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Infections and antimicrobial prescribing in patients hospitalized with coronavirus disease 2019 (COVID-19) during the first pandemic wave

Published online by Cambridge University Press:  17 April 2023

Lynn ChanOpen the ORCID record for Lynn Chan[Opens in a new window],
Simran GuptaOpen the ORCID record for Simran Gupta[Opens in a new window],
Alicia J. SaccoOpen the ORCID record for Alicia J. Sacco[Opens in a new window],
Sabirah N. Kasule,
Hally Chaffin,
Fionna F. FellerOpen the ORCID record for Fionna F. Feller[Opens in a new window],
Lanyu MiOpen the ORCID record for Lanyu Mi[Opens in a new window],
Elisabeth S. LimOpen the ORCID record for Elisabeth S. Lim[Opens in a new window] and
Maria Teresa SevilleOpen the ORCID record for Maria Teresa Seville[Opens in a new window]
Lynn Chan*
Affiliation:
Department of Pharmacy, Ronald Reagan UCLA Medical Center, Los Angeles, California
Simran Gupta
Affiliation:
Department of Internal Medicine, Mayo Clinic Hospital, Phoenix, Arizona
Alicia J. Sacco
Affiliation:
Department of Pharmacy, Mayo Clinic Hospital, Phoenix, Arizona
Sabirah N. Kasule
Affiliation:
Department of Quantitative Health Sciences, Division of Clinical Trials and Biostatistics, Mayo Clinic Arizona, Scottsdale, Arizona
Hally Chaffin
Affiliation:
Department of Internal Medicine, Mayo Clinic Hospital, Phoenix, Arizona
Fionna F. Feller
Affiliation:
Division of Infectious Diseases, Yale New Haven Hospital, New Haven, Connecticut
Lanyu Mi
Affiliation:
Department of Quantitative Health Sciences, Division of Clinical Trials and Biostatistics, Mayo Clinic Arizona, Scottsdale, Arizona
Elisabeth S. Lim
Affiliation:
Department of Quantitative Health Sciences, Division of Clinical Trials and Biostatistics, Mayo Clinic Arizona, Scottsdale, Arizona
Maria Teresa Seville
Affiliation:
Division of Infectious Diseases, Mayo Clinic Hospital, Phoenix, Arizona
*
Author for correspondence: Lynn Chan, Department of Pharmacy, Ronald Reagan UCLA Medical Center, 757 Westwood Plaza, Ste B140. Los Angeles, CA 90095. E-mail: lynnchan@mednet.ucla.edu

Abstract

Objective:

To evaluate the rate of coinfections and secondary infections seen in hospitalized patients with COVID-19 and antimicrobial prescribing patterns.

Methods:

This single-center, retrospective study included all patients aged ≥18 years admitted with COVID-19 for at least 24 hours to a 280-bed, academic, tertiary-care hospital between March 1, 2020, and August 31, 2020. Coinfections, secondary infections, and antimicrobials prescribed for these patients were collected.

Results:

In total, 331 patients with a confirmed diagnosis of COVID-19 were evaluated. No additional cases were identified in 281 (84.9%) patients, whereas 50 (15.1%) had at least 1 infection. In total, of 50 patients (15.1%) who were diagnosed with coinfection or secondary infection had bacteremia, pneumonia, and/or urinary tract infections. Patients who had positive cultures, who were admitted to the ICU, who required supplemental oxygen, or who were transferred from another hospital for higher level of care were more likely to have infections. The most commonly used antimicrobials were azithromycin (75.2%) and ceftriaxone (64.9%). Antimicrobials were prescribed appropriately for 55% of patients.

Conclusions:

Coinfection and secondary infections are common in patients who are critically ill with COVID-19 at hospital admission. Clinicians should consider starting antimicrobial therapy in critically ill patients while limiting antimicrobial use in patients who are not critically ill.

