Antimicrobial Resistance Profile and Longitudinal Trends of Morganella morganii Clinical Isolates in a University Hospital

Abstract

Objectives

Morganella morganii is an opportunistic Gram-negative pathogen increasingly associated with healthcare-associated infections and antimicrobial resistance. However, long-term epidemiological data from Türkiye remain scarce.

Methods

This retrospective study analyzed M. morganii isolates obtained between January 2015 and December 2024 at a 1500-bed tertiary care hospital. Demographic data, clinical specimen sources, and antimicrobial susceptibility results were retrieved from the laboratory database. Identification was performed using conventional methods and MALDI-TOF MS, while antimicrobial susceptibility was determined according to EUCAST guidelines. Linear regression analysis was applied to evaluate resistance trends over time.

Results

A total of 673 non-duplicate isolates were included, predominantly from urine (68.6%), followed by wound (19.2%), blood (4.7%), respiratory (3.6%), abscess (1.9%), and sterile body fluid (1.0%) specimens. The annual incidence ranged from 0.47% in 2015 to 1.9% in 2024, with a transient decline during 2020–2022, likely related to the COVID-19 pandemic. Male patients accounted for 63% of isolates, with a median age of 52 years. Meropenem and amikacin showed the highest overall activity (>98% susceptibility), while cefoxitin demonstrated the lowest efficacy (≈50%). Trend analysis revealed statistically significant increases in resistance to amikacin, imipenem, meropenem, ertapenem, ceftriaxone, ceftazidime, cefoxitin, cefepime, piperacillin–tazobactam, trimethoprim–sulfamethoxazole, and ciprofloxacin (all p<0.05), whereas gentamicin showed no significant change. Notably, carbapenem and aminoglycoside resistance increased markedly after 2022.

Conclusion

This study highlights the rising clinical importance of M. morganii, with increasing resistance across multiple antibiotic classes, including carbapenems. The findings underscore the need for continuous surveillance, prudent antimicrobial use, and further genomic studies to elucidate resistance mechanisms and guide effective therapy.

Morganella morganii is a Gram-negative, facultative anaerobic, motile bacillus belonging to the family Morganellaceae within the order Enterobacterales.^[1] M. morganii, a non-lactose-fermenting species, possesses virulence factors such as urease, hemolysin, lipopolysaccharide, and IgA protease.^[2] Although this bacterium exists as a commensal organism in the human intestinal flora, it can also be detected in environmental settings and isolated as an opportunistic pathogen in individuals with risk factors such as advanced age, diabetes, or immunodeficiency. While the frequency of M. morganii in community-acquired infections is quite low, it is more frequently isolated in postoperative infections in surgical wards of hospitals, particularly as a causative agent of urinary tract infections. In recent years, the reported increase in community-acquired cases has necessitated a re-evaluation of the clinical importance of this species.^[1,3,4]

Current epidemiological and genomic studies report a rising trend in the clinical significance of M. morganii. Laupland et al.^[5] reported an increasing incidence trend of bloodstream infections caused by M. morganii in Queensland between 2000 and 2019. This upward trend paralleled the findings of a multicenter study covering the years 2015–2022, which demonstrated a high comorbidity burden, age-related increases in mortality rates, and rising multidrug resistance.^[2] In addition, a study on the genomic epidemiology of clinical M. morganii isolates collected between 2016 and 2023 highlighted the marked predominance of urinary and respiratory tract isolates, revealed the circulation of numerous resistance genes, and showed the presence of nosocomial transmission clusters.^[6] Furthermore, the detection of carbapenemase-producing M. morganii strains in different geographical regions has indicated that the selective pressure of antibiotics has accelerated the emergence of this bacterium, thereby increasing the clinical visibility of the pathogen.^[7,8]

Epidemiological analyses of Gram-negative opportunistic pathogens such as M. morganii are of critical importance for both the early detection of resistance mechanisms and the prevention of hospital infections. These analyses make it possible to monitor the emergence of multidrug-resistant strains, identify transmission chains, and develop appropriate antibiotic stewardship policies.^[9] However, in our country, sufficient data demonstrating the frequency and antimicrobial resistance status of M. morganii, an increasingly clinically important pathogen, have not yet been published.

