Saeed NK, Almusawi SK, Albalooshi NA, Al-Beltagi M. Unveiling the impact: COVID-19's influence on bacterial resistance in the Kingdom of Bahrain. World J Virol 2025; 14(1): 100501 [DOI: 10.5501/wjv.v14.i1.100501]
Corresponding Author of This Article
Mohammed Al-Beltagi, MD, PhD, Chief Physician, Professor, Department of Paediatrics, Faculty of Medicine, Tanta University, 1 Hassan Radwan Street, Tanta 31511, Alghrabia, Egypt. mbelrem@hotmail.com
Research Domain of This Article
Microbiology
Article-Type of This Article
Retrospective Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Nermin K Saeed, Safiya K Almusawi, Noor A Albalooshi, Medical Microbiology Section, Department of Pathology, Salmaniya Medical Complex, Governmental Hospitals, Manama 12, Bahrain
Nermin K Saeed, Safiya K Almusawi, Medical Microbiology Section, Department of Pathology, Royal College of Surgeons in Ireland–Medical University of Bahrain, Busaiteen 15503, Muharraq, Bahrain
Mohammed Al-Beltagi, Department of Paediatrics, Faculty of Medicine, Tanta University, Tanta 31511, Alghrabia, Egypt
Mohammed Al-Beltagi, Department of Pediatric, University Medical Center, King Abdulla Medical City, Arabian Gulf University, Manama 26671, Algharbia, Bahrain
Author contributions: Saeed NK conceived the study and supervised the entire research process, including the study's design and the interpretation of the results, and contributed to revising the manuscript critically for important intellectual content; Almusawi SK was involved in acquiring data and played a key role in analyzing the laboratory results and organizing the data collection process, and contributed to revising the manuscript; Albalooshi NA contributed to the interpretation of the findings and ensured the accuracy of the clinical context in the manuscript, revised the manuscript and provided feedback on the final draft; Al-Beltagi M wrote the manuscript, performed the statistical analyses, and was responsible for revising it, communicated with the authors and journal reviewers, ensuring the manuscript met submission requirements; all of the authors read and approved the final version of the manuscript to be published.
Institutional review board statement: This study was conducted in accordance with the ethical standards of the Declaration of Helsinki. It was approved by the Institutional Review Board (IRB) of Salmaniya Medical Complex, Kingdom of Bahrain, on April 2024. Given the retrospective nature of the study and the use of de-identified patient data, the requirement for informed consent was waived by the IRB.
Informed consent statement: This retrospective study did not involve the direct collection of patient data or the identification of individual patients. As such, the Institutional Review Board of Salmaniya Medical Complex, Kingdom of Bahrain, waived informed consent in accordance with institutional guidelines and ethical standards.
Conflict-of-interest statement: The authors declare no conflict of interest. No financial, personal, or professional interests influenced this manuscript's research, authorship, or publication.
Data sharing statement: The data supporting this study's findings are available upon reasonable request from the corresponding author, Al-Beltagi M. However, the data are not publicly available due to privacy and ethical restrictions.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Mohammed Al-Beltagi, MD, PhD, Chief Physician, Professor, Department of Paediatrics, Faculty of Medicine, Tanta University, 1 Hassan Radwan Street, Tanta 31511, Alghrabia, Egypt. mbelrem@hotmail.com
Received: August 18, 2024 Revised: October 22, 2024 Accepted: November 15, 2024 Published online: March 25, 2025 Processing time: 101 Days and 16.7 Hours
Abstract
BACKGROUND
Antibiotic resistance is a growing global health threat, and understanding local trends in bacterial isolates and their susceptibility patterns is crucial for effective infection control and antimicrobial stewardship. The coronavirus disease 2019 (COVID-19) pandemic has introduced additional complexities, potentially influencing these patterns.
AIM
To analyze trends in bacterial isolates and their antibiotic susceptibility patterns at Salmaniya Medical Complex from 2018 to 2023, with a specific focus on the impact of the COVID-19 pandemic on these trends.
METHODS
A retrospective analysis of microbiological data was conducted, covering the period from 2018 to 2023. The study included key bacterial pathogens such as Escherichia coli (E. coli), Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Staphylococcus aureus, among others. The antibiotic susceptibility profiles of these isolates were assessed using standard laboratory methods. To contextualize the findings, the findings were compared with similar studies from other regions, including China, India, Romania, Saudi Arabia, the United Arab Emirates, Malaysia, and United States.
RESULTS
The study revealed fluctuating trends in the prevalence of bacterial isolates, with notable changes during the COVID-19 pandemic. For example, a significant increase in the prevalence of Staphylococcus aureus was observed during the pandemic years, while the prevalence of E. coli showed a more variable pattern. Antibiotic resistance rates varied among the different pathogens, with a concerning rise in resistance to commonly used antibiotics, particularly among Klebsiella pneumoniae and E. coli. Additionally, the study identified an alarming increase in the prevalence of multidrug-resistant (MDR) strains, especially within Klebsiella pneumoniae and E. coli isolates. The impact of the COVID-19 pandemic on these trends was evident, with shifts in the frequency, resistance patterns, and the emergence of MDR bacteria among several key pathogens.
CONCLUSION
This study highlights the dynamic nature of bacterial isolates and their antibiotic susceptibility patterns at Salmaniya Medical Complex, particularly in the context of the COVID-19 pandemic. The findings underscore the need for continuous monitoring and effective anti-microbial stewardship programs to combat the evolving threat of antibiotic resistance. Further research and policy initiatives are required to address the identified challenges and improve patient outcomes in the face of these ongoing challenges.
