Country-wide HIV incidence study complementing HIV surveillance in Germany.
ABSTRACT Serological methods exist that allow differentiating between recent and long-standing infections in persons infected with HIV. During a pilot study in Berlin between 2005 and 2007 methodologies have been evaluated. In a cross-sectional study blood samples, demographic, laboratory, clinical and behavioural data based on a KABP survey were collected from patients with newly diagnosed HIV infections. The BED-CEIA was used to determine recency of infection. Recent HIV infections contributed 54% (CI [95%]: 45; 64) in MSM and 16% (CI [95%]: 0; 39) in patients with other transmission risks (p=0.041). Proportions of recent infections were significantly higher in MSM <or=30 years (p=0.019). The mean age was 33.9 (median 34 years) in recent compared with 38.6 years (median: 38 years) in long-standing infections (p=0.011). High-risk behaviour indicated through very low condom use in recently HIV infected MSM could be identified. The results of the pilot study support expectations that the modified application of the method may contribute to improving HIV prevention efforts in Germany. On this basis the Robert Koch Institute implemented a countrywide HIV incidence study to complement HIV surveillance in early 2008. The study is funded by the German Ministry of Health. Data on recent HIV infections and current HIV transmission risks are collected. Design, methods and impact are described in detail. .
[show abstract] [hide abstract]
ABSTRACT: An HIV outbreak among Finnish injecting drug users (IDUs) occurred in 1998. By the end of 2005, 282 IDUs were in-fected, most of them by recombinant virus CRF01_AE of HIV. After a rapid spread, the outbreak subsided, and the prevalence of HIV among IDUs remained low (<2%). The purpose of the study was to describe the outbreak in order to recognise factors that have influenced the spread and restriction of the outbreak, and thus to find tools for HIV preven-tion. Data on Finnish IDUs newly diagnosed HIV-positive between 1998 and 2005 was collected through interviews and patient documents. Study I compared markers of disease progression between 93 Finnish IDUs and 63 Dutch IDUs. In study II, geographical spread of the HIV outbreak was examined and compared with the spatial distribution of employed males. In study III, risk behaviour data from interviews of 89 HIV-positive and 207 HIV-negative IDUs was linked, and prevalence and risk factors for unprotected sex were evaluated. In study IV, data on 238 newly diagnosed IDUs was combined with data on 675 sexually transmitted HIV cases, and risk factors for late HIV diagnosis (CD4 cell count <200/µL, or AIDS at HIV diagnosis) were analysed. Finnish IDUs infected with CRF01_AE exhibited higher viral loads than did Amsterdam IDUs infected with subtype B, but there was no difference in CD4 development. The Finnish IDU outbreak spread and was restricted socially in a marginalised IDU population and geographically in areas characterised by low proportions of employed males. Up to 40% of the cases in the two clusters outside the city centre had no contact with the centre, where needle exchange services were available since 1997. Up to 63% of HIV-positive and 80% of HIV-negative sexually active IDUs reported inconsistent condom use, which was associated with steady relationships and recent inpatient addiction care. Com-pared to other transmission groups, HIV-positive IDUs were diagnosed earlier in their infection. The proportion of late diagnosed HIV cases in all transmission groups was 23%, but was only 6% among IDUs diagnosed during the first four years of the epidemic. The high viral load in early HIV infection may have contributed to the rapid spread of recombinant virus in the Finnish outbreak. The outbreak was restricted to a marginalised IDU population, and limited spatially to local pockets of pov-erty. To prevent HIV among IDUs, these pockets should be recognised and reached early through outreach work and the distribution of needle exchange and other prevention activities. To prevent the sexual transmission of HIV among IDUs, prevention programmes should be combined with addiction care services and targeted at every IDU. The early detection of the outbreak and early implementation of needle exchange programmes likely played a crucial role in re-versing the IDU outbreak. Pistoshuumeiden käyttäjien HIV-epidemia todettiin pääkaupunkiseudulla vuonna 1998. Epidemia levisi aluksi nopeasti, mutta