Skip to main content

Factors associated with testing for HIV and hepatitis C among behaviorally vulnerable men in Germany: a cross-sectional analysis upon enrollment into an observational cohort

Abstract

Background

HIV and hepatitis C virus (HCV) have shared routes of transmission among men who have sex with men (MSM). Routine testing facilitates early diagnosis and treatment, thereby preventing morbidity and onward transmission. We evaluated factors associated with HIV and HCV testing in a behaviorally vulnerable cohort of predominantly MSM.

Methods

From June 2018 through June 2019, the BRAHMS study enrolled adults at ten German outpatient clinics that serve gender and sexual minority populations. Participants completed behavioral questionnaires that captured prior experience with HIV and HCV testing. Multivariable robust Poisson regression was used to evaluate factors potentially associated with testing in the previous 6 months.

Results

Among 1017 participants with median age 33 (interquartile range 28–39) years, 1001 (98.4%) reported any lifetime history of HIV testing and 787 (77.4%) reported any HCV testing, including 16 (1.6%) known to be living with HCV. Testing within the last 6 months was reported by 921 (90.6%) and 513 (50.4%) for HIV and HCV, respectively. Recent HIV testing was more common among participants with higher education level and recent HCV testing. Recent HCV testing was more common among participants with non-cisgender identity, lifetime history of illicit drug use, hepatitis B immunity or infection, and recent HIV testing.

Conclusion

Prior testing for HIV was common in this cohort, but interventions are needed to improve HCV risk stratification and access to testing. HIV testing infrastructure can be successfully leveraged to support HCV testing, but differentiated preventive care delivery is needed for some vulnerable populations.

Introduction

For persons living with HIV unaware of their status, HIV testing is the critical first step toward diagnosis, initiation of antiretroviral therapy (ART), and further HIV care. Routine testing with prompt treatment after diagnosis drastically decreases HIV-related morbidity [1, 2], is one of the most cost-effective strategies for preventing onward HIV transmission [3, 4], and is key to curbing the HIV pandemic [5, 6].

Despite partial decreases in HIV incidence among men who have sex with men (MSM) in Germany and other Western European countries in recent years, substantial HIV transmission continues [7,8,9,10,11]. The European Centre for Disease Prevention and Control recommends annual testing of sexually active MSM for HIV and other sexually transmitted infections (STIs) with consideration for more frequent testing [12]. U.S. recommendations are similar [13] and add 3-monthly testing for MSM who are prescribed HIV pre-exposure prophylaxis (PrEP) [14]. Despite such recommendations, in 2016, about one-sixth of MSM living with HIV in six European countries were undiagnosed and one-third of diagnoses occurred late in the disease course, after CD4 had declined below 350 cells/μL [15]. In a survey from 13 European cities, almost two-thirds of MSM with undiagnosed HIV had evidence of infection within the past year, underscoring a need for more frequent testing to catch infection earlier in its course [16].

Due to shared routes of transmission, including sexual transmission via condomless anal intercourse, MSM who are behaviorally vulnerable to HIV are also at risk for hepatitis C virus (HCV) [17, 18]. Across Europe, an estimated 3.9 million individuals are living with chronic HCV [19] though many are unaware [20]. Outbreaks of sexually transmitted acute HCV have been documented among MSM living with HIV in Europe, the U.S., Australia, and Southeast Asia [21,22,23,24,25,26]. Coinfection with HIV and HCV worsens clinical outcomes as compared to either disease alone [27,28,29]. Direct-acting antiretrovirals are highly effective therapy for HCV but, as with ART for HIV, screening and diagnosis of HCV are prerequisite to therapy [30].

Data on factors associated with HCV testing are scarce, but factors associated with HIV testing have been evaluated in many settings. Studies of European MSM have identified factors associated with no or infrequent testing that included younger age, living in rural communities, lower reported number of sexual partners, less self-reported condomless anal intercourse, and low perceived HIV risk [31,32,33,34,35,36,37]. However, many of these prior studies were conducted before the expansive roll-out of PrEP in Germany and other European countries. In September 2017, the monthly cost of PrEP dropped about 90% to less than 50 Euros in Germany [38]. Since September 2019, PrEP has been available for only 5–10 Euros per month to behaviorally vulnerable individuals over 16 years old through statutory health insurance [39].