Core Tip: This study highlights the critical role of continuous surveillance in tracking bacterial isolates and their antibiotic susceptibility patterns, especially during the coronavirus disease 2019 pandemic. The findings underscore the need for robust antimicrobial stewardship programs to address the emergence of multidrug-resistant organisms. Regularly updated treatment protocols, informed by local epidemiological data, are essential for optimizing therapeutic strategies. The collaboration between microbiology laboratories and clinical teams is vital for timely diagnostics, which guide effective antimicrobial therapy. This study provides valuable insights that can inform healthcare practices and contribute to global efforts in combating antimicrobial resistance.
Citation: Saeed NK, Almusawi SK, Albalooshi NA, Al-Beltagi M. Unveiling the impact: COVID-19's influence on bacterial resistance in the Kingdom of Bahrain. World J Virol 2025; 14(1): 100501
The emergence of the coronavirus disease 2019 (COVID-19) pandemic, caused by the severe acute respiratory syndrome-coronavirus 2 virus, has profoundly impacted global healthcare systems and posed a significant global health challenge. This has led to significant shifts in medical practices, patient care protocols, and antimicrobial usage[1]. As the world grapples with the multifaceted repercussions of the COVID-19 pandemic, one critical aspect that demands attention is its effect on bacterial resistance, especially in healthcare settings[2]. The Kingdom of Bahrain, like many other nations, faced unprecedented challenges as it navigated the complexities of managing a novel infectious disease while simultaneously addressing the ongoing burden of bacterial infections. In this context, our research on the potential influence of COVID-19 on bacterial resistance patterns is of utmost significance[3].
Bacterial resistance, where bacteria develop mechanisms to resist the effects of antibiotics, is a growing public health threat, significantly complicating the treatment of infections and leading to increased morbidity, mortality, and healthcare costs[4]. The COVID-19 pandemic has introduced several factors that could potentially influence bacterial resistance patterns. Increased antibiotic use, often to treat secondary bacterial infections associated with the COVID-19 pandemic, may exert selective pressure for resistant strains[5]. Additionally, changes in healthcare-seeking behavior and potential resource limitations during the pandemic could have impacted the diagnosis and treatment of bacterial infections, leading to inappropriate antibiotic use[6]. The heightened focus on COVID-19 pandemic testing may have also diverted resources away from routine bacterial diagnostics, delaying identifying and treating susceptible bacterial infections. These pandemic-related changes have raised concerns about the acceleration of antimicrobial resistance (AMR) and the potential for fostering an environment conducive to the emergence and spread of resistant bacterial strains[7].
Moreover, the strain on healthcare resources during the pandemic may have led to inconsistent application of antimicrobial stewardship (AMS) programs, further complicating efforts to manage bacterial resistance[8]. Diagnostic delays, the reduced routine monitoring of bacterial infections, and the diversion of medical resources to focus on COVID-19 pandemic care likely impacted the timely and appropriate use of antibiotics[9]. Understanding these changes is crucial for developing effective strategies to combat AMR and ensure the continued efficacy of antibiotics[10]. By examining the interplay between pandemic-related healthcare adaptations and bacterial resistance patterns, we can inform future public health policies, optimize AMS programs, and strengthen the resilience of healthcare systems against both viral and bacterial threats.
In Bahrain, the healthcare system had to adapt rapidly to the demands of the pandemic, implementing measures such as enhanced diagnostic capabilities, increased hospitalizations, changes in infection control practices, and the deployment of broad-spectrum antibiotics[11]. While essential for managing COVID-19, these adaptations may have inadvertently influenced bacterial resistance patterns. The hospitalization surge led to higher patient densities and increased the likelihood of nosocomial infections, necessitating more frequent and broader use of antibiotics[12]. Changes in infection control practices, such as the use of personal protective equipment (PPE) and isolation protocols, altered the dynamics of bacterial transmission within healthcare settings[13]. The widespread deployment of broad-spectrum antibiotics, often used prophylactically or to treat suspected secondary bacterial infections in COVID-19 patients, may have exerted selective pressure on bacterial populations, accelerating the emergence of resistant strains[14].
This retrospective study aims to uncover the impact of COVID-19 on bacterial resistance in the Kingdom of Bahrain. We analyzed resistance rates before, during, and after the pandemic to identify significant shifts in bacterial resistance patterns associated with the COVID-19 era. This analysis provided valuable insights into the interplay between viral pandemics and bacterial resistance, which help inform future public health policies and AMS programs. Through this study, we hope to contribute to a broader understanding of the long-term implications of the COVID-19 pandemic on bacterial resistance and guide efforts to mitigate the rise of resistant infections in Bahrain and beyond. This involves informed decision-making regarding antibiotic use and stewardship practices in a post-pandemic setting.
MATERIALS AND METHODS
Study design and setting
This retrospective study was conducted at the Salmanyia Medical Complex, a major tertiary care hospital in the Kingdom of Bahrain. It lasted six years, covering two years before, two years during, and two years after the peak of the COVID-19 pandemic. This timeframe was chosen to comprehensively capture changes in bacterial resistance patterns associated with the pandemic.
Bacteriologic testing methods
The causative microorganisms were identified using standard microbiologic methods, including matrix-assisted laser desorption ionization time-of-flight (Bruker Daltonics, Bremen, Germany). Antimicrobial susceptibility testing was conducted on all isolates obtained from patients included in the study. The hospital’s microbiology laboratory tested susceptibility with an automated system (Phoenix, Becton, Dickinson and Company, Franklin Lakes, NJ, United States). The minimum inhibitory concentration breakpoints were determined for 14 antimicrobial agents: (1) Amikacin; (2) Ampicillin; (3) Aztreonam; (4) Ceftazidime; (5) Ceftriaxone; (6) Cefuroxime; (7) Cefepime; (8) Imipenem; (9) Meropenem; (10) Piperacillin/tazobactam; (11) Ciprofloxacin; (12) Gentamicin; (13) Tigecycline; and (14) Trimethoprim-sulfamethoxazole. Amoxicillin-clavulanic acid was tested using the disk diffusion method. Clinical and Laboratory Standards Institute interpretive criteria were used to interpret susceptibility results and breakpoints.
