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Surveillance systems have evolved and continue to evolve in response to the changing HIV epidemic. An effective surveillance system is essential for health professionals, national governments and for an adequate national response to HIV. This supplement is devoted to the bio-behavior component of the Bulgarian HIV Surveillance System. In Bulgaria, epidemiological case-based data and CD4 counts have been collected since the first diagnosed HIV case in 1986. After the introduction of antiretroviral therapy (ART) in 1997, patient-based monitoring was started, including viral load. Later on, data on viral resistance was added to monitoring (2000), and in 2008 molecular HIV epidemiology was introduced. Bulgaria is a low-prevalence country for HIV, with the epidemic being concentrated among hard-to-reach populations. In this regard, the implementation of a National biological and behavior HIV surveillance system among key populations [injecting drug users (PWID), men having sex with men (MSM), sex workers, Roma men at higher risk and prisoners] in 2004 was a significant step in the development of HIV surveillance in Bulgaria. In order to monitor the effectiveness of the National Program interventions, program products recommended by UNAIDS for modeling of HIV epidemic were adopted in 2007 with the All these steps have helped the building of a comprehensive HIV epidemiological surveillance system, comprising the components of integrated biological and behavioral surveillance. A detailed description of the National HIV Surveillance System is provided in the article “Bulgarian HIV Surveillance System in the context of continuum of care 90-90-90 strategy.”

The article “National HIV biological and behavioral surveillance among hard-to-reach populations in Bulgaria (2004 -2016)” in three parts describes in detail the formative research, methodology and ethical issues of the National bio-behavioral survey carried out in the period 2004-2016 (NBBS-04-16). Within five cycles, a detailed assessment of HIV risk at the municipality level was made, with estimations of the size of hard-to-reach populations and mapping of 2,276 venues for contact with group representatives. Based on this assessment, nine cycles of  survey (NBBS-04-16) were conducted, and information from 27,210 participants was collected in the selected municipalities.

The second part of the article describes in details NBBS-04-16 methodology: cross-sectional surveys, with two-stage clusters and probability time-location sampling, fully  aligned with the WHO recommendations and the current best practices for bio-behavioral surveys in high-risk groups. The developed protocols, questionnaires, standard operating procedures, and other documents are a valuable manual not only for conducting HIV NBBS but also for other studies among hard-to-reach populations.

The third part is devoted to a very important issue - the ethics of vulnerable population’s research. It should be emphasized that NBBS-04-16 follows the guidelines of all international and national documents concerning research on human subjects. Strict compliance with these guidelines has enabled NBBS-04-16 to be successful amongst stigmatized and criminalized groups, contributing to their widespread recruitment and enrollment, as well as to avoiding the risks arising from the study itself and from legislations. NBBS-04-16 is the first major national study on the spread of HIV and sexually transmitted infections among key populations, which simultaneously provides a characterization of their risk behaviors. The results from NBBS-04-16 study were used to assess the effectiveness of the National HIV prevention and control programs in 2001-2007 and 2008-2015, as well as of the Global Fund grant. They served as a scientific basis for the development of National HIV Programs for 2008-2015 and 2017-2020, as well as for the reprogramming of their activities. In this supplement, the results from NBBS surveys carried among MSM and PWID in 2016 are presented. Results from previous NBBS-04-16 cycles are published elsewhere (1-5) The modeling of epidemic for assessment of the current situation and prognosis is an  important element of the National HIV Surveillance System. Estimations of the number of HIV-infected individuals and new HIV infections is essential for both antiretroviral therapy planning and for monitoring the cascade of continuum for care in the light of 90-90-90 strategy. In Bulgaria, the modeling of HIV epidemic began in 2007, following the recommendations and methodology of UNAIDS and ECDC. The article “Using case surveillance data for estimation and projection of HIV infection in PWID and MSM population by combining ECDC-HIV modeling tool and Spectrum-Estimation and projection package” explores modeling problems in terms of low HIV prevalence and concentrated epidemic. An original algorithm allowing to derive epidemiological parameters for assessment and prognosis of the epidemic among MSM and PWID is provided. This algorithm can be used in other subpopulations, as well.