We evaluated factors associated with self-report of prior HIV and HCV testing upon enrollment into a cohort of predominantly MSM with sexual risk profiles suggesting vulnerability to HIV and HCV who were receiving care at ten German clinics in the era of widely available PrEP. Our objective was to determine demographic and behavioral characteristics that were associated with testing uptake in order to inform the design of targeted interventions to increase HIV and HCV testing among MSM.

Methods

Study population

The BRAHMS study was a prospective observational study that enrolled participants who were behaviorally vulnerable to HIV at ten German outpatient clinics and private practices that serve gender and sexual minority populations. Eligibility criteria included a non-reactive HIV test, age 18–55 years, and male sex (either at birth, chosen, or intersexual). Participants also needed, in the preceding 24 weeks, either documented diagnosis of an STI or self-reported condomless anal intercourse with 2 or more male partners known to be living with HIV or with unknown HIV status. Enrolled participants received risk reduction counseling and underwent testing for HIV and other STIs every 3 months for up to 12 months.

All participants provided written informed consent in either German or English. The study was approved by institutional review boards at all collaborating institutions.

Data collection

Data for these cross-sectional analyses were collected at the screening and enrollment visits, which occurred 2–4 weeks apart. The screening visit included a computer-assisted self-interview (CASI) questionnaire that collected detailed information regarding participant demographics, sexual behaviors, STIs, and substance use.

To evaluate previous HIV testing experience, participants were asked, “Have you ever been tested for HIV?” If the answer was affirmative, then they were asked, “When did you last have an HIV test?” To characterize prior testing for HCV, participants were asked, “Have you ever been tested for hepatitis C?” If the answer was affirmative and the test result was negative, then they were asked, “When was the last negative test for hepatitis C?” If a participant reported a prior positive test for HCV, then they were asked “Was the hepatitis C infection treated?” with answer choices that included “yes, successfully,” “yes, without success,” “no, the infection cleared without treatment,” and “no, and I still have it.”

All participants underwent point-of-care HIV testing using the Alere HIV Combo rapid test (Abbott GmbH & Co. KG, Wiesbaden, Germany). Centralized confirmatory testing was performed using the Alinity I HIV Ag/Ab Combo assay (Abbott GmbH & Co. KG, Wiesbaden, Germany) and Aptima HIV-1 Quant Dx assay (Hologic, Marlborough, MA, USA). Hepatitis B status was determined using the Alinity HBsAg Qualitative II assay (Abbott Ireland, Sligo, Ireland), Alinity Anti-HBs assay (Abbott Ireland, Sligo, Ireland), and Alinity Anti-HBc assay (Abbott GmbH & Co. KG, Wiesbaden, Germany). HCV testing was performed using the Aptima HCV Quant Dx assay (Hologic, Marlborough, MA, USA). All testing was performed according to manufacturer instructions.

Statistical analyses

All enrolled participants were included in these analyses. Comparisons between groups of interest were made using the Chi-squared test for categorical variables or Student’s t-test for continuous variables. In separate analyses for prior HIV testing and prior HCV testing, unadjusted and adjusted robust Poisson regression models were used to estimate risk ratios (RRs) and 95.0% confidence intervals (CIs) for pre-specified factors potentially associated with testing in the previous 6 months [40]. All enrolled participants were potentially at risk for HIV and were included in modeling of factors associated with recent HIV testing; only participants without a known diagnosis of HCV were included in modeling of factors associated with recent HCV testing since such testing would not be indicated for individuals known to be living with HCV. For each outcome, factors with p < 0.10 in unadjusted models were included in the adjusted multivariable model. All analyses were performed using Stata 15.0 (StataCorp LP, College Station, TX).

Results

Study population and lifetime history of testing

From June 2018 through June 2019, a total of 1017 participants enrolled with median age 33 (interquartile range 28–39) years. Participants were predominantly cisgender men (n = 1002, 98.5%), but also included five (0.5%) non-binary individuals, one (0.1%) transgender woman, one (0.1%) transgender man, one (0.1%) participant who identified as gender queer, and seven (0.7%) who did not report a gender identity at the screening or enrollment visit. Most participants self-identified as homosexual (n = 936, 92.0%). Undergraduate or higher education was reported by 535 (52.6%) and 624 (61.4%) were single or never married. HIV risk was self-reported as none/small by 438 (43.1%) participants, some by 357 (35.1%), and large/very large by 217 (21.3%) with 5 (0.5%) not responding to this question. Any lifetime history of illicit drug use was reported by 668 (65.7%) and binge drinking in the last year was reported by 345 (33.9%; Table 1).

