Home J Young Pharm. Vol 15/Issue 3/2023 Healthcare-Associated Infections: A Ten-Year Bibliometric Analysis

Healthcare-Associated Infections: A Ten-Year Bibliometric Analysis

by admin

Corresponding author.

Correspondence: Mrs. Rehab Ismaeil, PhD Student, Department of Pharmacy Practice, Kulliyah of Pharmacy, International Islamic University Malaysia (IIUM), Jalan Sultan Ahmad Shah, Kuantan, Pahang, MALAYSIA. Email: [email protected]
Received March 12, 2023; Revised March 25, 2023; Accepted April 02, 2023.
Copyright ©2023 Author (s)
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

Citation

1.Ismaeil R, Fata Nahas AR, Kamarudin NB, Mat Nor MB, Abubakar U, Mohamed MHN. Healthcare-Associated Infections: A Ten-Year Bibliometric Analysis. Journal of Young Pharmacists [Internet]. 2023 Aug 25;15(3):397–405. Available from: http://dx.doi.org/10.5530/jyp.2023.15.55
Copy to clipboard
Published in: Journal of Young Pharmacists, 2023; 15(3): 397-405.Published online: 22 August 2023DOI: 10.5530/jyp.2023.15.55

ABSTRACT

Healthcare-Associated Infections (HCAIs) pose a significant threat to the safety of patients and Healthcare Workers (HCWs). HCAIs increase morbidity and mortality, as well as healthcare costs. Therefore, prevention is a key goal for healthcare organisations and systems. In this regard, this study aims to conduct a bibliometric analysis of research and review papers published in journals indexed in the PubMed database between 2013 and 2023 on HCAIs in order to investigate areas of concentration and developing trends in the field. There was a total of 356 core zone publications, and the number of articles published is expected to reach its high in 2020. Most of the papers were found to have been published in the journals of hospital infection and antibiotic resistance and infection control. European countries conduct the most and more collaborative scientific research in this area, followed by the United States, Australia, and China. Surveillance, infection control, hand hygiene and COVID-19 represent the leading frontiers and research hotspots for HCAIs. HCAIs and Infection Prevention and Control (IPC) also co-occurred in most of the study discussions. The analysis is expected to yield meaningful data by illuminating the overall structure and direction of previous research on HCAIs, as well as by providing important ideas for future research.

Keywords: Bibliometric analysis, Healthcare associated infection, Infection prevention and control

INTRODUCTION

Healthcare-Associated Infections (HCAIs) are the most common type of complication experienced by patients. It includes Ventilator-Associated Infections or Events (VAE), Pneumonia (PNEU), Surgical Site Infection (SSI), Bloodstream Infection (BSI), and Urinary Tract Infection (UTI).1,2 HCAIs continue to be a leading cause of morbidity and mortality despite advances in infection detection and control.35 Along with longer hospital stays, antibiotic overuse, and the development of multidrug-resistant bacteria, which place a significant financial strain on health care systems.68 The global burden of HCAIs is estimated by the World Health Organization (WHO) to be between 3.6% and 12.0% in high-income countries and between 5.4% and 19.1% in low- and middle-income countries (LMIC).9 Infection Prevention and Control (IPC) has been acknowledged as an essential component of the healthcare system, emphasising the importance of Standard Precautions (SP) in preventing and mitigating the risk of infectious disease transmission.3,10 The persistently high rates of HCAIs can be traced partly to the healthcare sector’s failure to adhere to IPC requirements.3,11 The global spread of COVID-19 has placed a heavy strain on the medical community and the world, introducing new challenges and potential to IPC strategies.12,13 COVID-19 prevention attempts may have hindered or diverted IPC efforts, leading to a substantial increase in HCAI infections among COVID-19 patients.1315

Bibliometrics analysis is a quantitative statistical method used to examine the evolution of research topics and the structure of existing knowledge.16,17 It is a popular strategy used to pinpoint trends, hotspots, and developing areas in particular fields.18,19 It utilises various analysis techniques, such as performance-based analyses by grouping publications by country, university, or author and a study of citations.18,19 Many topics, including surgical site infections, antibiotic stewardship, and infectious disease in liver transplant patients, have been evaluated by bibliometric analyses.16,20,21 Despite the prevalence of HCAIs, bibliometric
research in this area is still limited. Currently, only one known bibliometric study focuses on HCAIs in Asia.22 Therefore, this study aims to highlight the general structure of the literature on HCAIs by assessing and reviewing the research in English language articles core source of Bradford’s law zone published in journals scanned in the PubMed database between 2013 and 2023.

