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Review article

Rational use of antibiotics during the COVID-19 pandemic

Jovica Milovanović1,2, Ana Jotić1,2, Zorana Radin3, Ivana Ćirković4
  • Clinic for Otorhinolaryngology and Maxillofacial Surgery, University Clinical Center of Serbia, Belgrade, Serbia
  • Faculty of Medicine, University of Belgrade, Belgrade, Serbia
  • Ear, Nose and Throat Clinic, Medical Center Zvezdara, Belgrade, Serbia
  • Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia

ABSTRACT

Introduction/Aim: The global COVID-19 pandemic has long been considered an emergency, with the number of cases growing exponentially, despite constant efforts to control the infection. Although the disease is caused by the SARS-CoV-2 virus, most patients are treated with antibiotic therapy. The long-term effects of such broad antibiotics use on antimicrobial resistance are still unknown and are a matter for concern. The aim of this paper is: to determine, based on the available literature, the impact of the COVID-19 pandemic on the use of antibiotics; to determine the global situation regarding antimicrobial resistance; to identify key areas where urgent changes are needed.

Methods: A systematic review of the current literature on the use of antibiotics in COVID-19 treatment was conducted. The PubMed and MEDLINE databases were searched for papers published between March 2020 and September 2021.

Results: Between 76.8% and 87.8% of patients with COVID-19 were treated with antibiotics. Antibiotics were less frequently prescribed to children, as compared to adults (38.5%, compared to 83.4%). The most commonly administered antibiotics were fluoroquinolones (20.0%), macrolides (18.9%), β-lactam antibiotics (15.0%), and cephalosporins (15.0%). Self-medication with antibiotics to prevent and treat COVID-19 has been identified as one of the important factors contributing to antimicrobial resistance.

Conclusion: The impact of COVID-19 on global antimicrobial resistance is still unknown and is likely to be unevenly distributed in the general population. Although various antibiotics have been used to treat patients with COVID-19, their role and the need for their application in the treatment of this infection remains to be determined. For now, there are no reliable data as to whether the use of antibiotics in COVID-19 cases without associated bacterial infections has any effect on the course of the disease and mortality.


INTRODUCTION

The global pandemic caused by the SARS-CoV-2 virus has long been considered an unprecedented crisis. On January 30, 2020, the World Health Organization (WHO) officially declared an international state of emergency in public health, due to the increase in infections caused by the SARS-CoV-2 virus, while the pandemic was declared on March 11, 2020 [1]. Despite constant efforts to curb the spread of the infection, the number of cases is growing exponentially. There is great variability in the clinical characteristics of the disease, from mild symptoms of infection in the upper respiratory tract, to life-threatening infections of the lower respiratory tract. Almost 80.0% of patients are asymptomatic or have a mild form of the disease, 15.0% have a severe form of the disease and require oxygenation, while 5.0% have a life-threatening form of the disease and require mechanical ventilation. Disease mortality is 3.4% [2]. Although the clinical symptoms are caused by the SARS-CoV-2 virus, most patients were prescribed antibiotic therapy, in 76.8% of cases, while antiviral drugs were prescribed in 68.7% of cases [3]. Increased bacterial resistance to available antibiotics was detected even before the pandemic [4]. Therefore, the question of what the future long-term outcomes of such widespread use of antibiotics will be is a matter for concern.

The aim of this paper is: to determine, based on the available literature, the impact of the COVID-19 pandemic on the use of antibiotics; to determine the global situation regarding antimicrobial resistance; to identify key areas where urgent changes are needed.

METHODS

A systematic review of the current literature on the use of antibiotics in COVID-19 treatment was conducted. The PubMed and MEDLINE databases were searched for papers published between March 2020 and September 2021. All papers in English were included, as well as retrospective analyses, systematic reviews, and meta-analyses. The terms: "antibiotics", "COVID-19", "SARS-CoV-2", "treatment'', ''bacterial resistance '', ''antimicrobial resistance'', ''anti-bacterial agents'', ''drug resistance'', were used to identify relevant articles. Reports of case reports and animal studies were excluded, as well as duplicate references.

TREATMENT OPTIONS IN COVID-19 PATIENTS

A national multi-centric study conducted by Bendala Estrada et al. included data on 13,932 registered patients treated for COVID-19 in Spain [5]. Antibiotics were prescribed to 12,238 (87.8%) patients, while only 1,498 (10.8%) patients did not receive antibiotic therapy. Meta-analysis of 41 studies from 11 countries involving 16,495 patients compared treatment modalities in patients with severe and other forms (mild to moderate) [3]. Most patients received antibiotic therapy (76.8%, 95.0% CI: 70.2% – 83.5%), followed by antiviral therapy (68.7%, 95.0% CI: 53.6% – 83.8%), oxygen therapy (55.5%, 95% CI: 41.9% – 69.1%), and corticosteroid therapy (35.4%, 95.0% CI: 27.4% – 43.5%) Compared to patients with less severe forms of the disease, patients with severe forms of the disease were more likely to be treated with antibiotic therapy (OR = 6, 95.0% CI: 3.4 – 10.7, p < 0.00001) and antiviral therapy (OR = 2.2, 95.0% CI: 1.4–3.3, p = 0.0003). No statistically significant difference was found in the use of oxygen therapy between groups (p = 0.710). Langford et al. [6] conducted another meta-analysis of 154 studies and the available data on antibiotic therapy in 30,623 patients. The prevalence of prescribing antibiotics did not considerably vary from what had been reported previously, and it was 74.6% (95.0% CI: 68.3% – 80.0%). Antibiotics were prescribed to children to a lesser extent than to adults (38.5%, compared to 83.4%). The older the patient, the more likely he/she was to be prescribed antibiotic therapy (OR 1.5 per 10 years of age, 95.0% CI: 1.2 – 1.8). Also, antibiotics were prescribed depending on the severity of clinical presentation. Antibiotics were less prescribed in patients who were not hospitalized (59.3%) as compared to those who were hospitalized with a mild or moderate form of the disease (74.8%), and to those in intensive care (86.4%).