Information

Type
Original Article
Information
Antimicrobial Stewardship & Healthcare Epidemiology , Volume 3 , Issue 1 , 2023, e75
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

The coronavirus disease 2019 (COVID-19) pandemic, caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), challenged healthcare systems to adapt to evolving infection prevention and control and therapeutic recommendations and diverted antimicrobial stewardship efforts to the pandemic response. At the start of the pandemic, healthcare providers were prescribing antibiotics based on evidence (1) that 18%–30% of bacterial coinfections co-occur with viral respiratory infections such as severe influenza, Reference Morens, Taubenberger and Fauci1–Reference Gill, Sheng and Ely4 (2) that morbidity and mortality is high in patients with bacterial coinfections with severe influenza, and (3) that differentiating SARS-CoV-2 infection from bacterial pneumonia is challenging because patients often present with similar symptoms and abnormalities on chest imaging. Reference Liu, Ling and Wong5

As the pandemic continued, studies showed a low prevalence of bacterial coinfection in patients with COVID-19. In a meta-analysis of 24 studies by Langford et al, Reference Langford, So and Raybardhan6 ∼3.5% of patients with COVID-19 had bacterial coinfection at presentation and 14.3% of patients developed a secondary bacterial infection. Reference Langford, So and Raybardhan6 In a review of 18 studies by Rawson et al, Reference Rawson, Moore and Zhu7 only 8% of patients had bacterial coinfections at hospital admission; however, 72% received antimicrobial therapy.

Also, critically ill patients with COVID-19 are susceptible to the development of secondary bacterial and fungal infections due to prolonged hospitalization, presence of invasive medical devices, and drug-induced immunosuppression. In a multicenter study by Rouze et al, Reference Rouze, Martin-Loeches and Povoa8 the incidence of ventilator-associated pneumonia (VAP) in patients with COVID-19 was 50%. Reference Rouze, Martin-Loeches and Povoa8 In another multicenter study by Russell et al, Reference Russell, Fairfield and Drake9 70.6% of patients with COVID-19 had secondary infections and the antimicrobial prescribing rate was 85.2% during the study period. Reference Russell, Fairfield and Drake9

The disproportionally high rate of antimicrobial prescribing in the setting of a low prevalence of bacterial coinfection places a high burden on antimicrobial stewardship programs, places patients at avoidable risk of toxicity from antibiotics, and can lead to antimicrobial resistance. Reference Ripa, Galli and Poli10

In this study, we characterized the rate of coinfections and secondary infections in hospitalized patients with COVID-19, with a focus on clinical outcomes and antimicrobial utilization. We sought to determine appropriate or inappropriate use of antimicrobial therapy.

Methods

This single-center, retrospective cohort study included all patients aged ≥18 years admitted between March 1, 2020, and August 31, 2020, to a 280-bed, academic, tertiary-care hospital. All patients hospitalized from late March 2020 onward had nasopharyngeal swabs for SARS CoV-2 polymerase chain reaction (PCR) testing on admission and all those who tested positive and were hospitalized for at least 24 hours were included.

Data obtained from the medical record included demographics, comorbidities, oxygenation status, chest imaging, indwelling medical devices, microbiology, laboratory results at admission, medications including COVID-19 therapy immunosuppressants, and antimicrobials within 30 days of admission and during the hospitalization, mortality, and readmission within 30 days after hospital discharge.

Microbiology results from blood, respiratory, and urinary specimens were included. Antimicrobial susceptibility testing was performed with BD Phoenix automated identification and susceptibility testing system (Becton-Dickinson, Franklin Lakes, NJ).

Patients with organisms identified on microbiologic testing of blood, respiratory, and urine, specimens were reviewed for the presence of infection using the 2020 National Healthcare Safety Network (NHSN) Patient Safety Component Manual definitions of bacteremia, pneumonia, and urinary tract infections. 11 Coinfection was defined as infection onset before hospital day 3 and secondary infection was defined as infection with onset on hospital day 3 or later. Coinfections and secondary infections were aggregated in the analysis because of the small number of infections.

