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Effectiveness of traditional non-carbapenem β-lactams vs. novel β-lactams for the treatment of carbapenem-resistant Pseudomonas aeruginosa: a retrospective cohort study

BMC Infectious Diseases volume 24, Article number: 1455 (2024) Cite this article

Abstract

Background

The World Health Organization (WHO) has identified carbapenem-resistant Pseudomonas aeruginosa (CRPA) as one of the three critical priority pathogens. There is scarce literature evaluating the treatment outcomes in patients with CRPA infections treated with traditional non-carbapenem β-lactam (NCBL) agents. Thus, this study aims to assess the effectiveness of traditional NCBL compared to novel β-lactam agents (NVL) for treating non-carbapenem β-lactam -susceptible CRPA.

Methods

A single-center retrospective cohort study was conducted between January 2016 and December 2022. The study included adult patients 18 years and older with infection due to CRPA who were treated based on microbiology sensitivity with traditional NCBL or NVL for more than 48 h. The primary outcome was 30-day mortality.

Results

124 patients were included: 98 (79%) in the NCBL group and 26 (20.9%) in the NVL group. 78 (62.9%) patients were male. The median (interquartile range (IQR)) age of included patients was 64 (45, 77) years. A total of 84 (67.7%) patients were critically ill, with an overall median (IQR) APACHE II score of 18 (13.5, 23). The rates of 30-day mortality in NCBL and NVL groups were 41 (41.8%) and 12 (46.2%), respectively; P = 0.692.

Conclusion

In patients with CRPA infections susceptible to traditional NCBL, there was no statisticallly significant difference in 30-day mortality among patients who were treated with traditional NCBL compared with NVL. Further studies with larger sample sizes are needed to confirm these findings.

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Background

Carbapenem-resistant Pseudomonas aeruginosa (CRPA) is ranked second highest among the four common Gram-negative species isolated in the United States [1, 2]. In 2019, the Centers for Disease Control and Prevention (CDC) reported that multidrug-resistant P. aeruginosa is a severe threat to the healthcare system [3]. The World Health Organization (WHO) has identified CRPA as one of the three critical priority pathogens [4]. Patients with CRPA infections have a longer hospital stay and increased mortality compared to susceptible P. aeruginosa isolates [5,6,7,8].

Carbapenem resistant (Carb-R)/cephalosporin sensitive (Ceph-S) P. aeruginosa mechanism of resistance was mainly attributed to overexpression of efflux systems and decreased expression of OprD [9]. The epidemiology of carbapenemase-producing CRPA varies by region, with 69% reported in South and Central America and 30% in the Middle East. These infections are associated with higher adjusted mortality rates compared to non-carbapenemase-producing CRPA infections [10]. Thus, many practitioners use novel β-lactams to overcome the carbapenemase-producing CRPA type of resistance.

Although novel β-lactams (NVL) showed better outcomes compared to more traditional regimens such as colistin or aminoglycoside-containing regimens to treat CRPA [11, 12], many studies found that overutilization of NVL leads to emergence of resistance to these agents [13,14,15]. Therefore, 2024 IDSA guidelines recommended susceptible traditional beta-lactams for CRPA, although comparative effectiveness studies to guide treatment decisions for infections caused by P. aeruginosa resistant to carbapenems but susceptible to traditional non-carbapenem β-lactams are unavailable [16]. This study aims to assess the effectiveness of traditional non-carbapenem β-lactam (NCBL) compared to Novel β-lactam (NVL) agents for treating β-lactam -susceptible CRPA.

