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  • Systematic Review
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25 January 2024

Systematic Review: Strategies for Improving HIV Testing and Detection Rates in European Hospitals

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1
Section Infectious Diseases, Department of Internal Medicine, Erasmus University Medical Center, 3015 CN Rotterdam, The Netherlands
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Astar Medical Center, 79041 Lviv, Ukraine
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Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, 3015 CN Rotterdam, The Netherlands
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HIV and Infectious Diseases Section, Department of Internal Medicine, Hospital Universitario La Paz-Carlos III, IdiPAZ, 28029 Madrid, Spain
Microorganisms2024, 12(2), 254;https://doi.org/10.3390/microorganisms12020254
This article belongs to the Special Issue Late Presentation to HIV Care
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Abstract

Undiagnosed HIV infection is a prominent clinical issue throughout Europe that requires the continuous attention of all healthcare professionals and policymakers to prevent missed testing opportunities and late diagnosis. This systematic review aimed to evaluate interventions to increase HIV testing rates and case detection in European hospitals. Out of 4598 articles identified, 29 studies fulfilled the selection criteria. Most of the studies were conducted in single Western European capital cities, and only one study was from Eastern Europe. The main interventions investigated were test-all and indicator-condition-based testing strategies. Overall, the prevalence of undiagnosed HIV was well above 0.1%. The studied interventions increased the HIV testing rate and the case detection rate. The highest prevalence of undiagnosed HIV was found with the indicator-condition-driven testing strategy, whereas the test-all strategy had the most profound impact on the proportion of late diagnoses. Nevertheless, the HIV testing rates and case-finding varied considerably across studies. In conclusion, effective strategies to promote HIV testing in European hospitals are available, but relevant knowledge gaps regarding generalizability and sustainability remain. These gaps require the promotion of adherence to HIV testing guidelines, as well as additional larger studies representing all European regions.

1. Introduction

Human immunodeficiency virus (HIV) warrants the continued attention of healthcare professionals and policymakers in Europe to prevent missed opportunities and facilitate timely diagnosis. Over the course of the last three decades, over 2.4 million people have been diagnosed with HIV in the European region as defined by the World Health Organization (WHO) []. With a prevalence of around 0.5%, HIV is still a serious continental public health concern, with its epicenter in Eastern Europe []. The United Nations’ aim of achieving a 75% reduction in new HIV infections in Europe was not reached. Between 2010 and 2020, Western/Central Europe showed an 11% decrease in new infections, while Eastern Europe showed a 43% increase []. The European Centre for Disease Prevention and Control (ECDC) estimated that 14% of persons living with HIV in Europe are still unaware of their diagnosis []. Additionally, 51% of those newly diagnosed with HIV presented late in the disease, with a CD4+ T-cell count of <350 cells/mm3 []. These numbers are concerning, given that late diagnosis is linked to increased rates of illness [,], mortality [,], costs [,], and HIV transmission [].
HIV testing is offered in both healthcare and non-healthcare settings []. It is well described that HIV testing rates among those eligible vary by the testing venue used []. In hospitals specifically, the testing rates showed a wide distribution and differences among the emergency department (4–66%), inpatient department (17–73%), and outpatient department (35–98%) []. While aggregated European data are lacking, in the Netherlands, approximately one in three new HIV diagnoses occur within hospital settings []. The hospital setting provides an opportunity for testing individuals when symptoms and signs associated with HIV that are indicative of potential indicator conditions or risk factors for HIV are identified []. However, even in the presence of an indicator condition, HIV diagnosis could be missed because of insufficient awareness among healthcare professionals in hospitals about the need to offer an HIV test []. Ensuring the utilization of all testing opportunities is crucial to promote improved health by facilitating proper diagnosis that enables access to care and initiation of HIV treatment.
In the WHO’s European region, multiple HIV testing guidelines exist to facilitate appropriate HIV testing in the right individuals presenting to hospitals with indicator conditions or known risk factors (Table 1). The ECDC and WHO both recommend testing all persons with indicators for HIV and promote universal testing in settings and populations with a high HIV prevalence [,]. Universal opt-out testing strategies can also be recommended by national guidelines from high-income countries, e.g., as the British guidelines do when the HIV prevalence exceeds 2/1000 individuals in a region [].
Table 1. HIV test indications within the hospital setting based on European guidelines.
Despite clear guidelines, adherence to HIV testing guidelines in healthcare settings proved to be poor in the United Kingdom, with test coverage of only 27%, which was due to the low provider test offer as opposed to low patient acceptance []. Health service providers throughout Europe have highlighted gaps in HIV testing guidelines related to specific settings and population groups, as well as in the process of offering an HIV test []. A recent pan-European analysis revealed that still less than 50% of the guidelines on HIV indicator conditions included specific HIV testing recommendations []. These observations, taken together, can likely explain the inadequate HIV testing rates in hospitals.
A push forward for healthcare professionals in indicator-condition-based HIV testing was provided by the EuroTEST initiative in 2014 by publishing the practical guideline “HIV Indicator conditions: Guidance for Implementing HIV testing in Adults in Health Care Settings” []. This document strongly recommends HIV testing in any person presenting with an indicator condition associated with an undiagnosed HIV prevalence of >0.1%. The evidence base, including feasibility and effectiveness for the listed conditions, was provided by two large multicenter studies called the HIV Indicator Diseases across Europe Study (HIDES) 1 and HIDES 2 [,]. However, a systematic review conducted in Western countries revealed a low HIV testing rate of less than 50% in clinical settings with selected common indicator conditions []. These results indicate an important implementation gap [].
Emphasizing the role of healthcare professionals in hospitals in facilitating timely HIV diagnoses is a priority, given their crucial role in the HIV care continuum to prevent late-stage disease and reduce transmission. Therefore, the objective of this systematic review was to identify the strategies employed in European hospitals to help healthcare professionals to enhance HIV testing rates and the detection of HIV cases, as well as to evaluate their efficacy.

