Abstract
The widespread evolution of phenotypic resistance in clinical isolates over the years, coupled with the COVID-19 pandemic onset, has exacerbated the global challenge of antimicrobial resistance. This study aimed to explore changes in bacterial infection patterns and antimicrobial resistance during the COVID-19 pandemic. This study involved the periods before and during COVID-19: the pre-pandemic and pandemic eras. The surveillance results of bacterial isolates causing infections in cancer patients at an Egyptian tertiary oncology hospital were retrieved. The Vitek®2 or Phoenix systems were utilized for species identification and susceptibility testing. Statistical analyses were performed comparing microbiological trends before and during the pandemic. Out of 2856 bacterial isolates, Gram-negative bacteria (GNB) predominated (69.7%), and Gram-positive bacteria (GPB) comprised 30.3% of isolates. No significant change was found in GNB prevalence during the pandemic (P = 0.159). Elevated rates of Klebsiella and Pseudomonas species were demonstrated during the pandemic, as was a decrease in E. coli and Acinetobacter species (P < 0.001, 0.018, < 0.001, and 0.046, respectively) in hematological patients. In surgical patients, Enterobacteriaceae significantly increased (P = 0.012), while non-fermenters significantly decreased (P = 0.007). GPB species from either hematological or surgical wards exhibited no notable changes during the pandemic. GNB resistance increased in hematological patients to carbapenems, amikacin, and tigecycline and decreased in surgical patients to amikacin and cefoxitin (P < 0.001, 0.010, < 0.001, < 0.001, and 0.016, respectively). The study highlights notable shifts in the microbial landscape during the COVID-19 pandemic, particularly in the prevalence and resistance patterns of GNB in hematological and surgical wards.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The corresponding author will provide any needed data from the collected and analyzed data upon reasonable request.
References
Abebe M, Tadesse S, Meseret G, Derbie A (2019) Type of bacterial isolates and antimicrobial resistance profile from different clinical samples at a referral hospital, northwest ethiopia: five years data analysis. BMC Res Notes 12:568. https://doi.org/10.1186/s13104-019-4604-6
Ahmed EF, Rasmi AH, Darwish AMA, Gad GFM (2023) Prevalence and resistance profile of bacteria isolated from wound infections among a group of patients in upper egypt: a descriptive cross-sectional study. BMC Res Notes 16:106. https://doi.org/10.1186/s13104-023-06379-y
Akpan MR, Isemin NU, Udoh AE, Ashiru-Oredope D (2020) Implementation of antimicrobial stewardship programmes in african countries: a systematic literature review. J Glob Antimicrob Resist 22:317–324. https://doi.org/10.1016/j.jgar.2020.03.009
Alhumaid S, Al Mutair A, Al Alawi Z, Alzahrani AJ, Tobaiqy M, Alresasi AM et al (2021) Antimicrobial susceptibility of gram-positive and gram-negative bacteria: a 5-year retrospective analysis at a multi-hospital healthcare system in saudi arabia. Ann Clin Microbiol Antimicrob 20:43. https://doi.org/10.1186/s12941-021-00450-x
Alshaikh FS, Godman B, Sindi ON, Seaton RA, Kurdi A (2022) Prevalence of bacterial coinfection and patterns of antibiotics prescribing in patients with COVID-19: a systematic review and meta-analysis. PLoS ONE 17:e0272375. https://doi.org/10.1371/journal.pone.0272375
Azzam A, Khaled H, Mosa M, Refaey N, AlSaifi M, Elsisi S, Elagezy FK, Mohsen M (2023) Epidemiology of clinically isolated methicillin-resistant staphylococcus aureus (MRSA) and its susceptibility to linezolid and vancomycin in egypt: a systematic review with meta-analysis. BMC Infect Dis 23:263. https://doi.org/10.1186/s12879-023-08202-2