Methods

Study design and setting

A retrospective cohort study was conducted at King Faisal Specialist Hospital and Research Center-Jeddah (KFSHRC-J), a tertiary care and teaching hospital with 388 beds. The study was approved by the institutional review board of KFSHRC-J (IRB 2023-81). The study included adult patients 18 years and older with infection due to CRPA between January 1st, 2016 and December 31st, 2022 and treated based on the susceptibility data with NCBL including ceftazidime, cefepime, or piperacillin/tazobactam or NVL including ceftolozane-tazobactam (C-T) or ceftazidime-avibactam (CAZ/AVI) for more than 48 h. Patients were followed until discharge or death. Patients were excluded if the isolates’ sensitivity was intermediate or resistant to all antipseudomonal non-carbapenem β-lactam agents; if the isolate was colonization; if the patient isolated CRPA was not treated with NCBL or NVL; if the patient received the study drug for < 48 h or died before receiving the study drug (Fig. 1).

Fig. 1
figure 1

Patients screening

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Study outcomes

The primary outcome was 30-day mortality. Secondary outcomes included 30-day infection-related mortality, clinical cure rate, microbiologic eradication, 90–day recurrence, 30-day readmission due to infection, intensive care unit (ICU), and hospital length of stay(LOS) calculated from the admission date.

Data collection

The data was collected using the electronic medical records system and entered in REDCap (10.8.0 - © 2021 Vanderbilt University). All patients’ records were assigned unique codes. All patients with documented CRPA sensitivity to one of the non-carbapenem β-lactams were allocated into two groups (NCBL vs. NVL) based on their definitive treatment. Variables extracted from the medical record include demographics, comorbidities, indwelling devices, the severity of illness, infection, and infusion type; microbiological data; and clinical outcomes data. Data on empiric, definitive, and concurrent antibiotics were collected (Table e1 supplementary appendix). The antibiotic dosing appropriateness was evaluated based on the patient’s renal function status (Table e2, Table e3 supplementary appendix).

Microbiology

Antibiotic susceptibility testing was conducted using the automated systems Vitek 2 system (bioMérieux, Marcy-l’Étoile, France). Microbial susceptibility breakpoints were determined based on the Clinical and Laboratory Standards Institute (CLSI) guidelines. C-T and CAZ/ AVI Minimum Inhibitory Concentration (MIC) of ≤ 4/4 was considered susceptible. While Cefepime and ceftazidime MIC of ≤ 8 and piperacillin-tazobactam MIC of ≤ 16 were considered susceptible [17].

Definitions

30- day mortality was assessed from the time of antibiotics initiation. Clinical cure was defined as the resolution of signs and symptoms of infection with the study drug without treatment needing modification due to toxicity or failure [18]. Clinical cure was assessed from antibiotic initiation to resolution of signs and symptoms of infection while in the same definitive antibiotic therapy. Laboratory and radiologic findings were included in the evaluation of the clinical cure, including resolution of fever, decrease or lack of progression of radiographic abnormalities, improvement or normalization of arterial blood gas, and improvement or return to baseline of the white blood cells, procalcitonin, and C-reactive protein (CRP), when applicable. Infection-related mortality was considered if patients had direct complications of infection or persistent signs of infection, including fever, persistent positive blood cultures, leukocytosis, and elevated CRP at the time of death [19]. Definitive treatment is defined as the treatment given to the patient based on the microbiological sensitivity results. Microbiologic eradication was defined as no further growth of the baseline pathogen in patients with repeated cultures. In contrast, microbiologic failure was defined as a positive repeat culture of the same causative pathogen at the same infection site. 90-day recurrence of infection was defined as positive cultures of the same species regardless the site of infection, as the index culture isolates after evidence of at least one negative growth of microorganisms during 90 days of the primary infection episode. Colonization was defined as the microbiological isolation of the pathogen without causing any clinical sings of infection, and the patient did not receive treatment that target the isolated pathogen. Sepsis and septic shock were defined based on sepsis- 3 definition [20].