2. Materials and Methods

2.1. Selection Criteria

A systematic search of the literature was conducted using Medline, Embase, and Web of Science from inception to 4 October 2023. Predefined inclusion and exclusion criteria were established based on the Population, Intervention, Comparison, Outcome (PICO) framework, outlined in Supplement S1. Regarding population, the studies needed to be hospital-based; those conducted in primary care units, community services, or dedicated clinics for sexually transmitted infections (STIs), tuberculosis (TB), or antenatal care (ANC) were excluded. For the intervention, the study’s primary objective needed to evaluate intervention strategies aimed at improving HIV testing rates or HIV case-finding. Studies solely establishing prevalence rates, focusing primarily on other outcomes like acceptability, or examining the effects of passive system changes were excluded (for example, retrospective assessments of guideline changes without active implementation). All study types published after peer-review in journals were considered for inclusion, excluding reviews and conference abstracts.

2.2. Search

The detailed search, available in Supplement S2, employed key terms including “HIV testing” or “HIV infections” coupled with terms indicating hospitals and the 53 individual countries in the WHO’s European region []. The screening process was conducted using Rayyan. It followed a two-step approach involving an initial assessment of titles and abstracts followed by a full-text evaluation of selected eligible articles. Discrepancies in article selection between the two inter-blinded reviewers (K.J.V.-J. and M.V.) were resolved through discussion with a third reviewer (C.R.) until consensus. The reference lists of the identified articles were cross-checked for relevant articles missed by the search.

2.3. Data Extraction and Presentation

Two reviewers (K.J.V.-J. and M.V.) individually extracted data from half of the selected studies using a standardized data extraction table. Data entry was cross-validated by the reviewers cross-checking one another’s findings. The data were categorized by the main interventions studied. A test-all strategy was considered to be the primary intervention if combined with other interventions because of the impact on the number of eligible persons. Data were collected on the setting, HIV testing strategy, and consent mode. Additionally, we delineated the testing continuum, comprising the entire population, the eligible population for an HIV test, HIV testing offer, test acceptance, and test rate (defined as the number of tests performed as a proportion of the eligible population). Both total and new diagnoses were tabulated, and the HIV detection rate was defined as the number of new HIV diagnoses as a proportion of the tested population. Comparisons consisted of changes in HIV testing rate or changes in HIV case-finding, in contrast to either a control group or baseline measurements. HIV case-finding was defined as the number of newly diagnosed HIV infections as a proportion of the entire studied population. The PRISMA guidelines were used for reporting [] (Supplement S3).

2.4. Quality Assessment

Quality assessment was performed using the Risk of Bias in Non-randomized Studies of Interventions (ROBINS-I) tool for non-randomized studies [,,] and the Revised Cochrane Risk-of-Bias tool (RoB 2) for randomized studies [,]. Two independent reviewers (K.J.V.-J. and M.V.) evaluated each study, assessing seven domains. To ensure the accuracy and reliability of the quality assessment, a cross-checking process was conducted by two additional reviewers (C.C.E.J. and O.S.). Discrepancies identified during this phase were resolved through discussion with the first author.

3. Results

The initial search yielded a total of 4598 articles, resulting in 2702 records after duplicates were removed (Figure 1). Following the screening of titles and abstracts, 103 articles were selected for full-text review. After the application of the inclusion and exclusion criteria and the exclusion of a duplicate publication, 27 studies were included in the qualitative synthesis. Two studies were added by cross-reference checking, making a total of 29 studies [,].
Figure 1. PRISMA 2020 flowchart for the inclusion of studies on HIV testing strategies in European hospitals.

3.1. HIV Testing Strategies

Table 2 summarizes the settings and HIV testing strategies described in the 29 included studies. The studies were published between 2012 and 2023. The majority of the studies were conducted in the United Kingdom (n = 14) [,,,,,,,,,,,,,], followed by France (n = 4) [,,,], Italy [,], Spain [,], the Netherlands [,], and Ireland [,] (each n = 2), while the other countries (Poland [], Portugal [], and Switzerland []) contributed one study each. The study settings primarily revolved around capitals or major teaching hospitals. The studies were conducted in the emergency department (ED; n = 14) [,,,,,,,,,,,,,], inpatient department (IPD; n = 8) [,,,,,,,], outpatient department (OPD; n = 5) [,,,,], or a combination of OPD with ED or IPD (n = 2) [,]. The primary strategy studied was a test-all strategy (n = 15), of which over half were conducted in the ED (n = 9) [,,,,,,,,], followed by IPD (n = 3) [,,] or OPD settings (n = 3) [,,]. Another key strategy used was indicator-condition-based testing (n = 8) [,,,,,,,]. The remaining studies primarily evaluated key-population-targeted testing (n = 2) [,], organizing a facility for rapid testing in the OPD (n = 1) [], nurse-based point-of-care testing (n = 1) [], or plan–do–check–act (PDCA) learning cycles (n = 2) [,]. Many studies consisted of multiple strategies. Table 3 summarizes the HIV testing rates and outcomes regarding case-finding for the different strategies.
Table 2. Summary of peer-reviewed studies on HIV testing strategies in European hospitals—descriptors and interventions.
Table 3. Summary of peer-reviewed studies on HIV testing strategies in European hospitals—results.

3.2. Quality Assessment

Two randomized controlled trials showed minor and low concerns, respectively (Supplement S4). The non-randomized studies had variations in the risk of bias (Supplement S5). Overall, only 3 studies (11%) were categorized as having low risk, 15 (56%) showed moderate risk, and 9 (33%) showed serious risk of bias. Notably, the domains patient selection and deviations from intended interventions posed significant biases, indicating potential limitations in representativeness and adherence rates within the eligible population. Conversely, the measurement of outcomes and reporting of results were straightforward, with HIV tests as the primary method (Supplement S5).

3.3. Test-All Strategy

ED test-all strategy studies had variable HIV testing rates, ranging from 3.9% in a study in France [] to 89% in a study in Portugal []. In IPD settings, HIV testing rates ranged from 22% to 46% [,,]. Six studies reported changes compared to a control group or baseline data [,,,,,]. Where evaluated, testing rates significantly increased [,,], resulting in a rise from 0.5 to 2.6% in a Spanish ED [], from 3 to 45% in an OPD in London for returning travelers [], and from 4 to 23% among acute medical admissions in Leicester []. The ED test-all strategy found HIV detection rates ranging from 0.06% in the Netherlands and England to 0.86% in France [,,]. IPD test-all strategies reported detection rates ranging from 0.42% to 2.2% [,,,]. Three studies were able to evaluate case-finding [,,]. In EDs, a test-all strategy combined with either an electronic prompt or a nurse-driven test offer increased the case-finding in Portugal (from 13 to 27 per 100,000) [] and Spain (from 3.2 to 22 per 100,000) []. Similar increases were observed at an IPD in England [].