In conclusion, the above shows that a robust HIV epidemiological surveillance system exists in Bulgaria that treats the infection in all its aspects. The implementation of this system, together with the successful interventions of the national programs, has contributed to keep the low HIV prevalence in the country.

Professor Hristo Taskov, MD, DSc.
National Center of Infectious and Parasitic Diseases, Sofia

                                                                                                                                                                                                  1. Varleva T, Georgieva V, Naseva E, Yakimova T, Zamfirova M, Taskov H, et al. Report of integrated bio-behavioral surveillance of HIV among prisoners, 2006-2012, Bulgaria. Problems of Infectious and Parasitic Diseases, Supliment. 2015;43:6-9
2. Varleva T, Raicheva T, Naseva E, Yakimova T, Georgieva V, Zamfirova M, et al. Report of integrated bio-behavioral surveillance of HIV among people who inject drugs, 2004-2012, Bulgaria. Problems of Infectious and Parasitic Diseases, Suplement. 2015;43:10-3
3. Varleva T, Kabakchieva E, Naseva E, Yakimova T, Georgieva V, Zamfirova M, et al. Report of integrated bio-behavioral surveillance of HIV among 18-25 years old males in Roma community, 2005-2012, Bulgaria. Problems of Infectious and Parasitic Diseases, Suplement. 2015;43:14-8
4. Varleva T, Boneva S, Naseva E, Yakimova T, Georgieva V, Zamfirova M, et al. Report of integrated bio-behavioral surveillance of hiv among males and females sex workers, 2004-2012, Bulgaria. Problems of Infectious and Parasitic Diseases, Suplement. 2015;43:14-8
5. Varleva T, Tsintsarski P, Naseva E, Yakimova T, Georgieva V, Zamfirova M, et al. Report of integrated bio-behavioral surveillance of hiv among men who have sex with men, 2006-2012, Bulgaria. Problems of Infectious and Parasitic Diseases, Suplement. 2015;43:14-8

  ABBREVIATONS

AIDS Acquired Immuno-Deficiency Syndrome
ART Anti-retroviral Therapy
BBS Bio-behaviour surveillance
CBBSU Central Bio-behaviour survey Unit
CCS Conventional Cluster Sampling
CDC Centers for Disease Control and Prevent
CDSD Communicable Diseases Surveillance Directorate
CI Confidence Interval
CIOMS Council for International Organizations of Medical Sciences
CSRE Commission of Scientific Research Ethics
ECDC European Centre of Diseases Control
EMCCDA European Monitoring Centre for Drugs and Drug Addiction
EMIS The European MSM Internet Survey
EQAS External Quality Assurance System
FPC Finite population correction
FSW Female Sex Worker
GARPR Global AIDS response report
GFATM Global Fund to Fight AIDS, Tuberculosis and Malaria
HBV Hepatitis B virus
HCT HIV Counseling and Testing
HCV Hepatitis C virus
HIS HIV incidence surveillance
HIV Human Immuno-deficiency Virus
HRG High Risk Group
HTRP Hard-to-reach- populations
IBBS Integrated Biological and Behavioural Surveillance
KP Key populations
LTHTS Low threshold HIV testing site (former Voluntary counselling and testing site)

 

   MMC Mobile medical cabinet
MoH Ministry of Health
MOS Measure of size
MSM Men who have Sex with Men
MSW Male sex worker
NBBS National Biological and Behavioral Surveillance
NCIPD National Center of Infectious and Parasitic Diseases Probl. Inf. Parasit. Dis. Vol. 46, 2018, 1
NGO Non-Governmental Organization
NHID national HIV identification number
NHP National program for prevention and control of HIV and STI
NHSS National HIV Surveillance System
NRCL of HIV National Reference Confirmatory Laboratory of HIV
NRLI National Reference Laboratory of Immunology
NSE Needles and syringes exchange
NSI National Statistical Institute
PLH People living with HIV
PPS Probability proportional to size
PWID People who inject drugs
RHI Regional Health Inspectorate
RMHR Roma men at higher risk
SEC Scientific Ethics Committee
SID Survey Identification number
SOP standard operating procedure
STI Sexual transmitted infection
SW Sex workers
TLS Time-location sampling
TPHA Treponema pallidum hemagglutination assay
UNGASS United Nation General Assembly Special Session
VCT Voluntary and Counselling and Testing
YRMHR Young Roma at higher risk