Table 1 Study population characteristics, overall and by testing history

Of the 1017 participants enrolled, 1001 (98.4%) reported having been tested for HIV at least once in their lifetime, including 921 (90.6%) who reported HIV testing within the 6 months prior to enrollment (Fig. 1A).

Fig. 1
figure1

Interval since last reported HIV and HCV tests. At cohort enrollment, participants were asked if they had ever been tested for HIV and hepatitis C. If the answer was affirmative, they were asked when the last test was performed. Participants who were known to be living with hepatitis C were categorized separately because repeat testing is not indicated in this population

Any lifetime history of testing for HCV was reported by 787 (77.4%) participants, including 16 (1.6%) known to be living with HCV and 513 (50.4%) who reported HCV testing within the 6 months prior to enrollment (Fig. 1B).

Factors associated with recent HIV and HCV testing

After adjusting for potentially confounding factors, HIV testing within the 6 months prior to enrollment was more common among participants with advanced education and recent HCV testing (Table 2). Recent HCV testing was more common among participants with non-cisgender identity, lifetime history of illicit drug use, hepatitis B immunity or infection, and recent HIV testing (Table 2).

Table 2 Factors associated with testing for HIV and hepatitis C virus in the last 6 months

Discussion

Prior screening for HIV and HCV was common in this cohort of predominantly cisgender men with known risk factors for infection who were receiving care at specialized clinics. Remarkably, over half of participants had been screened for HIV within the month prior to enrollment, perhaps reflecting some sampling bias due to the targeted enrollment of participants with sexual risk behaviors for which current guidelines recommend frequent STI testing. Fewer than 5% of participants had not been screened for HIV within the year prior to enrollment in our study, while a less targeted online survey of German MSM found that 35% of respondents had never been tested for HIV and 62% had not been tested within the preceding 12 months [31]. Our study was conducted at German outpatient clinics and private practices that serve sexual and gender minorities and are likely to be particularly attuned to HIV risk assessment and screening needs of these key populations.

Non-cisgender identity was associated with significantly increased HCV testing uptake in our study, but no significant difference in HIV testing. Studies in other settings have found that HIV testing tends to be similar [41] or lower [42,43,44] among transgender, non-binary, and other non-cisgender people as compared to other key populations. Our finding of increased HCV testing in non-cisgender participants may reflect provider biases toward testing in this population, though inferences should be made with caution due to the small sample size of persons identifying as non-cisgender in our study and the small overall effect size associated with this factor.

There was a strong correlation between recent testing for HIV and HCV, which is appropriate given the potential for shared routes of transmission and guideline recommendations for HCV testing to follow HIV testing due to sexual risk [12]. The World Health Organization has set a target to diagnose 90% of people living with HCV by 2030 [45], but only about 20% of the estimated 71 million people worldwide who are living with chronic HCV had been diagnosed by 2015 [46]. Despite shared risk factors for acquisition, prior studies have shown that HCV testing tends to be less common than HIV testing among vulnerable populations [47, 48]. The testing gap appears to be smaller when HIV and HCV testing are offered together as one package [49, 50]. Leveraging existing screening infrastructure focused on HIV diagnosis could be helpful for facilitating earlier HCV diagnosis in some populations, but even in our study only about three-quarters of participants had ever been tested for HCV and about half of those at risk had been tested in the previous 6 months. Further efforts are need to ensure adequate linkage to care for people at risk for HCV, raise awareness, and scale-up testing services to include point-of-care options [51].

Nearly half of study participants perceived themselves to be at low or no risk for HIV despite entry criteria that required risk behaviors. Self-perception of HIV risk was not associated with increased recent HIV or HCV testing uptake. One meta-analysis found that HIV risk perception was associated with increased uptake of HIV testing across studies mostly conducted in Africa and the Americas [52]. Among the few European studies on this topic, one conducted in African migrant communities in London observed a significant association between HIV risk perception and testing uptake among women but not men [53], while one in Paris found an association among men but not women [54]. A German study observed a correlation between perceived risk and HIV testing in MSM [35]. Conflicting data on this topic underscore the variability of risk perception across communities, the ambiguity of measuring risk perception across studies, and likely multifactorial motivations for testing. Our findings suggest that, among German MSM, there is a need for outreach and extension of prevention interventions outside the clinical setting to encourage testing of individuals who do not self-identify their risk.

