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. 2024 Jul 3;38(4):1965–1972. doi: 10.21873/invivo.13653

Bloodstream Coinfections and Antimicrobial Resistance in Hospitalized COVID-19 Patients: A Single-center Retrospective Study

YU-HSIN TSAI 1, TAI-CHENG HOU 2, PO-YU LIU 3, CHIH-JUNG CHEN 1,4,5, JIUNN-MIN WANG 6
PMCID: PMC11215599  PMID: 38936952

Abstract

Background/Aim

Bloodstream infections in patients with COVID-19 are linked to higher mortality rates, whilst data on epidemiology and resistance patterns remains scarce to guide management and prevent antibiotic resistance. This research focuses on the prevalence, clinical features, causative microorganisms, and antimicrobial susceptibility of bacterial and fungal secondary bloodstream co-infections in hospitalized patients with COVID-19.

Patients and Methods

In this retrospective study analysis of 230 patients with COVID-19 from Central Taiwan (June 2021 to June 2022), pathogens were identified via MALDI-TOF MS and Vitek 2 system with Clinical & Laboratory Standards Institute (CLSI) standards.

Results

In the cohort, 17.8% experienced bloodstream infections, resulting in a total of 45 isolates from the 41 bloodstream infection patients: predominantly gram-positive bacteria (Staphylococcus and Enterococcus) at 69%, gram-negative at 29% (Escherichia coli and Klebsiella pneumoniae), and fungi at 2%. Infected patients showed significantly elevated levels of white blood count (WBC), C-reactive protein (CRP) and procalcitonin (PCT). Of note, resistance to common antibiotics, such as fluoroquinolones, cephalosporins, and oxacillin was significant, especially in K. pneumoniae, Acinetobacter species, and S. aureus infections.

Conclusion

Our study highlights the influence of bacterial infections in hospitalized patients with COVID-19. The bacterial infections were discovered to impact the clinical trajectory of COVID-19, potentially exacerbating or mitigating its symptoms, severity and fatality. These insights are pivotal to addressing clinical challenges in COVID-19 management and underscoring the need for tailored medical interventions. Understanding these co-infections is thus essential for optimizing patient care and improving overall outcomes in the post COVID-19 pandemic era.

Keywords: COVID-19, bloodstream infection, microorganisms, antimicrobial susceptibility

The COVID-19 pandemic, caused by the SARS-CoV-2 virus, has led to an unparalleled global crisis, exerting profound impacts on millions of people worldwide and straining healthcare systems to their limits. As researchers scramble to comprehend intricacies of the disease, the occurrence of bloodstream infections in patients with COVID-19 has emerged as an urgent topic of scholarly interest (1). In the first quarter of 2023 alone, Taiwan reported more than 3,000 fatalities (2).

Previous studies have reported that clinical risk factors for a fatal outcome associated with coronavirus encompass chronic medical conditions, such as acute kidney injury, chronic obstructive pulmonary disease, diabetes, hypertension, cardiovascular disease, cancer, increased D-dimer, male sex, older age, current smoker, and obesity (3). The incidence of bloodstream infections is 3.88-fold higher in patients with COVID-19 compared to those testing negative by laboratory analyses (4). Further, the incidence of central line-associated bloodstream infections has witnessed an escalation in the wake of COVID-19 pandemic (5). Patients with severe COVID-19 manifestations in intensive care units are particularly susceptible to bloodstream infections, a complication closely associated with heightened mortality rates (3). The 30-day mortality rate in patients with COVID-19 stands at 40.2%, with a sharp contrast to the 23.7% observed in the non-COVID-19 cohorts. Notably, these bloodstream infections often involve multidrug-resistant organisms, with their distribution and prevalence eliciting considerable variability across medical institutions and geographical regions (6).

From an epidemiological standpoint, the surge in COVID-19 cases has somewhat overshadowed the criticality of concurrent bloodstream infections, grappling with data paucity. Preliminary investigations suggest the incidence of these infections is modulated by geographical, demographic, and healthcare-related factors. Despite the urgent need to prevent these dangerous infections, comprehensive data on local antimicrobial resistance patterns remain largely absent. Recent findings of reduced effectiveness of COVID-19 vaccines in hospitalized patients further underscore the continued threat posed by severe disease manifestations (7). Contemporary epidemiological insights are thus data pivotal to therapeutic strategies and reinforce infection control measures. However, most current literature derives from early pandemic phases and is often limited to single-center studies, rendering current microbiological profiles relatively unclear.