Statistical analysis

The study included all patients meeting the inclusion criteria from January 1st, 2016 and December 31st, 2022 resulting in a total sample size of 124 patients. Categorical data were reported as frequencies (n) and percentages (%). Continuous data were reported as median and interquartile ranges (IQR). The Mann-Whitney U test and the Chi-square tests were used in univariate analysis. Data with a P-value of less than 0.05 was considered significant. Data that was significant in the univariate analysis was included in the multivariable analysis. Multivariable analysis was done using a logistic regression model. Multicollinearity among independent variables was not explicitly assessed; however, variables were chosen based on statistical significance. A sub-group analysis for patients admitted to ICU was added to evaluate differences in outcome compared to the overall data. A p-value less than 0.05 was considered significant. Data analysis was done using STATA software version 18.

Results

Among 289 cases screened, 124 patients met the inclusion criteria: 79% in the NCBL group and 20.9% in the NVL group (Fig. 1). Around 63% of included patients were male, and the median age was 64 years. Around 43% of patients were admitted to the hospital due to infection; the infection type was mainly hospital/ ventilator acquired pneumonia (61.3%). The median for charlson’s comorbidity index (CCI) score was 5 and was similar between groups. Around 68% of patients were admitted to the ICU with an overall mean APACHE II score of 18, which was significantly higher in the NCBL group 18 vs. 14 in NVL; P = 0.017. Cefepime was the main definitive antibiotic used in the NCBL group (54.1%), while CAZ/AVI was mainly used in the NVL group (76.9%). The median duration of definitive therapy was comparable between groups ( 8 vs.9.5 days; P = 0.06) (Table 1).

Table 1 Baseline characteristics for patients with carbapenem resistant pseudomonas aeruginosa
Full size table

For outcome analysis, no statistically significant difference was found in 30-day mortality (41.8% vs. 46.2%; P = 0.692), 30-day infection-related mortality (29.6% vs. 38.5%; P = 0.387), or clinical cure rate (47.7% vs. 59.3%; P = 0.283) in the NCBL vs. NVL group, respectively. However, microbiological eradication (33.7% vs. 57.7%; P = 0.025) was higher and 90-day infection recurrence (61.2% vs.38.5%; P = 0.037) was lower in NVL compared to NCBL group. 30- day hospital readmission rate and length of stay was comparable between both groups (Table 2).

Table 2 Outcomes for patients with carbapenem resistant pseudomonas aeruginosa
Full size table

In the univariate analysis, among patients who died vs. those who survived, ICU admission (59.2% vs. 79.3%; P = 0.018), vasopressor use (21.1% vs. 54.7%; P = < 0.001), and APACHE II score (17 vs. 20; P = 0.02) were the identified contributing factors for the 30-day mortality (Table 3). However, in the multivariable logistic model, only vasopressor use contributed to 30-day mortality, with an odd ratio (95% confidence interval) of 3.6 [1.4, 9.1]; P = 0.007 (Table 4).

Table 3 Univariable analysis of 30-day all-cause mortality
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Table 4 Multivariable logistic model for factors affecting 30- days all-cause mortality
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In the univariate analysis of factors associated with infection recurrence, the use of NCBL antibiotics (85.7% vs. 70.4%; P = 0.037), pneumonia (70% vs. 50%; P = 0.023), and infusion type were the independent risk factors of this outcome (Table 5). In the multivariable analysis of factors affecting infection recurrence, only pneumonia was associated with infection recurrence (Table 5). Among patients with infection recurrence, only one third of the isolated cultures were CRPA sensitive to non-carbapenem β-lactam (35% vs. 30%; P = 0.095) (Table 6). While in the subgroup analysis of the outcome of ICU patients, no statistically significant differences were observed in all outcomes (Table e4 supplementary appendix).

Table 5 Analysis of infection recurrence
Full size table
Table 6 Microbiology data for infection recurrence (n = 70)
Full size table

Discussion

This retrospective cohort study showed that treating CRPA infections with traditional NCBL has a comparable outcome to NVL antibiotics.

In our research, around 42% of CRPA patients died within 30 days, with no statistically significant difference in 30-day mortality among patients treated with traditional NCBL versus NVL. The overall mortality rate in our study was higher than the reported CRPA mortality in the literature, around 15–18% [5, 7, 8].