Most of the data in these analyses were assessed by self-report and could be susceptible to social desirability bias, though collection of data by CASI would be expected to reduce this bias. Data were collected cross-sectionally at enrollment into a study that included routine HIV and HCV screening, so analyses were based primarily on historic experiences and temporal associations could not be evaluated. The study was conducted at German outpatient clinics and private practices serving sexual and gender minorities; our findings may not be generalizable to other populations or settings.

Conclusion

Despite high overall uptake of HIV and HCV testing among at-risk German MSM, there is room for improvement particularly in uptake of HCV testing. Lessons learned from the successful deployment of frequent HIV screening to vulnerable sexual and gender minority populations in Germany can be applied to testing for HCV and could inform differentiated preventive care delivery to other populations.

Availability of data and materials

The Henry M. Jackson Foundation for the Advancement of Military Medicine (HJF) and the Water Reed Army Institute of Research (WRAIR) are committed to safeguarding the privacy of research participants. Distribution of data will require compliance with all applicable regulatory and ethical processes, including establishment and approval of an appropriate data-sharing agreement. To request a minimal data set, please contact the data coordinating and analysis center (DCAC) at PubRequest@hivresearch.org and indicate the BRAHMS/RV500 study along with the name of the manuscript.

Abbreviations

ART:

Antiretroviral therapy

CASI:

Computer-assisted self-interview

CI:

Confidence intervals

HCV:

Hepatitis C virus

HIV:

Human immunodeficiency virus

MSM:

Men who have sex with men

PrEP:

Pre-exposure prophylaxis

RR:

Risk ratio

STIs:

Sexually transmitted infections

References

  1. 1.

    TEMPRANO ANRS Study Group, Danel C, Moh R, Gabillard D, Badje A, Le Carrou J, et al. A trial of early antiretrovirals and isoniazid preventive therapy in Africa. N Engl J Med. 2015;373(9):808–22.

    Article  CAS  Google Scholar 

  2. 2.

    INSIGHT START Study Group, Lundgren JD, Babiker AG, Gordin F, Emery S, Grund B, et al. Initiation of antiretroviral therapy in early asymptomatic HIV infection. N Engl J Med. 2015;373(9):795–807.

    Article  CAS  Google Scholar 

  3. 3.

    Jordan MR, Bennett DE, Wainberg MA, Havlir D, Hammer S, Yang C, et al. Update on World Health Organization HIV drug resistance prevention and assessment strategy: 2004–2011. Clin Infect Dis. 2012;54(Suppl 4):S245–9.

    PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Sullivan PS, Carballo-Dieguez A, Coates T, Goodreau SM, McGowan I, Sanders EJ, et al. Successes and challenges of HIV prevention in men who have sex with men. Lancet. 2012;380(9839):388–99.

    PubMed  PubMed Central  Article  Google Scholar 

  5. 5.

    Beyrer C, Baral SD, van Griensven F, Goodreau SM, Chariyalertsak S, Wirtz AL, et al. Global epidemiology of HIV infection in men who have sex with men. Lancet. 2012;380(9839):367–77.

    PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    UNAIDS. AIDS by the Numbers 2015. Geneva: Joint United Nations Programme on HIV/AIDS; 2015. https://www.unaids.org/sites/default/files/media_asset/AIDS_by_the_numbers_2015_en.pdf

  7. 7.

    Punyacharoensin N, Edmunds WJ, De Angelis D, Delpech V, Hart G, Elford J, et al. Modelling the HIV epidemic among MSM in the United Kingdom: quantifying the contributions to HIV transmission to better inform prevention initiatives. AIDS. 2015;29(3):339–49.

    PubMed  Article  PubMed Central  Google Scholar 

  8. 8.

    van Sighem A, Vidondo B, Glass TR, Bucher HC, Vernazza P, Gebhardt M, et al. Resurgence of HIV infection among men who have sex with men in Switzerland: mathematical modelling study. PLoS ONE. 2012;7(9):e44819.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  9. 9.