Thus far, there are no data on antimicrobial resistance in COVID-19 positive patients, in Serbia.

ANTIBIOTIC OPTIONS IN COVID-19 PATIENTS

The most commonly administered antibiotics were fluoroquinolones (20.0%), macrolides (18.9%), β-lactam antibiotics (15.0%) and cephalosporins (15.0%) [6]. A combination of antibiotics was most commonly used in patients with the severe form of the disease, predominantly for the treatment of pneumonia. The most common combinations contained cephalosporins, fluoroquinolone, and macrolide antibiotics [7].

The use of antibiotics varied widely in different parts of the world. In Europe it was 63.1% (95.0% CI: 41.7% – 80.4%), in North America it amounted to 64.8% (95.0% CI: 54.0% – 74.2%), in China it was 76.2% (95.0% CI: 66.8% – 82.3%), in the Middle East it amounted to 86.0% (95.0% CI: 77.4% – 91.7%), while in East and Southeast Asia it was 87.5% (95.0% CI: 47.8% – 98.2%). In Europe, β-lactam antibiotics, macrolides and cephalosporins were the ones most commonly prescribed, while in North America macrolides, cephalosporins and β-lactam antibiotics were the ones used the most. In China, patients were most often prescribed fluoroquinolones, β-lactam antibiotics, and cephalosporins, while in East and Southeast Asia, cephalosporins, macrolides, and fluoroquinolones were the ones most commonly used [6].

In the first few months of the pandemic, the use of azithromycin in the treatment of COVID-19 infections was expanded. In vitro studies provided evidence of azithromycin’s antiviral properties against many respiratory viruses (including the rhinovirus, the SARS-CoV-2 virus, and the Zika virus) [8]. Also, its immunomodulatory properties had been proven, which to some extent, theoretically justified its use in the treatment of COVID-19 [9]. Subsequent studies on its application in clinical practice have not justified its use. A comparison between the population which had been receiving azithromycin and the population of patients which had been receiving symptomatic therapy revealed that there was no effect of this drug on the worsening or improving of the patient’s condition, on the number of days of hospitalization, or on the mortality rate, regardless of whether the patients had been at home or hospitalized [10],[11],[12]. The conclusion was that azithromycin should be prescribed only when there was a clear indication for its administration, especially in the case of hospitalized patients.

Although various antibiotics have been used in treating patients with COVID-19, their role and the need for their use in the treatment of this infection is still being examined. For now, there are no reliable data proving that the use of antibiotics in cases of COVID-19 without associated bacterial infections has any effect on the course of the disease and mortality [10]. In milder forms of the disease, antibiotics should be avoided in therapy, because they do not affect the progression of the disease, mortality and length of hospitalization [13]. Clinicians should avoid prolonged and inappropriate use of antimicrobial drugs that can cause antimicrobial resistance and reduce the efficacy of these drugs.

MICROBIOLOGY OF CO-INFECTION AND SUPERINFECTION IN COVID-19 PATIENTS

For the purpose of determining the extent of bacterial or fungal co-infection or secondary infection, a national retrospective study was conducted in the UK, which included all patients with laboratory-confirmed COVID-19, between January 1 and June 2, 2020 (221,134 patients) [14]. Co-infection involved isolating the causative agent the day before, on the day, or one day after the confirmation of SARS-CoV-2 infection. Secondary infection involved the isolation of the causative agent 2 to 21 days after confirmation of the SARS-CoV-2 infection. The presence of infection was determined by isolating the causative agent from blood samples or samples taken from the respiratory tract. Only 2,279 (1.0%) patients had a confirmed co-infection or secondary infection. Secondary infections were more common than co-infections (61.4% vs. 38.6%, 95.0% CI: 36.56% – 40.60%). Most of these infections were isolated from blood samples (in 66.0% of cases), i.e., in 0.7% of all COVID-19 cases. Bacteremia and sepsis were 6.5 times more common than respiratory co-infections and twice as common as secondary respiratory infections. Patients who had co-infections and secondary infections were more often older (≥ 40 years) and male (p <0.001). Mortality in patients with coinfections/secondary infections was significantly higher compared to patients without such infections (23.0% and 26.6%, respectively, compared to 7.6%). The most commonly isolated hematogenous bacteria were Escherichia coli, Staphylococcus aureus, Klebsiella pneumoniae, Enterococcus faecium, and non-pyogenic streptococci, while the most commonly isolated respiratory bacteria were Pseudomonas aeruginosa, Haemophilus influenzae, Staphylococcus aureus, and Klebsiella pneumoniae. The most common respiratory mycotic infections were caused by Aspergillus fumigatus, while the most common hematogenous infections were caused by Candida albicans.

If only bacterially induced pulmonary coinfections/ superinfections are taken into consideration, the prevalence ranges from 8.6% to 16.0% [6],[15],[16],[17]. The differences probably exist due to previous antibiotic administration, poor sample quality, variations in the interpretation of sample growth, and challenges associated with cultivating microorganisms [18]. The prevalence of coinfections/secondary infections drastically increased in patients in intensive care (up to 33.0%), with the antibiotics use before sampling amounting to 28.0% - 79.0% [19].

Spanish authors [17] found, based on 1,251 samples taken from the respiratory tract, that bacterial pulmonary co-infections were, in most cases, monomicrobial (92.5%). The most commonly isolated bacteria were Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella pneumoniae/Klebsiella aerogenes, and Escherichia coli. In 10.8% of the samples multidrug-resistant rare bacteria (Achromobacter spp., Burkholderia spp., Stenotrophomonas spp., Chryseobacterium spp., Corynebacterium spp.) were isolated. Clinical isolates were very similar to the isolates in viral pneumonias not associated with COVID-19 [20].

When it comes to secondary lung infections, the results of a systematic review, which included 5,047 hospitalized patients with COVID-19-associated pneumonia in 49 studies, indicated that the most commonly isolated bacterial pathogens were Pseudomonas aeruginosa (21.1%), Klebsiella species (17.2%), Staphylococcus aureus (13.5%), Escherichia coli (10.4%), and Stenotrophomonas maltophilia (3.1%). The incidence of secondary mycotic infection was 6.3%. Mycotic infections were caused predominantly by fungi belonging to the Aspergillus genus, with Aspergillus fumigatus being the species most commonly isolated. Other less commonly isolated fungi were Aspergillus flavus, Aspergillus calidoustus, Aspergillus citrinoterreus, Aspergillus niger, Aspergillus terreus, Aspergillus versicolor, Mucor species, Fusarium proliferatum, and Pneumocystis jirovecii [16]. Mycotic infections were more frequently detected in the Asian population than in the European population of COVID-19 patients [21]. In patients with secondary mycotic infections, mortality was 0.2%. It was significantly higher in persons hospitalized in the intensive care units than in the mixed hospital population (0.4% vs. 0.2%) [21].

SELF-MEDICATION WITH ANTIBIOTICS IN THE COVID-19 ERA

Self-medication with antibiotics has been identified as one of the important factors contributing to antimicrobial resistance. Even in countries with strict regulations and advanced models of health care, this is a common problem [22],[23],[24]. Self-medication with antibiotics is defined as the inappropriate and irrational use of antibiotics, where individuals self-treat their symptoms or illness without a physician's examination, prescribed therapy, or supervision [25].

The pandemic has significantly affected mental health in the general population, resulting in an increase in the levels of stress, fear, anxiety and depression [26]. This has also led to some extreme forms of behavior, to the spreading of misinformation, and to the misinterpreting of the advice given by the medical profession. In a study conducted by Zhang et al. on 2,217 subjects from Australia [27], 19.5% of subjects took antibiotics to prevent getting infected with the SARS-CoV-2 virus. Higher levels of stress, the presence of anxiety, fear of infection, and overall concern were noted in subjects who took antibiotics, as compared to those who did not. Also, these subjects were not sufficiently informed about the antibiotics themselves. A larger number of patients believed that antibiotics treat viral infections (34.1%) and did not know that antibiotics only treat bacterial infections (25.6%). A total of 35.6% of patients used antibiotics to cure the flu or a cold. They obtained antibiotics from friends or relatives (17.9%), from their doctor (47.1%), or used what they had left from before (23.2%). It was noted that subjects who self-medicated were more educated and more often worked in a health-related profession. They knew the difference between viral and bacterial infections, although they knew less about the effects of antibiotics during viral and bacterial infections. This leaves room for the possibility of educating this part of the population on the use of antibiotics in treatment and on the exact ways that antibiotics act.

In a systematic review of literature conducted by Quincho-Lopez et al. [28], the most commonly used antibiotics for the prevention and self-medication of COVID-19 were azithromycin, penicillin, and amoxicillin. According to the data from that study, vitamins and other supplements, non-steroidal anti-inflammatory drugs, acetaminophen, hydroxychloroquine and ivermectin were taken before the antibiotics.

TELEMEDICINE AND THE ADMINISTRATION OF ANTIBIOTICS IN THE AGE OF COVID-19

During the pandemic, countries with better organized healthcare systems switched to telemedicine and virtual patient examinations, in order to preserve health resources and staff, as well as to reduce the risk of exposure and infection with the SARS-CoV-2 virus [29]. Although conducting telemedicine visits is not without its challenges, it was a necessary step in overcoming the period when there were still no vaccines available.

There were some differences between the pediatric and adult population. In adults, antibiotics were prescribed less often during telemedicine visits than during office examinations. The most common condition treated with antibiotics was acute pharyngitis (21.2% during telemedicine visits and 39.7% during doctor visits; p < 0.001). In cases of other respiratory tract infections, antibiotic prescribing was significantly less frequent (1.6% compared to 19.9%; p < 0.001). Antibiotics were prescribed according to current recommendations (in pharyngitis in 96.4% versus 94.4%, and in other infections of the upper respiratory tract 96.3% versus 74.0%) [30]. The opposite happened in the pediatric population. Children were more likely to receive antibiotics during telemedicine visits (52.0%) than during emergency room visits (42.0%) or visits to their pediatrician (31.0%). Antibiotics were prescribed according to current recommendations in 92.5% of telemedicine visits, and in 90.7% of office examinations (p = 0.004) [31],[32].

ANTIMICROBIAL RESISTANCE DURING THE COVID-19 PANDEMIC

Antimicrobial resistance, which had been a health issue even before the pandemic, will definitely become an even greater cause for concern in the upcoming period. As we have already stated in the previous sections, the pandemic has almost completely destroyed the stewardship of antibiotics and single-handedly increased their use worldwide. In addition, the constant use of disinfectants has led to the formation of an environment that favors some microbial phenotypes, as well as to the development of the resistance to certain antimicrobial agents [33]. By changing their phenotypic and genotypic characteristics, these microbial subpopulations also change the target of antibiotic action and become highly tolerant to them [34]. Biocides promote tolerance and reduce antibiotic sensitivity, developing cross-resistance and co-resistance in pathogenic bacteria [35].

The pandemic has affected the monitoring, prevention and control of antimicrobial resistance. Cooperation with institutions that control antimicrobial resistance has been limited; funds, human and medical resources (medical staff, sanitation staff, administrative staff, protective equipment, drugs, reagents for microbiological tests) have been reallocated for treatment of COVID-19 patients [36].

Bacteria such as Staphylococcus aureus, MRSA, Streptococcus pneumoniae, and penicillin-resistant Streptococcus pneumoniae have been isolated in smaller numbers during the pandemic. It is believed that the increased use of disinfectants, hand washing, the limitation of social contacts, wearing face masks, as well as the occasional closing of schools are responsible for this [37],[38]. On the other hand, bacteria such as Escherichia coli and Klebsiella pneumoniae (especially Escherichia coli and Klebsiella pneumoniae resistant to 3rd generation cephalosporins) have been isolated in greater percentages and have also demonstrated an extended spectrum of antibiotic resistance during the pandemic [37].

In Serbia, during the pandemic in 2020, the most frequently isolated bacteria from blood samples were the following: Acinetobacter spp. (28.3%), Staphylococcus aureus (15.5%), Klebsiella pneumoniae (15.4%), Enterococcus faecalis (12.4 %), Escherichia coli (11.3%), and Enterococcus faecium (10.9%). There was a significant increase in the number of Pseudomonas aeruginosa resistant strains in 2020 (for ceftazidime from 59.0% to 64.0%, for ciprofloxacin from 59.0% to 70.0%, for meropenem from 55.0% to 62.0%). Also, Staphylococcus aureus showed an increase in the number of resistant strains in 2020, as compared to 2019 (for ciprofloxacin from 21.0% to 34.0%, and for rifampicin from 12.0% to 18.0%). The data are based on the study results conducted in the Laboratory of the Institute of Microbiology and Immunology of the Medical Faculty of the University of Belgrade.

CONCLUSION

The effect of COVID-19 on global antimicrobial resistance remains unknown and is likely to be distributed unevenly in the general population. The disproportionate use of antibiotics in patients with COVID-19 can significantly influence the current situation, especially in countries where significantly high antimicrobial resistance already exists. The areas where activities should be intensified are the following: education of the population and medical staff, monitoring of the application of clinical practice guides and the use of antibiotics in viral infections, monitoring of antimicrobial resistance by competent microbiological laboratories, and development of strategies for its prevention.

  • Conflict of interest:
    None declared.

Informations

Volume 2 No 4

December 2021

Pages 399-408
  • Keywords:
    antibiotics, COVID-19, antimicrobial resistance, bacteria
  • Received:
    15 November 2021
  • Revised:
    13 December 2021
  • Accepted:
    18 December 2021
  • Online first:
    20 December 2021
  • DOI:
  • Cite this article:
    Milovanović J, Jotić A, Radin Z, Ćirković I. Rational use of antibiotics during the COVID-19 pandemic. Serbian Journal of the Medical Chamber. 2021;2(4):399-408. doi: 10.5937/smclk2-34935
Corresponding author

Ana Jotić
Clinic for Otorhinolaryngology and Maxillofacial Surgery, Clinical Center of
Serbia
2 Pasterova Street, 11000 Belgrade, Serbia
E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.


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    35. Rizvi SG, Ahammad SZ. COVID-19 and antimicrobial resistance: A crossstudy. Sci Total Environ. 2021 Oct 8;807(Pt 2):150873. doi: 10.1016/j.scitotenv.2021.150873.[CROSSREF]

    36. Tomczyk S, Taylor A, Brown A, de Kraker MEA, El-Saed A, Alshamrani M, et al.; WHO AMR Surveillance and Quality Assessment Collaborating Centres Network. Impact of the COVID-19 pandemic on the surveillance, prevention and control of antimicrobial resistance: a global survey. J Antimicrob Chemother. 2021 Oct 11;76(11):3045-58. doi: 10.1093/jac/dkab300.[CROSSREF]

    37. Hirabayashi A, Kajihara T, Yahara K, Shibayama K, Sugai M. Impact of the COVID-19 pandemic on the surveillance of antimicrobial resistance. J Hosp Infect. 2021 Nov;117:147-56. doi: 10.1016/j.jhin.2021.09.011.[CROSSREF]

    38. McNeil JC, Flores AR, Kaplan SL, Hulten KG. The Indirect Impact of the SARSCoV-2 Pandemic on Invasive Group a Streptococcus, Streptococcus Pneumoniae and Staphylococcus Aureus Infections in Houston Area Children. Pediatr Infect Dis J. 2021 Aug 1;40(8):e313-e6. doi: 10.1097/INF.0000000000003195.[CROSSREF]


REFERENCES

1. World Health Organization. WHO announces COVID-19 outbreak a pandemic [Internet]. World Health Organization Regional Office for Europe; [Pristupljeno: 2021 Sept 8]. Dostupno na: http://www.who.int/en/health-topics/health-emergencies/coronavirus-covid-19/news/news/2020/3/who-announces-covid-19-outbreak-a-pandemic[HTTP]

2. Ioannidis JPA. Infection fatality rate of COVID-19 inferred from seroprevalence data. Bull World Health Organ. 2021 Jan 1;99(1):19-33F. doi: 10.2471/ BLT.20.265892. Epub 2020 Oct 14.[CROSSREF]

3. Giri M, Puri A, Wang T, Guo S. Comparison of clinical manifestations, pre-existing comorbidities, complications and treatment modalities in severe and non-severe COVID-19 patients: A systemic review and meta-analysis. Sci Prog. 2021 Jan-Mar;104(1):368504211000906. doi: 10.1177/00368504211000906.[CROSSREF]

4. Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, et al. Antibiotic resistance-the need for global solutions. Lancet Infect Dis. 2013 Dec;13(12):1057-98. doi: 10.1016/S1473-3099(13)70318-9.[CROSSREF]

5. Bendala Estrada AD, Calderón Parra J, Fernández Carracedo E, Muiño Míguez A, Ramos Martínez A, Muñez Rubio E, et al. Inadequate use of antibiotics in the covid-19 era: effectiveness of antibiotic therapy. BMC Infect Dis. 2021 Nov 8;21(1):1144. doi: 10.1186/s12879-021-06821-1.[CROSSREF]

6. Langford BJ, So M, Raybardhan S, Leung V, Soucy JR, Westwood D, et al. Antibiotic prescribing in patients with COVID-19: rapid review and meta-analysis. Clin Microbiol Infect. 2021 Apr;27(4):520-31. doi: 10.1016/j.cmi.2020.12.018.[CROSSREF]

7. Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA. 2020 Mar 17;323(11):1061-9. doi: 10.1001/jama.2020.1585.[CROSSREF]

8. Damle B, Vourvahis M, Wang E, Leaney J, Corrigan B. Clinical Pharmacology Perspectives on the Antiviral Activity of Azithromycin and Use in COVID-19. Clin Pharmacol Ther. 2020 Aug;108(2):201-11. doi: 10.1002/cpt.1857.[CROSSREF]

9. Vitiello A, Ferrara F. A short focus, azithromycin in the treatment of respiratory viral infection COVID-19: efficacy or inefficacy? Immunol Res. 2021 Nov 5:1–5. doi: 10.1007/s12026-021-09244-x.[CROSSREF]

10. Popp M, Stegemann M, Riemer M, Metzendorf MI, Romero CS, Mikolajewska A, et al. Antibiotics for the treatment of COVID-19. Cochrane Database Syst Rev. 2021 Oct 22;10(10):CD015025. doi: 10.1002/14651858.CD015025.[CROSSREF]

11. RECOVERY Collaborative Group. Azithromycin in patients admitted to hospital with COVID-19 (RECOVERY): a randomised, controlled, open-label, platform trial. Lancet. 2021 Feb 13;397(10274):605-12. doi: 10.1016/S0140-6736(21)00149-5.[CROSSREF]

12. PRINCIPLE Trial Collaborative Group. Azithromycin for community treatment of suspected COVID-19 in people at increased risk of an adverse clinical course in the UK (PRINCIPLE): a randomised, controlled, open-label, adaptive platform trial. Lancet. 2021 Mar 20;397(10279):1063-74. doi: 10.1016/S0140-6736(21)00461-X.[CROSSREF]

13. Yin X, Xu X, Li H, Jiang N, Wang J, Lu Z, et al. Evaluation of early antibiotic use in patients with non-severe COVID-19 without bacterial infection. Int J Antimicrob Agents. 2021 Oct 23:106462. doi: 10.1016/j.ijantimicag.2021.106462.[CROSSREF]

14. Gerver SM, Guy R, Wilson K, Thelwall S, Nsonwu O, Rooney G, et al. National surveillance of bacterial and fungal coinfection and secondary infection in COVID-19 patients in England: lessons from the first wave. Clin Microbiol Infect. 2021 Nov;27(11):1658-65. doi: 10.1016/j.cmi.2021.05.040.[CROSSREF]

15. Lansbury L, Lim B, Baskaran V, Lim WS. Co-infections in people with COVID-19: a systematic review and meta-analysis. J Infect. 2020 Aug;81(2):266-75. doi: 10.1016/j.jinf.2020.05.046.[CROSSREF]

16. Chong WH, Saha BK, Ananthakrishnan Ramani, Chopra A. State-of-the-art review of secondary pulmonary infections in patients with COVID-19 pneumonia. Infection. 2021 Aug;49(4):591-605. doi: 10.1007/s15010-021-01602-z.[CROSSREF]

17. Ruiz-Bastián M, Falces-Romero I, Ramos-Ramos JC, de Pablos M, García-Rodríguez J; SARS-CoV-2 Working Group. Bacterial co-infections in COVID-19 pneumonia in a tertiary care hospital: Surfing the first wave. Diagn Microbiol Infect Dis. 2021 Nov;101(3):115477. doi: 10.1016/j.diagmicrobio.2021.115477.[CROSSREF]

18. Metlay JP, Waterer GW, Long AC, Anzueto A, Brozek J, Crothers K, et al. Diagnosis and Treatment of Adults with Community-acquired Pneumonia. An Official Clinical Practice Guideline of the American Thoracic Society and Infectious Diseases Society of America. Am J Respir Crit Care Med. 2019 Oct 1;200(7):e45-e67. doi: 10.1164/rccm.201908-1581ST.[CROSSREF]

19. Timbrook TT, Hueth KD, Ginocchio CC. Identification of bacterial co-detections in COVID-19 critically Ill patients by BioFire® FilmArray® pneumonia panel: a systematic review and meta-analysis. Diagn Microbiol Infect Dis. 2021 Nov;101(3):115476. doi: 10.1016/j.diagmicrobio.2021.115476.[CROSSREF]

20. Ruuskanen O, Lahti E, Jennings LC, Murdoch DR. Viral pneumonia. Lancet. 2011 Apr 9;377(9773):1264-75. doi: 10.1016/S0140-6736(10)61459-6.[CROSSREF]

21. Peng J, Wang Q, Mei H, Zheng H, Liang G, She X, et al. Fungal co-infection in COVID-19 patients: evidence from a systematic review and meta-analysis. Aging (Albany NY). 2021 Mar 19;13(6):7745-57. doi: 10.18632/aging.202742.[CROSSREF]

22. Torres NF, Chibi B, Middleton LE, Solomon VP, Mashamba-Thompson TP. Evidence of factors influencing self-medication with antibiotics in low and middle-income countries: a systematic scoping review. Public Health. 2019 Mar;168:92-101. doi: 10.1016/j.puhe.2018.11.018.[CROSSREF]

23. Lescure D, Paget J, Schellevis F, van Dijk L. Determinants of Self-Medication With Antibiotics in European and Anglo-Saxon Countries: A Systematic Review of the Literature. Front Public Health. 2018 Dec 17;6:370. doi: 10.3389/fpubh.2018.00370.[CROSSREF]

24. Sunny TP, Jacob R, Krishnakumar K, Varghese S. Self-medication: Is a serious challenge to control antibiotic resistance? Natl. J. Physiol. Pharm. Pharmacol. 2019; 9:821–7. doi: 10.5455/njppp.2019.9.0620508062019.[HTTP]

25. Morgan DJ, Okeke IN, Laxminarayan R, Perencevich EN, Weisenberg S. Non-prescription antimicrobial use worldwide: a systematic review. Lancet Infect Dis. 2011 Sep;11(9):692-701. doi: 10.1016/S1473-3099(11)70054-8.[CROSSREF]

26. Rajkumar RP. COVID-19 and mental health: A review of the existing literature. Asian J Psychiatr. 2020 Aug;52:102066. doi: 10.1016/j.ajp.2020.102066.[CROSSREF]

27. Zhang A, Hobman EV, De Barro P, Young A, Carter DJ, Byrne M. Self-Medication with Antibiotics for Protection against COVID-19: The Role of Psychological Distress, Knowledge of, and Experiences with Antibiotics. Antibiotics (Basel). 2021 Feb 25;10(3):232. doi: 10.3390/antibiotics10030232.[CROSSREF]

28. Quincho-Lopez A, Benites-Ibarra CA, Hilario-Gomez MM, Quijano-Escate R, Taype-Rondan A. Self-medication practices to prevent or manage COVID-19: A systematic review. PLoS One. 2021 Nov 2;16(11):e0259317. doi: 10.1371/ journal.pone.0259317.[CROSSREF]

29. Monaghesh E, Hajizadeh A. The role of telehealth during COVID-19 outbreak: a systematic review based on current evidence. BMC Public Health. 2020 Aug 1;20(1):1193. doi: 10.1186/s12889-020-09301-4.[CROSSREF]

30. Entezarjou A, Calling S, Bhattacharyya T, Milos Nymberg V, Vigren L, Labaf A, et al. Antibiotic Prescription Rates After eVisits Versus Office Visits in Primary Care: Observational Study. JMIR Med Inform. 2021 Mar 15;9(3):e25473. doi: 10.2196/25473.[CROSSREF]

31. Ray KN, Shi Z, Gidengil CA, Poon SJ, Uscher-Pines L, Mehrotra A. Antibiotic Prescribing During Pediatric Direct-to-Consumer Telemedicine Visits. Pediatrics. 2019 May;143(5):e20182491. doi: 10.1542/peds.2018-2491.[CROSSREF]

32. Ray KN, Martin JM, Wolfson D, Schweiberger K, Schoemer P, Cepullio C, et al. Antibiotic Prescribing for Acute Respiratory Tract Infections During Telemedicine Visits Within a Pediatric Primary Care Network. Acad Pediatr. 2021 Sep-Oct;21(7):1239-43. doi: 10.1016/j.acap.2021.03.008.[CROSSREF]

33. Merchel Piovesan Pereira B, Tagkopoulos I. Benzalkonium Chlorides: Uses, Regulatory Status, and Microbial Resistance. Appl Environ Microbiol. 2019 Jun 17;85(13):e00377-19. doi: 10.1128/AEM.00377-19.[CROSSREF]

34. Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol. 2007 Jan;5(1):48-56. doi: 10.1038/nrmicro1557.[CROSSREF]

35. Rizvi SG, Ahammad SZ. COVID-19 and antimicrobial resistance: A crossstudy. Sci Total Environ. 2021 Oct 8;807(Pt 2):150873. doi: 10.1016/j.scitotenv.2021.150873.[CROSSREF]

36. Tomczyk S, Taylor A, Brown A, de Kraker MEA, El-Saed A, Alshamrani M, et al.; WHO AMR Surveillance and Quality Assessment Collaborating Centres Network. Impact of the COVID-19 pandemic on the surveillance, prevention and control of antimicrobial resistance: a global survey. J Antimicrob Chemother. 2021 Oct 11;76(11):3045-58. doi: 10.1093/jac/dkab300.[CROSSREF]

37. Hirabayashi A, Kajihara T, Yahara K, Shibayama K, Sugai M. Impact of the COVID-19 pandemic on the surveillance of antimicrobial resistance. J Hosp Infect. 2021 Nov;117:147-56. doi: 10.1016/j.jhin.2021.09.011.[CROSSREF]

38. McNeil JC, Flores AR, Kaplan SL, Hulten KG. The Indirect Impact of the SARSCoV-2 Pandemic on Invasive Group a Streptococcus, Streptococcus Pneumoniae and Staphylococcus Aureus Infections in Houston Area Children. Pediatr Infect Dis J. 2021 Aug 1;40(8):e313-e6. doi: 10.1097/INF.0000000000003195.[CROSSREF]

1. World Health Organization. WHO announces COVID-19 outbreak a pandemic [Internet]. World Health Organization Regional Office for Europe; [Pristupljeno: 2021 Sept 8]. Dostupno na: http://www.who.int/en/health-topics/health-emergencies/coronavirus-covid-19/news/news/2020/3/who-announces-covid-19-outbreak-a-pandemic[HTTP]

2. Ioannidis JPA. Infection fatality rate of COVID-19 inferred from seroprevalence data. Bull World Health Organ. 2021 Jan 1;99(1):19-33F. doi: 10.2471/ BLT.20.265892. Epub 2020 Oct 14.[CROSSREF]

3. Giri M, Puri A, Wang T, Guo S. Comparison of clinical manifestations, pre-existing comorbidities, complications and treatment modalities in severe and non-severe COVID-19 patients: A systemic review and meta-analysis. Sci Prog. 2021 Jan-Mar;104(1):368504211000906. doi: 10.1177/00368504211000906.[CROSSREF]

4. Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, et al. Antibiotic resistance-the need for global solutions. Lancet Infect Dis. 2013 Dec;13(12):1057-98. doi: 10.1016/S1473-3099(13)70318-9.[CROSSREF]

5. Bendala Estrada AD, Calderón Parra J, Fernández Carracedo E, Muiño Míguez A, Ramos Martínez A, Muñez Rubio E, et al. Inadequate use of antibiotics in the covid-19 era: effectiveness of antibiotic therapy. BMC Infect Dis. 2021 Nov 8;21(1):1144. doi: 10.1186/s12879-021-06821-1.[CROSSREF]

6. Langford BJ, So M, Raybardhan S, Leung V, Soucy JR, Westwood D, et al. Antibiotic prescribing in patients with COVID-19: rapid review and meta-analysis. Clin Microbiol Infect. 2021 Apr;27(4):520-31. doi: 10.1016/j.cmi.2020.12.018.[CROSSREF]

7. Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA. 2020 Mar 17;323(11):1061-9. doi: 10.1001/jama.2020.1585.[CROSSREF]

8. Damle B, Vourvahis M, Wang E, Leaney J, Corrigan B. Clinical Pharmacology Perspectives on the Antiviral Activity of Azithromycin and Use in COVID-19. Clin Pharmacol Ther. 2020 Aug;108(2):201-11. doi: 10.1002/cpt.1857.[CROSSREF]

9. Vitiello A, Ferrara F. A short focus, azithromycin in the treatment of respiratory viral infection COVID-19: efficacy or inefficacy? Immunol Res. 2021 Nov 5:1–5. doi: 10.1007/s12026-021-09244-x.[CROSSREF]

10. Popp M, Stegemann M, Riemer M, Metzendorf MI, Romero CS, Mikolajewska A, et al. Antibiotics for the treatment of COVID-19. Cochrane Database Syst Rev. 2021 Oct 22;10(10):CD015025. doi: 10.1002/14651858.CD015025.[CROSSREF]

11. RECOVERY Collaborative Group. Azithromycin in patients admitted to hospital with COVID-19 (RECOVERY): a randomised, controlled, open-label, platform trial. Lancet. 2021 Feb 13;397(10274):605-12. doi: 10.1016/S0140-6736(21)00149-5.[CROSSREF]

12. PRINCIPLE Trial Collaborative Group. Azithromycin for community treatment of suspected COVID-19 in people at increased risk of an adverse clinical course in the UK (PRINCIPLE): a randomised, controlled, open-label, adaptive platform trial. Lancet. 2021 Mar 20;397(10279):1063-74. doi: 10.1016/S0140-6736(21)00461-X.[CROSSREF]

13. Yin X, Xu X, Li H, Jiang N, Wang J, Lu Z, et al. Evaluation of early antibiotic use in patients with non-severe COVID-19 without bacterial infection. Int J Antimicrob Agents. 2021 Oct 23:106462. doi: 10.1016/j.ijantimicag.2021.106462.[CROSSREF]

14. Gerver SM, Guy R, Wilson K, Thelwall S, Nsonwu O, Rooney G, et al. National surveillance of bacterial and fungal coinfection and secondary infection in COVID-19 patients in England: lessons from the first wave. Clin Microbiol Infect. 2021 Nov;27(11):1658-65. doi: 10.1016/j.cmi.2021.05.040.[CROSSREF]

15. Lansbury L, Lim B, Baskaran V, Lim WS. Co-infections in people with COVID-19: a systematic review and meta-analysis. J Infect. 2020 Aug;81(2):266-75. doi: 10.1016/j.jinf.2020.05.046.[CROSSREF]

16. Chong WH, Saha BK, Ananthakrishnan Ramani, Chopra A. State-of-the-art review of secondary pulmonary infections in patients with COVID-19 pneumonia. Infection. 2021 Aug;49(4):591-605. doi: 10.1007/s15010-021-01602-z.[CROSSREF]

17. Ruiz-Bastián M, Falces-Romero I, Ramos-Ramos JC, de Pablos M, García-Rodríguez J; SARS-CoV-2 Working Group. Bacterial co-infections in COVID-19 pneumonia in a tertiary care hospital: Surfing the first wave. Diagn Microbiol Infect Dis. 2021 Nov;101(3):115477. doi: 10.1016/j.diagmicrobio.2021.115477.[CROSSREF]

18. Metlay JP, Waterer GW, Long AC, Anzueto A, Brozek J, Crothers K, et al. Diagnosis and Treatment of Adults with Community-acquired Pneumonia. An Official Clinical Practice Guideline of the American Thoracic Society and Infectious Diseases Society of America. Am J Respir Crit Care Med. 2019 Oct 1;200(7):e45-e67. doi: 10.1164/rccm.201908-1581ST.[CROSSREF]

19. Timbrook TT, Hueth KD, Ginocchio CC. Identification of bacterial co-detections in COVID-19 critically Ill patients by BioFire® FilmArray® pneumonia panel: a systematic review and meta-analysis. Diagn Microbiol Infect Dis. 2021 Nov;101(3):115476. doi: 10.1016/j.diagmicrobio.2021.115476.[CROSSREF]

20. Ruuskanen O, Lahti E, Jennings LC, Murdoch DR. Viral pneumonia. Lancet. 2011 Apr 9;377(9773):1264-75. doi: 10.1016/S0140-6736(10)61459-6.[CROSSREF]

21. Peng J, Wang Q, Mei H, Zheng H, Liang G, She X, et al. Fungal co-infection in COVID-19 patients: evidence from a systematic review and meta-analysis. Aging (Albany NY). 2021 Mar 19;13(6):7745-57. doi: 10.18632/aging.202742.[CROSSREF]

22. Torres NF, Chibi B, Middleton LE, Solomon VP, Mashamba-Thompson TP. Evidence of factors influencing self-medication with antibiotics in low and middle-income countries: a systematic scoping review. Public Health. 2019 Mar;168:92-101. doi: 10.1016/j.puhe.2018.11.018.[CROSSREF]

23. Lescure D, Paget J, Schellevis F, van Dijk L. Determinants of Self-Medication With Antibiotics in European and Anglo-Saxon Countries: A Systematic Review of the Literature. Front Public Health. 2018 Dec 17;6:370. doi: 10.3389/fpubh.2018.00370.[CROSSREF]

24. Sunny TP, Jacob R, Krishnakumar K, Varghese S. Self-medication: Is a serious challenge to control antibiotic resistance? Natl. J. Physiol. Pharm. Pharmacol. 2019; 9:821–7. doi: 10.5455/njppp.2019.9.0620508062019.[HTTP]

25. Morgan DJ, Okeke IN, Laxminarayan R, Perencevich EN, Weisenberg S. Non-prescription antimicrobial use worldwide: a systematic review. Lancet Infect Dis. 2011 Sep;11(9):692-701. doi: 10.1016/S1473-3099(11)70054-8.[CROSSREF]

26. Rajkumar RP. COVID-19 and mental health: A review of the existing literature. Asian J Psychiatr. 2020 Aug;52:102066. doi: 10.1016/j.ajp.2020.102066.[CROSSREF]

27. Zhang A, Hobman EV, De Barro P, Young A, Carter DJ, Byrne M. Self-Medication with Antibiotics for Protection against COVID-19: The Role of Psychological Distress, Knowledge of, and Experiences with Antibiotics. Antibiotics (Basel). 2021 Feb 25;10(3):232. doi: 10.3390/antibiotics10030232.[CROSSREF]

28. Quincho-Lopez A, Benites-Ibarra CA, Hilario-Gomez MM, Quijano-Escate R, Taype-Rondan A. Self-medication practices to prevent or manage COVID-19: A systematic review. PLoS One. 2021 Nov 2;16(11):e0259317. doi: 10.1371/ journal.pone.0259317.[CROSSREF]

29. Monaghesh E, Hajizadeh A. The role of telehealth during COVID-19 outbreak: a systematic review based on current evidence. BMC Public Health. 2020 Aug 1;20(1):1193. doi: 10.1186/s12889-020-09301-4.[CROSSREF]

30. Entezarjou A, Calling S, Bhattacharyya T, Milos Nymberg V, Vigren L, Labaf A, et al. Antibiotic Prescription Rates After eVisits Versus Office Visits in Primary Care: Observational Study. JMIR Med Inform. 2021 Mar 15;9(3):e25473. doi: 10.2196/25473.[CROSSREF]

31. Ray KN, Shi Z, Gidengil CA, Poon SJ, Uscher-Pines L, Mehrotra A. Antibiotic Prescribing During Pediatric Direct-to-Consumer Telemedicine Visits. Pediatrics. 2019 May;143(5):e20182491. doi: 10.1542/peds.2018-2491.[CROSSREF]

32. Ray KN, Martin JM, Wolfson D, Schweiberger K, Schoemer P, Cepullio C, et al. Antibiotic Prescribing for Acute Respiratory Tract Infections During Telemedicine Visits Within a Pediatric Primary Care Network. Acad Pediatr. 2021 Sep-Oct;21(7):1239-43. doi: 10.1016/j.acap.2021.03.008.[CROSSREF]

33. Merchel Piovesan Pereira B, Tagkopoulos I. Benzalkonium Chlorides: Uses, Regulatory Status, and Microbial Resistance. Appl Environ Microbiol. 2019 Jun 17;85(13):e00377-19. doi: 10.1128/AEM.00377-19.[CROSSREF]

34. Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol. 2007 Jan;5(1):48-56. doi: 10.1038/nrmicro1557.[CROSSREF]

35. Rizvi SG, Ahammad SZ. COVID-19 and antimicrobial resistance: A crossstudy. Sci Total Environ. 2021 Oct 8;807(Pt 2):150873. doi: 10.1016/j.scitotenv.2021.150873.[CROSSREF]

36. Tomczyk S, Taylor A, Brown A, de Kraker MEA, El-Saed A, Alshamrani M, et al.; WHO AMR Surveillance and Quality Assessment Collaborating Centres Network. Impact of the COVID-19 pandemic on the surveillance, prevention and control of antimicrobial resistance: a global survey. J Antimicrob Chemother. 2021 Oct 11;76(11):3045-58. doi: 10.1093/jac/dkab300.[CROSSREF]

37. Hirabayashi A, Kajihara T, Yahara K, Shibayama K, Sugai M. Impact of the COVID-19 pandemic on the surveillance of antimicrobial resistance. J Hosp Infect. 2021 Nov;117:147-56. doi: 10.1016/j.jhin.2021.09.011.[CROSSREF]

38. McNeil JC, Flores AR, Kaplan SL, Hulten KG. The Indirect Impact of the SARSCoV-2 Pandemic on Invasive Group a Streptococcus, Streptococcus Pneumoniae and Staphylococcus Aureus Infections in Houston Area Children. Pediatr Infect Dis J. 2021 Aug 1;40(8):e313-e6. doi: 10.1097/INF.0000000000003195.[CROSSREF]


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