Antimicrobial use was deemed inappropriate when antibiotics were used for colonization or contaminated cultures, when there was a lack of de-escalation following susceptibility results, or if an antimicrobial prescribed was not effective for the isolated pathogen.

The study was approved by the Mayo Clinic Institutional Review Board.

Statistical analysis

Patient characteristics were summarized as median with interquartile range for continuous variables or count with percentage for categorical variables. Comparisons were made between groups using Wilcoxon rank-sum test or the Fisher exact test as appropriate. Multivariable logistic regression was used to investigate the association between the outcome of infection identification and patient clinical characteristics factors. The analysis was conducted using RStudio version 4.0.3 software (RStudio Team, PBC, Boston, MA, 2022). All tests were 2-sided and P values <.05 were considered significant.

Results

In total, 331 patients with confirmed diagnosis of COVID-19 were evaluated (Fig. 1). The median patient age was 60.0 (IQR, 48.0–72.0) years and 202 (61.0%) patients were male. Moreover, 243 patients (73.6%) were admitted to the hospital from the emergency department, and 80 (24.2%) were transferred from outside hospitals (OSH) for higher level of care (P < .001) (Table 1). There were no significant differences in comorbidities such as diabetes mellitus, immunodeficiency, transplantation or underlying structural lung disease between patients with or without infection. Patients who were on steroids for any reason prior to admission were more likely to have an infection (36% vs 14.9%; P = .001).

Fig. 1.

Patient selection.

Table 1.

Baseline Characteristics of Patients With or Without Infection

Note. CRP, C-reactive protein; ECMO, extracorporeal membrane oxygenation; ED, emergency department; HFNC, high-flow nasal cannula; ICU, intensive care unit; IQR, interquartile range; LFNC, low-flow nasal cannula; WBC, white blood cells.

a Other immunosuppressant agents include: abatacept, adalimumab, anakinra, azathioprine, certolizumab, IV/PO chemotherapy, cyclosporine, etanercept, everolimus, infliximab, leflunomide, mycophenolate, natalizumab, rituximab, sirolimus, tacrolimus, tofacitinib, vedolizumab

Of the 331 patients, 281 (84.9%) had no coinfection or secondary infection and 50 (15.1%) had at least 1 infection. Of the 50 patients with infections, 17 (34.0%) were admitted to the ICU: 13 (26.0%) in the progressive care unit and 20 (40.0%) on the medical floor. Also, 25 patients (7.6%) had coinfections, 24 patients (7.3%) had secondary infections, and 1 patient (0.3%) had both a coinfection and a secondary infection. Patients who were admitted to the ICU were more likely to have an infection (P < .001). Of the 281 patients with no infection, 65% were admitted to the medical floor and 6.4% were admitted to the ICU. The median ICU length of stay was significantly longer for patients with infections at 28.0 days (IQR, 16.0–51.0) compared to patients without infection at 6.0 days (IQR, 2.5–12.0; P < .001).

On admission, compared to patients with no infection, patients with infections had a greater requirement for supplemental oxygenation (74.0% with infection vs 60% without infection) and abnormal chest imaging (92.0% with infection vs 78.9% without infection). These patients also had more invasive medical devices: urinary catheters (54.0% with infection vs 23.5% without infection), central venous catheters (50.0% with infection vs 14.6% without infection), and endotracheal tubes (46.0% with infection vs 7.1% without infection; P < .001). Length of hospital stay was longer in patients with infections compared to those without: 20.5 days (IQR, 6.0–35.0) versus 6.0 days (IQR, 3.0–10.0 days; P < .001) (Table 2). Patients who had infections were more likely to be readmitted to the hospital within 30 days of discharge (20.0% vs 9.3%; P = .05).

Table 2.

Outcomes of Patients With or Without Infection

Note. IQR, interquartile range; ICU, intensive care unit.

a COVID-19 therapies include convalescent plasma, dexamethasone, hydroxychloroquine, lenzilumab, remdesivir, and tocilizumab.