Our current study endeavors to bridge these knowledge gaps, focusing on bloodstream infections within the cohorts of hospitalized patients with COVID-19 in central Taiwan. Patient clinical profiles, distribution of causative organisms and antimicrobial susceptibility profiles were meticulously investigated. As COVID-19 gradually transitions to post-pandemic phase, the threat of complications such as nosocomial infections remain unabated. Our findings offer timely insights into the prevailing microbiological landscapes for guiding clinical interventions. In the current context of escalating antimicrobial resistance and attenuated vaccine potency, secondary infections may increasingly contribute to severe clinical outcomes. Our investigation thus also lays the groundwork for monitoring evolving epidemiological trends regionally.

Patients and Methods

A retrospective cohort study was conducted, encompassing hospitalized patients with COVID-19 who underwent blood culture testing at a medical center in central Taiwan from June 1, 2021, to June 30, 2022. The cohort comprised 230 hospitalized patients with laboratory-confirmed COVID-19, yielding 45 blood culture isolates. Medical records were extracted from the HIS (Healthcare Information System). COVID-19 diagnosis was confirmed using reverse-transcriptase quantitative polymerase chain reaction (RT-qPCR) in nasopharyngeal swabs. Data collected included patient demographics (age, sex), SARS-CoV-2 PCR results, blood culture outcomes, microorganisms identified and results of antimicrobial susceptibility tests from positive blood cultures. In addition, biomarkers including white blood count (WBC), C-reactive protein (CRP) and procalcitonin (PCT) levels were also collected.

Age and sex distribution were quantified as count and percentage, stratified by the presence or absence of bloodstream infections. An independent t-test was employed to compare the two cohorts based on the biomarkers (WBC count, CRP and PCT levels). Identification of blood culture isolates was conducted using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) on the Vitek 2 system (BioMérieux, Craponne, France). Antimicrobial susceptibility testing was executed via the Vitek 2 system according to the Clinical and Laboratory Standards Institute (CLSI) M07 guidelines (8). Antibiotic panel for gram-negative bacteria encompassed Ertapenem, Ceftazidime/Avibactam, Piperacillin/Tazobactam, Cefepime, Ceftazidime, Tigecycline, Gentamicin, Ampicillin/Sulbactam, Ceftriaxone, Ciprofloxacin, Imipenem, and Trimethoprim/Sulfamethoxazole. For gram-positive bacteria, the panel included Teicoplanin, Trimethoprim/Sulfamethoxazole, Penicillin, Oxacillin (to identify methicillin-resistant staphylococci), Clindamycin, Linezolid, Erythromycin, and Daptomycin. These antibiotic panels were customized according to established recommendations for each bacterial species. All isolates were subjected to a comprehensive range of antimicrobial agents to thoroughly assess their susceptibility profiles. Minimum inhibitory concentration (MIC) values were interpreted as susceptible, intermediate, or resistant, conforming to the clinical breakpoints outlined in the CLSI M100 document.

Results

In this study, we first examined 230 patients admitted due to SARS-CoV-2 infections, with blood cultures performed between June 1, 2021, and June 30, 2022. Of these, 41 patients (17.8%) exhibited at least one positive blood culture during their hospitalization, indicating bloodstream infections. The majority of these infected patients were male aged 65 or older. The patient demographic details (age distribution and sex) are presented in Table I. Of note, we also collected and analyzed key biomarkers, including WBC count, CRP and PCT levels. The results of the one-way ANOVA are depicted in Table II. Patients with bloodstream infections demonstrated significantly higher levels of WBC, CRP and PCT as compared to those patients without bloodstream infections (11,114 cells/mm3, 12.2 mg/l, and 6.56 ng/ml versus 8,815 cells/mm3, 5.23 mg/l, and 1.37 mg/l). The p-values for the differences in all three biomarkers between the two groups were less than 0.05, indicating statistical significance.

Table I. Demographics (age and sex) of hospitalized COVID-19 patients.

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Table II. Inflammatory biomarker profiles of the hospitalized COVID-19 patients.

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WBC: White blood cells; CRP: C-reactive protein; PCT: procalcitonin.

