Laboratory-based surveillance of antimicrobial non-susceptibility in Enterobacter species over 12 years at a tertiary-care hospital in Saudi Arabia
10 affiliations
- 1Department of Microbiology and Clinical Parasitology, College of Medicine, King Khalid University, Abha, Saudi Arabia
- 2Khamis Mushait General Hospital, Khamis Mushait, Saudi Arabia
- 3Department of Pathology, College of Medicine, King Saud University, Riyadh, Saudi Arabia
- 4Consultant Nephrology and Assistant Professor at King Khalid University, Abha, Saudi Arabia
- 5Department of Internal Medicine, Aseer Central Hospital, Abha, Saudi Arabia
- 6Department of Medicine, College of Medicine, King Khalid University, Abha, Saudi Arabia
- 7Department of Haematology and Immunohaematology, Faculty of Medical Laboratory Sciences, University of Khartoum, Khartoum, Sudan
- 8Department of Family Medicine, Aseer Central Hospital, Abha, Saudi Arabia
- 9Department of Internal Medicine, College of Medicine, King Khalid University, Abha, Saudi Arabia
- 10Department of Microbiology, Aseer Central Hospital, Abha, Saudi Arabia
Abstract
Background: Enterobacter species are increasingly associated with antimicrobial non-susceptibility, but long-term surveillance of temporal trends across antibiotic classes is limited in southern Saudi Arabia. Methods: We retrospectively studied non-duplicate Enterobacter isolates from adults at a tertiary-care hospital in southern Saudi Arabia (August 2012–August 2024), interpreted by contemporaneous CLSI criteria. Temporal trends were modelled by logistic regression as the annual percent change (APC) in the odds of non-susceptibility, adjusted for care setting, specimen source, age, and sex. Carbapenem-resistant Enterobacterales (CRE) and difficult-to-treat resistance (DTR; Kadri criteria) were analysed over time; sensitivity analyses excluded partial years and used breakpoint-comparable periods. Results: Of 1,319 Enterobacter isolates, 91.8% belonged to the Enterobacter cloacae complex. Adjusted trends declined for amikacin (APC −6.1%), gentamicin (−9.4%) and cefepime (−9.1%) and rose for carbapenems (+13.1% to +15.8%), levofloxacin (+6.3%) and piperacillin–tazobactam (+7.0%), with ciprofloxacin stable. The levofloxacin and piperacillin–tazobactam increases did not persist in breakpoint-comparable analyses and are not unequivocal biological increases. Inpatient isolates were more non-susceptible than outpatient isolates by approximately 16–39 percentage points (gentamicin 31.7% vs 14.8%; piperacillin–tazobactam 38.7% vs 23.1%; cefotaxime 63.9% vs 41.5%; cefepime 45.7% vs 28.8%; ceftazidime 61.4% vs 35.3%; ceftriaxone 57.4% vs 18.8%; all p ≤ 0.003). CRE rose early and remained common (APC + 22.8%; 28.7% overall), whereas DTR rose later and stayed infrequent (7.5% of eligible isolates; APC + 16.4%; highest annual value 20.2% in 2023); this difference in timing and overall frequency, not the partially sampled year 2024, indicates dissociation between carbapenem non-susceptibility and loss of all first-line agents. Conclusion: Non-susceptibility among Enterobacter species was heterogeneous and antibiotic-specific. The dissociation between CRE and DTR in timing and overall frequency supports using clinically meaningful phenotypes alongside antibiotic-specific trend analysis for stewardship and reporting; the levofloxacin and piperacillin–tazobactam increases warrant caution, as they did not persist in breakpoint-comparable analyses.