Moreover, 56 patients (17.0%) received antibiotics within 30 days prior to admission for COVID-19 and of those, 16 (32.7%) patients had infection during hospitalization. The most commonly prescribed antibiotics before and during hospitalization were azithromycin and ceftriaxone (Fig. 2).

Fig. 2.

Most frequently prescribed antimicrobials within 30 days prior to admission.

The most common types of infection were ventilator-associated pneumonia (36.6%), followed by urinary tract infection (22.0%), community-acquired pneumonia (19.5%), and bacteremia (14.6%) (Fig. 3).

Fig. 3.

Infectious disease syndromes identified. Note. CAUTI, catheter-associated UTI; CLABSI, central-line–associated bloodstream infection; CAP, community-acquired pneumonia; HAP, hospital-acquired pneumonia; UTI, urinary tract infection; VAP, ventilator-associated pneumonia.

In total, 66 patients (19.9%) had positive cultures. Among them, 25 patients (8.9%) without an infection had at least 1 positive culture, and 41 patients (82%) with an infection had at least 1 positive culture along with criteria for infection (P < .001). The most common organisms identified in patients who did not have infection were Candida albicans, coagulase-negative Staphylococci (CoNS) and Enterococcus faecalis whereas Klebsiella pneumoniae, Escherichia coli, Staphylococcus aureus (methicillin resistant and methicillin susceptible), and CoNS were the most common organisms identified in patients who had infections (Fig. 4).

Fig. 4.

Organisms identified from cultures.

The prevalence of antibiotic use was 100% in those with infections and 68.3% in patients without infections. Patients with coinfections or secondary infections were treated with a median of 5.0 antimicrobials compared to 2.0 in patients without infection (P < .001). The most commonly used antimicrobials were azithromycin (75.2%) and ceftriaxone (64.9%) in patients with or without infection. Vancomycin, cefepime, and meropenem were administered to 60.0%, 42.0% and 34.0% of patients, respectively, who had coinfection or secondary infection (Table 3).

Table 3.

Commonly Used Antimicrobial Agents During Hospitalization

Note. TMP/SMX, trimethoprim-sulfamethoxazole; IV, intravenous.

Overall, 154 positive cultures were reviewed to determine the appropriateness of antimicrobial use. Among these cultures, 100 were from patients with infections and 54 were from patients without infection. Antimicrobials were prescribed inappropriately for the pathogen identified in 45 patients (45%) with infections, and the most common reasons were lack of de-escalation, treatment of colonization, and contaminated cultures.

Discussion

In this study, most patients had no infection, but we identified coinfections and secondary bacterial infections in 50 hospitalized patients (15.1%) with COVID-19 during the first wave of the COVID-19 pandemic. Of the 50 COVID-19 patients identified with infections, 25 (7.6%) had coinfection and 24 (7.3%) had secondary infection; 1 patient (0.3%) was identified as having both coinfection and secondary infections. These results are similar to reported rates from 6% to 29%. Reference Langford, So and Raybardhan6,Reference Ripa, Galli and Poli10,Reference Garcia-Vidal, Sanjuan and Moreno-Garcia12 Similarly, Westblade et al Reference Westblade, Simon and Satlin13 reported that <4% of patients with COVID-19 had documented bacterial coinfections on hospital admission. Reference Westblade, Simon and Satlin13 Ripa et al Reference Ripa, Galli and Poli10 found an overall 28-day cumulative incidence of secondary infections of ∼16.4%, with more bloodstream infections (7.9%) than respiratory tract infections (3.0%). Reference Ripa, Galli and Poli10

Severe hypoxemia, severe lymphopenia, need for intensive care in the first 48 hours after hospital admission, and receipt of steroids have been reported to be predictive factors for secondary infections in patients with COVID-19. Reference Ripa, Galli and Poli10,Reference Nasir, Rehman and Omair14 In our study, COVID-19 patients with the following factors were more likely to have infections: those who were transferred from OSH for higher level of care, those who required supplemental oxygenation with HFNC or mechanical ventilation at admission, those who had invasive medical devices, those who had consolidation or ground-glass opacities on initial imaging, and those who had longer lengths of hospitalization.