In this study, data on M. morganii isolates obtained over the last 10 years in a tertiary university hospital were examined to analyze the incidence of the pathogen and the frequency of resistance to selected antibiotics.

Methods

Study Design and Scope

This study was conducted in the Medical Microbiology Laboratory of Inonu University Turgut Ozal Medical Center, a tertiary care hospital with 1,500 beds, and included M. morganii strains isolated from various clinical samples between 2015 and 2024. The data included in the study were retrospectively obtained from the electronic databases of the hospital and laboratory automation system. Only one M. morganii isolate from each patient was included in the evaluation, and repeated isolates from the same patient were excluded. Within the scope of the research, demographic characteristics such as patient age and gender, the types of clinical specimens from which the isolates were obtained, and antimicrobial susceptibility test results were collected.

Isolates obtained from outpatients or within <48 hours after hospital admission were classified as community-acquired, while those isolated ≥48 hours after admission were classified as hospital-acquired.

The study included isolates obtained over a 10-year period between January 1, 2015, and December 31, 2024. These strains were included in the study based on the date of isolation, regardless of the request date.

This study was carried out with the approval of the Inonu University Health Sciences Scientific Research Ethics Committee (No. 8342). This study was conducted in accordance with the principles of the Declaration of Helsinki.

Bacterial Identification and Antimicrobial Susceptibility Testing

Morganella morganii strains isolated from various clinical samples were identified using classical bacteriological methods and the VITEK MS (bioMérieux, France) MALDI-TOF MS system.

The antimicrobial susceptibilities of the isolates were determined using the Kirby-Bauer disk diffusion method and, when necessary, the automated VITEK 2 (bioMérieux, France) system. Susceptibility testing and interpretation of the results were performed according to the European Committee on Antimicrobial Susceptibility Testing (EUCAST) breakpoints and criteria valid at the time of testing.^[10]

Data Analysis

Morganella morganii isolates obtained according to the study years and strains exhibiting antimicrobial resistance were expressed as numbers (n) and percentages (%). To determine the isolation frequency of Morganella morganii, the total number of isolates detected in the laboratory in the relevant year was calculated and proportioned. In this study, the term “incidence” refers to a laboratory-based proportion of M. morganii isolates among all clinical cultures processed in the corresponding year. Resistance trends in major antibiotic groups over the years were evaluated using linear regression analysis. P<0.05 was considered statistically significant. Because the analyses were exploratory and intended to describe temporal trends, no correction for multiple comparisons was applied.

Results

A total of 673 M. morganii isolates were examined in the study. Of the patients from whom the strains were isolated, 424 (63%) were male and 249 (37%) were female. The median age of the patients was 52 years, with a minimum–maximum range of 0–97.

While a total of 16 M. morganii isolates were obtained in 2015, the first year of the study, this number increased to 83 in 2018 and 105 in 2019. Between 2020 and 2023, the annual number of isolates varied between 64 and 70, whereas it increased to 114 in 2024. Considering the total number of isolations performed in the laboratory during the relevant periods, the incidence of M. morganii was found to be 0.47% in 2015, 1.88% and 2.28% in 2018 and 2019, respectively, and 1.9% in 2024. During the study years, the rates of hospital-acquired strains fluctuated between 91.9% and 81.5% in a nonlinear pattern. Linear regression analysis revealed that the increase in the incidence of M. morganii observed during the study years was not statistically significant (estimate=0.063, SE=0.059, p=0.314, 95% CI: −0.073 to 0.199). The incidence of M. morganii strains in our hospital during the study years is shown in Figure 1.

Figure 1.

Incidence of Morganella morganii by year.

In our study, M. morganii isolates were most frequently obtained from urine (68.6%; n=462), followed by wound samples (19.2%; n=129), blood (4.7%; n=32), sputum and lower respiratory tract samples (3.6%; n=24), abscesses (1.9%; n=13), and sterile body fluids (1%; n=7).