Description Results
Time span 2013-2023
Documents 356
Publication sources 6
Authors 2235
Co-authors per Doc 7.8
Author’s Keywords 754
Keywords Plus (ID) 677
Table 1:

Main information of the selected articles gathered by Biblioshiny.

MATERIALS AND METHODS

Data Sources

Relevant publications were found using the search terms “healthcare-associated infection” in PubMed, published between 2013 and 2023. With the exception of book chapters, conference proceedings, and editorials, the research covered all articles and review papers whose titles, abstracts, and keywords were related to HCAIs. Only English articles were selected. Information was identified and obtained by two reviewers independently. The bibliometric analysis was performed with the help of the R packages Bibliometrix and Biblioshiny.

Data Analysis

The present bibliometric analysis was conducted using the biblioshiny, a shiny app for bibliometrix from the R Statistical Package (https://www.bibliometrix.org/home/index.php/layout/biblioshiny). It provides a wide range of characteristics that make conducting comprehensive bibliometric analysis possible. The Bibliometrix package was installed and loaded through R Studio (Version 2022.07.2+576). The Biblioshiny application was started by typing biblioshiny () into the R console. Scholars can undertake thorough bibliometric analysis using a variety of Bibliometrix tools.23 The downloaded metadata were uploaded on Biblioshiny interface to be analysed. Several results are displayed in tables and graphs.23,24 The main objective of this study is to analyse general outcomes (publication trends and collaborations), publication sources, and keywords.

RESULTS

Analysis of Publication Outputs, Growth Trends, and Scientific Collaborations.

Table 1 shows that between 2013 and 2023, a total of 356 papers were published addressing HCAIs. Six journals, mostly dedicated to scientific research, published these papers. There has been a rise in publications recently. The total number of publications published in 2020 was a record high (Figure 1). There are 2235 authors on this topic, and they come from a wide variety of nations such as Switzerland, Germany, the United States, Australia, Brazil, China, and India and the average of co-authors seven to eight. Switzerland, Portugal, Germany, Spain, and other European countries were the most common collaborators in scientific research. In addition, there was also a collaboration between USA and Australia (Figure 2).

Figure 1:
The total number of annual publications. The year 2020 had the most publications between 2013 and 2023, with 50 articles published.

Figure 2:
Scientific collaboration world map. Countries with a darker blue shade have a higher number of publications. The red line connects the two countries with the highest frequency of collaboration.

Analysis of Publication Sources

According to bibliometric analysis, six journals with publications published between 2013 and 2023 were found. Figure 3 shows the journals that publish articles in this area of study. The Journal of Hospital Infection is the highest journal with 145 articles (40.7%), followed by Antimicrobial Resistance and Infection Control Journal with 61 articles (17.1%), Infection Control and Hospital Epidemiology journal with 49 articles and American Journal of Infection Control with 45 articles. Next are Clinical Infectious Diseases: An Official Publica Journal and BMC Infectious Disease journal with 24 and 23 articles respectively. According to the Bradford’s Law of Scattering, the number of core sources with the largest number of publications is the journal of hospital infection (Figure 4).

Figure 3:
Top journals that published healthcare-associated infection related articles.

Figure 4:
Core publication sources clustering through Bradford’s Law.