Phoenix, BD, detected extended-spectrum beta-lactamases (ESBL). Atypical ESBL detected by Phoenix were confirmed by double-disk synergy testing. Colistin susceptibility was tested using the Broth microdilution method (MICRONAUT). Phenotypically similar isolates from different specimens of the same patient were considered one sample. Molecular biological studies were not performed to identify the genetic similarities or dissimilarities of the bacterial isolates.
Definitions
Bacterial resistance is defined as the ability of bacteria to survive and proliferate in the presence of antibiotics that were previously effective against them. Bacterial resistance can complicate the treatment of infections, leading to increased morbidity, mortality, and healthcare costs. This study employs a specific categorization system to assess bacterial resistance patterns within the Kingdom of Bahrain. We differentiate bacterial strains based on their susceptibility to various antibiotic classes, focusing on potential changes associated with the COVID-19 pandemic. Following the approach outlined by Falagas and Karageorgopoulos[15], we define multidrug-resistant (MDR) strains as those exhibiting resistance to at least one agent in three or more distinct antibiotic classes. This categorization reflects a significant reduction in treatment options for infections caused by these bacteria. Our focus lies on MDR strains and their prevalence within the context of COVID-19[16,17]. Certain bacteria, such as Acinetobacter baumannii, Pseudomonas aeruginosa, and Klebsiella pneumoniae, will be assigned an MDR designation if they exhibit resistance to five or more out of the seven evaluated anti-pseudomonal antibiotic classes[18]. MDR strains of Mycobacterium tuberculosis fall outside the scope of this study. By employing this classification system, we aim to achieve a clear and concise understanding of bacterial resistance patterns within the context of the COVID-19 pandemic in Bahrain. For clinical isolates, the first bacterial pathogen growth from any clinical specimen for each patient was counted as a clinical isolate. Duplicate isolates, identified from the same patient with the same organism and antimicrobial profile, were not considered[19].
Data collection
Data were extracted from the electronic health records (EHR) of inpatients admitted to various departments within Salmanyia Medical Complex. The EHRs were reviewed for relevant microbiological information. The dataset included the microbiological profile: (1) Types of bacterial isolates; (2) Antimicrobial susceptibility profiles; and (3) Resistance patterns.
Inclusion criteria and exclusion criteria
Inclusion criteria: All inpatients admitted to Salmanyia Medical Complex who had documented bacterial cultures and antimicrobial susceptibility testing during the specified periods.
Exclusion criteria: Patients with incomplete records or missing key data elements were excluded from the study.
Data management
The extracted data were systematically organized and tabulated using Microsoft Excel. Each patient’s record was assigned a unique identifier to ensure anonymity and confidentiality. Data were manually extracted from the EHR system by trained personnel. Inconsistent or erroneous entries were identified and corrected. A random sample of records was cross-checked against the original EHR entries to verify accuracy.
Statistical analysis
Bacterial resistance rates were calculated for each of the three time periods (pre-pandemic, pandemic, and post-pandemic). Comparative analyses were conducted to identify significant shifts in resistance patterns over time. Statistical tests, such as χ2 tests for categorical variables and t-tests for continuous variables, were employed to assess the significance of observed differences.
Ethical considerations
This study was conducted according to the ethical principles of the Declaration of Helsinki. Ethical approval was obtained from the institutional review board of the Salmanyia Medical Complex. As the study was retrospective, the institutional review board granted a waiver of informed consent. Patient confidentiality was maintained throughout the study, with all data anonymized before analysis.
RESULTS
During the extensive six-year study period (2018-2023), a significant fluctuation in bacterial isolates was observed at Salmanyia Medical Complex, categorized into three crucial timeframes: (1) Pre-COVID-19 (2018-2019); (2) During COVID-19 (2020-2021); and (3) Post-COVID-19 (2022-2023).
Prevalence of bacterial isolates
Escherichia coli (E. coli) remained the most prevalent organism, decreasing from 2061 isolates in 2018 to 1316 in 2020 before a sharp rise to 3400 in 2023, likely due to improved detection methods or increased infections. Klebsiella pneumoniae declined from 1133 in 2018 to 809 in 2020, then recovered to 1354 in 2023, reflecting fluctuating infection rates or detection practices. Pseudomonas aeruginosa decreased from 835 isolates in 2018 to 550 in 2020, rebounding slightly to 683 in 2023, possibly due to changes in infection control. Acinetobacter baumannii showed variability, peaking at 353 isolates in 2023 after 336 in 2021, indicating its continued role in healthcare-associated infections (Table 1, Figure 1).
Figure 1 Most common Gram-negative and Gram-positive bacterial isolates Identified at Salmaniya Medical Complex over six years (2018-2023).
A: Gram-negative bacterial isolates; B: Gram-positive bacterial isolates. E. coil: Escherichia coli; H. influenzae: Haemaphilus influenzae.
Table 1 Comparison of bacterial isolates over three periods (before, during, and after the coronavirus disease 2019 pandemic).
Other notable organisms include (1) Enterobacter species, which declined from 307 in 2018 to 173 in 2020 and recovered to 279 in 2023; (2) Salmonella species, which spiked from 162 isolates in 2022 to 579 in 2023, possibly indicating an outbreak; and (3) Proteus mirabilis, which maintained stable numbers with slight fluctuations. In addition, Citrobacter species remained relatively stable throughout the study period, with minor fluctuations in the number of isolates, from 116 in 2018 to 159 in 2023, indicating a consistently low prevalence. In contrast, Serratia marcescens showed a notable increase in isolates, rising from 84 in 2018 to a peak of 119 in 2023. This upward trend suggests that Serratia may be playing an increasingly important role in infections at the facility. Stenotrophomonas maltophilia exhibited a gradual decline, with isolates decreasing from 133 in 2018 to 112 in 2023, which could indicate improvements in infection control or changes in the patient population. Haemophilus influenzae (H. influenzae) saw a sharp decrease in isolates, from 122 in 2018 to just 40 in 2021, followed by a recovery to 116 in 2023. This pattern may be influenced by vaccination programs or other public health measures to control H. influenzae infections.
