Efficiency of decentralized screening for hepatitis C in different healthcare settings: retrospective study over 6 years in southeastern Spain

Introduction

The eradication of hepatitis C virus (HCV) infection has become one of the most significant public health challenges worldwide (1). Thanks to the development of new drugs, a paradigm shift has occurred, and progress is being made towards its eradication through active case finding and treatment (2). It is estimated that the global prevalence of viremic HCV in 2020 was 0.7% of the world population, corresponding to 56.8 million people. However, this data is encouraging as it represents a decrease of between 6 and 8 million people compared to the 2015 available data (3). Nevertheless, it is estimated that globally, only 20% of infected patients are aware of their diagnosis, and of these, only 7% are treated. In terms of genotypes, genotype 1 is the most prevalent (44% of patients), followed by genotype 3 (25% of cases) (4).

The World Health Organization (WHO) has set a goal to eliminate hepatitis C by 2030, aiming to make this disease no longer a public health problem. One of the most important pathways to achieve this objective is the diagnosis of patients, as the available treatment is almost 100% effective with few side effects. Population-wide screening is not implemented in Spain because it is considered not cost-effective, but opportunistic screenings are conducted in various areas of the healthcare system (5). The Centers for Disease Control and Prevention (CDC) recommends universal screening for HCV at least once in a lifetime for every individual, and for all pregnant women in areas where the prevalence of HCV infection is higher than 0.1% (6). Specifically, in the USA, the CDC also recommends targeted screening for special populations such as justice-involved individuals (7). In the US, studies have shown that targeted screening in populations who use injectable drugs is more cost-effective than universal screening (8). Similarly, some studies report that decentralized screening increases the likelihood of identifying positive cases (9,10). In Spain, studies have also indicated that screening people who inject drugs is more cost-effective (11). However, no studies have compared the cost-effectiveness of screening conducted in primary healthcare centers versus decentralized screening strategies, such as dried blood spot testing or screening performed in prison settings.

In Spain, according to the 2017 Seroprevalence Study, the estimated prevalence of antibodies against HCV in the population is 0.85%, with active infection at 0.22%, suggesting that around 22,578 individuals remained undiagnosed in 2017–2018 (12). Currently, screening is recommended only in cases of clinical suspicion, history of exposure to risk, and in cases of transfusions, donations, or transplants (5). However, screening may also be considered for individuals belonging to high-risk groups.

This study analyzes the efficiency of these opportunistic screenings in our setting, including decentralized screening, which is carried out in Penitentiary centers and vulnerable populations using the Dry Blood Spot (DBS) system. We present this article in accordance with the STROBE reporting checklist (available at https://tgh.amegroups.com/article/view/10.21037/tgh-25-58/rc).

Methods

Design

This was a retrospective cross-sectional study aimed at determining the efficiency of opportunistic screenings conducted in various healthcare settings and through a decentralized diagnostic process in prisons and by DBS (disadvantaged people, in collaboration with Red Cross). The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by Institutional Ethics Committee for Research with Medicines of the Department of Health of Alicante-Dr. Balmis General University Hospital (Ref. CEIm: PI2023-157), individual consent for this retrospective analysis was waived due to the retrospective nature. All patients who were tested for HCV antibodies within these screening processes from 2017 to July 2023 in the Dr. Balmis General University Hospital of Alicante have been included, and only a sample per patient was considered. For each patient, data collected included age (<45, ≥45 years), gender (male, female), screening setting (emergency departments, gynecology, surgery, primary care, nephrology, prisons, occupational risk accidents, hematology). In addition, a screening was done on vulnerable populations (Patients receiving methadone maintenance treatment, people experiencing homelessness and shelter residents…) using DBS presence of HCV antibodies and genome, co-infection with hepatitis B and human immunodeficiency virus (HIV).

Protocol

All samples received for HCV antibody screening were processed using the Cobas 6800 system (Roche Diagnostics, Barcelona, Spain). Any positive result was confirmed by two techniques: antibody presence using the Alinity system (Abbott), and viral RNA (vRNA) detection using the Cobas 6800 system (Roche Diagnostics).