3.4. Indicator-Condition-Based Testing

Indicator-condition-based testing was assessed in eight studies. Where reported, the HIV testing rates increased [,,,]. Only one study was conducted in the ED, on 1.8 million attendees of 34 Spanish EDs, showing a 42% HIV testing rate after the implementation of an intensive training program []. Education and feedback were used to increase indicator-condition-based HIV testing in the Netherlands, reaching a testing rate of 37% []. Two studies used electronic prompts to promote indicator-condition-based testing, which resulted in increased HIV testing rates in people admitted to the ICU with pneumonia (from 28% to 73%) [] and in people attending the OPD (from 3.2% to 34%) []. An intervention to enhance HIV testing among patients with neurological indicator conditions [] or cervical dyskaryosis [] resulted in testing rates of 8.7% and 46%, respectively, among the eligible population. The HIV detection rates were generally higher than with test-all strategies and were all well above 0.1% [,,,]. However, in four small studies, no new cases were identified [,,,]. Two Italian studies in IPDs found HIV detection rates of 3.7% and 3.8%, respectively [,]. HIV detection rates were lower in a Dutch IPD setting (0.2%) [] and rose from 0.4% to 1.4% in the large Spanish ED study (1.4%) [].

3.5. Other Strategies

Two studies focused on targeted testing of key populations and found a moderate test acceptance of around 50% [,], with a 1.8% HIV detection rate amongst migrants in a Parisian OPD []. Nurse-driven strategies by risk assessment and rapid testing [], or by having nurse practitioners aid with indicator-based testing [], increased the testing rates. Although almost all interventions incorporated teaching efforts, only three studies used teaching as a primary intervention, which led to increased HIV testing rates when used in indicator condition strategies in the abovementioned Spanish and Dutch studies [,], but not in a Polish study with a test-all strategy []. Plan–do–check–act (PDCA) cycle interventions in two ED-based studies increased testing rates and found 0.30% and 0.08% HIV prevalence, respectively, after implementing the addition of blood testing and incorporation of nursing staff into the HIV testing services [], and through teaching, appointing an HIV advocate nurse, and adding HIV testing to a predefined care set []. Offering volunteer point-of-care testing in the OPD or ED also helped with the HIV case identification [,].

3.6. Late Diagnosis

In the ED, implementing universal HIV screening resulted in a reduction in the number of late presenters from 78% to 39% among the total diagnoses []. This was also observed among inpatients, where the percentage of late presenters among screened patients was 52%, as opposed to 92% among those who were tested within a targeted approach []. In Italian IPD settings using targeted testing, late presentation rates of around 75% were reported [,].

4. Discussion

In European hospital settings, the test-all and indicator-condition-based strategies were the most frequently studied interventions, and they successfully increased both HIV testing rates and HIV case detection. Nurse-delivered services, point-of-care testing, and PDCA cycles also showed positive effects. Electronic prompts, utilization of nurses, and educational activities were mostly used to support other strategies.
All controlled studies showed an increase in the HIV testing rates following the intervention [,,,,,,,,,], and nearly all of them reported increased HIV case-finding [,,,,]. In all but one study, the increases were the result of a multifaceted intervention including PDCA, point-of-care testing, electronic prompts, and/or nurse assistance. However, the improvement attained in HIV testing rates was generally moderate, at around or below 50%. Poor testing rates (9–42%) were observed on many occasions, regardless of the setting, even when using well-defined indicator conditions [,,]. Studies reported time pressure [,], lack of additional staff [], requirement of explicit consent [,], lack of automated support [,], turnover of staff [], HIV stigma [], variability in uptake among consultants [], and the clinician’s assessment that testing was not appropriate or not clinically indicated [] as reasons for not testing. Despite the modest testing rates, healthcare professionals found satisfaction in the evident rise [], the cost-effectiveness [,], or the success achieved in real-life scenarios [,,,]. Despite the availability of these clinically effective strategies, their suboptimal implementation perpetuates the existence of missed opportunities to test for HIV in European hospitals.

4.1. Test-All Strategy

The test-all strategy is arguably the strategy that could lead to the fewest missed opportunities. However, this strategy requires the availability of ample resources and personnel to execute it. Moreover, the HIV prevalence in the community should be high enough for a favorable cost–benefit ratio. Most of the test-all studies in EDs were conducted in capital cities in Western Europe, with reported community prevalences ranging from >1/1000 in Paris [] and >2/1000 in Dublin and the United Kingdom [,,] to 5.4/1000 in Wandsworth, London []. The HIV prevalence rates reported in the test-all studies in EDs were all above the 1/1000 (0.1%) cutoff point for cost-effectiveness [,,]. However, the HIV detection rate was sometimes lower [,,,]. This signals a barrier for populations with undiagnosed HIV to present in hospital settings or to accept testing. The solution would be to implement more targeted approaches, or to reevaluate cost-effectiveness considering the added benefit of relinkage to care [,,] and the necessity of accepting higher costs to identify new infections in low-prevalence settings.

4.2. Indicator-Condition-Based Testing

The highest prevalence of undiagnosed HIV was found with an indicator-condition-driven testing strategy [,,,]. This is a logical consequence of selecting people with a higher pretest likelihood of having HIV. Where assessed, the implemented interventions increased the HIV testing rates [,,,]. However, the selected indicator conditions varied; one study added chemsex and post-exposure prophylaxis [], and one study included all indicator conditions []. While identification was based on diagnostic coding in Spain [] and the Netherlands [], manual case review was conducted in neurological inpatients [] and patients attending the OPD [] in England. The selection of the indicator conditions can have a profound impact on the reported HIV testing, with a recent meta-analysis showing variable testing rates with TB (72%), viral hepatitis (45%), malignant lymphoma (35%), and cervical carcinoma and dysplasia (12%) []. Moreover, the indicator conditions differ, with lower (pneumonia or seborrheic dermatitis) or higher (STI or viral hepatitis) HIV prevalence rates []. The selected indicator conditions and limited study size can prevent case identification [,,,]. Given the high yield and favorable cost–benefit ratio, indicator-condition-driven testing practices should be promoted in Europe as a minimum standard.