Analysis of Keywords

Keywords are very useful for bibliometric analysis when looking at the most popular articles and recent developments in a given field of study. We opted for the author’s keywords since they help us zoom in on the topic and issues plaguing a given area of study.25,26 The ten most commonly used words are “healthcare-associated infection” (n=173), “infection control” (n=44), “surveillance” with occurrence 39 followed by “hand hygiene” and “Infection prevention and control” with occurrence 28,24 respectively. “Antimicrobial resistance” (n=22), “COVID-19” (n= 19) and “Infection control” (n=17). “Keywords “Healthcare-associated infection”, and “epidemiology” have 16 occurrences respectively (Figure 5). As the rate of publication went up, so did the average occurrence of the keywords (Figure 5). The term “healthcare-associated infection” has increased significantly, occurring over a hundred times in the reviewed 356 papers (Figure 6).

Figure 5:
Top 10 most frequent author’s keywords for healthcare associated infection articles.

Figure 6:
Cumulative authors’ keyword occurrences from 2013-2023.

Figure 7 presents the network of the most frequently used 50 keywords based on the analysis of their co-occurrence. A node’s size reflects a keyword’s frequency, while its colour represents its cluster and correlation with other nodes. Based on the analysis, all keywords were divided up into three distinct clusters, which were colour coded. Blue for “healthcare-associated infection, infection control, SARS-COV-2, COVID-19, Acinetobacter baumanni and prevention. The red for “healthcare-associated infection, surveillance, antimicrobial stewardship, surgical site infection, and bloodstream infection”. Purple color for “infection prevention and control, patient safety, hand hygiene, and implementation”. This keyword network map reveals that these three clusters have performed as the main driving forces behind the HCAIs research process in the last ten years (Figure 7).

Figure 7:
Co-occurrence network of the topics discussed. Nodes with the same colour indicate topics under the same cluster.

Thematic evaluation

By identifying the most commonly used terms, we may further analysis the evolution trend of the theme using the author’s keyword. The analysis of theme evolution is essential for showing how particular study fields have developed over time and for detecting shifts and changes in the way that research has been presented.18,27 Figure 8 illustrates the evaluation of the HCAIs research field. The number of keywords used in each of the coloured nodes, which indicate different research areas, determines their size. The grey flow band between nodes indicates the trend of the study topics’ evolution and the consistency of time between them.

Figure 8:
Thematic evolution over the decade. The figure shows the evolution of hotspots and trends of healthcare-associated infection.

Figure 8 demonstrated an evolution timeline for the topic, from 2013 to 2023. Research on HCAIs was also divided into three distinct periods to illustrate evolving trends better. Throughout the first phase, thematic evolution between 2013 and 2017, the study topics were “healthcare associated infection,” “clostridium difficile,” “infection prevention and control,” “surgical site infection,” and “blood stream infection”. This established a foundation for further investigation of the theme. Emerging themes from the second phase of research, covering the years 2018-2019, included “risk factor,” “length of stay,” “Acinetobacter buamannii,” and “environment,” while “healthcare-associated infection,” “bloodstream infection,” “clostridium difficile,” and “surgical site infection” remained constant. In the third stage, which ran from 2020 to 2023, new topics about “surveillance” and “implementation” were developed (Figure 8). The changing nature of these themes shows that scientists are paying more attention to the impact of HCAIs on patients and medical staff and are looking at the efficacy of IPC measures in reducing infection rates.4,2831 The potential for future research and improvements in the subject of HACIs can be further explored with the help of theme evolution analysis, which can help us grasp the current state of the field and its trajectory.

DISCUSSION

The prevalence of HCAIs is a major threat to the healthcare sector. HCAIs place a heavy financial strain on healthcare systems, prolonging hospital stay, and increasing morbidity.6,8 This bibliometric analysis highlights the basic structure of the literature on HCAIs. It detects emerging article trends and patterns of cooperation which, can provide the basis for consequential advances in the field. This allows researchers to survey the subject, spot areas where more information is needed and better frame how they contribute. As far as we are aware, this is the first bibliometric evaluation of HCAIs research. The overall findings indicated that relevant publications had grown more frequently during the last ten years. The prevention, management, and evaluation of HCAIs have all been the focus of research globally.5,8,30 From 2013, there has been an increase in the publications. In particular, from 2019 to 2020, HCAI has progressively gained greater attention in the study sector with the spread of COVID-19 that swept the world, affecting the health concerns of patients.1,12,15,32

