Determine phenotypical patterns of resistance to antibiotics in COVID-19 patients with associated bacterial infection: largest medical center in Iran
-
Esmaeil Mohammadnejad
,
Arash Seifi
,
Reza Ghanei Gheshlagh
,
Amir Aliramezani
,
Samrand Fattah Ghazi
,
Mohammadreza Salehi
,
Seyed Ali Dehghan Manshadi
,
Amirhossein Orandi
Abstract
Background and Objectives: Antibacterial resistance (AMR) is a serious threat and major concern, especially in developing countries. Therefore, we aimed to determine phenotypical patterns of resistance to antibiotics in COVID-19 patients with associated bacterial infection in intensive care units.
Materials and Methods: In this cross-sectional study, 6524 COVID-19 patients admitted for more than 48 h in the ICUs of Imam Khomeini Complex Hospital (IKCH) in Tehran from March 2020 to January 2022 were included in the study with initial diagnosis of COVID-19 (PCR test and chest imaging). Data were collected regarding severity of the illness, primary reason for ICU admission, presence of risk factors, presence of infection, length of ICU and hospital stay, microbial type, and antibiotic resistance. In this study, the pattern of antibiotic resistance was determined using the Kirby–Bauer disk diffusion method.
Results: In this study, 439 (37.5%) were ventilator-related events (VAEs), and 46% of all hospitalized patients had an underlying disease. The most common microorganisms in COVID-19 patients were carbapenem resistant Klebsiella pneumoniae (KPCs) (31.6%), Escherichia coli (E. coli) (15.8%), and Acinetobacter baumannii (A. baumannii) (15.7%), respectively. Prevalence of vancomycin-resistant enterococci (VRE) and KPCs were 88% and 82%, respectively.
Conclusion: A study on AMR surveillance is the need of the hour as it will help centers to generate local antibiograms that will further help formulate national data. It will guide doctors to choose the appropriate empiric treatment, and these studies will be the basis for establishing antimicrobial surveillance and monitoring and regulating of the use of antimicrobials.
1. Abdollahi A, Shakoori A, Khoshnevis H, Arabzadeh M, Dehghan Manshadi SA, Mohammadnejad E, et al. Comparison of patient-collected and lab technician-collected nasopharyngeal and oropharyngeal swabs for detection of COVID-19 by RT-PCR. Iran J Pathol 2020; 15: 313-319.
2. Mohammadnejad E, Abbaszadeh A, Soori H, Afhami S. Prevention and control of nosocomial infections proceeding in intensive care units: A content analysis study. Acta Med Mediterr 2016; 32: 1295-1301.
3. Mohammadnejad E, Manshadi SAD, Mohammadi MTB, Abdollai A, Seifi A, Salehi MR, et al. Prevalence of nosocomial infections in COVID-19 patients admitted to the intensive care unit of Imam Khomeini complex hospital in Tehran. Iran J Microbiol 2021; 13: 764-768.
4. Taher Al Barzin RMG, Ghafour Raheem S, Khudhur PK, Abdulkarimi R, Mohammadnejad E, Tabatabaee A. Interleukin-6 role in the severity of COVID-19 and intensive care unit stay length. Cell Mol Biol (Noisy-le-grand) 2020; 66: 15-18.
5. Moolchandani K, Sastry AS, Deepashree R, Sistla S, Harish B, Mandal J. Antimicrobial resistance surveillance among intensive care units of a tertiary care hospital in Southern India. J Clin Diagn Res 2017; 11: DC01-DC07.
6. Allameh SF, Nemati S, Ghalehtaki R, Mohammadnejad E, Aghili SM, Khajavirad N, et al. Clinical characteristics and outcomes of 905 COVID-19 patients admitted to Imam Khomeini hospital complex in the capital city of Tehran, Iran. Arch Iran Med 2020: 23: 766-775.
7. Podolsky SH. The evolving response to antibiotic resistance (1945–2018). Palgrave Commun 2018; 4: 124.
8. Getahun H, Smith I, Trivedi K, Paulin S, Balkhy HH. Tackling antimicrobial resistance in the COVID-19 pandemic. Bull World Health Organ 2020; 98: 442-442A.
9. Pérez de la Lastra JM, Anand U, González-Acosta S, López MR, Dey A, Bontempi E, et al. Antimicrobial resistance in the COVID-19 landscape: is there an opportunity for anti-infective antibodies and antimicrobial peptides? Front Immunol 2022; 13: 921483.
10. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et al. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist 2018; 11: 1645-1658.
11. Ukuhor HO. The interrelationships between antimicrobial resistance, COVID-19, past, and future pandemics. J Infect Public Health 2021; 14: 53-60.
12. Majumder MAA, Rahman S, Cohall D, Bharatha A, Singh K, Haque M, et al. Antimicrobial stewardship: Fighting antimicrobial resistance and protecting global public health. Infect Drug Resist 2020; 13: 4713-4738.
13. Rabirad N, Nejad EM, Hadizadeh MR, Begjan J, Ehsani SR. The prevalence of TB in HIV patients and risk factor with frequent referral (Iran, 2009-10). Iran Red Crescent Med J 2013; 15: 58-61.
14. Mohammad Nejad E, Jafari S, Mahmoodi M, Begjani J, Roghayyeh Ehsani S, Rabirad N. Hepatitis B virus antibody levels in high-risk health care workers. Hepat Mon 2011; 11: 662-663.
15. Akbari M, Nejad Rahim R, Azimpour A, Bernousi I, Ghahremanlu H. A survey of nosocomial infections in intensive care units in an Imam Reza hospital to provide appropriate preventive guides based on international standards. Studies Med Sci 2013; 23: 591-596.
16. Kumar A, Chaudhry D, Goel N, Tanwar S. Epidemiology of Intensive Care Unit-acquired Infections in a Tertiary Care Hospital of North India. Indian J Crit Care Med 2021; 25: 1427-1433.
17. Eggimann P, Pittet D. Infection control in the ICU. Chest 2001; 120: 2059-2093.
18. Yallew WW, Kumie A, Yehuala FM. Risk factors for hospital-acquired infections in teaching hospitals of Amhara regional state, Ethiopia: A matched-case control study. PLoS One 2017; 12(7): e0181145.
19. Sharifipour E, Shams S, Esmkhani M, Khodadadi J, Fotouhi-Ardakani R, Koohpaei A, et al. Evaluation of bacterial co-infections of the respiratory tract in COVID-19 patients admitted to ICU. BMC Infect Dis 2020; 20: 646.
20. Li J, Wang J, Yang Y, Cai P, Cao J, Cai X, 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: 153.
21. Sang L, Xi Y, Lin Z, Pan Y, Song B, Li C-A, et al. Secondary infection in severe and critical COVID-19 patients in China: a multicenter retrospective study. Ann Palliat Med 2021; 10: 8557-8570.
22. Kariyawasam RM, Julien DA, Jelinski DC, Larose SL, Rennert-May E, Conly JM, et al. Antimicrobial resistance (AMR) in COVID-19 patients: a systematic review and meta-analysis (November 2019–June 2021). Antimicrob Resist Infect Control 2022; 11: 45.
23. Khoshbakht R, Kabiri M, Neshani A, Khaksari MN, Sadrzadeh SM, Mousavi SM, et al. Assessment of antibiotic resistance changes during the COVID-19 pandemic in northeast of Iran during 2020–2022: an epidemiological study. Antimicrob Resist Infect Control 2022; 11: 121.
24. Langford BJ, So M, Raybardhan S, Leung V, Soucy J-PR, Westwood D, et al. Antibiotic prescribing in patients with COVID-19: rapid review and meta-analysis. Clin Microbiol Infect 2021; 27: 520-531.
25. Moradi N, Kazemi N, Ghaemi M, Mirzaei B. Frequency and antimicrobial resistance pattern of bacterial isolates from patients with COVID-19 in two hospitals of Zanjan. Iran J Microbiol 2021; 13: 769-778.
26. Maragakis LL, Perl TM. Acinetobacter baumannii: epidemiology, antimicrobial resistance, and treatment options. Clin Infect Dis 2008; 46: 1254-1263.
27. Bonomo RA, Szabo D. Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin Infect Dis 2006; 43 Suppl 2: S49-56.
28. Maraki S, Mantadakis E, Mavromanolaki VE, Kofteridis DP, Samonis G. A 5-year surveillance study on antimicrobial resistance of Acinetobacter baumannii clinical isolates from a tertiary Greek hospital. Infect Chemother 2016; 48: 190-198.
29. Souli M, Galani I, Giamarellou H. Emergence of extensively drug-resistant and pandrug-resistant Gram-negative bacilli in Europe. Euro Surveill 2008; 13: 19045.
30. Moradi J, Hashemi FB, Bahador A. Antibiotic resistance of Acinetobacter baumannii in Iran: a systemic review of the published literature. Osong Public Health Res Perspect 2015; 6: 79-86.
31. Chandra' P, V R, M S, Cs S, Mk U. Multidrug-resistant Acinetobacter baumannii infections: looming threat in the Indian clinical setting. Expert Rev Anti Infect Ther 2022; 20: 721-732.
32. Xie R, Zhang XD, Zhao Q, Peng B, Zheng J. Analysis of global prevalence of antibiotic resistance in Acinetobacter baumannii infections disclosed a faster increase in OECD countries. Emerg Microbes Infect 2018; 7: 31.
33. Giamarellou H, Antoniadou A, Kanellakopoulou K. Acinetobacter baumannii: a universal threat to public health? Int J Antimicrob Agents 2008; 32: 106-119.
34. Shields RK, Clancy CJ, Gillis LM, Kwak EJ, Silveira FP, Massih RCA, et al. Epidemiology, clinical characteristics and outcomes of extensively drug-resistant Acinetobacter baumannii infections among solid organ transplant recipients. PLoS One 2012; 7(12): e52349.
35. Mostafavi SN, Rostami S, Nokhodian Z, Ataei B, Cheraghi A, Ataabadi P, et al. Antibacterial resistance patterns of Acinetobacter baumannii complex: The results of Isfahan antimicrobial resistance surveillance-1 program. Asian Pac J Trop Med 2021; 14: 316-322.
36. Rump B, Timen A, Hulscher M, Verweij M. Ethics of infection control measures for carriers of antimicrobial drug–resistant organisms. Emerg Infect Dis 2018; 24: 1609-1616.
37. Toner E, Adalja A, Gronvall GK, Cicero A, Inglesby TV. Antimicrobial resistance is a global health emergency. Health Secur 2015; 13: 153-155.
38. Ghaffarpasand I, Moniri R, Kheradi E, Tehrani M. Antibiotic resistance in fecal enterococci in hospitalized patients. Indian J Pathol Microbiol 2010; 53: 898-899.
39. Asnaashari M, Eghbal MJ, Yaghmayi AS, Shokri M, Azari-Marhabi S. Comparison of antibacterial effects of photodynamic therapy, modified triple antibiotic paste and calcium hydroxide on root canals infected with Enterococcus faecalis: an in vitro study. J Lasers Med Sci 2019; 10(Suppl 1): S23-S29.
40. Lee M-C, Lu C-H, Lee W-Y, Lee C-M. Correlation between nosocomial carriage of vancomycin-resistant Enterococci and antimicrobial use in Taiwan. Am J Trop Med Hyg 2020; 104: 1131-1136.
41. Li G, Walker MJ, De Oliveira DM. Vancomycin resistance in Enterococcus and Staphylococcus aureus. Microorganisms 2022; 11: 24.
42. Nellore A, Huprikar S, AST ID Community of Practice. Vancomycin-resistant Enterococcus in solid organ transplant recipients: Guidelines from the American Society of Transplantation Infectious Diseases Community of Practice. Clin Transplant 2019; 33(9): e13549.
43. Linden PK. Treatment options for vancomycin-resistant enterococcal infections. Drugs 2002; 62: 425-441.
44. Kauffman CA. Therapeutic and preventative options for the management of vancomycin-resistant enterococcal infections. J Antimicrob Chemother 2003; 51 Suppl 3: iii23-30.
45. Markwart R, Willrich N, Haller S, Noll I, Koppe U, Werner G, et al. The rise in vancomycin-resistant Enterococcus faecium in Germany: data from the German antimicrobial resistance surveillance (ARS). Antimicrob Resist Infect Control 2019; 8: 147.
46. Moussally M, Zahreddine N, Kazma J, Ahmadieh R, Kan SS, Kanafan ZA. Prevalence of antibiotic-resistant organismsamong hospitalized patients at a tertiary care center in Lebanon, 2010–2018. J Infect Public Health 2021; 14: 12-16.
47. Molechan C, Amoako DG, Abia ALK, Somboro AM, Bester LA, Essack SY. Molecular epidemiology of antibiotic-resistant Enterococcus spp. from the farm-to-fork continuum in intensive poultry production in KwaZulu-Natal, South Africa. Sci Total Environ 2019; 692: 868-878.
2. Mohammadnejad E, Abbaszadeh A, Soori H, Afhami S. Prevention and control of nosocomial infections proceeding in intensive care units: A content analysis study. Acta Med Mediterr 2016; 32: 1295-1301.
3. Mohammadnejad E, Manshadi SAD, Mohammadi MTB, Abdollai A, Seifi A, Salehi MR, et al. Prevalence of nosocomial infections in COVID-19 patients admitted to the intensive care unit of Imam Khomeini complex hospital in Tehran. Iran J Microbiol 2021; 13: 764-768.
4. Taher Al Barzin RMG, Ghafour Raheem S, Khudhur PK, Abdulkarimi R, Mohammadnejad E, Tabatabaee A. Interleukin-6 role in the severity of COVID-19 and intensive care unit stay length. Cell Mol Biol (Noisy-le-grand) 2020; 66: 15-18.
5. Moolchandani K, Sastry AS, Deepashree R, Sistla S, Harish B, Mandal J. Antimicrobial resistance surveillance among intensive care units of a tertiary care hospital in Southern India. J Clin Diagn Res 2017; 11: DC01-DC07.
6. Allameh SF, Nemati S, Ghalehtaki R, Mohammadnejad E, Aghili SM, Khajavirad N, et al. Clinical characteristics and outcomes of 905 COVID-19 patients admitted to Imam Khomeini hospital complex in the capital city of Tehran, Iran. Arch Iran Med 2020: 23: 766-775.
7. Podolsky SH. The evolving response to antibiotic resistance (1945–2018). Palgrave Commun 2018; 4: 124.
8. Getahun H, Smith I, Trivedi K, Paulin S, Balkhy HH. Tackling antimicrobial resistance in the COVID-19 pandemic. Bull World Health Organ 2020; 98: 442-442A.
9. Pérez de la Lastra JM, Anand U, González-Acosta S, López MR, Dey A, Bontempi E, et al. Antimicrobial resistance in the COVID-19 landscape: is there an opportunity for anti-infective antibodies and antimicrobial peptides? Front Immunol 2022; 13: 921483.
10. Aslam B, Wang W, Arshad MI, Khurshid M, Muzammil S, Rasool MH, et al. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist 2018; 11: 1645-1658.
11. Ukuhor HO. The interrelationships between antimicrobial resistance, COVID-19, past, and future pandemics. J Infect Public Health 2021; 14: 53-60.
12. Majumder MAA, Rahman S, Cohall D, Bharatha A, Singh K, Haque M, et al. Antimicrobial stewardship: Fighting antimicrobial resistance and protecting global public health. Infect Drug Resist 2020; 13: 4713-4738.
13. Rabirad N, Nejad EM, Hadizadeh MR, Begjan J, Ehsani SR. The prevalence of TB in HIV patients and risk factor with frequent referral (Iran, 2009-10). Iran Red Crescent Med J 2013; 15: 58-61.
14. Mohammad Nejad E, Jafari S, Mahmoodi M, Begjani J, Roghayyeh Ehsani S, Rabirad N. Hepatitis B virus antibody levels in high-risk health care workers. Hepat Mon 2011; 11: 662-663.
15. Akbari M, Nejad Rahim R, Azimpour A, Bernousi I, Ghahremanlu H. A survey of nosocomial infections in intensive care units in an Imam Reza hospital to provide appropriate preventive guides based on international standards. Studies Med Sci 2013; 23: 591-596.
16. Kumar A, Chaudhry D, Goel N, Tanwar S. Epidemiology of Intensive Care Unit-acquired Infections in a Tertiary Care Hospital of North India. Indian J Crit Care Med 2021; 25: 1427-1433.
17. Eggimann P, Pittet D. Infection control in the ICU. Chest 2001; 120: 2059-2093.
18. Yallew WW, Kumie A, Yehuala FM. Risk factors for hospital-acquired infections in teaching hospitals of Amhara regional state, Ethiopia: A matched-case control study. PLoS One 2017; 12(7): e0181145.
19. Sharifipour E, Shams S, Esmkhani M, Khodadadi J, Fotouhi-Ardakani R, Koohpaei A, et al. Evaluation of bacterial co-infections of the respiratory tract in COVID-19 patients admitted to ICU. BMC Infect Dis 2020; 20: 646.
20. Li J, Wang J, Yang Y, Cai P, Cao J, Cai X, 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: 153.
21. Sang L, Xi Y, Lin Z, Pan Y, Song B, Li C-A, et al. Secondary infection in severe and critical COVID-19 patients in China: a multicenter retrospective study. Ann Palliat Med 2021; 10: 8557-8570.
22. Kariyawasam RM, Julien DA, Jelinski DC, Larose SL, Rennert-May E, Conly JM, et al. Antimicrobial resistance (AMR) in COVID-19 patients: a systematic review and meta-analysis (November 2019–June 2021). Antimicrob Resist Infect Control 2022; 11: 45.
23. Khoshbakht R, Kabiri M, Neshani A, Khaksari MN, Sadrzadeh SM, Mousavi SM, et al. Assessment of antibiotic resistance changes during the COVID-19 pandemic in northeast of Iran during 2020–2022: an epidemiological study. Antimicrob Resist Infect Control 2022; 11: 121.
24. Langford BJ, So M, Raybardhan S, Leung V, Soucy J-PR, Westwood D, et al. Antibiotic prescribing in patients with COVID-19: rapid review and meta-analysis. Clin Microbiol Infect 2021; 27: 520-531.
25. Moradi N, Kazemi N, Ghaemi M, Mirzaei B. Frequency and antimicrobial resistance pattern of bacterial isolates from patients with COVID-19 in two hospitals of Zanjan. Iran J Microbiol 2021; 13: 769-778.
26. Maragakis LL, Perl TM. Acinetobacter baumannii: epidemiology, antimicrobial resistance, and treatment options. Clin Infect Dis 2008; 46: 1254-1263.
27. Bonomo RA, Szabo D. Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin Infect Dis 2006; 43 Suppl 2: S49-56.
28. Maraki S, Mantadakis E, Mavromanolaki VE, Kofteridis DP, Samonis G. A 5-year surveillance study on antimicrobial resistance of Acinetobacter baumannii clinical isolates from a tertiary Greek hospital. Infect Chemother 2016; 48: 190-198.
29. Souli M, Galani I, Giamarellou H. Emergence of extensively drug-resistant and pandrug-resistant Gram-negative bacilli in Europe. Euro Surveill 2008; 13: 19045.
30. Moradi J, Hashemi FB, Bahador A. Antibiotic resistance of Acinetobacter baumannii in Iran: a systemic review of the published literature. Osong Public Health Res Perspect 2015; 6: 79-86.
31. Chandra' P, V R, M S, Cs S, Mk U. Multidrug-resistant Acinetobacter baumannii infections: looming threat in the Indian clinical setting. Expert Rev Anti Infect Ther 2022; 20: 721-732.
32. Xie R, Zhang XD, Zhao Q, Peng B, Zheng J. Analysis of global prevalence of antibiotic resistance in Acinetobacter baumannii infections disclosed a faster increase in OECD countries. Emerg Microbes Infect 2018; 7: 31.
33. Giamarellou H, Antoniadou A, Kanellakopoulou K. Acinetobacter baumannii: a universal threat to public health? Int J Antimicrob Agents 2008; 32: 106-119.
34. Shields RK, Clancy CJ, Gillis LM, Kwak EJ, Silveira FP, Massih RCA, et al. Epidemiology, clinical characteristics and outcomes of extensively drug-resistant Acinetobacter baumannii infections among solid organ transplant recipients. PLoS One 2012; 7(12): e52349.
35. Mostafavi SN, Rostami S, Nokhodian Z, Ataei B, Cheraghi A, Ataabadi P, et al. Antibacterial resistance patterns of Acinetobacter baumannii complex: The results of Isfahan antimicrobial resistance surveillance-1 program. Asian Pac J Trop Med 2021; 14: 316-322.
36. Rump B, Timen A, Hulscher M, Verweij M. Ethics of infection control measures for carriers of antimicrobial drug–resistant organisms. Emerg Infect Dis 2018; 24: 1609-1616.
37. Toner E, Adalja A, Gronvall GK, Cicero A, Inglesby TV. Antimicrobial resistance is a global health emergency. Health Secur 2015; 13: 153-155.
38. Ghaffarpasand I, Moniri R, Kheradi E, Tehrani M. Antibiotic resistance in fecal enterococci in hospitalized patients. Indian J Pathol Microbiol 2010; 53: 898-899.
39. Asnaashari M, Eghbal MJ, Yaghmayi AS, Shokri M, Azari-Marhabi S. Comparison of antibacterial effects of photodynamic therapy, modified triple antibiotic paste and calcium hydroxide on root canals infected with Enterococcus faecalis: an in vitro study. J Lasers Med Sci 2019; 10(Suppl 1): S23-S29.
40. Lee M-C, Lu C-H, Lee W-Y, Lee C-M. Correlation between nosocomial carriage of vancomycin-resistant Enterococci and antimicrobial use in Taiwan. Am J Trop Med Hyg 2020; 104: 1131-1136.
41. Li G, Walker MJ, De Oliveira DM. Vancomycin resistance in Enterococcus and Staphylococcus aureus. Microorganisms 2022; 11: 24.
42. Nellore A, Huprikar S, AST ID Community of Practice. Vancomycin-resistant Enterococcus in solid organ transplant recipients: Guidelines from the American Society of Transplantation Infectious Diseases Community of Practice. Clin Transplant 2019; 33(9): e13549.
43. Linden PK. Treatment options for vancomycin-resistant enterococcal infections. Drugs 2002; 62: 425-441.
44. Kauffman CA. Therapeutic and preventative options for the management of vancomycin-resistant enterococcal infections. J Antimicrob Chemother 2003; 51 Suppl 3: iii23-30.
45. Markwart R, Willrich N, Haller S, Noll I, Koppe U, Werner G, et al. The rise in vancomycin-resistant Enterococcus faecium in Germany: data from the German antimicrobial resistance surveillance (ARS). Antimicrob Resist Infect Control 2019; 8: 147.
46. Moussally M, Zahreddine N, Kazma J, Ahmadieh R, Kan SS, Kanafan ZA. Prevalence of antibiotic-resistant organismsamong hospitalized patients at a tertiary care center in Lebanon, 2010–2018. J Infect Public Health 2021; 14: 12-16.
47. Molechan C, Amoako DG, Abia ALK, Somboro AM, Bester LA, Essack SY. Molecular epidemiology of antibiotic-resistant Enterococcus spp. from the farm-to-fork continuum in intensive poultry production in KwaZulu-Natal, South Africa. Sci Total Environ 2019; 692: 868-878.
| Files | ||
| Issue | Vol 15 No 3 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i3.12893 | |
| Keywords | ||
| Pneumonia; COVID-19; Intensive care unit; Antimicrobial resistance; Surveillance | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Mohammadnejad E, Seifi A, Ghanei Gheshlagh R, Aliramezani A, Fattah Ghazi S, Salehi M, Dehghan Manshadi SA, Orandi A. Determine phenotypical patterns of resistance to antibiotics in COVID-19 patients with associated bacterial infection: largest medical center in Iran. Iran J Microbiol. 2023;15(3):336-342.