4.3. Consent Procedures

The methods for obtaining consent for HIV testing varied between studies. Some studies implemented an opt-out strategy [,,,,,,,,], while others required written informed consent [,,,]. Additional procedures may be applicable due to the specific research context. Currently, EuroTEST is in the process of assessing standard practices concerning consent procedures []. It is noteworthy that written informed consent poses a significant barrier to HIV testing [,]. Encouragingly, a recent rapid guidance issued in the UK has introduced the concept of assumed consent for opt-out testing in emergency departments []. International guidelines emphasize that consent for HIV testing should align with that for any other medical test, removing the necessity for written consent [,].

4.4. Late Diagnosis

A mutual goal of all testing efforts is to prevent late HIV diagnosis []. Universal testing is most effective to decrease the proportion of late diagnosis. Although hospital admission for an HIV indicator condition is linked to late diagnoses, clinicians are still accountable for detecting HIV. Neglecting this responsibility prevents the patient from initiating antiretroviral therapy, leading to disease progression. Hence, testing efforts in IPDs should ensure that no person admitted with indicator conditions remains untested for HIV.

4.5. Research Gaps

The common clinical gap deduced from the data in this systematic review is in the evidence base regarding the effective implementation of intervention strategies and their generalizability to other currently unstudied settings. First, no interventional studies have been conducted across hospitals in multiple European countries. Second, a major underrepresented region in all European research initiatives in this field has been Eastern Europe, despite its significant burden of disease. Third, attention should be given to implementation science factors within the study design. Fourth, impact assessments would be improved by adequate control data and long-term follow-up, necessary to evaluate the sustainability of interventional programs. Fifth, data are needed on the prioritization of indicator conditions used in testing strategies when human and financial resources are limited. Sixth, a comprehensive assessment of cost-effectiveness is necessary, encompassing not just the direct cost of the test but also factoring in the unrewarded contributions of on-site nurses and the deployment of research assistants. Ideally, cost-effectiveness evaluations should result in a compelling business case that supports the intervention’s sustainability and gains acceptance from management. Intelligent machine learning tools for case identification have the potential to significantly impact this scenario. Lastly, nurse-based interventions showed promising results [,] and in supporting project-based strategies [,], ED-based test-all studies [,], and specialized clinics []. This signals relevant synergy between doctors and nurses that should be further studied when implementing HIV testing strategies.

4.6. Limitations

Several limitations should be acknowledged. Most of the studies had a truncated methodological quality, with only two being randomized in design and many lacking comparator groups. This limitation affects the overall strength of the evidence and introduces the risk of selection bias and deviations from the intended interventions. Furthermore, the heterogeneity in healthcare systems, populations, and HIV prevalence rates makes generalizing statements regarding the effectiveness of the strategies challenging. In relation to this point, the geographic diversity of the studies considered was limited.

5. Conclusions

In conclusion, this comprehensive analysis of HIV testing strategies in European hospitals revealed a nuanced landscape marked by diversity in approaches and outcomes. Effective strategies to promote HIV testing in hospitals exist but are inconsistently applied. There is a critical need for further research and inclusive implementation to optimally address undiagnosed HIV cases in Europe. These efforts aim to bring solutions to the table of HIV testing strategies in Europe, necessitating international initiatives to address a similar global unmet need.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/2076-2607/12/2/254/s1, S1: PICO; S2: Full search; S3: PRISMA checklist; S4: Quality assessment RCT risk-of-bias tool; S5: Quality assessment ROBINS-I. References [,,,,,,,,,,,,,,,,,,,,,,,,,,,,] are cited in the supplementary file.

Author Contributions

Conceptualization, K.J.V.-J., M.V. and C.R.; methodology, article selection, data extraction, and formal analysis, K.J.V.-J. and M.V.; quality assessment, K.J.V.-J., M.V., C.C.E.J., and O.S.; writing—original draft preparation, K.J.V.-J. and M.V.; writing—review and editing, C.R., C.C.E.J., O.S., J.I.B., S.N., C.K.P., F.V., T.J.B. and A.S.-K.; supervision, C.R. All authors have read and agreed to the published version of the manuscript.

Funding

This review was supported by an unrestricted investigator-initiated study grant from Gilead Sciences (number: GR2020-006) and ViiV Healthcare (ID: 4459). The funding sources did not influence or participate in the study design, data collection, analysis, interpretation, or the drafting of this report. Furthermore, their support did not impact the decision to submit this work for publication.

Data Availability Statement

The findings presented in this systematic review are based on a comprehensive analysis of previously published data, referenced in the accompanying bibliography. No new data were generated or included.

Acknowledgments

The authors extend their gratitude to Wichor Bramer from the Erasmus MC Medical Library for developing the search strategies, and we acknowledge Kathryn Hensley for her advice on the quality assessment. The details regarding the #aware.hiv project can be accessed via the following website: https://awarehiv.com/en/.

Conflicts of Interest

K.J.V.-J. is conducting a PhD that is supported by investigator-initiated study grants from Gilead Sciences and ViiV Healthcare. C.C.E.J. received travel funding from Gilead Sciences and received speaker funding from ViiV Healthcare, both outside the submitted work. J.I.B. has received honoraria as a speaker from Gilead Sciences, ViiV Healthcare, and Johnson & Johnson outside the submitted work. F.V. reports personal fees, non-financial support from Gilead Sciences and ViiV Healthcare, and grants from MSD and B. Braun Melsungen AG outside the submitted work. A.S.-K. declares no conflicts of interest. O.S. has acted as speaker for Gilead Sciences and Johnson & Johnson, outside of the submitted work. C.R. received funding for investigator-initiated studies from Gilead Sciences and ViiV Healthcare.

Correction Statement

This article has been republished with a minor correction to the Funding statement. This change does not affect the scientific content of the article.