    Supervie V, Ndawinz JD, Lodi S, Costagliola D. The undiagnosed HIV epidemic in France and its implications for HIV screening strategies. AIDS. 2014;28(12):1797–804.

    PubMed  Article  PubMed Central  Google Scholar 

  10. 10.

    van der Heiden M, Marcus U, Kollan C, Schmidt D, Gunsenheimer-Bartmeyer B, Bremer V. Schätzung der Zahl der HIV-Neuinfektionen und der Gesamtzahl von Menschen mit HIV in Deutschland, Stand Ende 2019. Epidemiol Bull. 2020;48:3–16.

    Google Scholar 

  11. 11.

    European Centre for Disease Prevention and Control/WHO Regional Office for Europe. HIV/AIDS surveillance in Europe 2020–2019 data. Stockholm: ECDC; 2020.

    Google Scholar 

  12. 12.

    European Centre for Disease Prevention and Control. ECDC guidance: prevention and control. HIV and STI prevention among men who have sex with men. Stockholm: ECDC; 2015.

    Google Scholar 

  13. 13.

    DiNenno EA, Prejean J, Irwin K, Delaney KP, Bowles K, Martin T, et al. Recommendations for HIV screening of gay, bisexual, and other men who have sex with men—United States, 2017. MMWR Morb Mortal Wkly Rep. 2017;66(31):830–2.

    PubMed  PubMed Central  Article  Google Scholar 

  14. 14.

    Centers for Disease Control. US Public Health Service: preexposure prophylaxis for the prevention of HIV infection in the United States—2017 update: a clinical practice guideline. 2018. https://www.cdc.gov/hiv/pdf/risk/prep/cdc-hiv-prep-guidelines-2017.pdf. Updated 4 June 2020.

  15. 15.

    Brown AE, Attawell K, Hales D, Rice BD, Pharris A, Supervie V, et al. Monitoring the HIV continuum of care in key populations across Europe and Central Asia. HIV Med. 2018;19:431–9.

    Article  Google Scholar 

  16. 16.

    Marcus U, Nostlinger C, Rosinska M, Sherriff N, Gios L, Dias SF, et al. Behavioural and demographic correlates of undiagnosed HIV infection in a MSM sample recruited in 13 European cities. BMC Infect Dis. 2018;18(1):368.

    PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    European Centre for Disease Prevention and Control. Hepatitis B and C epidemiology in selected population groups in the EU/EEA. Stockholm: European Centre for Disease Prevention and Control; 2018.

    Google Scholar 

  18. 18.

    Hoornenborg E, Achterbergh RCA, Schim van der Loeff MF, Davidovich U, Hogewoning A, de Vries HJC, et al. MSM starting preexposure prophylaxis are at risk of hepatitis C virus infection. AIDS. 2017;31(11):1603–10.

    PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Hofstraat SHI, Falla AM, Duffell EF, Hahne SJM, Amato-Gauci AJ, Veldhuijzen IK, et al. Current prevalence of chronic hepatitis B and C virus infection in the general population, blood donors and pregnant women in the EU/EEA: a systematic review. Epidemiol Infect. 2017;145(14):2873–85.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    European Centre for Disease Prevention and Control. Hepatitis B and C testing activities, needs and priorities in the EU/EEA. Stockholm: European Centre for Disease Prevention and Control; 2017.

    Google Scholar 

  21. 21.

    Urbanus AT, van de Laar TJ, Stolte IG, Schinkel J, Heijman T, Coutinho RA, et al. Hepatitis C virus infections among HIV-infected men who have sex with men: an expanding epidemic. AIDS. 2009;23(12):F1-7.

    PubMed  Article  PubMed Central  Google Scholar 

  22. 22.

    van de Laar T, Pybus O, Bruisten S, Brown D, Nelson M, Bhagani S, et al. Evidence of a large, international network of HCV transmission in HIV-positive men who have sex with men. Gastroenterology. 2009;136(5):1609–17.

    PubMed  Article  PubMed Central  Google Scholar 

  23. 23.