We did not find a difference in mortality during hospitalization in patients with COVID-19 with or without infection. This may be because of thorough investigations and effective therapy provided during hospitalization. However, we did find a higher 30-day readmission in patients who had infections, which could be related to patient comorbidities.

Also 17.0% of patients had antimicrobial exposure within 30 days prior to hospitalization, and azithromycin was the most prescribed agent. Of the patients who had antimicrobial exposure 30 days prior to admission, 28.6% had infection during hospitalization for COVID-19. Patients hospitalized with COVID-19 who had no coinfections were started on empiric azithromycin (76.0%) and ceftriaxone (68.8%). This finding is similar to those reported by Vaughn et al, Reference Vaughn, Gandhi and Petty15 which showed that 56.6% were treated with early empiric antibacterial therapy despite only finding 3.5% of patients with community-onset bacterial coinfection. Routine use of empiric antibiotics for COVID-19 patients has since been discouraged on institutional protocols, with improvement in antimicrobial prescribing.

Broad-spectrum antimicrobials were utilized commonly in patients with infections. In our study, 45% of antimicrobials were inappropriately prescribed. Guidelines recommend broad-spectrum empiric antimicrobials in critically ill patients; however, antimicrobial therapy should be re-evaluated as microbiology results become available. With the ongoing pandemic, it will be necessary for antimicrobial stewardship programs to monitor the utilization of antimicrobial agents to ensure appropriate antimicrobial use in patients hospitalized with COVID-19.

Our study had several limitations. This study was conducted retrospectively, and the results are subject to potential sources of bias and confounding inherent to retrospective studies. This study was single-center retrospective study conducted at a tertiary-care hospital during the first wave of the COVID-19 pandemic. These findings may not be generalizable because of variations in microbiological epidemiology and because management strategies have evolved. Only patients who had positive cultures to determine coinfection and secondary infections were evaluated, which may have underrepresented the true infection rates. Timing of initiation and duration of antimicrobials, the frequency of antimicrobial changes during treatment and rates of resistance were not evaluated in this study. Finally, we utilized CDC NHSN surveillance definitions, which may not reflect clinical practice.

In conclusion, whereas most of our patients did not have any infection, coinfections and secondary infections were diagnosed in 15.1% of hospitalized patients with COVID-19. COVID-19 patients with the following factors had more infections: those who needed ICU admission, those who required supplemental oxygen, those who had consolidation or ground-glass opacities on imaging, underwent prolonged hospitalization, and those who had invasive medical devices. Initiating empiric antimicrobials may be reasonable for these patients. Further study of infection and antimicrobial use in patients hospitalized for COVID-19 could help inform appropriate antimicrobial stewardship efforts in these patients.

Acknowledgments

Financial support

No financial support was provided relevant to this article.

Conflict of interest

All authors report no conflict of interest relevant to this article.

