Learning from the covid-19 outbreaks in long-term care facilities: a systematic review

Background The COVID-19 pandemic has devastatingly affected Long-Term Care Facilities (LTCF), exposing aging people, staff members, and visitors. The world has learned through the pandemic and lessons can be taken to adopt effective measures to deal with COVID-19 outbreaks in LTCF. We aimed to systematically review the available evidence on the effect of measures to minimize the risk of transmission of COVID-19 in LTCs during outbreaks since 2021. Methods The search method was guided by the preferred reporting items for systematic reviews (PRISMA) and the reporting guideline synthesis without meta-analysis (SWiM) in systematic reviews. The search was performed in April 2023. Observational and interventional studies from the databases of PubMed, Web of Science, Scopus, Cochrane Systematic Reviews, CINAHL, and Academic Search were systematically reviewed. We included studies conducted in the LTCF with outbreaks that quantitatively assess the effect of non-pharmacological measures on cases of COVID-19. Two review authors independently reviewed titles for inclusion, extracted data, and undertook the risk of bias according to pre-specified criteria. The quality of studies was analyzed using the Joanna Briggs Institute Critical Appraisal. Results Thirteen studies were included, with 8442 LTCF experiencing COVID-19 outbreaks and 598 thousand participants (residents and staff members). Prevention and control of COVID-19 infection interventions were grouped into three themes: strategic, tactical, and operational measures. The strategic measures reveal the importance of COVID-19 prevention and control as LTCF structural characteristics, namely the LTCF size, new admissions, infection control surveillance, and architectural structure. At the tactical level, the lack of personal and long staff shifts is related to COVID-19's spread. Operational measures with a favorable effect on preventing COVID-19 transmission are sufficient. Personal protective equipment stock, correct mask use, signaling, social distancing, and resident cohorting. Conclusions Operational, tactical, and strategic approaches may have a favorable effect on preventing the spread of COVID-19 in LTCFs experiencing outbreaks. Given the heterogeneous nature of the measures, performing a meta-analysis was not possible. Future research should use more robust study designs to explore similar infection control measures in LTCFs during endemic situations with comparable outbreaks. Trial registration The protocol of this systematic review was registered in PROSPERO (CRD42020214566). Supplementary Information The online version contains supplementary material available at 10.1186/s12877-023-04319-w.