Among all isolates, the most effective antibiotics were meropenem (>98% susceptible) and amikacin (>98% susceptible), whereas the least effective antibiotic was cefoxitin (50% susceptible). The analysis revealed an increasing trend in resistance rates for all antibiotics over the years. This increase became particularly evident for imipenem, meropenem, amikacin, and ciprofloxacin starting in 2022. A statistically significant increase in resistance was demonstrated for amikacin, imipenem, meropenem, ertapenem, ceftriaxone, ceftazidime, cefoxitin, cefepime, piperacillin–tazobactam, trimethoprim–sulfamethoxazole, and ciprofloxacin (all p<0.05). Only gentamicin did not show a statistically significant increase in resistance (p=0.174). The annual resistance rates of the isolates to various antibiotics are shown in Table 1.

Table 1.

Percentage of antibiotic resistance in the past decade.

Slope (Estimate ± SE [95% CI])	p	2024	2023	2022	2021	2020	2019	2018	2017	2016	2015	Years
0.653±0.177([0.246–1.061)	0.006	%5.7	%6.3	%2.7	%0	%0	%1.0	%0	%0	%0	%0	AK
0.950±0.636([-0.517–2.417)	0.174	%19.3	%36.0	%14.1	%24.2	%18.8	%18.3	%18.2	%18.2	%16.8	%16.6	GN
0.126±0.440(-0.890–1.141)	0.024	%1.9	%1.5	%0	%0	%0	%0	%0	%0	%0	%0	MEM
1.313±0.438 (0.303–2.324)	0.017	%12.6	%14	%2.8	%0	%0	%0	%0	%1.8	%0	%0	IMP
1.279±0.497(0.133 – 2.424)	0.033	%12.3	%19.0	%4.0	%3.3	%3.2	%1.1	%2.6	%5.9	%2.6	%1.1	ETP
2.093±0.825 (0.192–3.995)	0.035	%25.5	%30.8	%30.9	%25	%18.7	%23.5	%12	%19.0	%27.6	%13.0	CRO
1.291±0.529(0.071–2.510)	0.041	%38.5	%46.2	%37.6	%31.7	%37.7	%42.1	%35.1	%28.1	%35.5	%26.7	CAZ
3.961±1.340 (0.871–7.051)	0.018	%40.6	%50	%67.6	%57.6	%57.1	%41.7	%42.3	%21.4	%32.1	%14.3	FOX
0.857±0.256 (0.268–1.447)	0.010	%13.7	%9.1	%7.8	%13.2	%5.6	%7.3	%7.1	%3.9	%4.1	%5.88	FEP
1.772±0.414(0.816–2.728)	0.003	%16.1	%15.1	%10.9	%3.0	%1.4	%0.9	%7.4	%0	%0	%0	TZP
1.724±0.744(0.007–3.440)	0.049	%37.9	%36.4	%29.2	%38.2	%43.5	%33.1	%23.2	%37.3	%24.0	%17.6	SXT
3.251±0.826 (1.345–5.157)	0.004	%41.1	%36.9	%28.8	%28.3	%28.6	%30.8	%14.8	%6.7	%4.8	%23.1	CIP

Abbreviations: AK: Amikacin; GN: Gentamicin; MEM: Meropenem; IMP: Imipenem; FOX: Cefoxitin; ETP: Ertapenem; CRO: Ceftriaxone; CIP: Ciprofloxacin; CAZ: Ceftazidime; FEP: Cefepime; TZP: Piperacillin–Tazobactam; SXT: Trimethoprim–Sulfamethoxazole

Resistance profiles were also compared between community-acquired and hospital-acquired M. morganii isolates. Overall, resistance rates were broadly similar between the two groups for most antimicrobials. However, hospital-acquired isolates exhibited significantly higher resistance to amoxicillin/clavulanate (90.7% vs. 98.2%, p=0.018), ciprofloxacin (19.0% vs. 30.4%, p=0.018), and cefoxitin (38.0% vs. 49.2%, p=0.049). No statistically significant differences were observed for carbapenems, third- and fourth-generation cephalosporins, trimethoprim–sulfamethoxazole, piperacillin–tazobactam, aminoglycosides, or ampicillin (p>0.05).