myös rajoittui muutamassa vuodessa. Tutkimuksen tavoitteena oli tunnistaa tekijöitä, jotka vaikuttivat epidemian leviämiseen ja rajoittumiseen, ja siten löytää keinoja HIV-epidemian ennaltaehkäisyyn. Aineisto käsitti 238 HIV-tartunnan saanutta pistoshuumeidenkäyttäjää, joiden tietoja verrattiin hollantilaisista HIV-positiivisista ja suomalaisista HIV-negatiivisista huumeidenkäyttäjistä kerättyihin tietoihin, miesten työllisyyslukujen alueelliseen jakaumaan ja pääkaupunkiseudun seksivälitteisiin HIV-tartuntoihin. HIV-epidemia levisi syrjäytyneiden pistoshuumeiden käyttäjien keskuudessa. Kaikki Helsingin keskustan ulkopuolella sijaitsevat huumeidenkäyttäjien rypäät sijaitsivat alueilla, joissa miesten työllisyysluvut olivat alle 70%. Muissa tutkimuksissa on osoitettu puhtaiden pistosvälineiden saatavuuden estävän HIV:n leviämistä. Pääkaupunkiseudun epidemiassa 40% keskustan ulkopuolella asuvista huumeidenkäyttäjistä jäi pistosvälineiden vaihdon ja terveysneuvonnan ulkopuolelle, koska heillä ei ollut yhteyksiä keskustaan, jossa terveysneuvonta ja pistosvälineiden vaihto aloitettin juuri ennen epidemiaa. Suomessa levinnyt viruksen alatyyppi (CRF01_AEfin) edesauttoi epidemian leviämistä, sillä suomalaisilla huumeidenkäyttäjillä todettiin korkeampia veren viruspitoisuuksia kuin hollantilaisilla B-alatyypin viruksella infektoituneilla huumeidenkäyttäjillä. Veren korkea viruspitoisuus lisää tartuttavuutta. HIV ei levinnyt ydinjoukon ulkopuolelle eikä uusille alueille. Epidemian rajoittumiseen vaikutti todennäköisesti sen varhainen toteaminen terveysneuvonnan kehittymisen ohella. Huumeidenkäyttäjien HIV-tartunnoista 1998-2001 vain 6% todettiin myöhäisessä vaiheessa (veren CD4-solut alle 200/µL tai AIDS-vaiheessa), kun kaikista pääkaupunkiseudun HIV-tartunnoista 23% todettiin myöhään. Yli puolet huumeidenkäyttäjien tartunnoista todettiin vankiloissa, päihdehoidossa tai terveysneuvontapisteissä; paikoissa joissa HIV-testiä tarjotaan aktiivisesti. HIV voi yhä levitä huumeiden käyttäjien keskuudessa joko pistämisen tai seksin välityksellä. Suojaamaton seksi on yleistä sekä HIV-positiivisten että HIV-negatiivisten huumeiden käyttäjien keskuudessa, etenkin vakituisissa suhteissa ja hiljattain päihdehoitoa tarvinneilla. Seksuaaliterveyden neuvontaa tulisi tarjota kaikille huumeidenkäyttäjille ja heidän seksikumppaneilleen. Terveysneuvonnan alueellinen hajauttaminen ja kohdistettu etsivä työ ovat avainasemassa huumeidenkäyttäjien HIV-tartuntojen toteamiseksi varhain ja epidemioiden ehkäisemiseksi.
EUROSURVEILLANCE Vol. 13 · Issues 7–9 · Jul–Sep 2008 · www.eurosurveillance.org
Cou ntry-wi de HiV i nCi de nCe stu dy Com ple m e nti ng HiV
su rVe i llanCe i n ge rmany
J Bätzing-Feigenbaum (firstname.lastname@example.org)1, S Loschen2, S Gohlke-Micknis1, R Zimmermann1, A Herrmann1,
O Kamga Wambo3, C Kücherer2, O Hamouda1
1. HIV/AIDS and STI Unit, Department for Infectious Disease Epidemiology, Robert Koch-Institute, Berlin, Germany
2. HIV Variability and Molecular Epidemiology, Robert Koch-Institute, Berlin, Germany
3. Postgraduate Training Applied Epidemiology (PAE), Department for Infectious Disease Epidemiology, Robert Koch-Institute,
Serological methods exist that allow differentiating between recent
and long-standing infections in persons infected with HIV. During
a pilot study in Berlin between 2005 and 2007 methodologies
have been evaluated. In a cross-sectional study blood samples,
demographic, laboratory, clinical and behavioural data based on
a KABP survey were collected from patients with newly diagnosed
HIV infections. The BED-CEIA was used to determine recency of
infection. Recent HIV infections contributed 54% (CI [95%]: 45;
64) in MSM and 16% (CI [95%]: 0; 39) in patients with other
transmission risks (p=0.041). Proportions of recent infections were
significantly higher in MSM ≤30 years (p=0.019). The mean age
was 33.9 (median 34 years) in recent compared with 38.6 years
(median: 38 years) in long-standing infections (p=0.011). High-risk
behaviour indicated through very low condom use in recently HIV
infected MSM could be identified. The results of the pilot study
support expectations that the modified application of the method
may contribute to improving HIV prevention efforts in Germany. On
this basis the Robert Koch Institute implemented a countrywide HIV
incidence study to complement HIV surveillance in early 2008. The
study is funded by the German Ministry of Health. Data on recent
HIV infections and current HIV transmission risks are collected.