Indeed, around half of our study patients were immunocompromised with approximately 68% of them critically ill with high mortality prediction score; which might explain the increased mortality in our cohort; however, many factors reported in the literature are associated with CRPA mortality. A multicenter cohort study that aimed to identify the risk factors related to CRPA bacteremia mortality found that multiple organ failure and higher Pitt bacteremia scores were mainly attributed to the increased mortality [21]. Another study aimed to identify predictors of outcome in patients with a hematologic malignancy found that the main risk factors contributing to the 28-day mortality were older age, the active stage of hematological diseases, high procalcitonin, septic shock, and neutropenia [8].

Although our study did not detect differences in mortality among the study groups, microbiological eradication was statistically significantly higher in the NVL group compared to the traditional NCBL group among patients with repeated cultures. Our findings are consistent with those of other published studies, which report similar or even higher rates of microbial eradication when novel beta-lactams (NVL) are used [22, 23]. On the other hand, our study found that 90-day infection recurrence was higher in the NCBL group, with type of infusion as a factor related to the recurrence. Several studies support the use of extended-infusion β-lactam to improve patient outcomes in patients with antibiotic-resistant infections [24, 25]. since most patients treated in the NCBL arm used intermittent infusion, that might explain the higher recurrence rate in this group. Moreover, some researchers hypothesize that the duration of therapy might be associated with the infection recurrence rate in patients with pseudomonal infections. However, our study did not detect the duration of treatment as a factor of infection recurrence. Similarly, a systematic review and meta-analysis that evaluated the outcome of patients with pseudomonal bacteremia using short vs. long-duration therapy found no difference between groups in the rate of infection recurrence [26]. Indeed, the increase in microbiological eradication in the NVL group and the increased recurrence of infection in the NCBL group might affect the prescriber’s decision regarding agent selection in treating resistant organisms.

In our study, the overall cure rate for CRPA among patients was 50% and around 59% in patients treated with NVL antibiotics. Our findings were similar to the reported cure rate in literature for MDR/XDR P. aeruginosa infections treated with NVL, which was ranging between 50% and 80% [27,28,29,30]. On the other hand, our study reported an infection-related readmission rate of around 29%, mainly among the NCBL group. Our finding was lower than reported in the literature, which was reaching 61% of infection-related readmission among patients with an MDR infection history [31].

Around 67% of included patients in our study were critically ill, however, the subgroup analysis did not show differences in outcomes between critically ill patients who were treated with traditional NCBL versus NVL antibiotics. Although evidence is limited, 2024 IDSA recommend the newer sensitive β-lactams over traditional NCBL in critically ill patients to account for the emergent of resistance from these agents upon treatment [16, 32].

This study is the first to assess the effectiveness of traditional sensitive NCBL for CRPA isolates; however, the study has several limitations. The retrospective design of the study might lead to selection bias. The study was not powered to test the association between study groups. The study did not investigate the mechanism of CRPA resistance. Microbiological eradication and failure were assessed only in patients with repeated cultures which may introduce selection bias to the reported results. Data on source control was not collected. A fundamental limitation of this study is the potential differences between pathogens in the two groups, as it is unclear if NCBL-susceptible Pseudomonas isolates are comparable in virulence to difficult-to-treat isolates resistant to all NCBLs. Additionally, bias may arise because patients with pathogens that are difficult to treat cannot receive NCBLs, highlighting a that should be acknowledged. Future antimicrobial stewardship studies are needed to design effective interventions to limit the overuse and misuse of antibiotics for resistant isolates.