Bengoechea JA, Bamford CG (2020) SARS-CoV-2, bacterial co-infections, and AMR: the deadly trio in COVID-19? EMBO Mol Med 12:e12560. https://doi.org/10.15252/emmm.202012560
Beović B, Doušak M, Ferreira-Coimbra J, Nadrah K, Rubulotta F, Belliato M et al (2020) Antibiotic use in patients with COVID-19: a “snapshot” infectious diseases international research initiative (ID-IRI) survey. J Antimicrob Chemother 75:3386–3390. https://doi.org/10.1093/jac/dkaa326
Bizri AR, El-Fattah AA, Bazaraa HM, Al Ramahi JW, Matar M, Ali RAN et al (2023) Antimicrobial resistance landscape and COVID-19 impact in egypt, iraq, jordan, and lebanon: a survey-based study and expert opinion. PLoS ONE 18:e0288550. https://doi.org/10.1371/journal.pone.0288550
Carroll M, Rangaiahagari A, Musabeyezu E, Singer D, Ogbuagu O (2016) Five-year antimicrobial susceptibility trends among bacterial isolates from a tertiary health-care facility in kigali, rwanda. Am J Trop Med Hyg 95:1277–1283. https://doi.org/10.4269/ajtmh.16-0392
Clinical and Laboratory Standards Institute (2017) Performance standards for antimicrobial susceptibility testing. CLSI supplement M100,27th ed. Clinical and Laboratory Standards Institute. https://clsi.org/standards/products/microbiology/documents/m100/
Cogliati Dezza F, Arcari G, Alessi F, Valeri S, Curtolo A, Sacco F et al (2022) Clinical impact of COVID-19 on multi-drug-resistant gram-negative bacilli bloodstream infections in an intensive care unit setting: two pandemics compared. Antibiot (Basel). https://doi.org/10.3390/antibiotics11070926
Di Carlo P, Serra N, Lo Sauro S, Carelli VM, Giarratana M, Signorello JC et al (2021) Epidemiology and pattern of resistance of gram-negative bacteria isolated from blood samples in hospitalized patients: a single center retrospective analysis from southern italy. Antibiot (Basel). https://doi.org/10.3390/antibiotics10111402
El-Kholy AA, Girgis SA, Shetta MAF, Abdel-Hamid DH, Elmanakhly AR (2020) Molecular characterization of multidrug-resistant gram-negative pathogens in three tertiary hospitals in cairo. Egypt Eur J Clin Microbiol Infect Dis 39:987–992. https://doi.org/10.1007/s10096-020-03812-z
El-Kholy A, El-Mahallawy HA, Elsharnouby N, Abdel Aziz M, Helmy AM, Kotb R (2021) Landscape of multidrug-resistant gram-negative infections in egypt: survey and literature review. Infect Drug Resist 14:1905–1920. https://doi.org/10.2147/IDR.S298920
El-Mahallawy HA, El Swify M, Abdul Hak A, Zafer MM (2022) Increasing trends of colistin resistance in patients at high-risk of carbapenem-resistant enterobacteriaceae. Ann Med 54:1–9. https://doi.org/10.1080/07853890.2022.2129775
Elrahem AA, El-Mashad N, Elshaer M, Ramadan H, Damiani G, Bahgat M, Mercuri SR, Elemshaty W (2023) Carbapenem resistance in gram-negative bacteria: a hospital-based study in egypt. Medicina (Kaunas). https://doi.org/10.3390/medicina59020285
Gao Y, Lin H, Xu Y, Yao Y, Shi D, Li J, Zhu H, Summah HD, Ni L, Feng Y (2022) Prognostic risk factors of carbapenem-resistant gram-negative bacteria bloodstream infection in immunosuppressed patients: a 7-year retrospective cohort study. Infect Drug Resist 15:6451–6462. https://doi.org/10.2147/IDR.S386342
Gustinetti G, Mikulska M (2016) Bloodstream infections in neutropenic cancer patients: a practical update. Virulence 7:280–297. https://doi.org/10.1080/21505594.2016.1156821