References

Morens, DM, Taubenberger, JK, Fauci, AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008;198:962–970.CrossRefGoogle ScholarPubMed
Martin-Loeches, I, Sanchez-Corral, A, Diaz, E, et al. Community-acquired respiratory coinfection in critically ill patients with pandemic 2009 influenza A(H1N1) virus. Chest 2011;139:555–562.Google ScholarPubMed
Rise, TW, Rubinson, L, Uyeki, TM, et al. Critical illness from 2009 pandemic influenza A virus and bacterial coinfection in the United States. Crit Care Med 2012;40:1487–1498.Google Scholar
Gill, JR, Sheng, ZM, Ely, SF, et al. Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch Pathol Lab Med 2010;134:235–243.CrossRefGoogle ScholarPubMed
Liu, Y, Ling, L, Wong, SH, et al. Outcomes of respiratory viral-bacterial coinfection in adult hospitalized patients. EClinicalMedicine 2021;37:100955.CrossRefGoogle ScholarPubMed
Langford, BJ, So, M, Raybardhan, S, et al. Bacterial coinfection and secondary infection in patients with COVID-19: a living rapid review and meta-analysis. Clin Microbiol Infect 2020;26:1622–1629.CrossRefGoogle ScholarPubMed
Rawson, TM, Moore, LS, Zhu, N, et al. Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to support COVID-19 antimicrobial prescribing. Clin Infect Dis 2020;71:2459–2468.Google ScholarPubMed
Rouze, A, Martin-Loeches, I, Povoa, P, et al. Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study. Intensive Care Med 2021;47:188–198.CrossRefGoogle ScholarPubMed
Russell, CD, Fairfield, CJ, Drake, TM, et al. Coinfections, secondary infections, and antimicrobial use in patients hospitalised with COVID-19 during the first pandemic wave from the ISARIC WHO CCP-UK study: a multicentre, prospective cohort study. Lancet Microbe 2021;2:e354–e365.CrossRefGoogle ScholarPubMed
Ripa, M, Galli, L, Poli, A, et al. Secondary infections in patients hospitalized with COVID-19: incidence and predictive factors. Clin Microbiol Infect 2021;27:451–457.CrossRefGoogle ScholarPubMed
The National Healthcare Safety Network (NHSN). Patient safety component manual. Centers for Disease Control and Prevention website. https://www.cdc.gov/nhsn/pdfs/validation/2020/pcsmanual_2020-508.pdf. Published 2020. Accessed March 21, 2023.Google Scholar
Garcia-Vidal, C, Sanjuan, G, Moreno-Garcia, E, et al. Incidence of coinfections and superinfections in hospitalized patients with COVID-19: a retrospective cohort study. Clin Microbiol Infect 2021;27:83–88.CrossRefGoogle ScholarPubMed
Westblade, L, Simon, MS, Satlin, MJ. Bacterial coinfections in coronavirus disease 2019. Trends Microbiol 2021;29:930–941.CrossRefGoogle ScholarPubMed
Nasir, N, Rehman, F, Omair, SF. Risk factors for bacterial infections in patients with moderate to severe COVID-19: a case–control study. J Med Virol 2021;93:4564–4569.CrossRefGoogle ScholarPubMed
Vaughn, VM, Gandhi, TN, Petty, LA, et al. Empiric antibacterial therapy and community-onset bacterial coinfection in patients hospitalized with coronavirus disease 2019 (COVID-19): a multihospital cohort study. Clin Infect Dis 2021;72:e533–e541.CrossRefGoogle Scholar
Russell, CD, Fairfield, CJ, Drake, TM, et al. Coinfections, secondary infections, and antimicrobial use in patients hospitalised with COVID-19 during the first pandemic wave from the ISARIC WHO CCP-UK study: a multicentre, prospective cohort study. Lancet Microbe 2021;2:e354–e365.CrossRefGoogle ScholarPubMed
Antibiotic Use in the United States, 2021 Update: Progress and Opportunities. Atlanta, GA: US Department of Health and Human Services, CDC; 2021.Google Scholar
Moreno-Garcia, E, Puerta-Alclde, P, Letona, L, et al. Bacterial coinfection at hospital admission in patients with COVID-19. Int J Infect Dis 2022;118:197–202.CrossRefGoogle ScholarPubMed