References

  1. European Centre for Disease Prevention and Control (ECDC); WHO Regional Office for Europe. HIV/AIDS Surveillance in Europe 2023 (2022 Data); European Centre for Disease Prevention and Control (ECDC): Stockholm, Sweden, 2023. Available online: https://www.ecdc.europa.eu/en/publications-data/hivaids-surveillance-europe-2023-2022-data (accessed on 21 December 2023).
  2. European Centre for Disease Prevention and Control (ECDC); WHO Regional Office for Europe. HIV/AIDS Surveillance in Europe 2022 (2021 Data); European Centre for Disease Prevention and Control (ECDC): Stockholm, Sweden, 2022. Available online: https://www.ecdc.europa.eu/en/publications-data/hiv-aids-joint-report-surveillance-2021-data (accessed on 21 December 2023).
  3. UNAIDS. UNAIDS Data 2021. 2021. Available online: https://aidsinfo.unaids.org/ (accessed on 21 December 2023).
  4. Tominski, D.; Katchanov, J.; Driesch, D.; Daley, M.B.; Liedtke, A.; Schneider, A.; Slevogt, H.; Arastéh, K.; Stocker, H. The late-presenting HIV-infected patient 30 years after the introduction of HIV testing: Spectrum of opportunistic diseases and missed opportunities for early diagnosis. HIV Med. 2017, 18, 125–132. [Google Scholar] [CrossRef]
  5. Marcus, J.L.; Leyden, W.A.; Alexeeff, S.E.; Anderson, A.N.; Hechter, R.C.; Hu, H.; Lam, J.O.; Towner, W.J.; Yuan, Q.; Horberg, M.A.; et al. Comparison of Overall and Comorbidity-Free Life Expectancy Between Insured Adults With and Without HIV Infection, 2000–2016. JAMA Netw. Open 2020, 3, e207954. [Google Scholar] [CrossRef]
  6. May, M.; Gompels, M.; Delpech, V.; Porter, K.; Post, F.; Johnson, M.; Dunn, D.; Palfreeman, A.; Gilson, R.; Gazzard, B.; et al. Impact of late diagnosis and treatment on life expectancy in people with HIV-1: UK Collaborative HIV Cohort (UK CHIC) Study. BMJ 2011, 343, d6016. [Google Scholar] [CrossRef]
  7. Nakagawa, F.; Lodwick, R.K.; Smith, C.J.; Smith, R.; Cambiano, V.; Lundgren, J.D.; Delpech, V.; Phillips, A.N. Projected life expectancy of people with HIV according to timing of diagnosis. AIDS 2012, 26, 335–343. [Google Scholar] [CrossRef]
  8. Popping, S.; Versteegh, L.; Nichols, B.E.; van de Vijver, D.A.M.C.; van Sighem, A.; Reiss, P.; Geerlings, S.; Boucher, C.A.B.; Verbon, A. Characteristics and short- and long-term direct medical costs among adults with timely and delayed presentation for HIV care in the Netherlands. PLoS ONE 2023, 18, e0280877. [Google Scholar] [CrossRef] [PubMed]
  9. Baggaley, R.F.; Irvine, M.A.; Leber, W.; Cambiano, V.; Figueroa, J.; McMullen, H.; Anderson, J.; Santos, A.C.; Terris-Prestholt, F.; Miners, A.; et al. Cost-effectiveness of screening for HIV in primary care: A health economics modelling analysis. Lancet HIV 2017, 4, e465–e474. [Google Scholar] [CrossRef] [PubMed]
  10. Rodger, A.J.; Cambiano, V.; Bruun, T.; Vernazza, P.; Collins, S.; Degen, O.; Corbelli, G.M.; Estrada, V.; Geretti, A.M.; Beloukas, A.; et al. Risk of HIV transmission through condomless sex in serodifferent gay couples with the HIV-positive partner taking suppressive antiretroviral therapy (PARTNER): Final results of a multicentre, prospective, observational study. Lancet 2019, 393, 2428–2438. [Google Scholar] [CrossRef] [PubMed]
  11. European Centre for Disease Prevention and Control. HIV Testing in Europe and Central Asia. Monitoring Implementation of the Dublin Declaration on Partnership to Fight HIV/AIDS in Europe and Central Asia: 2022 Progress Report; European Centre for Disease Prevention and Control (ECDC): Stockholm, Sweden, 2022. Available online: https://www.ecdc.europa.eu/en/publications-data/hiv-testing-europe-and-central-asia (accessed on 21 December 2023).
  12. Desai, S.; Tavoschi, L.; Sullivan, A.K.; Combs, L.; Raben, D.; Delpech, V.; Jakobsen, S.F.; Amato-Gauci, A.J.; Croxford, S. HIV testing strategies employed in health care settings in the European Union/European Economic Area (EU/EEA): Evidence from a systematic review. HIV Med. 2020, 21, 163–179. [Google Scholar] [CrossRef] [PubMed]
  13. Stichting HIV Monitoring (SHM). HIV Monitoring Report; Stichting HIV Monitoring (SHM): Amsterdam, The Netherlands, 2023; Available online: https://www.hiv-monitoring.nl/application/files/5717/0066/1002/NL_HIV_MONITORING_REPORT_2023.pdf (accessed on 21 December 2023).
  14. EuroTEST. HIV Indicator Conditions: Guidance for Implementing HIV Testing in Adults in Health Care Settings; EuroTEST: Brussels, Belgium, 2014; Available online: https://eurotest.org/projects-collaborations/indicator-condition-guided-hiv-testinghides/guidance-hiv-indicator-conditions (accessed on 21 December 2023).
  15. Bogers, S.J.; Hulstein, S.H.; Schim van der Loeff, M.F.; de Bree, G.J.; Reiss, P.; van Bergen, J.; Geerlings, S.E.; HIV Transmission Elimination AMsterdam (H-TEAM) Consortium. Current evidence on the adoption of indicator condition guided testing for HIV in western countries: A systematic review and meta-analysis. eClinicalMedicine 2021, 35, 100877. [Google Scholar] [CrossRef] [PubMed]