Conclusions

In patients with CRPA infections, there was no significant difference in 30-day mortality among patients treated with traditional sensitive NCBL compared with NVL. However, infection recurrence rate at 90 days was higher in patients treated with sensitive traditional NCBL. Further studies with larger sample sizes are needed to confirm these findings.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Abbreviations

Carb-R:

Carbapenem resistance

Ceph-S:

Cephalosporin sensitive

CRP:

C-reactive protein

CRPA:

Carbapenem-resistant Pseudomonas aeruginosa

CDC:

Centers for Disease Control and Prevention

CLSI:

Clinical and Laboratory Standards Institute

CAZ/AVI:

Ceftazidime- avibactam

C-T:

Ceftolazone -tazobactam

IDSA:

Infectious disses society of America

KFSHRC-J:

King Faisal Specialist Hospital and Research Center-Jeddah (KFSHRC-J)

WHO:

World Health Organization

NCBL:

Non-carbapenem β-lactam

NVL:

Novel β-lactam agents

MDR:

Multidrug resistance

MDRO:

Multidrug resistance organisms

XDR:

Extensive drug resistance

n:

Frequencies

IQR:

Interquartile ranges

P. aeruginosa:

Pseudomonas aeruginosa

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Acknowledgements

The authors wish to thank King Saud University, Riyadh, Saudi Arabia, for supporting this research project (RSP2024R74). We appreciate Dr. Abdullah Alraddadi, an infectious disease fellow at King Faisal Specialist Hospital and Research Center in Jeddah, Saudi Arabia, for sharing his insights on the study results, which contributed in the discussion writing. 

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Critical Care Clinical Pharmacy Consultant, Medical and Clinical Affairs Department, King Faisal Specialist Hospital and Research Center, P.O. Box 40047, Jeddah, 21499, Saudi Arabia

    Namareq F. Aldardeer

  2. Pediatric Antimicrobial Stewardship Clinical Pharmacist , King Saud Medical City, Riyadh, Saudi Arabia

    Hatun M. Labban

  3. Department of Pediatrics, King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia

    Raghad T. Alhuthil

  4. Pharmacist, Saudi German Hospital , Makkah, Saudi Arabia

    Seham H. Aljahdali

  5. Saudi German Hospital, Makkah, Saudi Arabia

    Moataz H. Alharbi

  6. Pharmacy Department, King Faisal Specialist Hospital and Research Center, Jeddah, Saudi Arabia

    Riham A. Alharbi

  7. Anti-Infective Research Laboratory, Department of Pharmacy Practice Eugene Applebaum College of Pharmacy and Health Sciences, Wayne State University, Detroit, MI, USA

    Mohammed I. Al Musawa

  8. Clinical Pharmacist, Medical and Critical Care Pharmacy, King Faisal Specialist Hospital and Research Center, Jeddah, Saudi Arabia

    Abdulrahman A. Almalki

  9. Clinical Pharmacy Department, College of Pharmacy, King Saud University, Riyadh, Saudi Arabia

    Thamer A. Almangour

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  1. Namareq F. Aldardeer
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  9. Thamer A. Almangour
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Contributions

N.A. conceptualized, supervised, and manuscript writing and critically reviewed the manuscript; T.A. critically reviewed the manuscript; H.L. data acquisition, manuscript writing, figure creation; R.H. data analysis; S.A., M.A., and RA data acquisition. M.M. and A.A. proposal writing. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Namareq F. Aldardeer.

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Ethics approval and consent to participate

The study was approved by the institutional review board of KFSHRC-J (IRB#2023-81). The data were kept confidential; no one except the research team had access to the files. As the data were collected retrospectively, the institutional review board of KFSHRC-J waived the consent to participate as per the rules and regulations of the Kingdom regarding the conduct of research and the IRB and international policies on human subject protection and confidentiality rights. This study was implemented following Good Clinical Research Practice (Declaration of Helsinki) and the rules and guidelines of the Ethics Committee in KFSHRC.

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The authors declare no competing interests.

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Aldardeer, N.F., Labban, H.M., Alhuthil, R.T. et al. Effectiveness of traditional non-carbapenem β-lactams vs. novel β-lactams for the treatment of carbapenem-resistant Pseudomonas aeruginosa: a retrospective cohort study. BMC Infect Dis 24, 1455 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-024-10365-5

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-024-10365-5

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BMC Infectious Diseases

ISSN: 1471-2334

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