Background
Long-term care facilities (LTCF) are characterized by being vulnerable to outbreaks of respiratory diseases, such as those caused by the influenza virus or the human coronavirus [1][2][3].These institutions are frequently residences for older people who are socially and medically vulnerable to COVID-19 complications because of the interaction between advanced age and multimorbidity [4].Additionally, LTCF-specific institutional and environmental characteristics, such as high occupancy density, shared living areas, people with cognitive and behavioral issues, a lack of human and material resources, and antiquated infrastructure, increase the sensitivity to COVID-19 [4].LTCF includes nursing homes, skilled nursing facilities, retirement homes, assisted-living facilities, and residential care homes.In the European Union/European Economic Area (EU/EEA), before December 2019, there were 2.9 million residents in 43,000 of these LTCF types, representing 0.7% of the overall population [5].
The pandemic caused by SARS-CoV2 has devastatingly affected LTCFs, exposing aging people, staff members, and visitors [6][7][8].More than 800,000 fatal cases of COVID-19 have been reported in EU/EEA LTCF since the beginning of the epidemic, with more than 88% affecting adults over 65 [9].
Despite high vaccination coverage, COVID-19 outbreaks continue to occur in LTCFs, including severe cases and fatalities.The vaccine is highly effective in preventing severe disease and death.However, current outbreaks in LTCF highlight the importance of early detection, rapid containment of COVID-19 outbreaks, and ensuring strict infection prevention and control measures [10,11].COVID-19 outbreaks in LTCF are defined as two or more cases linked by location and time, demonstrating an everyday exposure outside of a household [12].
Prominent international organizations have issued guidelines that guide these facilities to respond to the pandemic emergency [13,14].Still, these recommendations have not been subjected to the rigorous process of developing formal guidelines [15].In the same way, the available systematic reviews on infection prevention and control measures in LTCF were mainly in 2020.They had a low level of evidence due to the design and quality of available studies [15][16][17][18][19][20].Early studies were primarily focused on rapidly responding to the crisis rather than using interventional or experimental designs.Most of this research relied on case reports or cross-sectional methods and did not quantify the effect of containment measures in LTCF outbreaks.A recently published systematic review established the correlation between control measures and SARS-CoV-2 infection rates in residents and staff [21].Although it sheds light on the subject, this review's limitations include a restricted time frame until November 2021, which precluded the inclusion of infection control measures adapted to the LTCF outbreak caused by new coronavirus variants, such as Omicron.Also, the databases used could lead to incomplete coverage of published studies.Therefore, it is not fully understood what measures prevent COVID-19 from spreading during COVID-19 outbreaks in LTCF.Some studies have already shown the need for an organized response to outbreaks in LTCF, concentrating attention on specific moments [22][23][24].
So, it is interesting to reflect on the answers to the following question: What measures favorably reduce COVID-19 transmission during outbreaks in LTCF?
The answers to this question may fill the current frameworks for decision-making [25,26], enabling more scientifically supported future pandemic outbreak management practices.
We aim to systematically review the available evidence on the effect of measures to minimize the risk of transmission of COVID-19 in LTCs during outbreaks since 2021 We decided to concentrate on studies conducted since 2021 because we seek to distance ourselves from studies primarily focused on crisis response and lacking interventional or experimental designs [15][16][17][18][19][20].Additionally, this timeframe allows us to account for the evolving understanding of the virus and its variants, including the emergence of the Omicron variant.

Methods
This study has been undertaken as a systematic literature review based on the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) [27] and the reporting guideline synthesis without metaanalysis (SWiM) in systematic reviews [28].Its protocol was registered in the International Prospective Register of Systematic Reviews (PROSPERO) (CRD42020214566).

Eligibility criteria
Our research question assumed a PICOT format (Population (P) /Intervention (I) /Comparison (C) / Outcome (O) / Time (T)): which were the measures (I) implemented by LTCF with outbreaks (P) that have a favorable effect on reducing the risk of transmission of COVID-19 infection (O) since 2021 (T)?We understand that by "Measures" any non-pharmacological structured intervention, norm, action, or procedure implemented in the LTCF to prevent and control the spread of COVID-19 during outbreaks, different from usual care.
We focused on when the virus entered and remained in the LTCF.We considered LTCF with outbreaks in all settings dedicated to adults and aging people, including residents, staff members, and visitors (Table 1).An outbreak was defined as ≥ 2 residents with laboratory-confirmed COVID-19.We included studies that allowed comparison across different groups, such as interventional studies (randomized or before and after) and observational studies (cohort and case-control) centers pediatric In this sense, we decided to exclude cross-sectional studies because they do not allow us to establish the temporal relationship between disease occurrence and exposure [29].It is particularly troubling because of the instability of COVID-19 exposure conditions over time in LTCF, especially considering the introduction of new virus variants and the increasing vaccine coverage.
We decided to attend to Kesmodel's conclusion [29] "when cross-sectional data is used for analytical purposes, authors and readers should be careful not to make causal inferences, unless the exposure may safely be assumed to be stable over time" (p.388).
We excluded studies assessing other viral acute diseases, such as SARS, Middle East respiratory syndrome (MERS), and pandemic influenza.The most recent evidence has shown that, although there is epidemic/pandemic potential in these diseases, there are differences in pathogenicity that justify specific measures for preventing COVID-19 dissemination [16-18, 30, 31].