Regarding the DBS samples, they were sent to the reference laboratory at Microbiology Service of Dr. Balmis General University Hospital of Alicante at room temperature within 24 hours of extraction. Subsequently, the DBS were immersed in a medium with saline serum and processed for antibody detection. In samples positive for HCV antibodies, detection of vRNA presence was also performed using the same sample. Validation of this methodology, including the sample collection and sending process, as well as the technical-experimental procedure, was previously conducted through a preliminary study on patients with known infection, both with and without vRNA presence.

Statistical analysis

Primarily, a cross-sectional observational study of the characteristics of all patients included in the study was conducted. Absolute and relative frequencies in percentages of each category of the variables were calculated. Subsequently, patient characteristics (e.g., age, sex, sample origin) were compared according to the year of HCV test using the Chi-squared test. Following that, the prevalence of HCV antibodies and viral load was calculated for the total and for each patient characteristic (age, sex, etc.). The Chi-squared test was used to study the association between patient characteristics and prevalence, and to quantify the magnitude of the association, odds ratios (OR) with a 95% confidence interval (95% CI) were calculated. Variables that were statistically significant in the univariate analysis were included in a logistic regression model, calculating the adjusted OR (ORa) with its 95% CI. The level of statistical significance used for hypothesis testing was P<0.05. Statistical analysis was performed using the IBM-SPSS^® Statistics v.25.0 software. Finally, the total cost of HCV antibody and viral load tests was calculated as the product of the number of tests performed by the unit cost of each test (10.52 € and 89.29 €, respectively). The total cost of the study corresponds to the sum of the total costs (negative + positive) of antibody and viral load studies. The cost per case with detectable viral load was calculated by dividing the total cost by the number of patients with detectable viral load treated. All costs were calculated for all age groups, sex, sample origin, season, HIV co-infection, and hepatitis B co-infection, according to the Fees Law of the Valencian Community for the year 2024.

Results

In this study were included a total of 66,532 cases, the majority of the cases studied were in individuals under 45 years old (52%, 33,703/64,772), with the main source of samples being Primary Care, accounting for 51.7% (34,387/66,532) of the total, followed by the nephrology service (12.8% of the total, 8,539/66,532) and gynecology (12.7% of the total, 8,467/66,532). It is worth noting that cases from decentralized screening accounted for a total of 7.4% (4,938/66,532) of the cases, with 4.8% (3,178/66,532) coming from penitentiary centers and 2.6% (1,760/66,532) from DBS samples (Table 1).

During the study period, the presence of antibodies against HCV was analyzed in 66,532 samples, of which 855 were positive. Of these cases, viral genome presence was detected in 315 patients. The prevalence of the positive antibodies of HCV in our setting was 1.29% (855/66,532), and for viral load was 0.49% (315/66,532). In the healthcare setting, 61,594 cases were analyzed, with a prevalence of 0.44% (270/61,594) for positive HCV antibodies, and 0.14% (87/61,594) for the presence of viral genome. In primary care, the prevalence of positive HCV antibodies, and the presence of viral genome were 0.51% (178/34,387) and 0.16% (56/34,387), respectively. The emergency department showed the highest prevalence of positive antibodies and viral load (0.85%, 9/1,058 and 0.37%, 4/1,058, respectively). It is noteworthy that in the screening of patients from the gynecology service, only 0.11% (10/8,467) of samples showed positive antibodies for HCV, with vRNA presence detected in only 0.01% (1/8,467) of cases. With regard to decentralized screening, 4,938 cases were analyzed. The prevalence of positive HCV antibodies was 11.85% (585/4,938), and the prevalence of viral genome was 4.67% (228/4,938). Stratifying by place of origin, from penitentiary centers, 3,178 samples were analyzed, revealing a prevalence of antibodies and viral load of 7.39% (235/3,178) and 3.30% (105/3,178), respectively. In samples obtained through DBS, the prevalence of antibodies was 19.89% (350/1,760), with 6.98% (123/1,760) showing vRNA (Tables 2,3).