Important scientific progress is made through international collaboration, emphasizing knowledge sharing and synthesis of knowledge.33,34 While different nations may place different emphases on certain aspects of HCAI study, collaborating together might lead to resource synergy and steady progress. Our analysis shows that the leading contributors to the HCAI literature are located in the United States, Germany, the United Kingdom, Switzerland, Australia, Brazil, China, and France. We discovered that less research is conducted from Low- and Middle-Income Countries (LMIC), even though HCAIs are more prevalent in these areas.3538 Due to a lack of documented LMIC studies, the true extent of HAI burden is unknown.9 For this reason, it is essential to foster collaborations between scientists in countries with abundant and scarce resources and to motivate researchers to devote more time and energy to their work by providing them with technical and financial support.

Through the analysis of journals, the most highly published studies in the Journal of Hospital Infection followed by the Antimicrobial Resistance and Infection Control Journal with impact factor 3.35 and 5.8 respectively. According to the Bradford analysis, in the core zone the journals that are most frequently cited in the articles on any given research topic and are most likely to be of the greatest interest to those researchers who make up the core zone (Zone 1 out of 3).39 The core sources for this research field are journal of hospital infection; a substantial concentration of publications contributes 40% of the published articles.

The analysis of authors’ keywords may provide significant information about the trends in a certain field of study. Healthcare-associated infections and infection control were among the most frequently mentioned topics. Many studies have demonstrated that the implementation of IPC guidelines and the benefits of early detection4,5,29,31 can reduce the prevalence of HCAIs. The healthcare pandemic directly led to an expansion of the IPC programme, which is crucial for patient and healthcare worker safety.12,13 In particular, new terms have emerged in this field with the development of the COVID-19 pandemic, indicating a trend in studies linking HCAIs with COVID-19. Numerous studies have documented the frequency of HCAIs among COVID-19 patients.1,14,4042 Additionally, antimicrobial resistance (AMR) and the widespread use of antibiotics have also been the subject of numerous studies.6,43,44 According to the analysis the cumulative occurrences of these keywords have been increasing over time, suggesting that the related discussions are still timely and relevant. Large clusters in keyword co-occurrence networks represent active study areas. Apart from HCAIs, our findings show that features of IPC relevant to HCAI prevalence and management are the key topics of interest for most study.46,47 One important IPC strategy that has been shown to significantly reduce the incidence of HAIs and the propagation of antibiotic resistance is increased emphasis on hand hygiene and surveillance.28,31,48 Concerns have been raised after COVID-19 pandemic regarding the IPC rules’ application to the healthcare system. Numerous studies highlighted the significance of implementing automated monitoring and automated hand hygiene that increase the quality of safety and patient care.10,4851 The effects of HCAIs on hospital stays and associated risk factors have been discussed elsewhere.37,40,52 Keyword analysis by year demonstrates the centrality of themes in HCAIs research. The primary objective moving forward is to initiate additional studies connecting infection control, HCAIs, and COVID-19.13,15,30,41

The information offered in this article may assist researchers and scientists in focusing their attention on the most critical issues surrounding the investigation of HCAIs. Based on our findings, we suggest that future research on developing and implementing HCAI control methods should concentrate on different hospital environments. Further research is needed to decrease the prevalence of HCAIs and improve IPC policies and programmes in developing nations, such as increasing connection and cooperation across healthcare facilities.35,38 Education, organisational and cultural hurdles, infrastructure, and financial resources are where more evidence is needed to support IPC’s widespread implementation. Additionally, in healthcare settings where patient involvement is crucial to patient safety, more research is needed to highlight the importance of educating patients about nosocomial infection prevention and adopting IPC standards.53,54 Moreover, further studies are required to evaluate healthcare students’ knowledge of HCAIs and IPC to equip them with the tools they will need to succeed in the profession.