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BibTeX
@article{shabi2026laboratorybased,
title = {{Laboratory-based surveillance of antimicrobial non-susceptibility in Enterobacter species over 12 years at a tertiary-care hospital in Saudi Arabia}},
author = {Yahya Shabi and Fatimah Mohmmed Ali Asiri and Khalifa Binkhamis and Ali M. Somily and Mona M. Alshahrani and Tarik Alazraqi and Safia Abdullah Mohammed and Sara Habbash and Ali Al Bshabshe and Soliuman Mohamed and Abdullah Algarni and Ahmadiyah Siddiq and Abdulah O. S. Bawazeer and Abdulah J. Alqahtani and Abdullah A. Al-Shahrani},
journal = {PLOS One},
year = {2026},
month = oct,
doi = {10.1371/journal.pone.0358963},
url = {https://doi.org/10.1371/journal.pone.0358963},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Laboratory-based surveillance of antimicrobial non-susceptibility in Enterobacter species over 12 years at a tertiary-care hospital in Saudi Arabia
AU - Yahya Shabi
AU - Fatimah Mohmmed Ali Asiri
AU - Khalifa Binkhamis
AU - Ali M. Somily
AU - Mona M. Alshahrani
AU - Tarik Alazraqi
AU - Safia Abdullah Mohammed
AU - Sara Habbash
AU - Ali Al Bshabshe
AU - Soliuman Mohamed
AU - Abdullah Algarni
AU - Ahmadiyah Siddiq
AU - Abdulah O. S. Bawazeer
AU - Abdulah J. Alqahtani
AU - Abdullah A. Al-Shahrani
PY - 2026
DA - 2026/10/16
JO - PLOS One
DO - 10.1371/journal.pone.0358963
UR - https://doi.org/10.1371/journal.pone.0358963
AB - Background: Enterobacter species are increasingly associated with antimicrobial non-susceptibility, but long-term surveillance of temporal trends across antibiotic classes is limited in southern Saudi Arabia. Methods: We retrospectively studied non-duplicate Enterobacter isolates from adults at a tertiary-care hospital in southern Saudi Arabia (August 2012–August 2024), interpreted by contemporaneous CLSI criteria. Temporal trends were modelled by logistic regression as the annual percent change (APC) in the odds of non-susceptibility, adjusted for care setting, specimen source, age, and sex. Carbapenem-resistant Enterobacterales (CRE) and difficult-to-treat resistance (DTR; Kadri criteria) were analysed over time; sensitivity analyses excluded partial years and used breakpoint-comparable periods. Results: Of 1,319 Enterobacter isolates, 91.8% belonged to the Enterobacter cloacae complex. Adjusted trends declined for amikacin (APC −6.1%), gentamicin (−9.4%) and cefepime (−9.1%) and rose for carbapenems (+13.1% to +15.8%), levofloxacin (+6.3%) and piperacillin–tazobactam (+7.0%), with ciprofloxacin stable. The levofloxacin and piperacillin–tazobactam increases did not persist in breakpoint-comparable analyses and are not unequivocal biological increases. Inpatient isolates were more non-susceptible than outpatient isolates by approximately 16–39 percentage points (gentamicin 31.7% vs 14.8%; piperacillin–tazobactam 38.7% vs 23.1%; cefotaxime 63.9% vs 41.5%; cefepime 45.7% vs 28.8%; ceftazidime 61.4% vs 35.3%; ceftriaxone 57.4% vs 18.8%; all p ≤ 0.003). CRE rose early and remained common (APC + 22.8%; 28.7% overall), whereas DTR rose later and stayed infrequent (7.5% of eligible isolates; APC + 16.4%; highest annual value 20.2% in 2023); this difference in timing and overall frequency, not the partially sampled year 2024, indicates dissociation between carbapenem non-susceptibility and loss of all first-line agents. Conclusion: Non-susceptibility among Enterobacter species was heterogeneous and antibiotic-specific. The dissociation between CRE and DTR in timing and overall frequency supports using clinically meaningful phenotypes alongside antibiotic-specific trend analysis for stewardship and reporting; the levofloxacin and piperacillin–tazobactam increases warrant caution, as they did not persist in breakpoint-comparable analyses.
SN - 1932-6203
ER -