1. BULGARIA HIV SURVEILLANCE SYSTEM IN THE CONTEXT OF CONTINUUM OF CARE 90-90-90 STRATEGY

T. Varleva, M. Zamfirova, V. Georgieva, M. Nikolova, I. Alexiev and H. Taskov

ABSTRACT
The burden of HIV disease in Bulgaria is monitored by using a comprehensive surveillance system which includes case surveillance, incidence surveillance, and bio-behaviour surveillance. Data from this system are used for describing epidemics trends and risk behaviours associated with HIV acquisition, which are essential for effective public health interventions for HIV, to plan, implement, and evaluate public health policies and programs and monitoring of 90-90-90 strategy.
In this article we describe the elements of National HIV surveillance system.


2. NATIONAL HIV BIOLOGICAL AND BEHAVIORAL SURVELLANCE IN HARD-TO-REACH POPULATIONS IN BULGARIA (2004 -2016). PART 1: FORMATIVE RESEARCH

T. Varleva, H. Taskov, E. Naseva, V. Georgieva, E. Kabakchieva, P. Tsintsarski, T. Raycheva, S. Boneva and B. Petrunov

ABSTRACT
TBetween 2004 and 2016, in Bulgaria nine rounds of National bio-behavioural survey were conducted within the framework of the National programs for the prevention and control of HIV and STIs. Surveys were performed in five key populations: men who have sex with men (MSM), people who inject drugs (PWID), sex workers (SW), prisoners and young Roma at higher risk (YYRMHR). The total number of participant was 27,210.
All municipalities were included in the pre-assessment cycle. Based on criteria for HIV risk ten municipalities were selected for the first two rounds of the survey. Thereafter four formative assessments were performed in 19 municipalities in the country. The venues frequented by target population were listed and their number estimated. Total 2,276 venues were identified: 812 venues for PWID; 540 - for MSM; 817 for FSW and 229 for MSW. In 747 of the venues, mixing of the groups was associated with an increased risk of HIV infection. Municipalities with at least 800 high-risk group members were
selected for surveys.
In this article, we describe the outcomes of five formative research cycles. The methodology and ethical issues of the survey are described in Part 2 and 3 of the article.


3. NATIONAL HIV BIOLOGICAL AND BEHAVIOURAL SURVEY AMONG HARD-TO-REACH POPULATIONS IN BULGARIA (2004 -2016). PART 2: METHODOLOGY OF THE SURVEY

T. Varleva, H. Taskov, E. Naseva, V. Georgieva, E. Kabakchieva, P. Tsintsarski, T. Raycheva, S. Boneva and B. Petrunov

ABSTRACT
TBetween 2004 and 2016, in Bulgaria 9 rounds of bio-behavioural surveillance were conducted within the framework of the National Programs for the Prevention and Control of HIV and STIs. Surveys were performed in the major cities among five key populations: men who have sex with men (MSM), people who inject drugs (PWID), sex workers (SW), prisoners and young Roma at higher risk (YRMHR). The surveys were cross-sectional with a two-step complex cluster design with a time location sampling (TLS). The total number of participants in the NBBS-04-16 was 27,210 disaggregated by  studied groups as follows: MSM (4,725); PWID (8,626); SW (4,013); prisoners (4,557) and YRMHR (5,289). In this publication, we describe the survey methodology. The formative research and ethical issues are described in Part 1 and Part 3.


