5.3) | 6.1 ± 4.3 | 0.340 *, 0.288 ** |
Polymyxins | 22 (4.0) | 7.0 ± 5.8 | 8 (3.9) | 4.4 ± 1.7 | 14 (4.1) | 8.0 ± 6.5 | 0.898 *, 0.242 ** |
Other antibiotics | 43 (7.9) | 8.4 ± 5.4 | 29 (14.1) | 9.21 ± 5.90 | 14 (4.1) | 7.00 ± 4.32 | <0.001 *, 0.244 ** |
The number of applied groups of antibiotics | |||||||
One | 151 (30.0) | 64 (38.1) | 87 (25.9) | 0.03 * | |||
Two | 173 (34.3) | 55 (32.7) | 118 (35.1) | ||||
Three | 105 (20.8) | 30 (17.9) | 75 (22.3) | ||||
Four and more | 75 (14.9) | 19 (11.3) | 56 (16.7) |
Univariate Logistic Regression OR (95% CI) | Multivariate Logistic Regression OR (95% CI) | |
---|---|---|
Age | ||
Age under 65 years | ||
Age 65 years and above | 0.59 (0.38–0.89) | |
Comorbidities | ||
Without | ref. | ref. |
1 comorbidity present | 0.42 (0.22–0.77) | 0.54 (0.25–1.18) |
2 comorbidities present | 0.26 (0.14–0.48) | 0.34 (0.16–0.72) |
3 or more comorbidities present | 0.13 (0.06–0.25) | 0.20 (0.09–0.47) |
Season during the medical examination | ||
Winter | ref. | ref. |
Spring | 0.55 (0.32–0.96) | 0.64 (0.32–1.26) |
Summer | 0.32 (0.17–0.60) | 0.35 (0.17–0.73) |
Autumn | 9.82 (5.36–18.01) | 9.55 (4.69–19.44) |
Cephalosporins 3rd gen | 2.31 (1.59–3.35) | |
Cephalosporins 4th gen | 6.20 (2.78–13.82) | 6.13 (2.47–15.25) |
Aminoglycosides | 0.24 (0.11–0.52) | 0.23 (0.09–0.62) |
Fluoroquinolones | 2.80 (1.91–4.11) | 2.00 (1.21–3.31) |
Macrolides, lincosamines and streptogramins | 2.99 (1.51–5.88) | |
The number of applied groups of antibiotics | ||
One | ref. | |
Two | 1.58 (1.00–2.49) | |
Three | 1.84 (1.08–3.13) | |
Four and more | 2.17 (1.17–4.00) |
Antibiotic | Total | Non-COVID-19 | COVID-19 | p-Value |
---|---|---|---|---|
DDD Median (Min–Max) | ||||
Amikacin | 4.50 (1.00–6.00) | 5.00 (1.00–6.00) | 4.00 (2.00–6.00) | 1.000 |
Amoxicillin-clavulanate | 9.75 (2.00–14.00) | 14.00 (14.00–14.00) | 5.50 (2.00–13.00) | 0.137 |
Azithromycin | 5.75 (2.00–12.00) | 6.50 (5.00–11.00) | 5.00 (2.00–12.00) | 0.068 |
Cefepime | 5.00 (1.00–13.00) | 5.00 (1.00–11.00) | 5.00 (1.00–13.00) | 1.000 |
Cefixime | 4.50 (2.00–10.00) | 5.00 (5.00–5.00) | 4.00 (2.00–10.00) | 0.573 |
Ceftazidime | 3.50 (1.00–7.00) | 3.00 (1.00–5.00) | 4.00 (2.00–7.00) | 0.437 |
Ceftriaxone | 5.00 (1.00–20.00) | 4.00 (1.00–14.00) | 6.00 (1.00–20.00) | 0.007 |
Cefuroxime | 9.50 (2.00–12.00) | 7.00 (2.00–8.00) | 12.00 (12.00–12.00) | 0.276 |
Ciprofloxacin | 5.25 (1.00–10.00) | 5.00 (1.00–10.00) | 5.50 (1.00–10.00) | 0.724 |
Clindamycin | 2.00 (1.00–3.00) | 1.00 (1.00–1.00) | 3.00 (3.00–3.00) | 1.000 |
Colistimethate-sodium | 3.50 (3.00–4.00) | 4.00 (4.00–4.00) | 3.00 (3.00–3.00) | 0.248 |
Imipenem-cilastatin | 5.00 (3.00–8.00) | 4.00 (3.00–4.00) | 6.00 (4.00–8.00) | 0.164 |