Design, methods and impact are described in detail.
In Germany newly diagnosed human immunodeficiency virus
(HIV) infections reached a peak of 2,360 cases in 1993. The
number of cases reported to the Robert Koch Institute (RKI), the
institution responsible for the national surveillance of infectious
diseases in Germany, dropped continuously in the second half of the
1990s, reaching the lowest level so far in 2001 with 1,443 cases.
However, since 2001 this trend has been reversed and annual case
reports increased to more than 2,750 cases in 2007 [1; Figure
1]. There are several possible explanations for these changes: an
increase in HIV transmission (“true” incident infections); improved
(earlier) case detection and reporting following the implementation
of the “Protection against Infection Act” (Infektionsschutzgesetz
- IfSG) in 2001; an increased number of HIV tests performed;
changing attitudes towards HIV testing; and more widespread
availability of testing facilities and better access to these facilities.
The limited data available suggest that the increase in HIV cases is
partly due to a rising willingness to test for HIV in groups with a high
risk of transmission . The higher number of HIV tests (ELISA and
Western blot) performed in German laboratories when comparing the
year 1999 to 2004 and the augmented use of HIV-NAT in primary
HIV diagnosis additionally indicate changes regarding HIV testing
.The rising number of cases reported between 1996 and 1997
may reflect increased testing for HIV following the implementation
of highly active antiretroviral treatment (HAART). Recently the
upwards trend in syphilis cases reported in Germany was discussed
as a possible cofactor for increased HIV transmission in men having
sex with men (MSM) . However, the implications of these trends
have not yet been analysed systematically.
The proportion of reported HIV cases without information on the
underlying transmission risk decreased from 42% to 13% between
1993 and 2007, primarily reflecting amendments concerning case
reporting . In the same period the proportion of cases in MSM
increased from 48% to 65%, whilst the proportion of cases with
intravenous drug use decreased from 18% to 6%. Heterosexual
transmission was constant at around 15-20%; persons originating
from high prevalence countries (HPCs) as transmission risk for HIV
contributed 11% of the total in 1993 and in 2007, with a peak
of 25% in 2002 [1,2].
F i g u r e 1
Number of newly diagnosed HIV cases reported in Germany,
1993 – 2007 (n=31,404)
1993 1994 1995199619971998199920002001 200220032004200520062007
Number of cases (n)
* implementation of the “Protection against Infection Act”
(Infektionsschutzgesetz - IfSG)
2 EUROSURVEILLANCE Vol. 13 · Issues 7–9 · Jul–Sep 2008 · www.eurosurveillance.org
Standard reports of newly diagnosed HIV infections do not permit
the differentiation between recently acquired (incident) and long-
standing (prevalent) infections, since routinely applied serological
HIV tests (screening and confirmatory tests) do not provide such
information. The diagnosis of an HIV infection can be delayed by
up to several years and the time between infection and diagnosis
may be a number of years and vary considerably, thus estimating
incidence rates accurately and effectively is difficult. However,
incidence estimates are fundamental to understanding the current
dynamics of the HIV epidemic.
Several other methods have proved suitable for the identification
of recent (incident) HIV infections in patients with newly diagnosed
HIV infections. The concept of recent infections in HIV usually
covers a period up to six months prior to the diagnosis depending
on the diagnostic assay used [4-9]. Testing for recent HIV infections
was implemented as an additional component (anonymous and
unlinked) of the national HIV surveillance systems in France [10,11],
Switzerland  and in 22 federal states of the United States of
America  and was used in selected population groups at risk
for HIV infection in the United Kingdom and South Africa [14,15].
Collection of additional data on knowledge, attitudes, behaviour and
practices (KABP survey) concerning HIV from patients identified as
recently infected with HIV permits analysis of risks and protective
factors effective in HIV transmission. Subpopulations at increased
risk for acquiring HIV and with limited access to diagnostic services
can be identified by comparing KABP data between risk groups.
After encouraging results from a pilot study in Berlin, a
nationwide study including, testing for recent HIV infections and
a KABP survey was started in Germany in March 2008. The study
aims to provide a better picture of the current dynamics and drivers
of the HIV epidemic based on incidence estimates. The results are
expected to help amend the national prevention strategies.