Limitations

We acknowledge that our research has some limitations. Since only the PubMed database was utilised to extract the relevant literature, there is a possibility of bias and insufficient inclusion studies. Furthermore, our search strategy may not have uncovered all relevant studies because of constraints regarding keywords, time periods, zone source and languages, which would have led to insufficient findings in our analysis. In the end, the keyword analysis in this study was based entirely on the authors’ keywords.

CONCLUSION

Healthcare-Associated Infections (HCAIs) are a major cause of death and disability. We have provided a comprehensive review of the literature on HCAIs and demonstrated its potential as a growing research area. The bibliometric study of HCAIS studies over the past decade reveals a rising trend in the number of studies covering this topic. Journal of hospital infection and antimicrobial resistance and infection control journal were the most prolific publishers in this field, with the majority of researchers coming from European countries. According to the analysis of authors’ keyword, we found that “healthcare-associated infection,” “infection control,” “surveillance,” “hand hygiene,” and “antimicrobial resistance” are the most frequently used terms, each of which reflects an active area of study and a possible direction for future development. It is anticipated that this study will inspire researchers to continue their work in the field of HCAIs and provide insight into current trends, research hotspots, and future research directions.

References

  1. Baccolini V, Migliara G, Isonne C, Dorelli B, Barone LC, Giannini D, et al. The impact of the COVID-19 pandemic on healthcare-associated infections in intensive care unit patients: a retrospective cohort study. Antimicrob Resist Infect Control. 2021;10(1):87 [CrossRef] | [Google Scholar]
  2. Haque M, Sartelli M, McKimm J, Abu Bakar M. Health care-associated infections – an overview. Infect Drug Resist. 2018:2321-33. [PubMed] | [CrossRef] | [Google Scholar]
  3. Moralejo D, El Dib R, Prata RA, Barretti P, Corrêa I.. Improving adherence to Standard Precautions for the control of health care-associated infections. Cochrane Database Syst Rev. 2018;2(2) [PubMed] | [CrossRef] | [Google Scholar]
  4. Ershova K, Savin I, Kurdyumova N, Wong D, Danilov G, Shifrin M, et al. Implementing an infection control and prevention program decreases the incidence of healthcare-associated infections and antibiotic resistance in a Russian neuro-ICU. Antimicrob Resist Infect Control. 2018;7:94 [PubMed] | [CrossRef] | [Google Scholar]
  5. Rewley J, Koehly L, Marcum CS, Reed-Tsochas F.. A passive monitoring tool using hospital administrative data enables earlier specific detection of healthcare-acquired infections.. J Hosp Infect.. 2020;106(3):562-9. [PubMed] | [CrossRef] | [Google Scholar]
  6. Li P, Li Y, Zhang Y, Bao J, Yuan R, Lan H, et al. Economic burden attributable to healthcare-associated infections in tertiary public hospitals of Central China: a multi-center case-control study. Epidemiol Infect.. 2022;150:e155 [PubMed] | [CrossRef] | [Google Scholar]
  7. Liu X, Cui D, Li H, Wang Q, Mao Z, Fang L, et al. Direct medical burden of antimicrobial-resistant healthcare-associated infections: empirical evidence from China. J Hosp Infect. 2020;105(2):295-305. [PubMed] | [CrossRef] | [Google Scholar]
  8. Lü Y, Cai MH, Cheng J, Zou K, Xiang Q, Wu JY, et al. A multi-center nested case-control study on shospitalisation costs and length of stay due to healthcare-associated infection. Antimicrob Resist Infect Control. 2018;7:99 [PubMed] | [CrossRef] | [Google Scholar]