Sreenath, K, Batra, P, Vinayaraj, EV, et al. Coinfections with other respiratory pathogens among patients with COVID-19. Microbiol Spectr 2021;9:e0016321.CrossRefGoogle ScholarPubMed
Moreno-Torres, V, de Mendoza, CD, de la Fuente, S, et al. Bacterial infections in patients hospitalized with COVID-19. Intern Emerg Med 2022;17:431–438.CrossRefGoogle ScholarPubMed
Goncalves Mendes Neto, A, Lo, KB, Wattoo, A, et al. Bacterial infections and patterns of antibiotic use in patients with COVID-19. J Med Virol 2021;93:1489–1495.CrossRefGoogle ScholarPubMed
Karami, Z, Knoop, BT, Dofferhoff, ASM, et al. Few bacterial coinfections but frequent empiric antibiotic use in the early phase of hospitalized patients with COVID-19: results from a multicentre retrospective cohort study in The Netherlands. Infect Dis (Lond) 2021;53:102–110.CrossRefGoogle ScholarPubMed
Hughes, S, Troise, O, Donaldson, H, Mughal, N, Moore, LSP. Bacterial and fungal coinfection among hospitalized patients with COVID-19: a retrospective cohort study in a UK secondary-care setting. Clin Microbiol Infect 2020;26:1395–1399.CrossRefGoogle Scholar
Wang, L, Amin, AK, Khanna, P, et al. An observational cohort study of bacterial coinfection and implications for empirical antibiotic therapy in patients presenting with COVID-19 to hospitals in North West London. J Antimicrob Chemother 2021;76:796–803.CrossRefGoogle ScholarPubMed
Lehmann, CJ, Pho, MT, Pitrak, D, Ridgway, JP, Pettit, NN. Community-acquired coinfection in coronavirus disease 2019: a retrospective observational experience. Clin Infect Dis 2021;72:1450–1452.CrossRefGoogle ScholarPubMed
Bhatt, PJ, Shiau, S, Brunetti, L, et al. Risk factors and outcomes of hospitalized patients with severe coronavirus disease 2019 (COVID-19) and secondary bloodstream infections: a multicenter case-control study. Clin Infect Dis 2021;72:e995–e1003.CrossRefGoogle ScholarPubMed
Cheng, LS, Chau, SK, Tso, EY, et al. Bacterial coinfections and antibiotic prescribing practice in adults with COVID-19: experience from a single hospital cluster. Ther Adv Infect Dis 2020;7:2049936120978095.Google ScholarPubMed
Soriano, MC, Vaquero, C, Ortiz-Fernández, A, Caballero, A, Blandino-Ortiz, A, de Pablo, R. Low incidence of coinfection, but high incidence of ICU-acquired infections in critically ill patients with COVID-19. J Infect 2021;82:e20–e21.CrossRefGoogle ScholarPubMed
Stevenson, DR, Sahemey, M, Cevallos Morales, J, Martín-Lázaro, J, Buchanan, R, Serafino Wani, R. Improving antimicrobial stewardship in critically-ill patients with COVID-19. Clin Infect Dis 2021;72:e926.CrossRefGoogle ScholarPubMed
Rothe, K, Feihl, S, Schneider, J, et al. Rates of bacterial coinfections and antimicrobial use in COVID-19 patients: a retrospective cohort study in light of antibiotic stewardship. Eur J Clin Microbiol Infect Dis 2021;40:859–869.CrossRefGoogle ScholarPubMed
De Bruyn, A, Verellen, S, Bruckers, L, et al. Secondary infection in COVID-19 critically ill patients: a retrospective single-center evaluation. BMC Infect Dis 2022;22:207.CrossRefGoogle ScholarPubMed
Figure 0

Fig. 1.Patient selection.

Figure 1

Table 1.Baseline Characteristics of Patients With or Without Infection

Figure 2

Table 2.Outcomes of Patients With or Without Infection

Figure 3

Fig. 2.Most frequently prescribed antimicrobials within 30 days prior to admission.

Figure 4

Fig. 3.Infectious disease syndromes identified. Note. CAUTI, catheter-associated UTI; CLABSI, central-line–associated bloodstream infection; CAP, community-acquired pneumonia; HAP, hospital-acquired pneumonia; UTI, urinary tract infection; VAP, ventilator-associated pneumonia.

Figure 5

Fig. 4.Organisms identified from cultures.

Figure 6

Table 3.Commonly Used Antimicrobial Agents During Hospitalization