As for the associations of demographic variables with the detection of positive antibodies for HCV, it was found that in individuals under 45 years of age, there was a 0.4 times lower probability of detecting positive antibodies for HCV, and a 0.6 times lower probability of detecting viral genome compared to those over 45 years old. Taking gender into account, men were associated with 1.9 times higher detection of positive antibodies for hepatitis C and 2.5 times higher probability of vRNA presence. Regarding the origin, patients who underwent screening in prisons and through DBS testing had 35.5 times and 209.9 times higher probability of presenting positive antibodies for HCV, respectively, and 173.9 and 591.7 times more likely to present viral genome, respectively. By contrast, no association was found between the positivity of antibodies against HCV, nor the presence of viral genome in the screenings conducted in the gynecology service. Finally, studying the association between co-infections, patients with positive antibodies for HCV, had a 7.7 times higher probability of having positive antibodies to HIV, also patients with viral genome of HCV had a 5 times higher probability of being co-infected with HIV (Tables 2,3).

Upon analyzing the costs of screening processes, the screening conducted on patients who attended the gynecology service amounted to a total of 89,966 € per positive patient for vRNA. This amount decreased to 6,744 € in primary care and to 2,983 € in emergency care. When analyzing the cost in the decentralized setting, a patient with vRNA incurred a cost of 518 € if they originated from a penitentiary center and 405 € if they had been studied through DBS (Table 4).

Discussion

The data obtained in this study show a significant difference regarding the efficiency of screening in the different populations studied. In our setting, it is very useful the decentralized screening performed in prisons and vulnerable groups analyzed by DBS, being much less efficient in other scenarios, especially in the gynecological services. In our setting, systematic screening of this parameter is not performed in pregnant women. However, due to the clinical implications of this infection in this population, universal screening during pregnancy is recommended by some authors (13).

Hepatitis screening in different healthcare settings has been approached from multiple perspectives in the absence of a universal population-based screening strategy, with the aim of improving efficiency (14,15). Accordingly, both age-based and non-age-based screenings have been conducted among hospitalized patients and in primary care (16-18), among migrant populations attending primary care services (19), people who inject drugs (20), individuals with mental health disorders (21), penitentiary centers (22), patients attending sexual health clinics, individuals living with HIV, and men who have sex with men (23,24), as well as among other socially vulnerable groups (25). Previous literature has reported higher rates of HCV RNA positivity in men (26) and in patients coinfected with other viruses, particularly HIV (7), evidence that is also confirmed in the present study. The outcomes obtained across these different screening approaches vary depending on numerous organizational factors and the prevalence of infection within each target population. Nonetheless, it has been consistently reported that the absence of screening programs imposes a substantial economic burden on public healthcare systems due to the high disease burden associated with undiagnosed cases and delayed diagnosis (27,28).

When assessing the efficiency of screening within healthcare settings, the outstanding capacity of emergency departments to identify new cases becomes evident, representing, in our context, the most efficient strategy among those evaluated. These results are consistent with previously published evidence highlighting the critical role of implementing screening programs in this setting (29,30). Indeed, it has been reported that the prevalence of undiagnosed individuals is higher in emergency departments than in the general population (31), and significant diagnostic yields have been achieved through the implementation of automated hepatitis C opt-out screening systems (32) as well as no targeted screening approaches (33).

The decentralized diagnosis using the DBS technique is proposed as a very useful tool in our setting due to the high efficiency of the system, as it allows the study to be done in a single step (detection of antibodies and viral genome in the same sample), and also requires minimal infrastructure for sample collection, with no need for special transport conditions. Regarding its technical aspects, a high concordance has been reported with studies conducted by conventional methods, reaching a sensitivity of 98% regarding the study of the presence of the virus genome (34,35). Carty et al., in a meta-analysis, report a sensitivity of 95% for antibody detection and a specificity of 99%. For viral genome detection in the same sample, the sensitivity is 95% and the specificity is 97% (36).