    Wansom T, Pinyakorn S, Kolsteeg CJ, Kroon ED, Sacdalan CP, Chomchey N, et al. Group sex and methamphetamine use fuel an explosive epidemic of Hepatitis C among HIV-infected men who have sex with men in Bangkok, Thailand. J Acquir Immune Defic Syndr. 2020;84:331–5.

    PubMed  Article  PubMed Central  Google Scholar 

  24. 24.

    Ingiliz P, Martin TC, Rodger A, Stellbrink HJ, Mauss S, Boesecke C, et al. HCV reinfection incidence and spontaneous clearance rates in HIV-positive men who have sex with men in Western Europe. J Hepatol. 2017;66(2):282–7.

    PubMed  Article  PubMed Central  Google Scholar 

  25. 25.

    Martin NK, Jansen K, An der Heiden M, Boesecke C, Boyd A, Schewe K, et al. Eliminating hepatitis C virus among human immunodeficiency virus-infected men who have sex with men in Berlin: a modeling analysis. J Infect Dis. 2019;220(10):1635–44.

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Ingiliz P, Wehmeyer MH, Boesecke C, Schulze Zur Wiesch J, Schewe K, Lutz T, et al. Reinfection with the hepatitis C virus in men who have sex with men after successful treatment with direct-acting antivirals in Germany: current incidence rates, compared with rates during the interferon era. Clin Infect Dis. 2020;71(5):1248–54.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    Crowell TA, Berry SA, Fleishman JA, LaRue RW, Korthuis PT, Nijhawan AE, et al. Impact of hepatitis coinfection on healthcare utilization among persons living with HIV. J Acquir Immune Defic Syndr. 2015;68(4):425–31.

    PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Crowell TA, Gebo KA, Balagopal A, Fleishman JA, Agwu AL, Berry SA, et al. Impact of hepatitis coinfection on hospitalization rates and causes in a multicenter cohort of persons living with HIV. J Acquir Immune Defic Syndr. 2014;65(4):429–37.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Osibogun O, Ogunmoroti O, Michos ED, Spatz ES, Olubajo B, Nasir K, et al. HIV/HCV coinfection and the risk of cardiovascular disease: a meta-analysis. J Viral Hepat. 2017;24(11):998–1004.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30.

    Scott N, Doyle JS, Wilson DP, Wade A, Howell J, Pedrana A, et al. Reaching hepatitis C virus elimination targets requires health system interventions to enhance the care cascade. Int J Drug Policy. 2017;47:107–16.

    PubMed  Article  PubMed Central  Google Scholar 

  31. 31.

    Marcus U, Gassowski M, Kruspe M, Drewes J. Recency and frequency of HIV testing among men who have sex with men in Germany and socio-demographic factors associated with testing behaviour. BMC Public Health. 2015;15:727.

    PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    den Daas C, Doppen M, Schmidt AJ, Op de Coul E. Determinants of never having tested for HIV among MSM in the Netherlands. BMJ Open. 2016;6(1):e009480.

    Article  Google Scholar 

  33. 33.

    Fernandez-Davila P, Folch C, Ferrer L, Soriano R, Diez M, Casabona J. Who are the men who have sex with men in Spain that have never been tested for HIV? HIV Med. 2013;14(Suppl 3):44–8.

    PubMed  Article  PubMed Central  Google Scholar 

  34. 34.

    Carvalho C, Fuertes R, Lucas R, Martins A, Campos MJ, Mendao L, et al. HIV testing among Portuguese men who have sex with men—results from the European MSM Internet Survey (EMIS). HIV Med. 2013;14(Suppl 3):15–8.

    PubMed  Article  PubMed Central  Google Scholar 

  35. 35.

    Marcus U, Gassowski M, Drewes J. HIV risk perception and testing behaviours among men having sex with men (MSM) reporting potential transmission risks in the previous 12 months from a large online sample of MSM living in Germany. BMC Public Health. 2016;16(1):1111.

    PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    Mackellar DA, Hou SI, Whalen CC, Samuelsen K, Sanchez T, Smith A, et al. Reasons for not HIV testing, testing intentions, and potential use of an over-the-counter rapid HIV test in an internet sample of men who have sex with men who have never tested for HIV. Sex Transm Dis. 2011;38(5):419–28.

    PubMed  Article  PubMed Central  Google Scholar 

  37. 37.