  16. European Centre for Disease Prevention and Control (ECDC). Public Health Guidance on HIV, Hepatitis B and C Testing in the EU/EEA; European Centre for Disease Prevention and Control (ECDC): Stockholm, Sweden, 2018. Available online: https://www.ecdc.europa.eu/en/publications-data/public-health-guidance-hiv-hepatitis-b-and-c-testing-eueea (accessed on 21 December 2023).
  17. World Health Organization. Consolidated Guidelines on HIV Prevention, Testing, Treatment, Service Delivery and Monitoring: Recommendations for a Public Health Approach; World Health Organization: Geneva, Switzerland, 2021. Available online: https://www.who.int/publications/i/item/9789240031593 (accessed on 21 December 2023).
  18. British HIV Association. Adult HIV Testing Guidelines 2020; British HIV Association/British Association for Sexual Health and HIV/British Infection Association: London, UK, 2020; Available online: https://www.bhiva.org/HIV-testing-guidelines (accessed on 21 December 2023).
  19. Elmahdi, R.; Gerver, S.M.; Gomez Guillen, G.; Fidler, S.; Cooke, G.; Ward, H. Low levels of HIV test coverage in clinical settings in the UK: A systematic review of adherence to 2008 guidelines. Sex Transm. Infect. 2014, 90, 119–124. [Google Scholar] [CrossRef] [PubMed]
  20. Bell, S.; De Wit, J. HIV Testing Services: Analysis of Guidelines and Perceptions of Practice across the WHO European Region. Summary Report; Centre for Social Research in Health, UNSW Australia: Kensington, Australia, 2016. [Google Scholar]
  21. Jordans, C.C.E.; Vasylyev, M.; Rae, C.; Jakobsen, M.L.; Vassilenko, A.; Dauby, N.; Grevsen, A.L.; Jakobsen, S.F.; Raahauge, A.; Champenois, K.; et al. National medical specialty guidelines of HIV indicator conditions in Europe lack adequate HIV testing recommendations: A systematic guideline review. Eurosurveillance 2022, 27, 2200338. [Google Scholar] [CrossRef]
  22. Sullivan, A.K.; Raben, D.; Reekie, J.; Rayment, M.; Mocroft, A.; Esser, S.; Leon, A.; Begovac, J.; Brinkman, K.; Zangerle, R.; et al. Feasibility and effectiveness of indicator condition-guided testing for HIV: Results from HIDES I (HIV indicator diseases across Europe study). PLoS ONE 2013, 8, e52845. [Google Scholar] [CrossRef]
  23. Raben, D.; Sullivan, A.K.; Mocroft, A.; Kutsyna, G.; Hadžiosmanović, V.; Vassilenko, A.; Chkhartisvili, N.; Mitsura, V.; Pedersen, C.; Anderson, J.; et al. Improving the evidence for indicator condition guided HIV testing in Europe: Results from the HIDES II Study—2012–2015. PLoS ONE 2019, 14, e0220108. [Google Scholar] [CrossRef]
  24. Raben, D.; Sullivan, A. Implementation of indicator condition guided HIV testing still lagging behind the evidence. eClinicalMedicine 2021, 36, 100918. [Google Scholar] [CrossRef]
  25. World Health Organization. Countries. Available online: https://www.who.int/countries (accessed on 1 December 2023).
  26. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef]
  27. Sterne, J.A.C.; Hernán, M.A.; Reeves, B.C.; Savović, J.; Berkman, N.D.; Viswanathan, M.; Henry, D.; Altman, D.G.; Ansari, M.T.; Boutron, I.; et al. ROBINS-I: A tool for assessing risk of bias in non-randomised studies of interventions. BMJ 2016, 355, i4919. [Google Scholar] [CrossRef]
  28. ROBINS-I Tool. Available online: https://www.riskofbias.info/welcome/home/current-version-of-robins-i (accessed on 1 December 2023).
  29. McGuinness, L.A.; Higgins, J.P.T. Risk-of-bias VISualization (robvis): An R package and Shiny web app for visualizing risk-of-bias assessments. Res. Synth. Methods 2021, 12, 55–61. [Google Scholar] [CrossRef]
  30. Sterne, J.A.C.; Savović, J.; Page, M.J.; Elbers, R.G.; Blencowe, N.S.; Boutron, I.; Cates, C.J.; Cheng, H.Y.; Corbett, M.S.; Eldridge, S.M.; et al. RoB 2: A revised tool for assessing risk of bias in randomised trials. BMJ 2019, 366, l4898. [Google Scholar] [CrossRef]
  31. Cochrane Risk-of-Bias Tool for Randomized Trials (RoB 2). Available online: https://methods.cochrane.org/bias/resources/rob-2-revised-cochrane-risk-bias-tool-randomized-trials (accessed on 1 December 2023).
  32. Gómez-Ayerbe, C.; Martínez-Sanz, J.; Muriel, A.; Pérez Elías, P.; Moreno, A.; Barea, R.; Polo, L.; Cano, A.; Uranga, A.; Santos, C.; et al. Impact of a structured HIV testing program in a hospital emergency department and a primary care center. PLoS ONE 2019, 14, e0220375. [Google Scholar] [CrossRef] [PubMed]
  33. Bogers, S.J.; Schim van der Loeff, M.F.; Boyd, A.; Davidovich, U.; van der Valk, M.; Brinkman, K.; Sigaloff, K.; Branger, J.; Bokhizzou, N.; de Bree, G.J.; et al. Improving indicator-condition guided testing for HIV in the hospital setting (PROTEST 2·0): A multicenter, interrupted time-series analysis. Lancet Reg. Health Eur. 2022, 23, 100515. [Google Scholar] [CrossRef] [PubMed]
  34. Marchant, R.; Patterson, A.; Dragovic, B.; Kelly, B.; Hamzah, L.; Hempling, M. High-level compliance to opt-out HIV testing in the emergency department (ED) of a large teaching hospital using the biochemistry sample as the sample type for HIV screening. HIV Med. 2022, 23, 1214–1218. [Google Scholar] [CrossRef]