Helmy AK, Sidkey NM, El-Badawy RE, Hegazi AG (2023) Emergence of microbial infections in some hospitals of cairo, egypt: studying their corresponding antimicrobial resistance profiles. BMC Infect Dis 23:424. https://doi.org/10.1186/s12879-023-08397-4
Ince D, Fiawoo S, Choudhury R, Cosgrove SE, Dobrzynski D, Gold H et al (2023) Epidemiology of gram-negative bloodstream infections in the united states results from a cohort of 24 hospitals. Open Forum Infect Dis. https://doi.org/10.1093/ofid/ofad265
Kariyawasam RM, Julien DA, Jelinski DC, Larose SL, Rennert-May E, Conly JM et al (2022) Antimicrobial resistance (AMR) in COVID-19 patients: a systematic review and meta-analysis (November 2019–June 2021). Antimicrob Resist Infect Control 11:45. https://doi.org/10.1186/s13756-022-01085-z
Kotb S, Lyman M, Ismail G, Abd El Fattah M, Girgis SA, Etman A, Hafez S, El-Kholy J, Zaki MES, Rashed H-AG, Khalil GM, Sayyouh O, Talaat M (2020) Epidemiology of carbapenem-resistant enterobacteriaceae in egyptian intensive care units using national healthcare-associated infections surveillance data, 2011–2017. Antimicrob Resist Infect Control 9:2. https://doi.org/10.1186/s13756-019-0639-7
Lai C-C, Chen S-Y, Ko W-C, Hsueh P-R (2021) Increased antimicrobial resistance during the COVID-19 pandemic. Int J Antimicrob Agents 57:106324. https://doi.org/10.1016/j.ijantimicag.2021.106324
Lalaoui R, Javelle E, Bakour S, Ubeda C, Rolain J-M (2020) Infections due to carbapenem-resistant bacteria in patients with hematologic malignancies. Front Microbiol 11:1422. https://doi.org/10.3389/fmicb.2020.01422
Langford BJ, So M, Raybardhan S, Leung V, Soucy J-PR, Westwood D et al (2021) Antibiotic prescribing in patients with COVID-19: rapid review and meta-analysis. Clin Microbiol Infect 27:520–531. https://doi.org/10.1016/j.cmi.2020.12.018
Li Z, Zhuang H, Wang G, Wang H, Dong Y (2021) Prevalence, predictors, and mortality of bloodstream infections due to methicillin-resistant Staphylococcus aureus in patients with malignancy: systemic review and meta-analysis. BMC Infect Dis 21:74. https://doi.org/10.1186/s12879-021-05763-y
McCabe R, Schmit N, Christen P, D’Aeth JC, Løchen A, Rizmie D et al (2020) Adapting hospital capacity to meet changing demands during the COVID-19 pandemic. BMC Med 18:329. https://doi.org/10.1186/s12916-020-01781-w
Messias ACMC, Gama AR, de Almeida Prado LS, da Silva PAN, Galvão Filho AR, Coelho CJ et al (2023) Detection of oxacillin/cefoxitin resistance in Staphylococcus aureus present in recurrent tonsillitis. Microorg. https://doi.org/10.3390/microorganisms11030615
Montazeri EA, Khosravi AD, Khazaei S, Sabbagh A (2021) Prevalence of methicillin resistance and superantigenic toxins in Staphylococcus aureus strains isolated from patients with cancer. BMC Microbiol 21:262. https://doi.org/10.1186/s12866-021-02319-7
Nguyen NTH, Ou TY, Huy LD, Shih CL, Chang YM, Phan TP, Huang CC (2023) A global analysis of COVID-19 infection fatality rate and its associated factors during the delta and omicron variant periods: an ecological study. Front Public Health 11:1145138. https://doi.org/10.3389/fpubh.2023.1145138
Nori P, Szymczak W, Puius Y, Sharma A, Cowman K, Gialanella P et al (2020) Emerging co-pathogens: new delhi metallo-beta-lactamase producing enterobacterales infections in new york city COVID-19 patients. Int J Antimicrob Agents 56:106179. https://doi.org/10.1016/j.ijantimicag.2020.106179
Rawson TM, Ming D, Ahmad R, Moore LSP, Holmes AH (2020a) Antimicrobial use, drug-resistant infections and COVID-19. Nat Rev Microbiol 18:409–410. https://doi.org/10.1038/s41579-020-0395-y
Rawson TM, Moore LSP, Castro-Sanchez E, Charani E, Davies F, Satta G et al (2020b) COVID-19 and the potential long-term impact on antimicrobial resistance. J Antimicrob Chemother 75:1681–1684. https://doi.org/10.1093/jac/dkaa194
Rezasoltani S, Yadegar A, Hatami B, Asadzadeh Aghdaei H, Zali MR (2020) Antimicrobial resistance as a hidden menace lurking behind the COVID-19 outbreak: the global impacts of too much hygiene on AMR. Front Microbiol 11:590683. https://doi.org/10.3389/fmicb.2020.590683
Scaglione V, Reale M, Davoli C, Mazzitelli M, Serapide F, Lionello R et al (2022) Prevalence of antibiotic resistance over time in a third-level university hospital. Microb Drug Resist 28:425–435. https://doi.org/10.1089/mdr.2021.0109
Sharifipour E, Shams S, Esmkhani M, Khodadadi J, Fotouhi-Ardakani R, Koohpaei A et al (2020) Evaluation of bacterial co-infections of the respiratory tract in COVID-19 patients admitted to ICU. BMC Infect Dis 20:646. https://doi.org/10.1186/s12879-020-05374-z
Shih H-I, Wu C-J, Tu Y-F, Chi C-Y (2020) Fighting COVID-19: a quick review of diagnoses, therapies, and vaccines. Biomed J 43:341–354. https://doi.org/10.1016/j.bj.2020.05.021
Thoma R, Seneghini M, Seiffert SN, Vuichard Gysin D, Scanferla G, Haller S et al (2022) The challenge of preventing and containing outbreaks of multidrug-resistant organisms and candida auris during the coronavirus disease 2019 pandemic: report of a carbapenem-resistant acinetobacter baumannii outbreak and a systematic review of the literature. Antimicrob Resist Infect Control 11:12. https://doi.org/10.1186/s13756-022-01052-8
Tiri B, Sensi E, Marsiliani V, Cantarini M, Priante G, Vernelli C et al (2020) Antimicrobial stewardship program, COVID-19, and infection control: spread of carbapenem-resistant klebsiella pneumoniae colonization in ICU COVID-19 patients what did not work? J Clin Med. https://doi.org/10.3390/jcm9092744
World Health Organization (WHO) (2020) Strenghtening the Health System Response to COVID 19. Maintaining the Delivery of Essential Health Care Services While Mobilizing the Health Workforce for the COVID 19 Response. Copenhagen, Denmark: World Health Organization, Regional Office for Europe. https://www.who.int/europe/publications/i/item/WHO-EURO-2020-669-40404-54161
Funding
No funds, grants, or other support were obtained.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study’s conception and design. R. M. Abdel-Hamid and M. Elswify performed material preparation and data collection. R. M. Abdel-Hamid, H. A. El-Mahallawy, and R. M. Allam analyzed the data. The first draft of the manuscript was written by R. M. Abdel-Hamid and M. M. Zafer, edited and revised by H. A. El-Mahallawy. All authors commented on the manuscript’s previous versions and approved the final copy.
Corresponding author
Ethics declarations
Conflict of interest
There are no financial or non-financial conflicts of interest among the authors.
Ethics approval and consent to participate
The study adhered to the Helsinki Declaration’s guidelines. It was approved by the NCI ethics committee at Cairo University with permission number CP2023-503–059, and it was determined that no informed consent was required.
Consent to publish
Not applicable.
Additional information
Communicated by Yusuf Akhter.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Abdel-Hamid, R.M., El-Mahallawy, H.A., Allam, R.M. et al. Changing patterns of bacterial profile and antimicrobial resistance in high-risk patients during the COVID-19 pandemic at a tertiary oncology hospital. Arch Microbiol 206, 250 (2024). https://doi.org/10.1007/s00203-024-03965-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-024-03965-x