Information sources and search strategy
We performed a literature search using the online databases of PubMed, Web of Science, Scopus, Cochrane Systematic Reviews, Cumulative Index to Nursing and Allied Health Literature (CINAHL), and Academic Search Complete.Previous reviews were consulted to create the current strategy [15][16][17][18][19][20].The following medical subject headings (MeSH) and non-MeSH keywords were used as keywords in our search strategy, according to the PICOT domains, and using Boolean operators (Table 2).We searched in "ALL fields" to ensure better coverage.Because we wanted structured and planned care, different from usual care, we opted for using focused keywords on interventions.The search was performed on 2/04/2023 by one researcher (HRH).
In addition, we manually searched for potential records in the bibliographic reference list of systematic reviews on the topic in the previous search.

Selection process
All detected references (identification) were exported to the Rayyan QCRI tool (Rayyan Systems Inc., Cambridge, MA, USA).It supported collaborative work throughout the team [32].The research team was divided into small groups of two or three members who worked collaboratively on the screening process (AC, AH, CD, DS, HRH, JF, JP).The small teams' work was supervised by one researcher (HRH).
We started by removing duplicates.Then, two researchers (all team members) independently reviewed the title and abstract of the retrieved studies and decided if they met the predetermined eligibility criteria.We followed a decision tree that started by evaluating the type of study.If these criteria were met, we would proceed to the evaluation of the population.Once these criteria were met, we assessed the intervention, the outcome, and finally, the date of the study.All articles that successfully met the eligibility criteria were evaluated during the full-text review.When two screeners disagree on whether an article fulfils the eligibility criteria, they resolve this disagreement through discussion.If the two screeners cannot reach a consensus for a particular article, a third person (HRH) acts as an arbitrator to decide on the contested article.The librarian was involved in finding articles that were not fully available.

Data collection process and data items
Two researchers independently collected the data using a form that has been developed and piloted.Two researchers (HRH, CD) independently developed the searchable database, informed by the research question and the Taxonomic classification of planning decisions in health care [25].These two versions were agreed upon and presented to the rest of the team in a meeting.All the team could improve and clarify the document to avoid misunderstandings or later disagreements.
Data related to study identification, research country, aim, study design, study period, LTCF involved, participants, outcomes, context, and conclusion were extracted.
Regarding the intervention, we categorized prevention and infection control measures as strategic, tactical, and operational measures according to the Taxonomic classification of planning decisions in health care [25].
Three teams of two reviewers extracted data from the included studies, and a third author resolved disagreements between the teams.At this point, to foster greater researcher consensus, each small group took on studies that were distinct from the ones they had previously examined.A third reviewer (HRH) double-checked all the data in the tables.Whenever data were unavailable, we contacted the study's author, requesting to provide this data.Data collection forms were designed using Microsoft Excel spreadsheets.

Study risk of bias assessment
Each study was assessed independently according to the Joanna Briggs Institute (JBI) Critical Appraisal Checklist tools (Moola et al., 2020) [33].
The risk of bias disagreements was mitigated through discussion, which included the participation of a third author to ensure the quality of the appraisal process when necessary.

Effect measures
All effects estimates were reported as OR or RR with 95% confidence intervals.When research provided information on both the unadjusted and adjusted intervention effects, we utilized the adjusted effects with information on the variables for which the models had been adjusted.

Data synthesis
Given the methodological and clinical heterogeneity of the studies, each study was subjected to a descriptive analysis according to the "Synthesis Without Meta-analysis" (SWiM) reporting guideline [28].Studies were grouped according to study design.
A narrative approach was used to describe the evidence, referring to the level of evidence supporting the interventions for each outcome in each domain of interest.