Gram-positive organisms also show fluctuation in their rate before, during, and after the pandemic. Staphylococcus aureus isolates decreased from 1631 in 2018 to 1102 in 2020, then steadily rising to 1591 in 2023. Enterococcus species dropped significantly from 730 isolates in 2018 to 486 in 2019, followed by a substantial increase to 856 in 2023, indicating a growing concern with Enterococcus-related infections. Coagulase-negative Staphylococci showed a sharp rise, peaking at 1734 isolates in 2021, then slightly declining to 1433 in 2023. Streptococcus pyogenes experienced a dramatic decline from 127 isolates in 2018 to just 16 in 2022 before recovering to 99 in 2023. Similarly, Streptococcus pneumoniae isolates consistently declined from 106 in 2018 to 33 in 2020, with a modest recovery to 86 in 2023.
Antibiotic susceptibility patterns
E. coli susceptibility to Amoxicillin-Clavulanate decreased slightly from 47% in 2018 to 49% in 2023, while Cefuroxime remained stable at 50%. Ceftriaxone and Ciprofloxacin susceptibility declined from 60% and 72% in 2018 to 57% and 64%, respectively, by 2023. Klebsiella pneumoniae susceptibility to Meropenem dropped from 92% in 2018 to 88% in 2023, while Tigecycline remained effective (82%+ susceptibility). Pseudomonas aeruginosa maintained high susceptibility to Piperacillin-Tazobactam, Ceftazidime, and Cefepime (73%+), though Meropenem and Imipenem showed slight declines to 85% in 2023. Acinetobacter baumannii displayed persistently low susceptibility, with rates below 30% for most antibiotics and Gentamicin dropping to 31% in 2023. Enterobacter species showed stable susceptibility to Meropenem (97%+) but slight declines in Ceftriaxone and Ciprofloxacin. Proteus mirabilis maintained 100% susceptibility to Meropenem, though Ciprofloxacin decreased from 82% in 2018 to 74% in 2023 (Figure 2, Supplementary Tables 1, 2 and 3).
Figure 2 Percentage of antibiotic susceptibility.
A: Percentage of Escherichia coli antibiotic susceptibility; B: Percentage of Klebsiella pneumoniae antibiotic susceptibility; C: Percentage of Pseudomonas aeruginosa antibiotic susceptibility; D: Percentage of Acinetobacter baumannii antibiotic susceptibility; E: Percentage of Staphylococcus aureus antibiotic susceptibility; F: Percentage of Enterococcus spp. antibiotic susceptibility. Pipe.Taz: Piperacillin-Tazobactam.
Staphylococcus aureus exhibited a drop in Erythromycin susceptibility (75% in 2018 to 64% in 2023), but Clindamycin improved to 90% in 2023. Methicillin-resistant Staphylococcus aureus (MRSA) rates also increased during this period. Enterococcus species maintained stable susceptibility to Vancomycin and Daptomycin but fluctuating susceptibility to Penicillin, Ampicillin, and Ciprofloxacin. Streptococcus pneumoniae remained highly susceptible to Penicillin and Ceftriaxone (95%+), while Erythromycin susceptibility decreased from 79% in 2018 to 62% in 2023.
Multidrug-resistant trends
E. coli: ESBL-producing strains increased from 39% in 2018 to 47% in 2021, with a slight decrease to 42% in 2023. Carbapenem-resistant (CRE) remained low, peaking at 3% during the pandemic.
Klebsiella pneumoniae: ESBL rates rose from 38% in 2018 to 49% in 2019, stabilizing post-pandemic. CRE peaked at 30% in 2021 before decreasing to 12% in 2023.
Acinetobacter baumannii: MDR rates remained high (89% in 2020), dropping slightly to 80% in subsequent years.
Pseudomonas aeruginosa: MDR rates increased slightly during the pandemic, peaking at 17%, then declining to 9% post-pandemic.
Staphylococcus aureus: MRSA rates rose from 36% in 2018 to 53% in 2023, particularly post-pandemic.
Enterococcus species: Vancomycin-resistant Enterococci (VRE) rates increased from 9% in 2018 to 20% in 2021, stabilizing at 23% by 2023.
These trends suggest the COVID-19 pandemic had a notable impact on AMR, particularly in MDR pathogens like Klebsiella pneumoniae, Acinetobacter baumannii, MRSA, and VRE. While post-pandemic resistance rates decreased for some organisms, high resistance levels persist, highlighting the need for continuous AMS (Table 2, Figure 3).
We previously reported the bacterial co-infections in the very early phase of COVID-19. We observed a significant increase in bacterial and fungal co-infection in the early phase of the pandemic in the Kingdom of Bahrain[3]. Therefore, this six-year study (2018–2023) conducted at Salmaniya Medical Complex provides crucial insights into the evolving landscape of bacterial infections and AMR, particularly emphasizing the impact of the COVID-19 pandemic. The findings highlight significant changes in bacterial prevalence and resistance patterns, underscoring the ongoing challenges in managing healthcare-associated infections during and after the pandemic.
Fluctuations in bacterial isolates
Our data reveal notable fluctuations in bacterial isolate numbers across various organisms over the study period. E. coli consistently emerged as the most prevalent organism, with a marked increase in 2023. This spike may be attributable to rising infection rates and improved detection techniques. Similar trends were observed with Klebsiella pneumoniae and Enterococcus species, which both experienced post-pandemic surges. This resurgence suggests that the healthcare system's response to the pandemic, including altered infection control practices and the increased use of antibiotics during COVID-19 patient management.
Interestingly, Salmonella isolates saw a dramatic rise in 2023, which could indicate an outbreak or the result of enhanced surveillance measures, similar to trends reported in China[20]. Conversely, organisms such as Stenotrophomonas maltophilia and H. influenzae demonstrated a declining trend, likely reflecting the success of vaccination programs and improved infection control efforts. These shifts in bacterial prevalence underscore the dynamic nature of bacterial infections in the context of evolving healthcare challenges. This aligns with findings from other regions, such as India[21] and Romania[22], where similar trends in E. coli, Klebsiella pneumoniae, and Staphylococcus aureus were noted.
Interestingly, Salmonella isolates saw a dramatic rise in 2023, which may suggest an outbreak or increased detection through enhanced surveillance systems. This sharp increase mirrors similar findings from China in 2023[20], where heightened awareness and targeted surveillance efforts resulted in the identification of more Salmonella cases than in previous years. The rise in Salmonella could be linked to several factors, including changes in food safety practices, increased incidence of foodborne outbreaks, or improved diagnostic capabilities in detecting bacterial pathogens[23]. Additionally, the increased use of routine microbiological screening and molecular diagnostic tools in healthcare settings may have contributed to the surge in reported cases, especially in light of the post-pandemic recovery in healthcare services. Such outbreaks often call for prompt public health interventions, including heightened surveillance, food safety regulations, and outbreak investigations to identify potential sources of infection[24].
Conversely, organisms such as Stenotrophomonas maltophilia and H. influenzae have a declining trend over the same period. This reduction is likely the result of improved infection control protocols and public health measures. For Stenotrophomonas malt philia, a pathogen often associated with immunocompromised patients and healthcare-associated infections, the decline could reflect better environmental hygiene, the increased use of isolation precautions, and more judicious use of broad-spectrum antibiotics that have been linked to its emergence. Improvements in hospital sanitation and a renewed focus on AMS during and after the pandemic may have also contributed to the reduced incidence of this pathogen[25].
The decline in H. influenzae isolates, on the other hand, is most likely due to the widespread success of vaccination programs, particularly the H. influenzae type B vaccine, which has been effective in reducing the incidence of invasive diseases caused by this pathogen[26]. The disruption of regular vaccination schedules during the pandemic was initially a concern. Still, the return to routine immunization practices post-pandemic may have contributed to the observed decline. Furthermore, the widespread use of non-pharmaceutical interventions during the pandemic, such as masking and social distancing, may have indirectly decreased the transmission of respiratory pathogens, including H. influenzae[27].
These shifts in bacterial prevalence underscore the dynamic nature of bacterial infections, particularly as healthcare systems adapt to evolving challenges such as the COVID-19 pandemic. Changes in infection control measures, public health policies, and diagnostic practices all shape bacterial epidemiology. The fluctuations in bacterial prevalence in Bahrain align with trends in other regions. For instance, studies from India[21] and Romania[22] have reported similar patterns in bacterial isolates, particularly with E. coli, Klebsiella pneumoniae, and Staphylococcus aureus. These organisms have shown fluctuations in response to shifting healthcare priorities, the widespread use of antimicrobials, and the influence of infection control practices. Such comparative data suggest that while the impact of the pandemic on bacterial prevalence and AMR is global, regional healthcare practices and public health strategies significantly influence the specific trends observed[28].
Staphylococcus aureus isolates decreased from 1631 in 2018 to 1102 in 2020, followed by a steady increase to 1591 in 2023. A similar trend was observed in Romania, where Staphylococcus aureus isolates initially rose from 2017 to 2019, then declined during 2020 and 2021, before surging again in 2022[22]. This fluctuation highlights the organism's persistent role in both community and healthcare-associated infections. The significant drop in Enterococcus spp isolates from 730 in 2018 to 486 in 2019, followed by a sharp increase to 856 in 2023, highlighting the growing concern regarding Enterococcus-related infections. This resurgence may be attributed to changes in infection control practices, increased use of antibiotics during the COVID-19 pandemic, and the pathogen’s ability to acquire resistance to commonly used treatments like vancomycin[29]. Coagulase-negative Staphylococci also exhibited notable trends, peaking at 1734 isolates in 2021 before slightly declining to 1433 in 2023. This pattern could reflect a rise in device-related infections or shifts in clinical practices during the pandemic[30]. Streptococcus pyogenes experienced a dramatic decline, with isolates dropping from 127 in 2018 to just 16 in 2022, followed by a resurgence to 99 in 2023. These fluctuations may reflect variations in community-acquired infections or differences in reporting practices. Similarly, Streptococcus pneumoniae isolates consistently decreased from 106 in 2018 to 33 in 2020, with a modest recovery to 86 in 2023. This trend is likely influenced by vaccination efforts or other public health initiatives, as seen in the United Arab Emirates, where Streptococcus pneumoniae peaked in 2019, declined in 2020, and slightly increased in 2021[31].
A study conducted in Malaysia identified Acinetobacter baumannii as the most frequently isolated organism, followed by Klebsiella pneumoniae, Coagulase-negative Staphylococci, E. coli, Enterococcus faecalis, and Enterococcus faecium[32]. In the United States, a multicenter study reported that Staphylococcus aureus and Gram-negative rods were the most commonly isolated bacterial pathogens from patients hospitalized during the pandemic[33]. These comparative analyses emphasize the broader context of bacterial isolation trends worldwide, underscoring the global nature of these challenges and the need for continued vigilance in managing bacterial infections.