    Kellerman SE, Lehman JS, Lansky A, Stevens MR, Hecht FM, Bindman AB, et al. HIV testing within at-risk populations in the United States and the reasons for seeking or avoiding HIV testing. J Acquir Immune Defic Syndr. 2002;31(2):202–10.

    PubMed  Article  PubMed Central  Google Scholar 

  38. 38.

    van de Vijver D, Richter AK, Boucher CAB, Gunsenheimer-Bartmeyer B, Kollan C, Nichols BE, et al. Cost-effectiveness and budget effect of pre-exposure prophylaxis for HIV-1 prevention in Germany from 2018 to 2058. Euro Surveill. 2019;24(7):1800398.

    PubMed Central  Google Scholar 

  39. 39.

    AIDS Action Europe. Free access to PrEP in Germany 2019. https://www.aidsactioneurope.org/en/news/free-access-prep-germany-2019.

  40. 40.

    Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol. 2004;159(7):702–6.

    PubMed  Article  PubMed Central  Google Scholar 

  41. 41.

    Poteat T, Ackerman B, Diouf D, Ceesay N, Mothopeng T, Odette KZ, et al. HIV prevalence and behavioral and psychosocial factors among transgender women and cisgender men who have sex with men in 8 African countries: a cross-sectional analysis. PLoS Med. 2017;14(11):e1002422.

    PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Habarta N, Wang G, Mulatu MS, Larish N. HIV testing by transgender status at Centers for Disease Control and Prevention-funded sites in the United States, Puerto Rico, and US Virgin Islands, 2009–2011. Am J Public Health. 2015;105(9):1917–25.

    PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Pitasi MA, Oraka E, Clark H, Town M, DiNenno EA. HIV testing among transgender women and men—27 states and Guam, 2014–2015. MMWR Morb Mortal Wkly Rep. 2017;66(33):883–7.

    PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Stephenson R, Riley E, Rogers E, Suarez N, Metheny N, Senda J, et al. The sexual health of transgender men: a scoping review. J Sex Res. 2017;54(4–5):424–45.

    PubMed  Article  PubMed Central  Google Scholar 

  45. 45.

    World Health Organization. Global health sector strategy on viral hepatitis, 2016–2021: towards ending viral hepatitis. Geneva: World Health Organization; 2016.

    Google Scholar 

  46. 46.

    World Health Organization. Global hepatitis report, 2017. Geneva: World Health Organization; 2017.

    Google Scholar 

  47. 47.

    Tunnage J, Yates A, Nwoga C, Sing’oei V, Owuoth J, Polyak CS, et al. Hepatitis and tuberculosis testing are much less common than HIV testing among adults in Kisumu, Kenya: results from a cross-sectional assessment. BMC Public Health. 2021;21(1):1143.

    PubMed  PubMed Central  Article  Google Scholar 

  48. 48.

    Fitzpatrick T, Pan SW, Tang W, Guo W, Tucker JD. HBV and HCV test uptake and correlates among men who have sex with men in China: a nationwide cross-sectional online survey. Sex Transm Infect. 2018;94(7):502–7.

    PubMed  Article  PubMed Central  Google Scholar 

  49. 49.

    Bartholomew TS, Tookes HE, Serota DP, Behrends CN, Forrest DW, Feaster DJ. Impact of routine opt-out HIV/HCV screening on testing uptake at a syringe services program: an interrupted time series analysis. Int J Drug Policy. 2020;84:102875.

    PubMed  Article  PubMed Central  Google Scholar 

  50. 50.

    Merchant RC, DeLong AK, Liu T, Baird JR. Factors influencing uptake of rapid HIV and hepatitis C screening among drug misusing adult emergency department patients: implications for future HIV/HCV screening interventions. AIDS Behav. 2015;19(11):2025–35.

    PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Lazarus JV, Picchio C, Dillon JF, Rockstroh JK, Weis N, Buti M. Too many people with viral hepatitis are diagnosed late—with dire consequences. Nat Rev Gastroenterol Hepatol. 2019;16(8):451–2.

    PubMed  Article  PubMed Central  Google Scholar 

  52. 52.

    Evangeli M, Pady K, Wroe AL. Which psychological factors are related to HIV testing? A quantitative systematic review of global studies. AIDS Behav. 2016;20(4):880–918.

    PubMed  Article  PubMed Central  Google Scholar 

  53. 53.

