Etiology and Antimicrobial Resistance of Secondary Bacterial Infections in Patients Hospitalized with COVID-19: A Retrospective Analysis

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access


Background. One of the complications in patients hospitalized with COVID-19 is a secondary bacterial infection. Its frequency can reach 15%, which makes it important to determine the etiology and antimicrobial resistance of the key pathogens responsible for the development of this pathology, in order to further improve the practice of prescribing and increase the effectiveness of antimicrobial chemotherapy. Aims — to assess the etiological structure and antibiotic resistance of the main pathogens of SBIs to improve the practice of antibiotic prescription. Methods. This retrospective study reviewed medical records of the patients hospitalized with COVID-19 in the Moscow city hospital No. 4 between April 28 and November 1, 2020. Demographic, clinical outcomes, etiology, and antimicrobial resistance data of the SBIs were collected. Outcomes were also compared between patients who were classified as severe and critical on admission. Results. Among 3180 patients hospitalized with COVID-19, 220 (6.9%) patients had acquired SBIs, and 50.0% of cases were fatal. The mean age was 72.7 ± 13.07 years. A higher mortality rate was observed in the group of critical patients (63%). 560 strains of bacteria isolated from the SBIs (58.8% isolated from lungs, 21% from urine and 20.2% from blood). 330 strains (58.9%) were Gram-negative bacteria. 109 patients had infections with mixed bacteria. 45 of them (20.5% of the total number of patients included in the study) had 2 pathogens, and 64 patients (29.1%) 3 or more strains. The top three bacteria of SBIs were A. baumannii (23.6%; 132/560), K. pneumoniae (22.9%; 128/560), and S. epidermidis (10.4%; 58/560). The isolation rates of carbapenem-resistant A. baumannii were 97%. Cefoperazone/sulbactam was the most active antibiotic against this pathogen with 62.1% sensitivity. Among K. pneumoniae strains, the level of resistance to carbapenems was 77.4% to meropenem and 54% to imipenem. The proportion of resistant strains to tigecycline and to colistin was 4 and 2.3% respectively. Meticillin resistance was present in 38.5% of S. aureus. 50% of E. faecium strains were vancomycin-resistant. Conclusions. Gram-negative bacteria, especially A. baumannii and K. pneumoniae, were the main pathogens, and the resistance rates of the major isolated bacteria were generally high, which indicates that more accurate use of antibacterial agents is necessary for SBIs in patients hospitalized with COVID-19.

Full Text

Restricted Access

About the authors

Konstantin I. Karnoukh

First Moscow State Medical University Named after I.M. Sechenov (Sechenov University)

ORCID iD: 0000-0003-2660-7583
Scopus Author ID: 57208185271

PhD Student

Russian Federation, 8 Trubetskaya Street, building 2, 119991, Moscow

Vladimir N. Drozdov

First Moscow State Medical University Named after I.M. Sechenov (Sechenov University)

ORCID iD: 0000-0002-0535-2916
SPIN-code: 8061-9382

MD, PhD, Professor

Russian Federation, 8 Trubetskaya Street, building 2, 119991, Moscow

Evgenia V. Shikh

I.M. Sechenov First Moscow State Medical University (Sechenov University)

ORCID iD: 0000-0001-6589-7654
SPIN-code: 2397-8414

Dr. of Sci. (Med.), Professor, Head of the Department of Clinical Pharmacology and Propaedeutics of Internal Diseases

Russian Federation, 8 Trubetskaya Street, building 2, 119991, Moscow

Svetlana V. Zhilina

Morozovskaya Children’s City Clinical Hospital

ORCID iD: 0000-0003-0084-1013
SPIN-code: 4910-5125

Cand. of Sci. (Med), Head of the Microbiological Research Group of the Clinical Diagnostic Laboratory

Russian Federation, 1/4th Dobryninsky lane, building 9, 119049, Moscow

Natalia B. Lazareva

First Moscow State Medical University Named after I.M. Sechenov (Sechenov University)

Author for correspondence.
ORCID iD: 0000-0001-6528-1585
SPIN-code: 5333-6239

Dr. of Sci. (Med), Professor of the Department of Clinical Pharmacology and Propaedeutics of Internal Diseases