Discussion

In this study, it was determined that M. morganii strains isolated in a regional tertiary hospital showed a remarkable increase in incidence over the past 10 years. While the incidence of the pathogen among all isolations was 0.47% in 2015, the first year of the study, this value showed a nearly linear increasing trend both numerically and proportionally until 2019, reaching 2.28%. However, this upward trend showed a marked decrease during the three years between 2020 and 2022, dropping first to 1.57% and then to 1.03% in 2022. This temporary decline coincided with the COVID-19 pandemic, during which the total number of cultures processed in our laboratory actually remained higher than in the pre-pandemic period. Considering that during this period, our hospital mainly admitted and treated patients with poor general condition who were highly immunosuppressed and required the use of antimicrobial agents, the numerical and proportional decline in M. morganii isolation can be explained by the increase in other opportunistic pathogens. Public health measures such as masking, social distancing, and lockdowns markedly reduced the incidence of several community-acquired infections.^[11-14] In addition, reduced healthcare access among elderly individuals and patients with chronic diseases may also have contributed to the decline in M. morganii isolation during this period.^[15] In 2023, when the effect of the pandemic had completely waned, the detected incidence of isolation showed a trend very similar to that of the previous three years. In the analysis, the most likely reason for this was considered to be the two major earthquakes in February 2023, with epicenters located 160 and 90 km from our city, respectively. During this period, there were changes in the routine operations of our hospital, the patient population differed, and a significant portion of the population temporarily moved to other regions. Ultimately, in 2024, the incidence of M. morganii isolation increased by approximately 50% compared with the average of the previous four years, reaching 1.9% (Fig. 1). Therefore, our study provided important data demonstrating how much the linear increasing trend observed in the incidence of M. morganii isolation since 2015 was suppressed during the pandemic period and how it returned to a similar upward trend from 2023 onward.

Although scarce, some published studies have investigated the reasons for the increase in M. morganii. Chen et al.^[16] reported that the bacterium undergoes a rapid adaptation–selection process as a result of the dissemination of mobile genetic elements among M. morganii species. In a study conducted between 2000 and 2019, it was reported that the pathogen showed a fluctuating but statistically significant upward trend in bloodstream infections, that the antimicrobial resistance developed by the bacterium did not have a noteworthy effect on this change, but that the increase in the number of patients in the community with comorbidities, such as advanced age in men, diabetes, kidney disease, and heart failure, was associated with the increased incidence of the pathogen.^[5] In a study conducted in Sweden, 201 patients with M. morganii growth in blood cultures between 2013 and 2023 were evaluated, and it was reported that the pathogen was significantly more common in elderly individuals with comorbidities and healthcare histories.^[17] Despite all these data, the factors influencing the increase in M. morganii are still not sufficiently clarified. Therefore, comprehensive analyses of the characteristics of patients in whom this pathogen is detected are needed to identify the associated risk factors. Proper elucidation of such risk factors will provide important data for controlling the increase in this pathogen.

In addition to temporal trends, resistance profiles were compared between community-acquired and hospital-acquired M. morganii isolates. Overall, resistance rates were broadly similar between the two groups for most antimicrobial agents. However, significantly higher resistance to amoxicillin/clavulanate, ciprofloxacin, and cefoxitin was observed among hospital-acquired isolates. These findings suggest that although healthcare exposure may contribute to higher resistance to certain agents, the resistance burden observed in our cohort is not restricted to hospital settings and may also reflect community-level selection pressure.

The detection of antimicrobial resistance in M. morganii strains and the analysis of changes in antibiotic resistance over the study years constituted the second important aspect of our study. Unlike many other Gram-negative bacteria, M. morganii is intrinsically resistant to a last-resort antibiotic such as colistin. Therefore, carbapenems have greater importance as last-resort antimicrobials against this pathogen. Throughout our study, while only a few strains were resistant to ertapenem until 2021, imipenem-resistant strains began to be detected in 2022, and from 2023 onward, meropenem-resistant M. morganii isolates were identified. Our findings demonstrated that meropenem was the most effective carbapenem against the pathogen. Studies have reported that penicillin-binding protein mutations significantly reduce the affinity of imipenem and that defects in outer membrane transport proteins and/or activation of efflux mechanisms, in combination, markedly decrease the effectiveness of this drug compared with meropenem.^[18] To date, carbapenem resistance genes such as NDM-1, KPC-2, and OXA-48-like have been detected in M. morganii strains, and the cefepime–zidebactam combination has been reported as a highly effective option in highly resistant strains.^[7] On the other hand, as in Enterobacter spp. and Citrobacter spp., M. morganii strains are also known to produce broad-spectrum beta-lactam resistance, including resistance to carbapenems, through overproduction of inducible chromosomal beta-lactamases, decreased permeability, or excessive activation of efflux pumps. Considering the lack of published studies from our country on this subject, there is a need to investigate the genomic and transcriptomic factors underlying resistance in carbapenem-resistant M. morganii isolates detected in Türkiye.