Among the 41 hospitalized patients who developed bloodstream infections, four cases involved bloodstream infections with two distinct pathogens, leading to the identification of a total of 45 isolates. These comprised 31 gram-positive bacteria isolates (69%), 13 gram-negative bacteria isolates (29%) and 1 fungus isolate (2%). Although the focus was on the most prevalent organisms, Figure 1 displays the broad spectrum of bacterial and fungal pathogens associated with secondary bloodstream infections in the context of viral respiratory illnesses. As COVID-19 evolves into an endemic disease, the changing epidemiology may introduce new and atypical organisms that necessitate vigilant surveillance. The gram-negative bacteria identified included Acinetobacter baumannii (15%), Acinetobacter pittii (8%), Acinetobacter ursingii (8%), Escherichia coli (38%), Klebsiella pneumoniae (15%), Proteus mirabillis (8%), and Salmonella Group D1 (8%). The gram-positive bacteria encompassed Enterococcus faecium (13%), Enterococcus raffinosus (3%), Kocuria spp. (3%), Staphylococcus aureus (10%), Staphylococcus capitis (7%), Staphylococcus epidermidis (7%), Staphylococcus haemolyticus (3%), Staphylococcus non-aureus (48%), Staphylococcus saprophyticus (3%), and Streptococcus mitis group (3%). The sole fungus isolated was Candida albicans.

Figure 1. Causative organisms of bloodstream infection in patients with COVID-19. (A) Distribution of organisms implicated in bloodstream infections among patients with COVID-19; (B) profiles of gram-negative bacteria; and (C) profile of gram-positive bacteria in bloodstream infections of COVID-19 patients.

Figure 1

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Antimicrobial susceptibility testing was performed on all 44 bacterial isolates, with specific tests tailored to each species. For gram-negative bacteria, the antibiotic panel included Ertapenem, Ceftazidime/Avibactam, Piperacillin/Tazobactam, Cefepime, Ceftazidime, Tigecycline, Gentamicin, Ampicillin/ Sulbactam, Ceftriaxone, Ciprofloxacin, Imipenem, and Trimethoprim/Sulfamethoxazole. The antibiotic panel for gram-positive bacteria consisted of Teicoplanin, Trimethoprim/ Sulfamethoxazole, Penicillin, Oxacillin, Clindamycin, Linezolid, Erythromycin, and Daptomycin. We next categorized seven reported gram-negative bacteria species into five groups, with three Acinetobacter species considered as a single category. Similarly, the 10 gram-positive bacteria species identified were grouped into five categories, where two Enterococcus species were combined, and all Staphylococcus species other than Staphylococcus aureus were collectively analyzed as Staphylococcus non-aureus.

The resistance profile of gram-negative bacteria, as presented in Table III, demonstrates that subsets of all species tested exhibited susceptibility to Trimethoprim/ Sulfamethoxazole and Ceftazidime/Avibactam. Nonetheless, one or more species were not susceptible to the remaining antibiotics. Predominantly, gram-negative bacteria showed complete susceptibility to at least two antibiotics. Of note, all isolated Klebsiella pneumoniae and Acinetobacter spp. were only susceptible to Tigecycline. Collectively analyzing the data, gram-negative bacteria demonstrated the greatest susceptibility to Tigecycline (92%), followed by Ceftazidime/Avibactam (77%), Piperacillin/Tazobactam (69%), Imipenem and Cefepime (both at 62%). Susceptibility to Ceftazidime was 58%, while that to Trimethoprim/ Sulfamethoxazole, Ceftriaxone, Ampicillin/Sulbactam, Gentamicin and Ertapenem was uniformly 54%. The least susceptibility was observed with Ciprofloxacin (45%). Furthermore, certain Acinetobacter species were susceptible to all the tested antibiotics, except Ertapenem, and yet all were susceptible to Tigecycline. Some isolates of Escherichia coli were susceptible to all antibiotics in the panel, with universal susceptibility to Imipenem, Tigecycline, Ceftazidime/Avibactam, and Ertapenem. All isolates of Klebsiella pneumoniae were susceptible to Tigecycline, with a portion showing susceptibility to Trimethoprim/Sulfamethoxazole and Ceftazidime/Avibactam. Proteus mirabilis was susceptible to all antibiotics, except for Imipenem and Tigecycline. Lastly, Salmonella exhibited susceptibility to all antibiotics examined in this study, with sole exception of Gentamicin.

Table III. Antimicrobial susceptibility profiles of susceptible gram-negative bacteria in bloodstream infections of COVID-19 patients.