4. NATIONAL HIV BIOLOGICAL AND BEHAVIOURAL SURVEY AMONG HARD-TO-REACH POPULATIONS IN BULGARIA (2004 -2016). PART 3: ETHICAL ASPECTS OF THE SURVEY

T. Varleva, H. Taskov, E. Naseva, V. Georgieva, E. Kabakchieva, P. Tsintsarski, T. Raycheva, S. Boneva and B. Petrunov

ABSTRACT
Between 2004 and 2016, in Bulgaria nine rounds of bio-behavioral survey were conducted among hard-to-reach populations within the framework of the National Programs for Prevention and Control of HIV and STIs. The surveys were performed in ten of 28 municipalities were selected according their HIV risk. The total number of participant in the survey was 27,210 disaggregated by groups as follow: MSM (4,725); PWID (8,626); SW (4,013); prisoners (4,557) and Roma population at higher risk (5,289).
In Part 1 and 2 of the article, we described in detail the methodological aspect of survey. This article describes the ethical issues faced in all phases of the study. The results are published elsewhere.


5. INJECTION RISK BEHAVIORS AND HIV/STI PREVALENCE AMONG PEOPLE WHO INJECT DRUGS IN BULGARIA IN YEARS 2012 AND 2016: DATA FROM A CROSS-SECTIONAL BIO-BEHAVIOR STUDY

T. Varleva, Ts. Raycheva, E. Naseva, V. Georgieva, H. Taskov, B. Petrunov

ABSTRACT
Introduction: The aim of this study was to assess injecting and sexual risk behaviors and measure HIV and STI prevalence among people who inject drugs (PWID) in Bulgaria in 2016.
Methods: We conducted a cross-sectional study from April to September 2016 in five major cities of Bulgaria. The time location sampling was used to recruit PWID. Behavioral data were collected by interviewer-administered questionnaires. HIV and STIs status was assess by ELISA blood test.
Results: A total 421 PWID were enrolled in this study. The most commonly used illicit drugs injected in the last month were heroin (75.9%) and amphetamines (51.5%), followed by methadone hydrochloride (46.8%) and heroin&hetamines (39.8%). PWID were engaged in various high-risk injection practices in the last month including injection with used needle/syringe (50.9%), selling used needle (57.4%), using pre-filled syringes (34.0%)  or common equipment for sharing/preparation (46.3%). Casual sexual partner in last 12 months was declared by 64.0% of PWID and 57.6% had used condoms in last sexual intercourse. Almost one fifth of participants (17.5%) had had sex for money or gift in past 12 months and 90.3% had used condoms in this case. HIV prevalence rate for HIV, HVB, HCV and syphilis was respectively 1.6%, 9.1%, 65.5% and 0.8%.
Conclusions: This study confirms the observed trend of reduction of new HIV diagnoses among the PWID in Bulgaria started by 2012. Nevertheless, PWID continue to be one of the main subpopulation for transmission of HIV and HCV in Bulgaria because of persistent high risk of injection and sexual behaviours. Developing innovative strategies that can improve accessibility of current harm reduction services and incorporate prevention that is more
comprehensive are needed.


6. SEXUAL RISK BEHAVIORS AND HIV/STI PREVALENCE IN MEN WHO HAVE SEX WITH MEN IN THE BULGARIA IN 2016: DATA FROM A CROSS-SECTIONAL BIO-BEHAVIOR STUDY