  9. World Health Organization report on the burden of endemic health care-associated infection worldwide. 2011 [8 October 2022].
  10. Cawthorne KR, Cooke RPD. A survey of commercially available electronic hand hygiene monitoring systems and their impact on reducing healthcare-associated infections. J Hosp Infect. 2021;111:40-6. [PubMed] | [CrossRef] | [Google Scholar]
  11. . Health care without avoidable infections: the critical role of infection prevention and control. World Health Organization (WHO). associated module. Am J Infect Control.. 2016;44:1495-504. [CrossRef] | [Google Scholar]
  12. Abbas M, Robalo Nunes T, Martischang R, Zingg W, Iten A, Pittet D, et al. Nosocomial transmission and outbreaks of coronavirus disease 2019: the need to protect both patients and healthcare workers. Antimicrob Resist Infect Control. 2021;10(1):7 [PubMed] | [CrossRef] | [Google Scholar]
  13. Alsuhaibani M, Kobayashi T, McPherson C, Holley S, Marra AR, Trannel A, et al. Impact of COVID-19 on an infection prevention and control program, Iowa 2020-2021. Am J Infect Control. 2022;50(3):277-82. [PubMed] | [CrossRef] | [Google Scholar]
  14. Baccolini V, Migliara G, Isonne C, Dorelli B, Barone LC, Giannini D, et al. The impact of the COVID-19 pandemic on healthcare-associated infections in intensive care unit patients: a retrospective cohort study. Antimicrob Resist Infect Control. 2021;10(1):87 [PubMed] | [CrossRef] | [Google Scholar]
  15. Stevens MP, Doll M, Pryor R, Godbout E, Cooper K, Bearman G, et al. Impact of COVID-19 on traditional healthcare-associated infection prevention efforts. Infect Control Hosp Epidemiol. 2020;41(8):946-7. [PubMed] | [CrossRef] | [Google Scholar]
  16. Turhan Damar H, ÖĞÇE AKTAŞ F. Bibliometric analysis of studies on surgical site infections in nursing (2000-2022). Gevher nesibe journal of medical and health sciences. 2022;7(20):111-20. [CrossRef] | [Google Scholar]
  17. Yu Y, Li Y, Zhang Z, Gu Z, Zhong H, Zha Q, et al. A bibliometric analysis using VOSviewer of publications on COVID-19. Ann Transl Med. 2020;8(13):816 [PubMed] | [CrossRef] | [Google Scholar]
  18. Donthu N, Kumar S, Mukherjee D, Pandey N, Lim WM. How to conduct a bibliometric analysis: an overview and guidelines. J Bus Res. 2021;133:285-96. [CrossRef] | [Google Scholar]
  19. Donthu N, Kumar S, Pandey N, Gupta P. Forty years of the International Journal of Information Management: A bibliometric analysis. Int J Inf Manag. 2021;57:102307 [CrossRef] | [Google Scholar]
  20. Sweileh WM. Bibliometric analysis of peer-reviewed literature on antimicrobial stewardship from 1990 to 2019. Global Health. 2021;17(1):1 [PubMed] | [CrossRef] | [Google Scholar]
  21. Zhong H, Liu CY, Dai YQ, Zhu C, Le KJ, Pang XY, et al. A bibliometric analysis of infectious diseases in patients with liver transplantation in the last decade. Ann Transl Med. 2021;9(22):1646 [PubMed] | [CrossRef] | [Google Scholar]
  22. Cahyadin AW, Maula AW, Fuad A. Healthcare-Associated Infections (HAI) research in Asian countries: a bibliometric analysis. JMedScie. 2018;50 [CrossRef] | [Google Scholar]
  23. Aria M, Cuccurullo C. bibliometrix: an R-tool for comprehensive science mapping analysis. J Inf. 2017;11(4):959-75. [CrossRef] | [Google Scholar]
  24. Ahmi A. Bibliometric Analysis using R for Non-Coders: A practical handbook in conducting bibliometric analysis studies using Biblioshiny for Bibliometrix R package. 2022 [CrossRef] | [Google Scholar]
  25. Li H, An H, Wang Y, Huang J, Gao X. Evolutionary features of academic articles co-keyword network and keywords co-occurrence network: based on two-mode affiliation network. Phys A. 2016;450:657-69. [CrossRef] | [Google Scholar]