Russian Federation, 8 Trubetskaya Street, building 2, 119991, Moscow


  1. Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. doi:
  2. Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet. 2020;395(10229):1054–1062. doi:
  3. Li J, Wang J, Yang Y, et al. Etiology and antimicrobial resistance of secondary bacterial infections in patients hospitalized with COVID-19 in Wuhan, China: A retrospective analysis. Antimicrob Resist Infect Control. 2020;9(1):153. doi:
  4. Alhazzani W, Møller MH, Arabi YM, et al. Surviving Sepsis Campaign: Guidelines on the Management of Critically Ill Adults with Coronavirus Disease 2019 (COVID-19). Crit Care Med. 2020;48(6):e440–e469. doi:
  5. Jin Y-H, Cai L, Cheng Z-S, et al. A rapid advice guideline for the diagnosis and treatment of 2019 novel coronavirus (2019-nCoV) infected pneumonia (standard version). Mil Med Res. 2020;7(1):4. doi:
  6. Song J-C, Wang G, Zhang W, et al. Chinese expert consensus on diagnosis and treatment of coagulation dysfunction in COVID-19. Mil Med Res. 2020;7(1):19. doi:
  7. Wang Z, Yang B, Li Q, et al. Clinical Features of 69 Cases with Coronavirus Disease 2019 in Wuhan, China. Clin Infect Dis. 2020;71(15):769–777. doi:
  8. Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: A descriptive study. Lancet. 2020;395(10223):507–513. doi:
  9. Goyal P, Choi JJ, Pinheiro LC, et al. Clinical Characteristics of COVID-19 in New York City. N Engl J Med. 2020;382(24):2372–2374. doi:
  10. Профилактика, диагностика и лечение новой коронавирусной инфекции (COVID-19): Временные методические рекомендации Минздрава России, версия 9 от 26.10.2020. [Profilaktika, diagnostika i lecheniye novoy koronavirusnoy infektsii (COVID-19): Vremennyye metodicheskiye rekomendatsii Minzdrava Rossii, versiya 9 ot 26.10.2020. (In Russ.)] Available at: (аccessed: 26.03.2021).
  11. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36(5):309–332. doi:
  12. Jorgensen JH, Pfaller MA, Carroll KC, et al. Manual of clinical microbiology. 11th ed. Washington, DC: ASM Press; 2015.
  13. Leber, Amy L (ed.). Clinical Microbiology Procedures Handbook. 4th ed. Washington, DC: ASM Press; 2016.
  14. Определение чувствительности микроорганизмов к антимикробным препаратам: Клинические рекомендации Межрегио-нальной ассоциации по клинической микробиологии и антимикробной химиотерапии, 2018. [Opredelenie chuvstvitel’nosti mikroorganizmov k antimikrobnym preparatam: Klinicheskie rekomendacii of Mezhregional’naja associacija po klinicheskoj mikrobiologii i antimikrobnoj himioterapii, 2018. (In Russ.)] Available at: (accessed: 26.03.2021).
  15. EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. Ver. 2.0. 2017. Available at: (accessed: 24.06.2019).
  16. Van der Zwaluw K, de Haan A, Pluister GN, et al. The carbapenem inactivation method (CIM), a simple and low-cost alternative for the Carba NP test to assess phenotypic carbapenemase activity in gram-negative rods. PLoS One. 2015;10(3):e0123690. doi:
  17. Seymour CW, Liu VX, Iwashyna TJ, et al. Assessment of Clinical Criteria for Sepsis: For the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315(8):762–774. doi:
  18. Garcia-Vidal C, Sanjuan G, Moreno-García E, et al. Incidence of co-infections and superinfections in hospitalized patients with COVID-19: A retrospective cohort study. Clin Microbiol Infect. 2021;27(1):83–88. doi:
  19. Li X, Wang L, Yan S, et al. Clinical characteristics of 25 death cases with COVID-19: A retrospective review of medical records in a single medical center, Wuhan, China. Int J Infect Dis. 2020;94:128–132. doi:
  20. Ali S, Birhane M, Bekele S, et al. Healthcare associated infection and its risk factors among patients admitted to a tertiary hospital in Ethiopia: Longitudinal study. Antimicrob Resist Infect Control. 2018;7:2. doi:
  21. Vijay S, Bansal N, Rao BK, et al. Secondary Infections in Hospitalized COVID-19 Patients: Indian Experience. Infect Drug Resist. 2021;14:1893–1903. doi:
  22. Клыпа Т.В., Бычинин М.В., Мандель И.А., и др. Клиническая характеристика пациентов с COVID-19, поступающих в отделение интенсивной терапии. Предикторы тяжелого течения // Клиническая практика. — 2020. — Т. 11. — № 2. — С. 6–18. [Klypa TV, Bychinin MV, Mandel IA, et al. Clinical Characteristics of Patients Admitted to an ICU with COVID-19. Predictors of the Severe Disease. Journal of Clinical Practice. 2020;11(2):6–20. (In Russ.)] doi:
  23. Qin C, Zhou L, Hu Z, et al. Dysregulation of Immune Response in Patients with Coronavirus 2019 (COVID-19) in Wuhan, China. Clin Infect Dis. 2020;71(15):762–768. doi:

Copyright (c) 2022 "Paediatrician" Publishers LLC

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies