Healthcare-associated infections in COVID-19 and non-COVID-19 patients during the SARS-CoV-2 pandemic in an Indonesian Referral Hospital
DOI:
https://doi.org/10.3396/ijic.v22.23869Keywords:
Healthcare-Associated Infections, infection prevention and control (IPC), carbapenem resistance, COVID-19Abstract
Background: Low- and middle-income countries (LMICs) face more challenges in overcoming healthcare-associated infections (HAIs) due to limited data surveillance, especially during the COVID-19 pandemic. We investigated the epidemiology and relationships between HAIs and COVID-19 status in a referral hospital in Indonesia.
Methods: A retrospective study was conducted at Universitas Indonesia Hospital from 2021 to 2022. HAI types were categorized into ventilator-associated event (VAE), central line-associated bloodstream infection (CLABSI), and catheter-associated urinary tract infections (CAUTIs). Data were collected from the inpatient ward, emergency department, and intensive care unit. The association among HAIs, COVID-19, and isolated bacteria was analyzed descriptively, and multivariate logistic regression for potential risk factors.
Results: We evaluated 255 patients who experienced HAIs, including 159 patients with COVID-19. The incidence of CLABSI was significantly associated with COVID-19 patients (P < 0.001), whereas the occurrence of VAE was significantly lower (P = 0.001). There was no significant association with CAUTI (P = 0.870). Acinetobacter baumannii was isolated as a common cause of HAIs (19%). Carbapenem resistance rates were high among A. baumannii (89.8%) and Pseudomonas aeruginosa (86.9%). Risk factors of CLABSI included COVID-19 status and chronic renal disease, while that of VAE included sex-male (aOR = 1.97).
Conclusions: CLABSI was significantly associated with the occurrence of HAIs in patients with COVID-19, while VAE was low, and CAUTI was not significantly impacted. In addition, the isolation rate of carbapenem-resistant bacteria was high. It highlights the urgent need to strengthen the infection prevention and control and antimicrobial stewardship (AMS) approaches through continuous education, monitoring, and enhanced surveillance efforts at the facility level.
Downloads
References
1.
World Health Organization (WHO). Report on the Burden of Endemic Health Care-Associated Infection Worldwide Clean Care is Safer Care. Geneva, Switzerland: WHO Document Production Services; 2011.
2.
Tartari E, Tomczyk S, Pires D, Zayed B, Coutinho Rehse AP, Kariyo P, et al. Implementation of the infection prevention and control core components at the national level: a global situational analysis. J Hosp Infect 2021; 108: 94–103. doi: 10.1016/j.jhin.2020.11.025
3.
Takaya S, Hayakawa K, Matsunaga N, Moriyama Y, Katanami Y, Tajima T, et al. Surveillance systems for healthcare-associated infection in high and upper-middle income countries: a scoping review. J Infect Chemother 2020; 26: 429–37. doi: 10.1016/j.jiac.2020.01.001
4.
Wah Goh LP, Marbawi H, Goh SM, bin Abdul Asis AK, Gansau JA. The prevalence of hospital-acquired infections in Southeast Asia (1990–2022). J Infect Dev Ctries 2023; 17: 139–46. doi: 10.3855/JIDC.17135
5.
Maki G, Zervos M. Health care–acquired infections in low- and middle-income countries and the role of infection prevention and control. Infect Dis Clin North Am 2021; 35: 827–39. doi: 10.1016/j.idc.2021.04.014
6.
Deiana G, Arghittu A, Gentili D, Dettori M, Palmieri A, Masia MD, et al. Impact of the COVID-19 pandemic on the prevalence of HAIs and the use of antibiotics in an Italian University Hospital. Healthcare (Switzerland) 2022; 10(9): 1597. doi: 10.3390/healthcare10091597
7.
Baker MA, Sands KE, Huang SS, Kleinman K, Septimus EJ, Varma N, et al. The impact of coronavirus disease 2019 (COVID-19) on healthcare-associated infections. Clin Infect Dis 2022; 74: 1748–54. doi: 10.1093/cid/ciab688
8.
Saleem Z, Godman B, Hassali MA, Hashmi FK, Azhar F, Rehman IU. Point prevalence surveys of health-care-associated infections: a systematic review. Pathog Glob Health 2019; 113: 191–205. doi: 10.1080/20477724.2019.1632070
9.
Jha DK, Khanal B, Sah BP, Baral R. Ventilator associated events: incidence, microbiological profile and outcome in the intensive care unit in a tertiary hospital of eastern Nepal. Indian J Microbiol Res 2023; 10: 29–32. doi: 10.18231/j.ijmr.2023.005
10.
Wee LEI, Conceicao EP, Tan JY, Magesparan KD, Amin IBM, Ismail BBS, et al. Unintended consequences of infection prevention and control measures during COVID-19 pandemic. Am J Infect Contr 2021; 49: 469–77. doi: 10.1016/j.ajic.2020.10.019
11.
O’Toole RF. The interface between COVID-19 and bacterial healthcare-associated infections. Clin Microbiol Infect 2021; 27: 1772–6. doi: 10.1016/j.cmi.2021.06.001
12.
Rosenthal VD, Myatra SN, Divatia JV, Biswas S, Shrivastava A, Al-Ruzzieh MA, et al. The impact of COVID-19 on health care–associated infections in intensive care units in low- and middle-income countries: International Nosocomial Infection Control Consortium (INICC) findings. Int J Infect Dis 2022; 118: 83–8. doi: 10.1016/j.ijid.2022.02.041
13.
Badger-Emeka L, Al Rashed AS, Aljindan RY, Emeka PM, Quadri SA, Almutairi HH. Incidence of drug-resistant hospital-associated gram-negative bacterial infections, the accompanying risk factors, and clinical outcomes with treatment. Antibiotics 2023; 12: 1425. doi: 10.3390/antibiotics12091425
14.
Meynaar IA, van Rijn S, Ottens TH, van Burgel ND, van Nieuwkoop C. Increased risk of central line-associated bloodstream infection in COVID-19 patients associated with dexamethasone but not with interleukin antagonists. Intensive Care Med 2022; 48: 954–7. doi: 10.1007/s00134-022-06750-w
15.
Youssef J, Novosad SA, Winthrop KL. Infection risk and safety of corticosteroid use. Rheumatic Dis Clin N Am 2016; 42: 157–76. doi: 10.1016/j.rdc.2015.08.004
16.
Kılıç Erol P, Erol K, Şahin AS. Corticosteroid use in severe COVID-19 and factors associated with secondary infection and mortality among patients admitted to the intensive care unit. Bagcilar Med Bull 2025: 182–192. doi: 10.4274/bmb.galenos.2025.43534
17.
Alsaffar MJ, Alsheddi FM, Humayun T, Aldalbehi FZ, Alshammari WHS, Aldecoa YS, et al. Impact of COVID-19 pandemic on the rates of central line. Associated bloodstream infection and catheter-associated urinary tract infection in an. Iintensive care setting: national experience. Am J Infect Control 2023; 51: 1108–13. doi: 10.1016/j.ajic.2023.03.016
18.
Gupta P, Thomas M, Patel A, George R, Mathews L, Alex S, et al. Bundle approach used to achieve zero central line-associated bloodstream infections in an adult coronary intensive care unit. BMJ Open Qual 2021; 10: e001200. https://doi.org/10.1136/bmjoq-2020-001200
19.
Laurent M, Bories PN, Le Thuaut A, Liuu E, Ledudal K, Bastuji-Garin S, et al. Impact of comorbidities on hospital-acquired infections in a geriatric rehabilitation unit: Prospective study of 252 patients. J Am Med Dir Assoc 2012; 13: 760.e7–760.e12. doi: 10.1016/j.jamda.2012.07.002
20.
Ganesan V, Sundaramurthy R, Thiruvanamalai R, Sivakumar VA, Udayasankar S, Arunagiri R, et al. Device-associated hospital-acquired infections: does active surveillance with bundle care offer a pathway to minimize them? Cureus 2021; 13(11): 1–8. doi: 10.7759/cureus.19331
21.
Avci M, Ozgenc O, Coskuner SA, Olut AI. Hospital acquired infections (HAI) in the elderly: comparison with the younger patients. Arch Gerontol Geriatr 2012; 54: 247–50. doi: 10.1016/j.archger.2011.03.014
22.
Indrawati L, Tjandrarini DH, Sulistiyowati N, Afifah T, Paramita A, Senewe FP, et al. Characteristics of hospitalized patients with confirmed COVID-19 and their hospital management. Asian Pac J Trop Med 2024; 17: 129–35. doi: 10.4103/apjtm.apjtm_520_23
23.
Surendra H, Elyazar IR, Djaafara BA, Ekawati LL, Saraswati K, Adrian V, et al. Clinical characteristics and mortality associated with COVID-19 in Jakarta, Indonesia: a hospital-based retrospective cohort study. Lancet Reg Health West Pac 2021; 9: 1–9. doi: 10.1016/j.lanwpc.2021.100108
24.
Erdem I, Yıldırım I, Safak B, Karaali R, Erdal B, Ardic E, et al. A 5-year surveillance of healthcare-associated infections in a university hospital: a retrospective analysis. SAGE Open Med 2022; 10: 1–7. doi: 10.1177/20503121221091789.
25.
Russo A, Gavaruzzi F, Ceccarelli G, Borrazzo C, Oliva A, Alessandri F, et al. Multidrug-resistant Acinetobacter baumannii infections in COVID-19 patients hospitalized in intensive care unit. Infection 2022; 50: 83–92. doi: 10.1007/s15010-021-01643-4
26.
Liu Y, Liu Y, Dai J, Liu A, Li Y, Xu J, et al. Klebsiella pneumoniae pneumonia in patients with rheumatic autoimmune diseases: clinical characteristics, antimicrobial resistance and factors associated with extended-spectrum β-lactamase production. BMC Infect Dis 2021; 21: 1–10. doi: 10.1186/s12879-021-06055-1
27.
Papic I, Bistrovic P, Cikara T, Busic N, Keres T, Ortner Hadziabdic M, et al. Corticosteroid dosing level, incidence and profile of bacterial blood stream infections in hospitalized COVID-19 patients. Viruses 2024; 16: 1–11. doi: 10.3390/v16010086
28.
Mai HTT, Espinoza JL. The impact of COVID-19 pandemic on ESBL-producing enterobacterales infections: a scoping review. Antibiotics 2023; 12: 1–13. doi: 10.3390/antibiotics12061064
29.
Obaid NA, Almarzoky Abuhussain S, Mulibari KK, Alshanqiti F, Malibari SA, Althobaiti SS, et al. Antimicrobial-resistant pathogens related to catheter-associated urinary tract infections in intensive care units: a multi-center retrospective study in the Western region of Saudi Arabia. Clin Epidemiol Glob Health 2023; 21: 1–6. doi: 10.1016/j.cegh.2023.101291
30.
Mobarak-Qamsari M, Jenaghi B, Sahebi L, Norouzi-Shadehi M, Salehi MR, Shakoori-Farahani A, et al. Evaluation of Acinetobacter baumannii, Klebsiella pneumoniae, and Staphylococcus aureus respiratory tract superinfections among patients with COVID-19 at a tertiary-care hospital in Tehran, Iran. Eur J Med Res 2023; 28: 1–11. doi: 10.1186/s40001-023-01303-3.
31.
Mohandas A, Valsan C, Joseph S, Varghese R, Baby J, Jacob S, et al. Impact of conducting hand hygiene audits during the COVID-19 pandemic in an intensive care unit at a tertiary care centre in Kerala, India. GMS Hyg Infect Contr 2024; 19: 1–6.
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2026 Gayatri Mauly Purwandari, Satoshi Kakiuchi , Masato Tashiro, Dimas Seto, Agustin Indracahyani, Irandi Putra Pratomo, Koichi Izumikawa, Takeshi Tanaka

This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright of their work, with first publication rights granted to IJIC. Read the full Copyright- and Licensing Statement.