  26. Tripathi M, Kumar S, Sonker SK, Babbar P. Occurrence of author keywords and keywords plus in social sciences and humanities research: A preliminary study. COLLNET J Scientometr Inf Manag. 2018;12(2):215-32. [CrossRef] | [Google Scholar]
  27. Cobo MJ, López-Herrera AG, Herrera-Viedma E, Herrera F. An approach for detecting, quantifying, and sVisualising the evolution of a research field: A practical application to the fuzzy sets theory field. J Informetr. 2011;5(1):146-66. [CrossRef] | [Google Scholar]
  28. Barnett AG, Page K, Campbell M, Brain D, Martin E, Rashleigh-Rolls R, et al. Changes in healthcare-associated bloodstream infections after the introduction of a national hand hygiene initiative. Infect Control Hosp Epidemiol. 2014;35(8):1029-36. [PubMed] | [CrossRef] | [Google Scholar]
  29. McAlearney AS, Hefner JL. Facilitating central line-associated bloodstream infection prevention: a qualitative study comparing perspectives of infection control professionals and frontline staff. Am J Infect Control. 2014;42(10):S216-22. [PubMed] | [CrossRef] | [Google Scholar]
  30. Paul E, Alzaydani Asiri IA, Al-Hakami A, Chandramoorthy HC, Alshehri S, Beynon CM, et al. Healthcare workers’ perspectives on healthcare-associated infections and infection control practices: a video-reflexive ethnography study in the Asir region of Saudi Arabia. Antimicrob Resist Infect Control. 2020;9(1):110 [PubMed] | [CrossRef] | [Google Scholar]
  31. 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. [PubMed] | [CrossRef] | [Google Scholar]
  32. Carter B, Collins JT, Barlow-Pay F, Rickard F, Bruce E, Verduri A, et al. Nosocomial COVID-19 infection: examining the risk of mortality. The COPE-nosocomial study (COVID in older PEople). J Hosp Infect. 2020;106(2):376-84. [PubMed] | [CrossRef] | [Google Scholar]
  33. Adams J. Collaborations: the fourth age of research. Nature. 2013;497(7451):557-60. [PubMed] | [CrossRef] | [Google Scholar]
  34. Qin Y, Chen R. Social network analysis of COVID-19 research and the changing international collaboration structure. Array. 2022:1-11. [PubMed] | [CrossRef] | [Google Scholar]
  35. . Infection control bundles in intensive care: an international cross-sectional survey in low- and middle-income countries. J Hosp Infect. 2019;101(3):248-56. [PubMed] | [CrossRef] | [Google Scholar]
  36. 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(3):827-39. [PubMed] | [CrossRef] | [Google Scholar]
  37. Murni IK, Duke T, Kinney S, Daley AJ, Wirawan MT, Soenarto Y, et al. Risk factors for healthcare-associated infection among children in a low-and middle-income country. BMC Infect Dis. 2022;22(1):406 [PubMed] | [CrossRef] | [Google Scholar]
  38. Rothe C, Schlaich C, Thompson S. Healthcare-associated infections in sub-Saharan Africa. JHosp Infect. 2013;85(4):257-67. [PubMed] | [CrossRef] | [Google Scholar]
  39. Nash-Stewart CE, Kruesi LM, Del Mar CB. Does Bradford’s law of Scattering predict the size of the literature in Cochrane Reviews?. J Med Libr Assoc.. 2012;100(2):135-8. [PubMed] | [CrossRef] | [Google Scholar]
  40. Aghdassi SJS, Schwab F, Peña Diaz LA, Brodzinski A, Fucini GB, Hansen S, et al. Risk factors for nosocomial SARS-CoV-2 infections in patients: results from a retrospective matched case-control study in a tertiary care university center. Antimicrob Resist Infect Control. 2022;11(1):9 [PubMed] | [CrossRef] | [Google Scholar]
  41. Rickman HM, Rampling T, Shaw K, Martinez-Garcia G, Hail L, Coen P, et al. Nosocomial transmission of coronavirus disease 2019: A retrospective study of 66 hospital-acquired cases in a London teaching hospital. Clin Infect Dis. 2021;72(4):690-3. [PubMed] | [CrossRef] | [Google Scholar]
