Carbapenem resistance and multidrug resistance in Morganellaceae: a 12-year retrospective cross-sectional study from southern Saudi Arabia

Abstract

Background: Morganellaceae (including Proteus, Providencia, and Morganella) are opportunistic pathogens increasingly associated with antimicrobial resistance (AMR). Long-term trend data, particularly from the Middle East, remain scarce. This study aimed to characterize the epidemiology, demographic and clinical characteristics, and antimicrobial resistance dynamics of Morganellaceae isolates in southern Saudi Arabia over a 12-year period, with a specific focus on carbapenem resistance (CRE), multidrug resistance (MDR), and difficult-to-treat resistance (DTR), as well as their genus-level variability and unique resistance phenotypes.

Methods: A 12-year retrospective cross-sectional study (2012-2024) was conducted at Aseer Central Hospital, southern Saudi Arabia. Non-duplicate clinical isolates from patients ≥ 12 years were identified using VITEK^® 2, with susceptibility interpreted according to CLSI guidelines. CRE, MDR, and DTR were defined by standardized criteria. Logistic regression was applied to model annual non-susceptibility trends, reported as odds ratios (ORs) and annual percent change (APC). Subgroup analyses explored genus-level differences, ICU versus non-ICU settings, and intra-genus variability.

Results: A total of 3,338 isolates were recovered, predominantly Proteus spp. (72.4%), followed by Providencia (18.6%) and Morganella (9.0%). Overall prevalence of CRE, MDR, and DTR was 25.7%, 44.8%, and 13.2%, respectively. Providencia showed the highest resistance burdens (CRE 33.6%, MDR 68.1%, DTR 23.2%), significantly exceeding Proteus (CRE 23.3%, MDR 39.1%, DTR 10.0%) and Morganella (CRE 29.3%, MDR 42.3%, DTR 9.2%) (all p < 0.001). Within CRE, 32.8% of isolates were non-susceptible to imipenem yet remained susceptible to meropenem and ertapenem. Compared with non-ICU isolates, ICU isolates exhibited higher MDR (49.6% vs. 41.5%, p < 0.001) but lower CRE (23.1% vs. 27.5%, p = 0.006), while DTR prevalence was comparable. Temporal analysis demonstrated significant declines in resistance to cephalosporins, fluoroquinolones, aminoglycosides, and Trimethoprim-Sulfamethoxazole, whereas imipenem resistance rose sharply (APC + 48.6%; OR 1.49, 95% CI 1.43-1.54, p < 0.001); meropenem and ertapenem remained stable.

Conclusions: Morganellaceae infections in southern Saudi Arabia carry substantial MDR and CRE burdens with pronounced genus-level variability,with Providencia posing the greatest therapeutic challenge. While several antibiotic classes showed declining resistance, the sharp rise in imipenem non-susceptibility is concerning. Strengthening species-level AST reporting and integrating Morganellaceae resistance data into healthcare-associated infection (HAI) surveillance frameworks are essential, particularly in ICU settings where outbreak risk is greatest.