Results
A total of 4053 references were exported from selected databases to the Rayyan application.We removed 151 duplicate records and concluded the first screening Table 2 Search strategy 1 We understand "attack rate" as a measure used in epidemiology to describe the frequency of new cases of a specific disease or condition within a population over a specified period.It is expressed as a percentage, representing the proportion of at-risk individuals developing the disease during the outbreak Population ("Residential Facilities" OR "Assisted Living Facilities" OR "Homes for the Aged" OR "Nursing Homes" OR "Long-Term Care" OR "residential aged care" OR "Long-Term Care Facilities") Intervention (("organization and administration" OR "health facility administration" OR "Guidelines" OR "practice guidelines" OR "Guidance" OR "Containment strategy" OR "Containment of Biohazards" OR "managed care programs" OR "training programs" OR "Risk assessment" OR "Guidelines as Topic" OR "Health Planning Guidelines" OR "Practice Guidelines as Topic" OR "Guideline") AND ("Disease Transmission" OR "Disease Transmission, Infectious" OR "Infectious Disease Transmission, Professional-to-Patient" OR "Infectious Disease Transmission, Patient-to-Professional" OR "Disease Transmission, Patient-to-Professional" OR "Disease Transmission, Professional-to-Patient" OR "Infection Control" OR "Risk Factors" OR "Risk reduction behaviour" OR "Harm reduction")) AND ("COVID-19" OR "2019-nCoV" OR "SARS-CoV2") stage with 3902 records.After analyzing their titles and abstracts, we excluded 3816 records because they did not meet the eligibility criteria.After analysing full-text, we included 12 references.
In the excluded study sample, we identified six reviews on the topic .Their lists of bibliographical references were manually analyzed, and from there, we included one extra-study (Fig. 1).

Characteristics of included studies
After selection, thirteen studies were included, around 598 thousand participants (between residents and staff members) and 8442 LTCF, from the Asian (n = 2), American (n = 4), and European (n = 7) continents.One study reports multiple interventions.Eleven studies were observational, and two was interventional (Table 3).
According to Joanna Briggs International's (JBI) criteria for critical appraisal, all articles had a low risk of bias.All studies fulfilled the JBI critical appraisal checklist, except for the control of some potential confounders.. Case-control studies responded to almost all JBI requirements [34][35][36][37][38].Of these, only one of the manuscripts   [37] clearly stated strategies for managing and controlling confounding factors.The cohort studies met most of the quality criteria outlined by JBI, demonstrating their alignment with established standards.. Still, we maintain reservations in two manuscripts [39,40] about how confounding factors were stated, managed, and outcomes measured.Both manuscripts have evident gaps regarding how they used statistics to handle potential issues that could affect the results (confounding factors).Green et al. [39] lack explicit confounding factor variables, hindering intervention impact understanding.Zimmerman et al. [40] do not detail the methods used to measure exposure, the instruments employed, or the steps taken to ensure the accuracy and consistency of measurements..One of the quasi-experimental studies [41] did not raise concerns; The second quasi-experimental study [42] exhibits limitations as it lacks consistent and comprehensive information regarding whether participants, in distinct comparison groups received comparable treatment or care, apart from the specified exposure or intervention being investigated.It is also unclear whether the followup was complete (Supplementary material).
We included all studies relevant to the research question that met the eligibility criteria (Table 4).
The interventions for preventing and controlling COVID-19 infection were grouped into three themes, as proposed by the taxonomy of Hulshof et al. (2012), for decision-making about the planning and control of health resources: strategic measures, tactical measures, and operational measures.The category of strategic measures includes actions that concern the organizational management structure.Tactical measures refer to those applied to team management.Operational measures are related to the management of residents' care.Given the significant variations in the type of interventions and their effects on LTCs during COVID-19 outbreaks, we have subcategorized the impact of these interventions: unfavorable effect, favorable effect, or null effect.This approach provides a comprehensive understanding of the direction of the effect of different interventions in controlling COVID-19 spread in LTCs during recent outbreaks(Table 5).
Since the set of studies reported the implementation of very different measures, the data collection time of each study varied greatly, and the participants probably had different vaccination coverage, we considered the sample extremely heterogeneous.Therefore, a synthesis without meta-analysis was performed [28].
The studies do not agree on the importance of the number of beds per room.Some results show that the number of beds per room has no significant association with the COVID-19 spread [34,38,39,44].However, others show that double or quadruple-occupancy rooms (with shared bathrooms) promote COVID-19 dissemination (compared with LTCF with single rooms, had double the COVID-19 incidence (relative risk [RR], 2.05; 1.49-2.70)and is associated with COVID-19 mortality (RR, 1.97; 1.36-2.84))[45].
Higher average occupancy rates were associated with increased COVID-19 cases (OR = 21.24-31.19)[36].Maximum occupancy limits in small, enclosed spaces, such as elevators, dressing/dining rooms, and WCs inside the bedroom, were associated with a lower prevalence of COVID-19 infection in LTCF with an active outbreak [35].
The data suggest a potential association between new admissions and increased odds of infection [46], highlighting the importance of testing and isolating residents upon entry to the LTCF.. Outbreak testing could prevent 54% (weekly testing with a 48-h turnaround) to 92% (daily testing with immediate results and 50% relative sensitivity) of SARS-CoV-2 infections.
Regular and voluntary RT-PCR SARS-CoV-2 testing of healthcare workers and visitors seems to have no significant effect on COVID-19 prevention in LTCF [42].
Facilities with multiple Infection prevention and control (IPC) deficiencies were more likely to report COVID-19 cases (OR:2.09[0.95, 4.60], p = 0.068) than those with only one IPC deficiency [36].Similarly, LTCFs with no cases of COVID-19 were those who were more likely to implement outbreak management procedures compared to homes with at least 1 case of COVID-19 (p = 0.060) [44].
Surface disinfection [34,35], closing residents' shared spaces [39], and meal places [34] seems to have no significance in the prevention of COVID-19 infection, as open to visitors post-first lockdown [38] and the use of