  42. Verberk JDM, van der Kooi TII, Kampstra NA, Reimes N, van Rooden SM, Hopmans TEM, et al. Healthcare-associated infections in Dutch hospitals during the COVID-19 pandemic. Antimicrob Resist Infect Control. 2023;12(1):2 [PubMed] | [CrossRef] | [Google Scholar]
  43. Mullié C, Lemonnier D, Adjidé CC, Maizel J, Mismacque G, Cappe A, et al. Nosocomial outbreak of monoclonal VIM carbapenemase-producing complex in an intensive care unit during the COVID-19 pandemic: an integrated approach. J Hosp Infect.. 2022;120:48-56. [PubMed] | [CrossRef] | [Google Scholar]
  44. Gashaw M, Berhane M, Bekele S, Kibru G, Teshager L, Yilma Y, et al. Emergence of high drug resistant bacterial isolates from patients with health care associated infections at Jimma University medical center: a cross sectional study. Antimicrob Resist Infect Control. 2018;7:138 [PubMed] | [CrossRef] | [Google Scholar]
  45. Kampmeier S, Tönnies H, Correa-Martinez CL, Mellmann A, Schwierzeck V. A nosocomial cluster of vancomycin resistant enterococci among COVID-19 patients in an intensive care unit. Antimicrob Resist Infect Control. 2020;9(1):154 [PubMed] | [CrossRef] | [Google Scholar]
  46. Ojanperä H, Ohtonen P, Kanste O, Syrjälä H. Impact of direct hand hygiene observations and feedback on hand hygiene compliance among nurses and doctors in medical and surgical wards: an eight-year observational study. J Hosp Infect. 2022;127:83-90. [PubMed] | [CrossRef] | [Google Scholar]
  47. Tartari E, Fankhauser C, Masson-Roy S, Márquez-Villarreal H, Fernández Moreno I, Rodriguez Navas ML, et al. Train-the-Trainers in hand hygiene: a sstandardised approach to guide education in infection prevention and control. Antimicrob Resist Infect Control. 2019;8(1):206 [PubMed] | [CrossRef] | [Google Scholar]
  48. van der Werff SD, Thiman E, Tanushi H, Valik JK, Henriksson A, Ul Alam M, et al. The accuracy of fully automated algorithms for surveillance of healthcare-associated urinary tract infections in shospitalised patients. J Hosp Infect. 2021;110:139-47. [PubMed] | [CrossRef] | [Google Scholar]
  49. Verberk JDM, Aghdassi SJS, Abbas M, Nauclér P, Gubbels S, Maldonado N, et al. Automated surveillance systems for healthcare-associated infections: results from a European survey and experiences from real-life utilisation. J Hosp Infect. 2022;122:35-43. [PubMed] | [CrossRef] | [Google Scholar]
  50. Kelly D, Purssell E, Wigglesworth N, Gould DJ. Electronic hand hygiene monitoring systems can be well-tolerated by health workers: findings of a qualitative study. J Infect Prev. 2021;22(6):246-51. [PubMed] | [CrossRef] | [Google Scholar]
  51. Xu Q, Liu Y, Cepulis D, Jerde A, Sheppard RA, Tretter K, et al. Implementing an electronic hand hygiene system improved compliance in the intensive care unit. Am J Infect Control. 2021;49(12):1535-42. [PubMed] | [CrossRef] | [Google Scholar]
  52. Stewart S, Robertson C, Pan J, Kennedy S, Haahr L, Manoukian S, et al. Impact of healthcare-associated infection on length of stay. J Hosp Infect. 2021;114:23-31. [PubMed] | [CrossRef] | [Google Scholar]
  53. McGuckin M, Storr JA, Govednik J. Patient awareness of healthcare-associated infection risk and prevention: has there been a change in 3 decades (1989-2019)?. Am J Infect Control. 2021;49(11):1448-9. [PubMed] | [CrossRef] | [Google Scholar]
  54. Mitchell BG, Northcote M, Rickett C, Russo PL, Amin M, De Sousa F, et al. Patients’ perspectives of healthcare-associated infection: ‘you don’t know what impacts it will have on your life’. J Hosp Infect. 2022;126:93-102. [PubMed] | [CrossRef] | [Google Scholar]