Levofloxacin | 4.75 (1.00–20.00) | 4.00 (3.00–10.00) | 5.50 (1.00–20.00) | 0.422 |
Meropenem | 4.25 (1.00–15.00) | 5.50 (4.00–15.00) | 3.00 (1.00–13.00) | 0.011 |
Metronidazole | 7.75 (1.00–13.00) | 5.50 (1.00–13.00) | 10.00 (10.00–10.00) | 0.525 |
Trimethoprim-sulfamethoxazole | 7.00 (3.00–10.00) | 4.00 (3.00–7.00) | 10.00 (10.00–10.00) | 0.500 |
Vancomycin | 4.50(4.00–5.00) | 4.00 (4.00–4.00) | 5.00 (5.00–5.00) | 0.479 |
Antibiotic | Total | Non-COVID-19 | COVID-19 |
---|---|---|---|
Days of Therapy Per 1000 Patient-Days | |||
Amikacin | 38.7 | 45.7 | 34.3 |
Amoxicillin-clavulanate | 28.9 | 5.5 | 43.8 |
Azithromycin | 87.1 | 46.8 | 129.2 |
Cefepime | 142.3 | 28.8 | 214.9 |
Cefixime | 41.7 | 2.3 | 66.9 |
Ceftazidime | 59.6 | 51.4 | 64.8 |
Ceftriaxone | 364.5 | 226.3 | 452.7 |
Cefuroxime | 7.1 | 11.9 | 4.1 |
Ciprofloxacin | 57.7 | 104.2 | 28.0 |
Clindamycin | 9.3 | 6.4 | 11.2 |
Colistimethate-sodium | 30.4 | 8.0 | 44.8 |
Imipenem-cilastatin | 32.1 | 32.9 | 31.6 |
Levofloxacin | 222.2 | 45.4 | 335.0 |
Meropenem | 108.3 | 108.1 | 125.0 |
Metronidazole | 62.4 | 117.2 | 27.4 |
Trimethoprim-sulfamethoxazole | 23.0 | 35.9 | 14.8 |
Vancomycin | 65.0 | 82.9 | 53.5 |
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Zdravkovic, D.; Markovic-Denic, L.; Nikolic, V.; Todorovic, Z.; Brankovic, M.; Radojevic, A.; Radovanovic, D.; Toskovic, B. Antibiotic Usage and Healthcare-Associated Clostridioides difficile in Patients with and Without COVID-19: A Tertiary Hospital Experience. Antibiotics 2025, 14, 303. https://doi.org/10.3390/antibiotics14030303
Zdravkovic D, Markovic-Denic L, Nikolic V, Todorovic Z, Brankovic M, Radojevic A, Radovanovic D, Toskovic B. Antibiotic Usage and Healthcare-Associated Clostridioides difficile in Patients with and Without COVID-19: A Tertiary Hospital Experience. Antibiotics. 2025; 14(3):303. https://doi.org/10.3390/antibiotics14030303
Chicago/Turabian StyleZdravkovic, Darko, Ljiljana Markovic-Denic, Vladimir Nikolic, Zoran Todorovic, Marija Brankovic, Aleksandra Radojevic, Dusan Radovanovic, and Borislav Toskovic. 2025. "Antibiotic Usage and Healthcare-Associated Clostridioides difficile in Patients with and Without COVID-19: A Tertiary Hospital Experience" Antibiotics 14, no. 3: 303. https://doi.org/10.3390/antibiotics14030303
APA StyleZdravkovic, D., Markovic-Denic, L., Nikolic, V., Todorovic, Z., Brankovic, M., Radojevic, A., Radovanovic, D., & Toskovic, B. (2025). Antibiotic Usage and Healthcare-Associated Clostridioides difficile in Patients with and Without COVID-19: A Tertiary Hospital Experience. Antibiotics, 14(3), 303. https://doi.org/10.3390/antibiotics14030303