Antibiotic susceptibility trends
The antibiotic susceptibility patterns highlight the growing challenge of antibiotic resistance, particularly among common pathogens like E. coli, Klebsiella pneumoniae, and Acinetobacter baumannii. E. coli's decreasing susceptibility to commonly used antibiotics such as Amoxicillin-Clavulanate, Cefuroxime, and Ciprofloxacin underscores continuous monitoring and development of new therapeutic strategies. Klebsiella pneumoniae also showed a declining trend in susceptibility to several antibiotics, with a notable decrease in susceptibility to Meropenem, a last-resort antibiotic. This trend is concerning as it points to the increasing difficulty in treating infections caused by this pathogen. A similar finding was observed in a study from India, where Sharma et al[34] found an increase of antibiotic resistance among the isolated Klebsiella pneumoniae from patients in intensive care units (ICUs) to reach about 87.5% of the isolated strains, especially during and after the peak of COVID-19 pandemic.
Acinetobacter baumannii, known for its role in healthcare-associated infections, displayed alarmingly low susceptibility rates to most antibiotics, with susceptibility rates for Piperacillin-Tazobactam, Ceftazidime, and Cefipime remaining below 30%. The persistently high MDR rates in Acinetobacter baumannii highlight the critical need for stringent infection control measures and the development of new antimicrobial agents. A systematic review by Sulayyim et al[35] found that Acinetobacter baumannii was the most commonly reported resistant gram-negative bacteria, followed by Klebsiella pneumonia, E. coli, and Pseudomonas aeruginosa.
MDR organisms
The rise of MDR organisms presents one of the most pressing challenges in modern healthcare. MDR organisms are defined as bacteria that are resistant to three or more antibiotics, making them particularly difficult to treat. This study highlights the increasing prevalence of MDR organisms at Salmaniya Medical Complex, particularly in pathogens like Klebsiella pneumoniae, Acinetobacter baumannii, and MRSA[36].
ESBL and CRE E. coli
E. coli is a common cause of both community-acquired and healthcare-associated infections, such as urinary tract infections (UTIs), bloodstream infections, and intra-abdominal infections. The emergence of ESBL-producing E. coli is a significant concern due to its resistance to many commonly used antibiotics, particularly cephalosporins and penicillins[37].
ESBL E. coli: ESBL-producing E. coli strains are resistant to third-generation cephalosporins like Ceftriaxone and Ceftazidime, necessitating the use of carbapenems as the primary treatment option. However, the overuse of carbapenems has led to the emergence of CRE E. coli, which poses an even greater therapeutic challenge[38]. The proportion of ESBL E. coli isolates in this study increased from 39% in 2018 to a peak of 47% in 2021 and 2022, likely influenced by the COVID-19 pandemic. A similar study in Thailand reported that 42.5% of E. coli isolates were ESBL-producing[39]. Conversely, a study in Finland observed a decreasing trend of ESBL E. coli during the pandemic compared to the pre-pandemic period[40].
CRE E. coli: CRE E. coli is resistant to nearly all available antibiotics, including carbapenems, which are often reserved for severe MDR infections. The rise in CRE E. coli has been associated with higher mortality rates, especially among critically ill patients in ICUs[41]. Our study found a concerning increase in CRE E. coli isolates during and after the pandemic, underscoring the need for strict infection control and prudent antibiotic use. Similar findings were reported in the Dominican Republic, where the CRE E. coli rate was about 0.15%[42], and in European countries, where CRE isolation rates rose significantly during the pandemic compared to the pre-pandemic period[43,44]. While ESBL-producing E. coli is more common in Asia, CRE E. coli and VRE are more prevalent in European countries.
MDR Klebsiella pneumoniae
Klebsiella pneumoniae is a major cause of healthcare-associated infections, including pneumonia, bloodstream infections, wound infections, and meningitis. During the pandemic, the prevalence of MDR Klebsiella pneumoniae increased significantly. A similar trend was reported in Shenzhen, China, where MDR Klebsiella pneumoniae isolates from hospitalized children increased during the pandemic[45]. An outbreak of hypervirulent MDR Klebsiella pneumoniae in COVID-19 patients in Italy was also associated with high mortality rates[46]. In Saudi Arabia, the rate of MDR Klebsiella pneumoniae reached 57.5% during the pandemic[47].
One of the most alarming findings in this study is the declining susceptibility of Klebsiella pneumoniae to carbapenems, such as Meropenem, which are often considered antibiotics of last resort for MDR infections. The emergence of CRE Klebsiella pneumoniae (CRKP) poses a significant threat, as it leaves few treatment options available[48]. In the Slovak Republic, the rate of CRKP increased 4.8 times during the pandemic, from 0.18% to 0.76%, with 47% of COVID-19 patients colonized with CRKP[49]. The rise in MDR Klebsiella pneumoniae during the pandemic may be due to the overuse of broad-spectrum antibiotics, prolonged hospital stays, and the increased use of invasive devices, all of which are known risk factors for the spread of MDR organisms[50].
MDR and CRE Pseudomonas aeruginosa
Pseudomonas aeruginosa is a common nosocomial pathogen, particularly in critically ill patients. Known for its intrinsic resistance to many antibiotics, Pseudomonas aeruginosa can also acquire resistance during treatment, resulting in MDR and CRE Pseudomonas aeruginosa (CRP)[51]. This study highlights the significant prevalence of MDR Pseudomonas aeruginosa, which is resistant to multiple antibiotic classes, including beta-lactams, aminoglycosides, and fluoroquinolones. The ability of Pseudomonas aeruginosa to form biofilms on medical devices, such as catheters and ventilators, contributes to its persistence and resistance in healthcare settings[52].