Pilot Study in Berlin 2005-2007
A pilot study conducted in Berlin from 2005 to 2007 assessed
the feasibility of the methodologies described above and the impact
of the results for future HIV surveillance in Germany. The design
was cross-sectional with voluntary sampling after obtaining patients’
written informed consent. Sampling was anonymous and unlinked
with no particular risk group being targeted. Exclusion criteria
were clinical stage C HIV infection according to the US Centres
for Diseases Control and Prevention (CDC) classification  and
antiretroviral treatment. Clinicians in specialised private practices
and clinic outpatient departments (OPD) collected venous blood
and clinical data from adults aged 18 years or older with newly
diagnosed HIV infections. Twenty of nearly 50 HIV-specialised
facilities agreed to participate in the study. To determine a recent
HIV infection the blood samples were tested using the BED-CEIA,
one of the methods able to detect recent HIV infections serologically
in patients with confirmed HIV diagnosis . The BED-CEIA was
established using a German HIV seroconverter sample panel with
known time of seroconversion. Optimal cut-offs separating recent
and long-standing samples in the reference panel were found with
an optical density (ODn) of ≤0.8 for the BED-CEIA and duration of
infection of 20 weeks . KABP data with regards to HIV/AIDS
were collected through patients’ questionnaires. Test results were
not delivered to the patients.
Of 132 cases sampled, 114 were included in the study, 18 did
not meet the eligibility criteria.
The 132 cases represent 27% of all newly diagnosed HIV
cases reported to the RKI from the Federal State of Berlin during
the study period between November 2005 and February 2007
(n=495). The total number of cases from Berlin accounted for 15%
of all notifications from Germany. As far as data were available,
all patients included had HIV-1 subtype B infections. Of the 114
cases meeting the eligibility criteria for the study, 102 were MSM
(89%) and 12 had other HIV transmission risks.
Proportions of recent out of newly diagnosed HIV infections were
found to be 54% in MSM (95% Confidence Interval (CI): 38-56)
and 16% (95% CI: 32-0) in patients stating other risks. Proportions
of recent infections were significantly higher in MSM ≤30 years
(p=0.019), mean age was 33.9 (median 34 years) in patients with
recent and 38.6 years (median: 38 years) in patients with long-
standing infections (p=0.011). Symptoms of acute seroconversion
correlated significantly with recent HIV infections (p=0.009). Mean
viral load (VL) was significantly higher in recent HIV infections
compared with long-standing infections (1,608,801 copies/μl and
141,951 copies/μl, respectively, p=0.009). A correlation was also
found between recency of HIV infection and CD4 cell counts: counts
>500/μml were indentified in recent HIV infections and counts
≤200/μml in long-standing infections; however, this correlation
was not statistically significant (p=0.08).
Patients recruited for the pilot study showed a selection bias
with samples from MSM being overrepresented (72% MSM in
all cases reported from Berlin compared with 89% in the study
sample). However, comparison of basic demographic variables in
case reports of MSM from Berlin and MSM in the Berlin pilot study
sample did not show statistically significant differences within
the study period. High-risk behaviour indicated through very low
condom use in recently HIV-infected MSM could be identified:
>90% did not use condoms during sexual intercourse in the six
months prior to HIV diagnosis and 19% stated that they did not use
condoms despite being aware that their sexual partner had tested
positive for HIV .
We were not able to produce incidence estimates since essential
denominators are currently not available in Germany. Nevertheless,
the results of the pilot study support expectations that the modified
application of the method will contribute to amending and improving
HIV prevention efforts in Germany.
National HIV Incidence Surveillance Programme 2008 - 2010
Since November 2007 the RKI initiated a nationwide study
funded by the German Ministry of Health (BMG) to collect data
on recent HIV infections and current HIV transmission risks. The
results are expected to complement the available data on HIV from
the general surveillance by identifying subpopulations presently
at increased risk for acquiring HIV infections and the risks most
recently having an impact on HIV transmission in Germany.
Design and methods
To obtain the desired information a cross-sectional unlinked
anonymous study, with a case control component will be conducted
from 1 March 2008 to 28 February 2010. Samples and data are
collected over this period through either laboratories or specialised
EUROSURVEILLANCE Vol. 13 · Issues 7–9 · Jul–Sep 2008 · www.eurosurveillance.org
clinical centres. Information on screening patterns for all cases is
gathered in both the laboratory and clinical study arm. As data from
the two study arms cannot be linked, overlapping of sampling from
patients in both study arms cannot be excluded.