Contact Limitation
To reduce the risk of infection transmission, care workers wore facemasks, plastic gloves, and face shields, and used hand sanitizers every time they cared for their patients The frequency of care was reduced from three times/day to two times/day.Regarding mealtimes, the patients usually ate their food in the lounges; however, they were now required to eat in their respective rooms during the pandemic.Further, the patients' families were restricted from meeting the patients, except in emergency situations     information and communication technology to share patient information between the clinic and nursing home [37].Likewise, official protocols/procedures on infection control and prevention, policies for managing personnel at risk of infection, an infection surveillance program, or procedures on standard and additional precautions appear to have no significant impact on the management of the outbreak [44].
The data suggest that a multicomponent intervention, like case and contact management, proactive case detection, rigorous infection control practices, and resource prioritization and stewardship, led to a reduction in the transmission of COVID-19 in LTCFs [41].

Tactical measures
Longer staff shifts seem to be a predictor of getting COVID-19.The infection rate was almost three times greater in nursing homes with longer staff shifts than in those that did not (OR 3.02 (1.68-5.43),p < 0.001) [34].The odds of infection in residents (1.30 [1.23-1.37],p < 0.0001) and staff (1.20 [1.13-1.29],p < 0.0001), as well as outbreaks (2.56 [1.94-3.49],p < 0.0001), were significantly higher in LTCF where staff frequently or always cared for both infected and uninfected residents, compared to those where staff cohort with either infected or uninfected residents [46].
Training staff on managing occupational exposures to biohazards, the correct hand hygiene procedure, how to prevent the spread of respiratory infections, and using personal protective equipment had no association with the median cumulative incidence of COVID-19 cases among residents [44].Nevertheless, training, and frequent audits for proper donning/ doffing of PPE (p.= 0.03) and mask use (p.= 0.02) occurred more in lower-prevalence COVID-19 infection LTCFs [35].Staff members in 100% of lowerprevalence LTCFs were observed to use masks properly in the COVID-19 unit compared to 45% in the higher-prevalence group (p < 0.01) [35].However, training staff and residents on procedures to contain COVID-19 [38] and daily monitoring and reporting of the staff 's health conditions (fever and symptoms) [37] seems to have no significant effect on COVID-19 prevention.
However, the favorable and significant effect of resident isolation has not been consistently demonstrated [37].Based on these conclusions, the package measures aimed at reducing the risk of infection transmission (which included care workers using personal protective equipment and reducing the frequency of care from three times per day to two times per day; meals began to take place in the resident's room, and family members were prevented from meeting the residents) failed in COVID-19 prevention.
The results strongly suggest that not using a mask outside the room significantly predicts SARS-CoV-2 infection in residents (OR: 3.37, 1.74-6.53,p. = 0.001), who use a cloth mask, or who do not wear a mask (OR: 2.47, 1.13-5.42,p = 0.024) [34].Masks used properly by staff inside the COVID unit are associated with a lower prevalence of COVID-19 in LTCF [35].Another vital predictor for residents becoming infected by SARS-CoV-2 is not having a glass barrier in visitors' space (OR: 1.95, 1.11-3.50,p = 0.25) [34].
The difficulty in transferring COVID-19 patients to a hospital or other facility (OR = 4.67, p 0.001) was also associated with COVID-19 infection [43].
Active surveillance for guests and the presence of written operational procedures [38], residents' symptom screening [35], the flu vaccine, using masks inside the room, the mask-wearing method, mask change time (daily), and physical distance from a roommate [34] have no significant effect on COVID-19 prevention.Also, conformity to quality standards, compliance, and regular checks of the quality of the cleaning/sanitation/disinfection, availability of hand hygiene supplies and hand hygiene, use of personal protective equipment, and procedure for the management of residents with suspected communicable diseases had no association with the median cumulative incidence of COVID-19 cases among residents [44].