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The susceptibility was interpreted as susceptible, intermediate, or resistant based on the clinical breakpoints as outlined in the CLSI M100 document.

The resistance profile of gram-positive bacteria is outlined in Table IV. All isolates showed susceptibility to Daptomycin and Linezolid, where at least a portion of each category was susceptible to all other tested antibiotics except Penicillin and Erythromycin, which were ineffective against S. aureus, eliciting complete resistance. Collectively, gram-positive bacteria elicited the highest susceptibility to Daptomycin and Linezolid (100 %), followed by Vancomycin (94%), Teicoplanin (92%), Trimethoprim/Sulfamethoxazole (80%), Clindamycin (54%), Erythromycin (44%), Oxacillin (25%), and Penicillin (10%). All Enterococcus isolates were 100% susceptible to Linezolid and Trimethoprim/Sulfamethoxazole, while Kocuria demonstrated susceptibility to Erythromycin, Clindamycin, Penicillin, and Vancomycin. In addition, Staphylococcus aureus was susceptible to Daptomycin, Linezolid, Teicoplanin and Vancomycin but not to Erythromycin. In contrast, Staphylococcus non-aureus was 100% susceptible not only to Daptomycin, Linezolid, but also to Teicoplanin and Vancomycin. In addition, the Streptococcus mitis group was entirely susceptible to Linezolid, Clindamycin and Vancomycin, but not to Penicillin.

Table IV. Resistance profiles of gram-positive bacteria in bloodstream infections of COVID-19 patients.

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The susceptibility was interpreted as susceptible, intermediate, or resistant, in accordance with the clinical breakpoints as outlined in the CLSI M100 document.

Discussion

As COVID-19 transitions globally from a pandemic to an endemic state, healthcare-associated infections remain a significant risk. Our findings contribute essential insights into the microbiological landscape, critically informing antibiotic therapy choices in the context of escalating antimicrobial resistance and diminishing vaccine efficacy over time. This is especially pertinent with the likelihood of periodic COVID-19 surges with potentially exacerbating severe outcomes through secondary infections. Our study establishes an important baseline for regional epidemiological data that can serve for continued surveillance, which will be a key to guiding treatment and infection control strategies as the COVID-19 endemic phase unfolds. In our analysis of the 230 patients, 41 (17.8%) developed bloodstream infections during hospitalization, surpassing the 8.5-9.4% reported in previous studies (9). This discrepancy likely stems from variations in patient demographics and local epidemiology. Our data in Figure 1 highlights a diverse range of potential pathogens that have been associated with secondary bloodstream infections in the literature, underscoring the necessity for ongoing surveillance to identify and adapt to changing microbiological trends as COVID-19 evolves.

Further, our data in Table I reveal older age and male sex as prevalent characteristics among patients with bloodstream infections, aligning with existing literature that identifies these factors as increasing the risk of severe COVID-19 and secondary bloodstream infections (10-12), further complicating their clinical course (13). It is thus crucial for healthcare providers to prioritize tailored strategies and vigilant monitoring for the risk factors when treating older male patients with COVID-19 to lessen clinical complications (7).

COVID-19 pandemic has potentially accelerated the emergence and spread of antimicrobial resistance (14,15), highlighting the urgent need for careful antibiotic surveillance and stewardship. The antimicrobial susceptibility tests conducted in our study shed light on a shifted resistance profile amongst the isolated microorganisms. For instance, gram-negative bacteria were found to be most vulnerable to certain antibiotics (such as Tigecycline, Ceftazidime/Avibactam, and Piperacillin/Tazobactam), while gram-positive bacteria were discovered to be most susceptible to a different set of antibiotics (such as Daptomycin, Linezolid, and Vancomycin). Gram-positive bacteria predominated (69%), followed by gram-negative bacteria (29%) and fungi (2%) among the causative organisms of bloodstream infections in our cohort. Since the most frequently identified gram-negative bacteria were E. coli and K. pneumoniae (16), while the most frequently identified gram-positive bacteria were S. aureus and non-aureus Staphylococci (17), it is important to select appropriate empirical antibiotic therapy for optimal patient outcomes and combating antimicrobial resistance. Furthermore, the elevated levels of WBC, CRP, and PCT that were significantly associated with bloodstream infections compared to those without in our cohorts suggested that these biomarkers could be potentially useful in early detection and interventions for patients with COVID-19 who are at risk for bloodstream infections. These results are in line with recent studies that correlate the rising incidence of bloodstream infections to leukocyte counts (16), levels of PCT and CRP (18).