T. Varleva, P. Tsintsarski, E. Naseva, V. Georgieva, H. Taskov and B. Petrunov

ABSTRACT
Introduction: The aim of this study was to assess sexual behavior and measure HIV and STI prevalence among men who have sex with men in Bulgaria in 2016.
Methods: We conducted a cross-sectional study from June to September 2016 in five major cities of Bulgaria. The time location sampling method was used to recruit MSM. Behavioral data were collected by interviewer-administered questionnaires. The blood tests were then carried out among MSM to assess their HIV and STIs status.
Results: A total 437 MSM were enrolled in this study, 44.4% of them in the capital, Sofia. Over the past month, 85.8% of MSM had had sexual intercourse with men and 31.9% of them had had sex with female partner. A sexual intercourse with a casual partner in last 12 months was reported by 85.8% of MSM and 75.2% of them had used condoms the last sexual intercourse. Having sex in exchange for money or gift in past 12 months was declared by 18.3% and buying of sex – by 6.3% of responders. An opportunity for a confidential HIV testing was reported by 95.8% of MSM. In the last 12 months, 52.4% of responders have been tested for HIV. The prevalence rate of HIV among MSM was 3.2% The prevalence rate of other STIs was as
follows: 3.1% for HBV, 4.2% for HCV and 6.3% for syphilis.
Conclusion: This study confirms that HIV prevalence among MSM is 46 times higher than the low risk general population (3.1%. vs 0.069%). Though our results reflect a relative good knowledge about HIV/AIDS infection, there is an increase of new HIV-positive cases and high-risk behavior, suggesting the need for more effective HIV prevention among MSM population in Bulgaria. Thus, there is a need to rethink HIV sensitization and prevention strategies targeting hidden and stigmatized populations such as MSM.


7. USING CASE SURVEILLANCE DATA FOR ESTIMATION AND PROJECTION OF HIV INFECTION IN PWID AND MSM POPULATION BY COMBINING ECDC-HIV MODELING TOOL AND SPECTRUM-ESTIMATION AND PROJECTION PACKAGE

H. Taskov and T. Varleva

ABSTRACT
Background
Bulgaria is low HIV prevalence country with concentrated epidemic. The National HIV surveillance system collect case-based data for MSM and PWID. The main objective of this study was to explore an appropriate method for estimation and projection of MSM and PWID case surveillance data.
Methods
We have used a combination of ECDC-HIV Modeling Tool with Spectrum-EPP to calculate the total number of persons infected with HIV, number of new HIV infections, HIV incidence and prevalence. For computing bio-behaviour surveys data for MSM and PWID Spectrum-EPP model was used.
Result
The present results show that both models led to similar results regarding the study parameters. Although the values obtained by the studied models differ, the estimations and projection curves show similar patterns.
Conclusions
We have demonstrated that the study approach is appropriate for analysis of MSM and PWID case-based data. It has several advantages. It applies a combination of established models that are widely used. Secondly, it allows parallel analyzes of data obtained from both case surveillance and other surveys e.g. population, sentinel, BBCs etc. Therefore, a more complete and accurate picture of the dynamics of the HIV epidemic can be obtained. Finally, the described approach uses models, which are constantly developing, free and accessible.


 Editor-in-Chief
Prof. Todor Kantardjiev, MD, PhD, DSc– NCIPD, Sofia, Bulgaria

Editorial Board:
Prof. Iva Christova, MD, DSc – NCIPD, Sofia, Bulgaria
Richard Anthony, PhD – RIVM, The Netherlands
Dale Barnard, PhD – Utah State University, USA
Roger Hewson, PhD – WHO Collaborating Centre for Virus Research & Reference, Porton Down, UK
Judith M. Hübschen – Luxembourg Institute of Health, Luxembourg
Emad Mohareb, PhD– U.S. Naval Medical Research Unit No.3, Egypt
Bruno Gottstein – Institute of Parasitology, University of Berne, Switzerland
Anton Andonov, PhD – Public Health agency, Canada
Anna Papa-Konidari, PhD- Aristotle University, Thessaloniki, Greece
Anna Erdei, DSc - Eötvös L. University, Budapest, Hungary
Lanfranco Fattorini – Instituto Superiore di Sanita, Italy
Hannes Stocklinger, PhD – Medical University, Vienna, Austria
Acad. Bogdan Petrunov, MD, DSc – NCIPD, Sofia, Bulgaria
Assoc. Prof. Iskra Rainova, MD, PhD – NCIPD, Sofia, Bulgaria
Assoc. Prof. Lubomira Nikolaeva-Glomb, MD, PhD – NCIPD, Sofia, Bulgaria

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