Combined measures
According to Vijh et al. [41], the combination of four different strategies -case and contact management, proactive case identification, strict infection control procedures, and resource prioritization and stewardship -positively impacts the prevention of COVID-19 transmission.

Discussion
LTCF remains a high-risk transmission setting where residents and staff are at risk of COVID-19 [47].Our sample included studies from seven countries, each one under specific government regulations and specific staff qualification levels.This circumstance should be addressed in the analysis of these rsults since it can strongly influence the measures taken locally and the pervasion of COVID in the community where the LTCF is located.However, this information was not always available.
The thirteen included studies identified measures that suggest influencing the outbreak management process in LTCFs.Operational, tactical, and strategic approaches positively prevented the spread of COVID-19 in LTCFs experiencing outbreaks.
We were unable to conduct a meta-analysis due to the heterogeneity between measures, what conditions the correlation between the outcomes and the measures adopted and a meta-analysis [48].
The strategic measures reveal the importance of COVID-19 prevention and control as LTCF structural characteristics, namely the LTCF size, new admissions, infection control surveillance, and architectural structure (Fig. 2).[36,38,43].These findings align with those who claim that single-site institutions have a higher attack rate than sites with multiple units, suggesting that aged care facilities should be designed to be smaller with enough space for social distancing [49].
Vijh's study [50] also concludes that older LTCFs in Canada were associated with the severity of COVID-19 outbreaks.These findings reinforce the importance of regularly assessing infection prevention and control measures tailored to architectural structures and outbreak preparedness in preventing large outbreaks.An integrated surveillance system for influenza, COVID-19, and potentially other respiratory virus infections in LTCF, is urgently needed to develop and sustain resilient responses [51][52][53].
Concerning tactical measures (Fig. 3), the healthcare workers' conditions at workplaces, mainly nurses working in LTCF, have been paramount in healthcare premises related to infection control, namely, to prevent the spread of the virus, improve care, and reduce the health impact of COVID-19 [54][55][56].Other studies suggest that the importation of SARS-CoV-2 by staff from the community is the primary driver of outbreaks [57].[34,36] Our findings support the notion that training, and audits predict lower COVID-19 infection LTCFs [35].Staff education is beneficial in achieving high adherence to the proper use of PPE and preventing COVID-19 infections in healthcare settings [58].
The LTCF, as units devoted to patients requiring regular supervision and nursing care, are recognised as a good setting for epidemics [59].The COVID-19 outbreak demanded additional practices besides legislation and policies protecting nurses and patients in LTCF.The recommendations prioritized personal protective equipment and social measures to protect nurses and patients.The health workforce was critical and scarce during the pandemic; however, it is essential to highlight some factors related to working conditions that may influence virus transmission, according to the studies reviewed.
Appropriate measures in LTCF include minimizing exposure, managing absences, and having the correct number of nurses working the proper number of hours in specific sectors (infected and noninfected) [16,17,52].Evidence imposes a necessary concern on the health community, given that it contrasts with the policies adopted in managing nurses to minimize their shortage, such as extending shift hours and hiring work agencies.
Although our study revealed no effect, other studies show that testing prevents the occurrence of an outbreak [42,[60][61][62].Outbreak testing should be implemented once it prevents 54% (weekly testing with 48-h test turnaround) to 92% (daily testing with immediate results and 50% relative sensitivity) of SARS-CoV-2 infections [62].Adding non-outbreak testing could prevent up to an additional 8% of SARS-CoV-2 infections, depending on test frequency and turnaround time [62].Tsoungui et al. [61] concluded that testing every five days with a good quality test and a processing time of 24 h can lead to a 40% reduction in infections in LTCF.