    Fenton KA, Chinouya M, Davidson O, Copas A, team Ms. HIV testing and high risk sexual behaviour among London’s migrant African communities: a participatory research study. Sex Transm Infect. 2002;78(4):241–5.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Massari V, Lapostolle A, Cadot E, Parizot I, Dray-Spira R, Chauvin P. Gender, socio-economic status, migration origin and neighbourhood of residence are barriers to HIV testing in the Paris metropolitan area. AIDS Care. 2011;23(12):1609–18.

    PubMed  Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to all study participants. We thank the BRAHMS study team for executing this important work. This study was supported by the U.S. Military HIV Research Program (MHRP) under cooperative agreements between the U.S. Army and the Henry M. Jackson Foundation for the Advancement of Military Medicine (W81XWH-11-2-0174; W81XWH-18-2-0040) with support from the US Army Medical Research and Development Command (W81XWH-18-C-0077), Pharmaceutical Systems PMO, HIV Vaccine Program, the Bundesministerium für Gesundheit (BMG), and the Division of AIDS (DAIDS), National Institutes of Health (NIH). We thank Hologic and Seegene for providing laboratory diagnostic support to the study.

Disclaimer

The views, opinions and/or findings contained in this report are those of the authors and should not be construed as an official Department of the Army position, policy or decision unless so designated by other documentation.

Prior presentation

This work was presented, in part, at the 23rd International AIDS Conference, 6–10 July 2020.

Funding

This study was supported by the U.S. Military HIV Research Program (MHRP) under cooperative agreements between the U.S. Army and the Henry M. Jackson Foundation for the Advancement of Military Medicine (W81XWH-11-2-0174; W81XWH-18-2-0040) with support from the US Army Medical Research and Development Command (W81XWH-18-C-0077), Pharmaceutical Systems PMO, HIV Vaccine Program, the Bundesministerium für Gesundheit (BMG), and the Division of AIDS (DAIDS), National Institutes of Health (NIH). We thank Hologic and Seegene for providing laboratory diagnostic support to the study.

Author information

Affiliations

Authors

Consortia

Contributions

TAC contributed to study design and implementation, conceptualized these analyses, conducted the analyses, and authored the first draft of the manuscript. HQ provided project management support during study implementation, conducted a review of relevant literature, and contributed to the drafting of key sections of the manuscript. CT coordinated laboratory testing for the study and assisted with interpretation of laboratory results. CL, CB, AS, JH, SE, MB, CDS, SS, CC, NB, and HJ oversaw the collection of clinical data as principal investigators at participating study sites and assisted with interpretation of data. MLR and NLM conceptualized the study, contributed to study design and implementation, and assisted with the interpretation of results. KJ contributed to study design and implementation, assisted in the design of these analyses, and assisted with the interpretation of results. HS conceptualized the study, contributed to the design of these analyses, assisted in the interpretation of results, and provided general oversight of the study and these analyses. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Trevor A. Crowell.

Ethics declarations

Ethics approval and consent to participate

All participants provided written informed consent in either German or English. The study was approved by institutional review boards at all collaborating institutions. In the conduct of research where humans are the subjects, the investigators adhered to the policies regarding the protection of human subjects as prescribed by Code of Federal Regulations (CFR) Title 45, Volume 1, Part 46; Title 32, Chapter 1, Part 219; and Title 21, Chapter 1, Part 50 (Protection of Human Subjects). The investigators have also adhered to the policies for protection of human subjects as prescribed in AR 70-25.

Consent for publication

Not applicable.

Competing interests

CDS reports grants and/or personal fees from AbbVie, Aperion, Eli Lilly, Formycon, Gilead Sciences, MSD, Janssen-Cilag, and GSK/ViiV Healthcare outside the submitted work. The other authors report no potential conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Crowell, T.A., Qian, H., Tiemann, C. et al. Factors associated with testing for HIV and hepatitis C among behaviorally vulnerable men in Germany: a cross-sectional analysis upon enrollment into an observational cohort. AIDS Res Ther 18, 52 (2021). https://doi.org/10.1186/s12981-021-00378-4

Download citation

Keywords

  • Screening practices
  • Sexual and gender minorities
  • Europe
  • Voluntary counseling and testing
  • Human immunodeficiency virus
  • Hepatitis C virus