In our study, amikacin was found to be one of the most effective antibiotics against M. morganii strains. However, the potential side effects of this drug on the kidneys and inner ear, its lack of use as monotherapy, and its low distribution to certain body sites reduce the importance of this high susceptibility; nonetheless, it highlights its potential as a strong secondary drug in certain indications and combination therapies. In our study, the effectiveness of third-generation cephalosporins such as ceftazidime and ceftriaxone ranged between 12% and 42%, while the effectiveness of cefoxitin, a second-generation cephamycin, ranged between 14% and 67%. On the other hand, ciprofloxacin, a quinolone, showed an effectiveness of approximately 5% to 41% during the study years. Linear regression analysis revealed a statistically significant increase in resistance to all antibiotics studied, except ceftazidime. Compared with data from developed countries, the resistance frequency detected in our study against cephalosporins and ciprofloxacin in M. morganii strains was quite high. Considering the long-standing high frequency of resistance in Gram-negative bacteria isolated in Türkiye, this emphasized once again the importance of proper antibiotic use in suppressing both individual resistance patterns and the increasing frequency of M. morganii, a pathogen selected as a result of the excessive use of antimicrobials.^[19]

This study had certain limitations. First, the incidence presented here reflects laboratory isolation proportions rather than patient-based or population-based incidence measures. Therefore, caution is warranted when comparing our findings with epidemiological surveillance data. Another limitation of our study is the lack of molecular characterization of carbapenem-resistant isolates, which prevented confirmation of the underlying resistance mechanisms.

Conclusion

In this study, it was found that the incidence of M. morganii in our hospital increased significantly over the past 10 years. Although this increasing trend declined during the COVID-19 pandemic, it rose again in the post-pandemic period. To the best of our knowledge, the absence of any other research from Türkiye on the incidence of M. morganii increases the importance of documenting how valid the increasing frequency of this pathogen, detected in our hospital and in many regions abroad, is in other regions of our country. Together with the significant increase in antibiotic resistance over time and the increasing carbapenem resistance observed particularly in recent years in M. morganii strains intrinsically resistant to colistin, our study has strengthened concerns that this pathogen may cause significant treatment challenges in infections. The increasing prevalence of elderly and chronically ill individuals in communities, who constitute the target population for this pathogen, emphasizes that M. morganii may be encountered more frequently in the future. Therefore, new and continuous studies on M. morganii are needed.

Disclosures

Ethics Committee Approval

This study was approved by Inonu University Health Sciences Scientific Research Ethics Committee (Date: September 16, 2025; Protocol Number: 8342).

Conflict of Interest

The authors declare that there is no conflict of interest.

Use of AI for Writing Assistance

The authors declare that no artificial intelligence tools were used in the production of this manuscript.

Financial Disclosure

The authors declared that this study received no financial support.

Authorship Contributions

Concept – Y.Y., B.O.; Design – E.S.T., Y.Y., B.O.; Supervision – Y.Y., B.O.; Materials – E.S.T., Y.Y., I.Y., B.O.; Data Collection and/or Processing – E.S.T., Y.Y., I.Y., B.O.; Analysis and/or Interpretation – E.S.T., Y.Y., I.Y., B.O.; Literature Search – E.S.T., Y.Y., B.O.; Writing – E.S.T., Y.Y., B.O.; Critical Reviews – E.S.T., Y.Y., I.Y., B.O..

Peer-review

Externally peer-reviewed.