Our study has identified significant carbapenem resistance in K. pneumoniae, a notable public health concern in Taiwan and the world. The emergence of carbapenemase-producing strains that confer resistance to a broad spectrum of β-lactam antibiotics exacerbates the challenge in currently available therapeutic options for K. pneumoniae-specific infections (19). As revealed in Table III, Tigecycline remained the only antibiotic option to which K. pneumoniae is 100% susceptible. Although the prevalence of carbapenem-resistant K. pneumoniae strains varies geographically, the association between alcoholism and community-acquired K. pneumoniae-induced pneumonia has been identified and linked to a distinctive species of K. pneumoniae that results in liver abscess and high mortality rates in Taiwan (20). Since the detection of carbapenem resistance in K. pneumoniae can technically be challenging through phenotypic antibiotic susceptibility tests alone, there is a need to improve novel molecular detection methods to support infection control measures (21,22). Data presented in our study for gram-negative bacteria thus deepened the current understanding in the epidemiology, clinical patterns and risk factors associated with carbapenem-resistant K. pneumoniae infections. Further research is needed to improve detection methods, develop effective preventive measures, and identify novel treatment options to combat this public health threat.

The observations in atypical cell count profiles in some patients of our cohorts that implicate the hematological manifestations of COVID-19 are consistent with reported atypical hematological profiles of SARS-CoV-2 infections (23). This variability emphasizes the importance of future research to differentiate typical and atypical hematological profiles and their implications for secondary infection risks and prognosis, especially in high-risk hospitalized patients. Our findings on the distinct susceptibility patterns of gram-negative and gram-positive strains highlight the necessity of accurate identification of bacterial infection for effective treatment selection. The results cast a spotlight on the significant incidence of bloodstream infections in hospitalized patients with COVID-19, with a particular emphasis on the presence of gram-positive bacteria that elicits a discernible alteration in resistance patterns. The study serves as a clarion call for medical professionals to focus on early identification of patients most susceptible to bloodstream infections. The organisms identified in the study, both at the genera and species levels, are well-acknowledged for being prime culprits in nosocomial or hospital-acquired infections environments, reflecting the importance of continuous monitoring and control measures. Moving forward, there is an expressed intention to incorporate epidemiological data from the hospital setting prior to the COVID-19 pandemic in subsequent research efforts (24,25). By deepening our understanding of these infections, especially in the context of COVID-19, the healthcare community can work towards better patient care and a more robust response to the ongoing challenges posed by antimicrobial resistance (26). In summary, the study offers valuable insights into the bloodstream infections among hospitalized patients with COVID-19 and stresses the need for a tailored approach to diagnosis and treatment for future investigations.

Conclusion

In conclusion, our study on hospitalized patients with COVID-19 in central Taiwan provides crucial insights into the epidemiology and microbial spectrum of bloodstream infections. In the analysis of 230 patients, we uncovered significant incidence of infections predominantly caused by gram-positive and gram-negative bacteria, along with fungi. This high prevalence underlines the importance of precise diagnostic and therapeutic strategies in the face of escalating antimicrobial resistance. Further, our findings also highlight the challenge and critical public health concern posed by the prevalence of carbapenem-resistant K. pneumoniae, emphasizing the need for innovative detection methods using biomarkers, such as WBC, CRP and PCT for early detection and intervention. As COVID-19 transitions from pandemic to endemic, our research underscores the atypical hematological manifestations of COVID-19 and their correlation with secondary infections, providing vital knowledge for improving patient healthcare in the era of evolving infectious diseases with antimicrobial resistance.

Funding

This work was supported by Taichung Veterans General Hospital (TCVGH-1115801D).

Conflicts of Interest

The Authors declare no conflicts of interest in relation to this study.

Authors’ Contributions

Conceptualization: Yu-Hsin Tsai and Chih-Jung Chen; Data curation: Po-Yu Liu and Jiunn-Min Wang; Formal analysis: Po-Yu Liu and Jiunn-Min Wang; Funding acquisition: Jiunn-Min Wang; Investigation: Po-Yu Liu and Jiunn-Min Wang; Resources: Tai-Cheng Hou and Jiunn-Min Wang; Supervision: Yu- Hsin Tsai; Validation: Yu- Hsin Tsai, Tai-Cheng Hou, and Chih-Jung Chen; Writing: Po-Yu Liu.

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