The COVID-19 pandemic also underlined the need for special approaches to LTCF at the operational level: personal protective equipment stock, mask use, signaling, social distancing and cohorting (Fig. 4).
Our study confirms that the most important aspect of infection prevention and control is understanding the transmission chain since it permits local and global action on each vector.Schmidt et al. [60] also concluded that applying non-pharmaceutical interventions with increasing rigor reduces the peak of infections.Based on the latest preliminary COVID-19 findings, the WHO [13] released detailed recommendations for using face masks and other personal protective equipment.These safety measures, evaluated during the pandemic, were shown to prevent viral transmission [35], although not using masks has had negative effects [34].These results are consistent with Bazant´s Guideline about Indoor Airborne Transmission of COVID-19 [63], which recommends the use of the mask.In their work, indoor airborne transmission of COVID-19 depends on ventilation and air filtration, room dimensions, breathing rate, respiratory activity, face mask use of its occupants, and the infectiousness of the respiratory aerosols [43,44,46].The prevention of COVID-19 transmission depends on educating staff, residents, and visitors on infection control and preventive practices [13].The measures implemented in LTCF brought several negative consequences for residents, staff, and families.Residents' behavioral problems, depression, anxiety, and loneliness were exacerbated by the pandemic and infection control measures [64].These negative consequences were more likely to affect residents who did not have cognitive impairments [65].Visitor restrictions greatly impact older adults' and their families' health and well-being [66,67].Staff faced several challenges that affected their wellbeing, like the care of the dying, their suffering, and the ethical, cultural, and spiritual care [68,69].Additionally, some evidence [70] reveals that staff in LTCFs had less training, higher staff mobility between working sites, similar personal protective equipment uses, and better selfreported compliance with at-work physical distancing.
The observational design of the bibliographic sample had weak robustness, raising doubts about the generalization of the results.Many infection and control measures integrate complex interventions and are applied in a bundle.In the absence of confounding variable control, it is prudent that these results are seen as suggestive.
The recommendation for applying a multisectoral intervention of combined measures comes from a single study [41] and integrates case and contact management, proactive case identification, strict infection control procedures, resource prioritization and stewardship (Fig. 5).
The application of combined measures is consistent with most available guidance that focus on a set of interventions [51,55,71,72].However, further research on this matter is needed, with more robust study designs, to elucidate better the implications of the measures in reducing the risk of transmission of covid-19 in LTCF during outbreaks, avoiding measures that might spread COVID-19 and threaten residents, staff, and relatives.
In each category (strategic, tactic, operational), we can find measures for outbreak containment of two natures: those that are taken in each situation (which result from an adjustment of practices) and those that result from accommodating existing conditions (which point to measures whose implementation are structural and require unique resources, namely financial) (Fig. 6).
Our results show that outbreak control measures, such as admissions precautions, infection control surveillance, staff training and audits, mask use, signalling, and social distancing, overlap with measures to prevent virus entry within the LTCF [15][16][17][18][19][20].This evidence highlights the importance of maintaining an ongoing risk assessment and adjusting infection prevention measures in LTCF.
Another noteworthy aspect of our study is that the sample of reports included evaluates interventions, which are consistently implemented in combination.This evidence highlights the importance of investigating outbreak containment measures in LTCF as complex interventions.Previous revisions on infection and control measures for LTCF suggested that combining several infection-control strategies may lower COVID-19 infection and mortality rates [16,17].