During the COVID-19 pandemic, the prevalence of MDR Pseudomonas aeruginosa increased by 70% compared to pre-pandemic levels, before returning to baseline after the pandemic. However, the prevalence of MDR Pseudomonas aeruginosa in Bahrain remained lower than in other countries[53]. CRP Pseudomonas aeruginosa is especially concerning due to its resistance to carbapenems, complicating treatment options. Our findings showed a significant decline in susceptibility to carbapenems like Meropenem and Imipenem, making infections caused by this pathogen more difficult to manage[54]. The use of more toxic antibiotics, such as colistin, is often required for CRP Pseudomonas aeruginosa, increasing morbidity and mortality[55]. Comparative studies show significantly higher rates of CRP Pseudomonas aeruginosa in regions outside Asia[56], with differences attributed to antibiotic prescribing practices, infection control measures, and public health policies[57].
MDR Acinetobacter baumannii
Acinetobacter baumannii is another notorious MDR pathogen, particularly in critical care settings, where it causes severe infections such as ventilator-associated pneumonia and bloodstream infections[58]. Our study showed that Acinetobacter baumannii had extremely low susceptibility rates to a wide range of antibiotics, with susceptibility to Piperacillin-Tazobactam, Ceftazidime, and Cefepime below 30%. The high prevalence of MDR Acinetobacter baumannii is concerning due to its ability to persist in hospital environments, making it a persistent threat[59]. Studies have shown a significantly increased risk of death in COVID-19 patients with MDR Acinetobacter baumannii co-infection[60]. In Croatia, Acinetobacter baumannii was the most common bloodstream infection in COVID-19 patients admitted to ICUs[61]. Similarly, a study in Mexico reported increased resistance of Acinetobacter baumannii to multiple antibiotics during the pandemic[62]. The emergence of CRE Acinetobacter baumannii further complicates treatment, with high mortality rates associated with these infections[63]. The persistence of MDR Acinetobacter baumannii during and after the pandemic highlights the urgent need for aggressive infection control measures and the development of alternative therapeutic strategies[64].
MRSA
MRSA has long been recognized as a significant cause of hospital-acquired infections. Our study observed an increase in MRSA isolates during the pandemic, likely due to the increased strain on healthcare systems, which may have led to lapses in infection control practices[65]. MRSA is resistant to all beta-lactam antibiotics, including penicillins and cephalosporins, limiting treatment options. The rise in MRSA during the pandemic aligns with global trends, which have reported an increase in healthcare-associated infections due to the pandemic’s impact on infection control practices[66].
The fluctuations in MRSA rates in Bahrain during the COVID-19 pandemic, with an initial decrease followed by a rise to levels exceeding pre-pandemic rates, can be attributed to multiple factors. Early in the pandemic, strict infection control measures were implemented to prevent COVID-19 transmission in healthcare settings, likely reducing MRSA spread. These measures included enhanced hygiene protocols, reduced elective surgeries, and minimized hospital admissions for non-COVID-19 conditions[67]. However, as the pandemic progressed, the focus on managing COVID-19 cases may have disrupted routine infection control practices for other pathogens like MRSA[68]. Additionally, the widespread use of broad-spectrum antibiotics to treat suspected bacterial infections in COVID-19 patients may have promoted the emergence and spread of resistant strains, including MRSA[3,69]. As healthcare facilities resumed normal operations, there was likely an increase in hospital admissions and surgeries, along with weakened infection control measures, creating conditions conducive to MRSA transmission[70]. Prolonged strain on healthcare systems, resource limitations, and staff fatigue during the pandemic may have also contributed to the resurgence of MRSA in the later stages[71].
VRE
Enterococcus species, particularly Enterococcus faecium, are important causes of healthcare-associated infections, including bacteremia, endocarditis, and UTIs[72]. VRE is a significant challenge in healthcare settings due to its resistance to vancomycin, one of the key antibiotics for serious Enterococcus infections[73]. The progressive increase in VRE during the pandemic, particularly in Bahrain in 2022 and 2023, can be attributed to several factors. The pandemic disrupted routine healthcare practices and infection control measures as the focus shifted toward managing COVID-19 patients. The increased use of broad-spectrum antibiotics, such as vancomycin, likely exerted selective pressure, favoring the proliferation of VRE[74]. The strain on healthcare systems, lapses in infection prevention, and the resumption of routine hospital operations likely contributed to rising VRE cases in the later years of the pandemic[75]. VRE is particularly problematic in immunocompromised patients and those with underlying chronic conditions, where infections are more severe and difficult to treat[76]. The rise in VRE underscores the importance of strict infection control practices, including hand hygiene, environmental cleaning, and appropriate antibiotic use[77].
Implications of MDR organisms
The rise of MDR organisms has profound implications for clinical practice, patient outcomes, and public health. Infections caused by MDR organisms are associated with higher morbidity and mortality rates, prolonged hospital stays, and increased healthcare costs[78]. The limited treatment options for these infections often necessitate the use of more toxic or less effective antibiotics, which can lead to adverse patient outcomes[79]. The findings of this study underscore the urgent need for robust AMS programs to curb the overuse and misuse of antibiotics. AMS involves optimizing the selection, dosage, and duration of antimicrobial treatment to maximize clinical outcomes while minimizing the risk of resistance[80]. Infection control measures are equally crucial in preventing the spread of MDR organisms within healthcare facilities. These measures include hand hygiene, environmental cleaning, PPE, and the appropriate isolation of infected patients[81]. Additionally, ongoing surveillance of antibiotic resistance patterns is essential for guiding empirical therapy and developing targeted interventions to combat the spread of MDR organisms[82]. The study's data provide a critical foundation for informing local antibiotic prescribing practices and tailoring infection control policies to the specific challenges faced at Salmaniya Medical Complex.
Impact of the COVID-19 pandemic
The COVID-19 pandemic appears to have significantly influenced various bacterial pathogens' prevalence and resistance patterns. The increase in MDR organisms during the pandemic years, particularly in Klebsiella pneumoniae, Acinetobacter baumannii, and MRSA, suggests a potential correlation between the pandemic and the emergence of resistance[83]. The pandemic's impact on healthcare practices, including the increased use of antibiotics, changes in infection control practices, and the strain on healthcare resources may have contributed to this trend[84]. Interestingly, the post-pandemic period showed reduced resistance rates for some pathogens, possibly due to a renewed focus on infection control and AMS[85]. However, the persistently high levels of resistance in several key pathogens underscore the ongoing challenges in managing bacterial infections in the post-pandemic era.