The microelimination of HCV in penitentiary centers becomes highly significant due to the high prevalence of this infection in this environment. Therefore, progress should be made towards a national screening program in these centers, as it would be cost-effective and significantly contribute to achieving WHO objectives (37,38). The International Network on Health and Hepatitis in Substance Users-Prisons Network works towards this goal by promoting seven priority areas: changing political will, ensuring access to HCV diagnosis and testing, promoting optimal models of HCV care and treatment, improving surveillance and monitoring of the HCV care cascade, reducing stigma and addressing the social determinants of health inequalities, implementing HCV prevention and harm reduction programs, and advancing prison-based research (39). Another noteworthy fact is the significant utility of rapid, secure, and smooth communication with the teams responsible for patient treatment, as it reduces patient follow-up losses and facilitates their prompt treatment (40).

The results of this study highlight that until this process is established, efforts should focus on three fronts: increasing opportunistic screening in various settings, ensuring treatment of detected patients, and promoting disease prevention. Our study provides additional information emphasizing the need to intensify these efforts in vulnerable populations at high risk of infection with this virus: immigrants, prisoners, drug users, HIV co-infected patients, and psychiatric patients (41). The efficiency of different opportunistic screenings may vary depending on the social characteristics of each geographical area, and priority should be given to those that are most efficient and involve the participation of society and the healthcare system, as they are key elements for their success (42).

Until population screening is implemented in our setting, there is a significant difference in the efficiency of opportunistic screenings conducted in different settings, highlighting the great usefulness of implementing them among high-risk and socially vulnerable groups, along with the high performance of DBS testing, due to its ease of use, ability to reach populations with difficulty accessing the healthcare system, and low cost. Additionally, it is essential to establish a rapid and reliable system for transmitting information between microbiology services and the team responsible for patient treatment to ensure that the vast majority of patients diagnosed in these opportunistic screening processes are promptly and correctly treated (42).

Limitations

In this study, demographic data and other microbiological data of patients enrolled in the risk reduction program for vulnerable populations, who underwent DBS testing, are not available. These variables were not collected to maintain patient anonymity and encourage their participation in screening. Furthermore, our study only calculates the cost of screening in the different services using a single diagnostic method. In the future, it would be interesting to compare the price of this screening with other methods in order to extrapolate the result to other laboratories.

Conclusions

Focusing on opportunistic screening, the most cost-effective approach is carried out in the emergency department. Regarding decentralized screening, this study has demonstrated that it is highly effective in our setting, as it targets disadvantaged populations with a high prevalence of infection. Therefore, this screening should be promoted and evaluated to establish its efficacy elsewhere and to advance the detection of patients infected with HCV.

Acknowledgments

The DBS samples were analyzed at the Microbiology Service of the Dr. Balmis General University Hospital of Alicante with the collaboration of the Microbiology Platform of the Alicante Institute of Health and Biomedical Research (ISABIAL).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tgh.amegroups.com/article/view/10.21037/tgh-25-58/rc

Data Sharing Statement: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-25-58/dss

Peer Review File: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-25-58/prf

Funding: This study was funded by Roche Diagnostic (project 2023-0449 to J.C.R.), granted from Gilead Sciences in the “III Grants for Projects on Diagnosis and Referral of HIV Patients to the National Health System” (project GLD21/14908 to S.R.), and a Public PTA Grant by Ministry of Science and Innovation/State Research Agency (PTA2021-020215-I to M.P.V.).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tgh.amegroups.com/article/view/10.21037/tgh-25-58/coif). M.P.V. reports the salary is funded by a public PTA Grant (PTA2021-020215-I) from Ministry of Science and Innovation/State Research Agency. S.R. reports part of this study was supported by Gilead Sciences in the “III Grants for Projects on Diagnosis and Referral of HIV Patients to the National Health System”. J.C.R. reports part of this study was funded by project PI2023-157 from Roche Diagnostic. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by Institutional Ethics Committee for Research with Medicines of the Department of Health of Alicante-Dr. Balmis General University Hospital (Ref. CEIm: PI2023-157), individual consent for this retrospective analysis was waived due to the retrospective nature.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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