Strengths and limitations
To the best of our knowledge, this is the first systematic review investigating the effect of containment interventions during COVID-19 outbreaks in LTCF, considering the new coronavirus variants, such as Omicron.The strengths of our review are the comprehensive literature searches and the rigorous methodology.Also, the high rigour level of the design and implementation of this systematic review, including the option for not to include case reports or cross-sectional studies due to their limitations, are strengths that must be highlighted.
The relevance of this study is justified by the continuity of outbreaks in LTCFs and the rapid evolution of studies and publications on the topic, being essential for the development of robust experimental studies that allow the elaboration of supported guidelines of measures to minimize the risk of transmission of COVID-19 in LTCFs and maybe other outbreaks.
However, this review has some limitations.The low number of studies and the impossibility of performing a Meta-analysis due to the methodological and clinical heterogeneity of the studies.Most studies do not consider variables such as country-specific government regulations, the epidemiological context in which the LTCF is inserted, staff qualification levels, and the characteristics that increase vulnerability to residents, such as comorbidities or situations of dependence.The confounding variables are not controlled, which makes it worthwhile to consider the direction of the effect on the spread of the COVID-19 infection during outbreaks in LTCF only suggestive.

Conclusions
LTCF remains a high-risk transmission setting where residents and staff are at risk of COVID-19.Operational, tactical, and strategic approaches may have a favorable effect on preventing the spread of COVID-19 in LTCFs experiencing outbreaks.Some of these infection prevention and control measures seem to be suitable for preventing COVID-19 dissemination in LTCF.Of course, in designing and using these measures, it is necessary to pay attention to aging people and staff 's needs and wellbeing, as well as work conditions.
Our review showed that there are measures for specific COVID-19 outbreak containment in LTCF that could guide policymakers.The bias assessment of the reviewed articles illuminated constraints in specific papers, underscoring the importance of carefully interpreting the systematic review's conclusions.Acknowledging these limitations is vital for accurately measuring the applicability and reliability of the review's findings, thus ensuring evidence-based decision-making in clinical and research contexts.This systematic review proves the need for higher-quality studies in this domain.Once the COVID-19 pandemic is controlled, and considering that the WHO has declared an end to the public health emergency [73], future studies should focus on endemic situations with similar outbreaks.Similar infection and control interventions should be tested n LTCF to allow comparison across studies and pooling of results to provide robust evidence.
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Fig. 2
Fig. 2 Strategic measures to prevent the spread of COVID-19 in LTCFs experiencing outbreaks

Fig. 3
Fig. 3 Tactic measures to prevent the spread of COVID-19 in LTCFs experiencing outbreaks

Fig. 4
Fig. 4 Operational measures to prevent the spread of COVID-19 in LTCFs experiencing outbreaks

Fig. 5 Fig. 6
Fig. 5 Combined measures to prevent the spread of COVID-19 in LTCFs experiencing outbreaks

Table 1
Eligibility criteria

Table 4
Included studies

Table 4
(continued) CI Confidence Interval, CNH Control Nursing Homes, HCW Health Care Workers, HPG Higher-prevalence group, IPC Infection prevention and control, INH Interventional Nursing Homes, LPG Lower-prevalence group, LTCF Long-Term Care Facility, NH Nursing Homes, NR Not reported, OD Odds ratio, p -p value, RR Rate Ratio

Table 5
Sub-group analyses of type of measures with unfavorable/favorable/null effects on COVID-19 transmission

Table 5
(continued) CI Confidence interval, HPG Higher-prevalence group, LPG Lower-prevalence group, LTCF Long-term care facilities, OR Odds ratio, p p value, RR Rates ratio