Implications for clinical practice and public health
The findings of this study have important implications for clinical practice and public health. The rising prevalence of MDR organisms, particularly post-pandemic, highlights the need for continued vigilance in antibiotic stewardship and infection control practices[86]. The data also underscore the importance of ongoing surveillance of bacterial infections and resistance patterns to inform treatment guidelines and public health interventions. In conclusion, the study highlights the dynamic nature of bacterial infections and resistance patterns at Salmaniya Medical Complex. The fluctuations in bacterial isolates and the increasing resistance to commonly used antibiotics underscore the need for continuous monitoring, effective infection control measures, and the development of new antimicrobial agents[87]. The impact of the COVID-19 pandemic on resistance patterns further emphasizes the need for a comprehensive approach to managing bacterial infections in the healthcare setting.
Limitation of the study
This study has several limitations that should be considered when interpreting its findings. Firstly, the retrospective design, relying on historical data from 2018-2023, may limit the ability to establish causality and may be subject to inaccuracies or incomplete records. Additionally, as a single-center study conducted at Salmaniya Medical Complex, the findings may not be generalizable to other healthcare settings within Bahrain or other regions, as local practices, patient populations, and healthcare infrastructures could differ significantly. Over the six-year study period, changes in laboratory practices, diagnostic criteria, and data recording methods may have introduced variability and bias, affecting the analysis of trends. Furthermore, the study did not control for potential confounding factors such as changes in hospital admission policies, antibiotic prescribing practices, or infection control measures, which could have influenced the observed trends in bacterial isolates and antibiotic resistance patterns.
The lack of detailed clinical correlation with patient outcomes, such as mortality, morbidity, or length of hospital stay, also limits the ability to assess the direct impact of these trends on patient care. Moreover, the focus on selected bacterial pathogens may have overlooked trends in less frequently isolated organisms or emerging pathogens, potentially missing significant developments in the microbial landscape. The reliance on standard antibiotic susceptibility testing methods may not fully capture more nuanced resistance mechanisms, and variations in testing protocols over time could affect the comparability of results. While the study highlights the impact of the COVID-19 pandemic, it does not fully explore the complex interplay between COVID-19 treatment protocols and the observed trends in bacterial infections and antibiotic resistance. Lastly, the absence of molecular data, such as genotyping or whole-genome sequencing, limits the ability to identify specific resistance genes or track the spread of particular clones within the hospital. These limitations underscore the need for caution in interpreting the results and point to areas for further research.
Recommendations
Based on the study's findings and limitations, several recommendations are suggested to enhance the understanding and management of bacterial infections and antibiotic resistance at Salmaniya Medical Complex and similar healthcare settings. Continuous and comprehensive surveillance of bacterial isolates and their antibiotic susceptibility patterns is crucial, with standardized methods to ensure data consistency over time, allowing for accurate trend analysis and early detection of emerging resistance patterns. Expanding surveillance to include a broader range of pathogens and integrating molecular techniques, such as genotyping or whole-genome sequencing, into routine practices would provide deeper insights into resistance mechanisms and the spread of specific clones. The study also underscores the importance of ongoing education and training of healthcare professionals in AMS practices, focusing on appropriate antibiotic use and infection control measures. Strengthening collaboration between microbiology laboratories, clinicians, and infection control teams is essential for translating surveillance data into effective clinical decision-making and policy development. Given the impact of the COVID-19 pandemic on bacterial infection trends, further investigation into the interplay between viral pandemics, treatment protocols, and bacterial resistance patterns is recommended to inform future healthcare responses. Additionally, improving data recording and reporting practices will enhance the accuracy of retrospective analyses. Lastly, conducting similar research in other healthcare settings within Bahrain and the wider region is advised to validate the findings and assess their generalizability, with comparative studies providing valuable insights into global trends in bacterial infections and resistance, aiding in developing coordinated public health strategies.
CONCLUSION
This study offers crucial insights into the evolving trends of bacterial isolates and their antibiotic susceptibility patterns at Salmaniya Medical Complex from 2018 to 2023, highlighting the significant impact of the COVID-19 pandemic on these dynamics. The fluctuating prevalence of key pathogens, including E. coli, Klebsiella pneumoniae, and Staphylococcus aureus, alongside varying levels of antibiotic resistance, underscores the persistent challenge of AMR in healthcare settings. The results emphasize the importance of continuous monitoring through robust AMS programs to mitigate the rising threat of antibiotic resistance. Moreover, the study calls for implementing standardized surveillance systems and enhanced data collection methods to generate accurate, real-time insights that can inform clinical decisions and guide health policy development. The observed shifts in bacterial infection patterns during the pandemic further stress the need for a holistic approach to infectious disease management, recognizing the complex interplay between viral and bacterial pathogens. By advancing our understanding of bacterial resistance trends in Bahrain, this study lays a foundation for future research and policy initiatives to combat AMR and improve patient outcomes. Addressing the identified limitations and applying the recommended strategies can equip healthcare facilities with the tools to better manage bacterial infections and optimize antibiotic therapies amidst evolving resistance challenges.
Footnotes
Provenance and peer review: Invited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Virology
Country of origin: Bahrain
Peer-review report’s classification
Scientific Quality: Grade B, Grade D
Novelty: Grade B, Grade B
Creativity or Innovation: Grade B, Grade C
Scientific Significance: Grade B, Grade C
P-Reviewer: Iskandar CF S-Editor: Luo ML L-Editor: A P-Editor: Zheng XM
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