Laboratory study arm
Newly diagnosed HIV cases in Germany are reported to the RKI
by more than 200 laboratories. Only 36 labs, however, contribute
significant numbers to the reporting of newly diagnosed HIV
infections (significant defined as providing each at least 1% of
the total number of cases reported nationally). These 36 labs are
responsible for almost 70% of all reported newly diagnosed HIV
cases in Germany, with the remaining approximately 170 labs
reporting another 30%. All 36 laboratories reporting high numbers
of HIV infections agreed to participate in the national HIV incidence
study (exhaustive sampling). Thirty-five of 51 randomly selected
laboratories with HIV case reporting on a smaller scale also agreed
to participate (random sample). Thus, a total of countrywide 71
laboratories will constitute the laboratory study arm.
Participating laboratories will collect plasma or serum samples
from all newly diagnosed HIV cases during the study period.
Samples are provided as “Dried Plasma Spots” (DPS) or “Dried
Serum Spots”  and sent every month to the project group HIV
Variability and Molecular Epidemiology at the RKI. All samples are
tested for recency of HIV infection using the BED-CEIA. Clinical data
are limited to information reported according to the national HIV
surveillance regulations . Data will allow to estimate recent HIV
infections and incidence proportions by using basic demographic
data and to analyse the risks to acquire an HIV infection. Data
collected in this study arm are expected to be representative for
Germany. The sample size is expected to include 1,600 cases
annually representing around 60% of all new HIV diagnoses.
Clinical study arm
Over 80 clinical facilities specialised in HIV diagnosis and care
from six regions in Germany will participate in the clinical study
arm. The regions selected include those reporting the highest
HIV case numbers nationally since 2001 (Figure 2) and they are
characterised by a concentration of medical facilities specialised
in HIV care compared with other regions. These facilities include
private practitioners, clinic OPDs and counselling centres run by
local health authorities or non-government organisations (NGO).
In this study arm clinicians specialised in HIV diagnosis and care
will recruit patients with newly diagnosed HIV infections (cases)
and patients undergoing an HIV test with negative result (controls).
Cases and controls will be matched by basic demographic variables
and their risk of HIV transmission. HIV testing for cases and their
respective controls has to be performed within a three month
period. After obtaining written informed consent, blood samples
are collected from case patients as DBS . The samples are
analysed for recency of HIV infection by BED-CEIA at the HIV
Variability and Molecular Epidemiology project group of the Robert
Koch Institute. Clinical and medical history data from case and
control patients are collected through a physician’s questionnaire.
KABP-data are collected from cases and controls by using a self-
administered patient’s questionnaire. The expected sample size is
600 cases and controls annually. Analyses of the data will allow
comparison between patients with recently acquired HIV infection
and persons undergoing HIV tests with a negative test result in
the same clinical institutions and in an identical time frame. The
analyses aim at obtaining information on the current status of
general knowledge about HIV/AIDS, on the behaviour and attitudes
towards prevention of HIV transmission, and on the risks taken with
regards to HIV transmission.
The study offers an outstanding opportunity to identify recent
HIV infections out of newly diagnosed cases and estimate HIV
incidence. As a result of this a deeper insight into the transmission
dynamics of the ongoing HIV epidemic in Germany will be available.
To prevent further HIV infections, comparative analyses are aimed
at identifying the risks for HIV transmission and the relevant
behaviour and attitudes. However, the major limitations of our
study are insufficient screening patterns that only reflect those
patients requesting an HIV test. True incidence estimates will be
F i g u r e 2
Cumulative incidence of newly diagnosed cases of HIV in Germany,
2001-2006 and six regions of the clinical study arm, Germany 2008
Per 1 million population
> 0 - 0,01
> 0,01 - 0,1
> 0,1 - 1
> 1 - 10
4 EUROSURVEILLANCE Vol. 13 · Issues 7–9 · Jul–Sep 2008 · www.eurosurveillance.org
difficult to obtain as the denominators needed are not available in
Germany. Despite these limitations the data are expected to have
an impact on amending and improving national prevention efforts
and strategies in Germany. Better knowledge of the factors driving
the HIV epidemic and of the most recent dynamics of the epidemic
revealing subgroups currently at increased risk of acquiring HIV will
help to design targeted and prompt interventions.
The authors would like to thank all collaborating laboratories and
clinical centres participating in this study for their excellent work
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This article was published on 4 September 2008.
Citation style for this article: Bätzing-Feigenbaum J, Loschen S, Gohlke-Micknis S,
Zimmermann R, Herrmann A, Kamga Wambo O, Kücherer C, Hamouda O. Country-wide
HIV incidence study complementing HIV surveillance in Germany. Euro Surveill.
2008;13(36):pii=18971. Available online: http://www.eurosurveillance.org/ViewArticle.