  35. Orkin, C.; Flanagan, S.; Wallis, E.; Ireland, G.; Dhairyawan, R.; Fox, J.; Nandwani, R.; O’Connell, R.; Lascar, M.; Bulman, J.; et al. Incorporating HIV/hepatitis B virus/hepatitis C virus combined testing into routine blood tests in nine UK Emergency Departments: The “Going Viral” campaign. HIV Med. 2016, 17, 222–230. [Google Scholar] [CrossRef]
  36. Bath, R.; O’Connell, R.; Lascar, M.; Ferrand, R.; Strachan, S.; Matin, N.; Bassnet, I.; Orkin, C. TestMeEast: A campaign to increase HIV testing in hospitals and to reduce late diagnosis. AIDS Care 2016, 28, 608–611. [Google Scholar] [CrossRef]
  37. Herbert, R.; Ashraf, A.N.; Yates, T.A.; Spriggs, K.; Malinnag, M.; Durward-Brown, E.; Phillips, D.; Mewse, E.; Daniel, A.; Armstrong, M.; et al. Nurse-delivered universal point-of-care testing for HIV in an open-access returning traveller clinic. HIV Med. 2012, 13, 499–504. [Google Scholar] [CrossRef]
  38. Burns, F.; Edwards, S.G.; Woods, J.; Haidari, G.; Calderon, Y.; Leider, J.; Morris, S.; Tobin, R.; Cartledge, J.; Brown, M. Acceptability, feasibility and costs of universal offer of rapid point of care testing for HIV in an acute admissions unit: Results of the RAPID project. HIV Med. 2013, 14 (Suppl. 3), 10–14. [Google Scholar] [CrossRef] [PubMed]
  39. Hill-Tout, R.; Cormack, I.; Elgalib, A. Routine HIV testing in acute medical admissions in a high prevalence area reduces morbidity and mortality of HIV: A full cycle audit. Int. J. STD AIDS 2016, 27, 591–594. [Google Scholar] [CrossRef]
  40. Palfreeman, A.; Nyatsanza, F.; Farn, H.; McKinnon, G.; Schober, P.; McNally, P. HIV testing for acute medical admissions: Evaluation of a pilot study in Leicester, England. Sex Transm. Infect. 2013, 89, 308–310. [Google Scholar] [CrossRef]
  41. Fox, M.; Pettit, R.; Mutengesa, E.; Harper, A.; Nakhoul, M.; Mitra, A. Improving detection of undiagnosed HIV through routine screening in a central London emergency department. BMJ Open Qual. 2022, 11, e001799. [Google Scholar] [CrossRef] [PubMed]
  42. Rayment, M.; Rae, C.; Ghooloo, F.; Doku, E.; Hardie, J.; Finlay, S.; Gidwani, S.; Atkins, M.; Roberts, P.; Sullivan, A.K. Routine HIV testing in the emergency department: Tough lessons in sustainability. HIV Med. 2013, 14 (Suppl. 3), 6–9. [Google Scholar] [CrossRef] [PubMed]
  43. Qureshi, N.S.; Manavi, K. The prevalence of HIV among women with high-grade cervical smear abnormalities in Birmingham, United Kingdom: A prospective cohort study. Eur. J. Obstet. Gynecol. Reprod. Biol. 2017, 212, 51–53. [Google Scholar] [CrossRef] [PubMed]
  44. Youssef, E.; Sanghera, T.; Bexley, A.; Hayes, M.; Perry, N.; Dosekun, O.; Perera, S. HIV testing in patients presenting with indicator conditions in outpatient settings: Offer and uptake rates, and educational and active interventions. Int. J. STD AIDS 2018, 29, 1289–1294. [Google Scholar] [CrossRef]
  45. Sharvill, R.; Fernandes, A.; Allen, K.; Astin, J. Adopting universal testing for HIV in intensive care for patients admitted with severe pneumonia: Results from our change in practice. Int. J. STD AIDS 2017, 28, 88–90. [Google Scholar] [CrossRef] [PubMed]
  46. Sokhi, D.S.; Oxenham, C.; Coates, R.; Forbes, M.; Gupta, N.K.; Blackburn, D.J. Four-Stage Audit Demonstrating Increased Uptake of HIV Testing in Acute Neurology Admissions Using Staged Practical Interventions. PLoS ONE 2015, 10, e0134574. [Google Scholar] [CrossRef] [PubMed]
  47. Freer, J.; Lascar, M.; Phiri, E. Tailoring HIV testing in a setting of late HIV diagnosis: Is the tide turning? Br. J. Hosp. Med. Lond. 2015, 76, 592–595. [Google Scholar]
  48. Casalino, E.; Bernot, B.; Bouchaud, O.; Alloui, C.; Choquet, C.; Bouvet, E.; Damond, F.; Firmin, S.; Delobelle, A.; Nkoumazok, B.E.; et al. Twelve months of routine HIV screening in 6 emergency departments in the Paris area: Results from the ANRS URDEP study. PLoS ONE 2012, 7, e46437. [Google Scholar] [CrossRef]
  49. d’Almeida, K.W.; Kierzek, G.; de Truchis, P.; Le Vu, S.; Pateron, D.; Renaud, B.; Semaille, C.; Bousquet, V.; Simon, F.; Guillemot, D.; et al. Modest public health impact of nontargeted human immunodeficiency virus screening in 29 emergency departments. Arch. Intern. Med. 2012, 172, 12–20. [Google Scholar] [CrossRef]
  50. Leblanc, J.; Hejblum, G.; Costagliola, D.; Durand-Zaleski, I.; Lert, F.; de Truchis, P.; Verbeke, G.; Rousseau, A.; Piquet, H.; Simon, F.; et al. Targeted HIV Screening in Eight Emergency Departments: The DICI-VIH Cluster-Randomized Two-Period Crossover Trial. Ann. Emerg. Med. 2018, 72, 41–53.e9. [Google Scholar] [CrossRef]
  51. Aparicio, C.; Mourez, T.; Simoneau, G.; Magnier, J.D.; Galichon, B.; Plaisance, P.; Bergmann, J.F.; Sellier, P. Proposal of HIV, HBV and HCV targeted screening: Short period feasibility study in a free-access outpatient medical structure. Presse Med. 2012, 41, e517–e523. [Google Scholar] [CrossRef]
  52. Barbanotti, D.; Tincati, C.; Tavelli, A.; Santoro, A.; Sala, M.; Bini, T.; De Bona, A.; d’Arminio Monforte, A.; Marchetti, G.C. HIV-Indicator Condition Guided Testing in a Hospital Setting. Life 2023, 13, 1014. [Google Scholar] [CrossRef]
  53. De Vito, A.; Colpani, A.; Mameli, M.S.; Bagella, P.; Fiore, V.; Fozza, C.; Montesu, M.A.; Fois, A.G.; Filigheddu, F.; Manzoni, N.; et al. HIV Infection Indicator Disease-Based Active Case Finding in a University Hospital: Results from the SHOT Project. Infect. Dis. Rep. 2023, 15, 94–101. [Google Scholar] [CrossRef]
  54. González Del Castillo, J.; Fuentes Ferrer, M.E.; Fernández Pérez, C.; Molina Romera, G.; Núñez Orantos, M.J.; Estrada Pérez, V. Efficiency of screening for human immunodeficiency virus infection in emergency departments: A systematic review and meta-analysis. Emergencias 2022, 34, 204–212. [Google Scholar]
  55. Luiken, G.P.M.; Joore, I.K.; Taselaar, A.; Schuit, S.C.E.; Geerlings, S.E.; Govers, A.; Rood, P.P.M.; Prins, J.M.; Nichols, B.E.; Verbon, A.; et al. Non-targeted HIV screening in emergency departments in the Netherlands. Neth. J. Med. 2017, 75, 386–393. [Google Scholar]
  56. Grant, C.; O’Connell, S.; Lillis, D.; Moriarty, A.; Fitzgerald, I.; Dalby, L.; Bannan, C.; Tuite, H.; Crowley, B.; Plunkett, P.; et al. Opt-out screening for HIV, hepatitis B and hepatitis C: Observational study of screening acceptance, yield and treatment outcomes. Emerg. Med. J. 2020, 37, 102–105. [Google Scholar] [CrossRef]
  57. O’Connell, S.; Lillis, D.; Cotter, A.; O’Dea, S.; Tuite, H.; Fleming, C.; Crowley, B.; Fitzgerald, I.; Dalby, L.; Barry, H.; et al. Opt-Out Panel Testing for HIV, Hepatitis B and Hepatitis C in an Urban Emergency Department: A Pilot Study. PLoS ONE 2016, 11, e0150546. [Google Scholar] [CrossRef]
  58. Cholewińska, G.; Siewaszewicz, E.; Robak, J.; Dawid, E.; Smykiewicz, J.; Skowron, W. Impact of a structured medical staff education program on the effect of HIV testing in four multi-specialist hospitals of the mazowieckie voivodeship as a part of the “Stop late presenters” project. Przegl. Epidemiol. 2020, 74, 133–146. [Google Scholar]
  59. Vaz-Pinto, I.; Gorgulho, A.; Esteves, C.; Guimarães, M.; Castro, V.; Carrodeguas, A.; Medina, D. Increasing HIV early diagnosis by implementing an automated screening strategy in emergency departments. HIV Med. 2022, 23, 1153–1162. [Google Scholar] [CrossRef]
  60. Gillet, C.; Darling, K.E.A.; Senn, N.; Cavassini, M.; Hugli, O. Targeted versus non-targeted HIV testing offered via electronic questionnaire in a Swiss emergency department: A randomized controlled study. PLoS ONE 2018, 13, e0190767. [Google Scholar] [CrossRef]
  61. Sanders, G.D.; Bayoumi, A.M.; Sundaram, V.; Bilir, S.P.; Neukermans, C.P.; Rydzak, C.E.; Douglass, L.R.; Lazzeroni, L.C.; Holodniy, M.; Owens, D.K. Cost-effectiveness of screening for HIV in the era of highly active antiretroviral therapy. N. Engl. J. Med. 2005, 352, 570–585. [Google Scholar] [CrossRef]
  62. Yazdanpanah, Y.; Sloan, C.E.; Charlois-Ou, C.; Le Vu, S.; Semaille, C.; Costagliola, D.; Pillonel, J.; Poullié, A.-I.; Scemama, O.; Deuffic-Burban, S.; et al. Routine HIV screening in France: Clinical impact and cost-effectiveness. PLoS ONE 2010, 5, e13132. [Google Scholar] [CrossRef]
  63. Yazdanpanah, Y.; Perelman, J.; DiLorenzo, M.A.; Alves, J.; Barros, H.; Mateus, C.; Pereira, J.; Mansinho, K.; Robine, M.; Park, J.-E.; et al. Routine HIV screening in Portugal: Clinical impact and cost-effectiveness. PLoS ONE 2013, 8, e84173. [Google Scholar] [CrossRef]
  64. Eurotest Survey on Blood Borne Virus (HIV, Hepatitis B and C) Testing Consent Requirements. Available online: https://eurotest.org/projects-collaborations/testing-consent-survey/ (accessed on 21 December 2023).
  65. Ehrenkranz, P.D.; Pagán, J.A.; Begier, E.M.; Linas, B.P.; Madison, K.; Armstrong, K. Written informed-consent statutes and HIV testing. Am. J. Prev. Med. 2009, 37, 57–63. [Google Scholar] [CrossRef]
  66. Wing, C. Effects of written informed consent requirements on HIV testing rates: Evidence from a natural experiment. Am. J. Public Health 2009, 99, 1087–1092. [Google Scholar] [CrossRef]
  67. British HIV Association. Rapid Guidance on Assumed Consent for Opt-Out Blood-Borne Virus Testing in Emergency Departments; BHIVA, BIA and BASHH: London, UK, 2023; Available online: https://www.bhiva.org/rapid-guidance-on-assumed-consent-for-opt-out-blood-borne-virus-testing (accessed on 21 December 2023).
  68. European Centre for Disease Prevention and Control (ECDC). ECDC Guidance HIV Testing: Increasing Uptake and Effectiveness in the European Union; European Centre for Disease Prevention and Control (ECDC): Stockholm, Sweden, 2010. Available online: https://www.ecdc.europa.eu/sites/default/files/media/en/publications/Publications/101129_GUI_HIV_testing.pdf (accessed on 21 December 2023).
  69. Croxford, S.; Stengaard, A.R.; Brännström, J.; Combs, L.; Dedes, N.; Girardi, E.; Grabar, S.; Kirk, O.; Kuchukhidze, G.; Lazarus, J.V.; et al. Late diagnosis of HIV: An updated consensus definition. HIV Med. 2022, 23, 1202–1208. [Google Scholar] [CrossRef]
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