Sharply rising prevalence of HIV infection in Bali : a critical assessment of the surveillance data.
Volume 24
Number 8
August 2013
Guidelines
2013 UK National Guideline for the management of
lymphogranuloma venereum: Clinical Effectiveness Group of the
British Association for Sexual Health and HIV (CEG/BASHH)
Guideline development group . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 593
J White, N O’Farrell and D Daniels
Sexual risk and HIV prevention behaviours among
African-American and Latino MSM social networking users . . . . . . 643
S D Young, G Szekeres and T Coates
Are teachers at higher risk of HIV infection than the general
population in Burkina Faso? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 651
F Kirakoya-Samadoulougou, N Nagot, S Yaro et al.
Review
Endocrine and metabolic abnormalities among HIV-infected
patients: A current review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 603
D Kibirige and R Ssekitoleko
Audit reports
Audit of the effect of electronic patient records on uptake
of HIV testing in a level 3 genitourinary medicine service . . . . . . . . 661
E Clarke, S Bhatt, R Patel and S Samraj
Original research articles
Increasing screening frequency in men who have sex with men:
impact of guidance on risk profiling on workload and earlier
diagnosis of sexually transmitted infection and HIV . . . . . . . . . . . . . . 613
A Baker, C Fleury, E Clarke et al.
Population-based prevalence of hepatitis B and C virus, HIV,
syphilis, gonorrhoea and chlamydia in male injection drug
users in Lagos, Nigeria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619
W Tun, L Vu, S B Adebajo et al.
Factors associated with asymptomatic non-chlamydial
non-gonococcal urethritis in heterosexual men: findings from
a case-control study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 627
J M Saunders, C H Mercer, L J Sutcliffe et al.
Sharply rising prevalence of HIV infection in Bali: a critical
assessment of the surveillance data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 633
P P Januraga, L P L Wulandari, P Muliawan et al.
A glimmer of hope? Evaluation of time for non-genitourinary
medicine physicians to diagnose HIV infection in patients
presenting with HIV-related illness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 639
E Clarke, O Drew, S Sundaram et al.
Case reports
Dilated common bile duct and deranged liver function tests
associated with ketamine use in two HIV-positive MSM . . . . . . . . . 667
J Zhou, S G Shaw and Y Gilleece
Testicular and kidney masses in a HIV-infected man . . . . . . . . . . . . . 671
R Liang and S Chaudhry
Raltegravir-induced Drug Reaction with Eosinophilia and
Systemic Symptoms (DRESS) syndrome – implications for
clinical practice and patient safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 675
M E O Perry, N Almaani, N Desai et al.
Letter to the Editor
Predictors of long-term HIV RNA suppression on
darunavir/ritonavir monotherapy in the MONET trial . . . . . . . . . . . . . . 679
J Arribas, F Pulido, A Hill et al.
Corrigendum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 683
This journal is abstracted/indexed in: MEDLINE, EMBASE/Excerpta Medica, ADONIS, AIDS ABSTRACTS, Global Health, CAB ABSTRACTS, Elsevier
BIOBASE/Current Awareness in Biological Sciences, PAPILLOMAVIRUS REPORT, CURRENT CONTENTSÕ , CLINICAL MEDICINE, SCISEARCHÕ , RESEARCH
ALERTÕ , CURRENT AIDS LITERATURE, VIROLOGY & AIDS ABSTRACTS, PSYCHOLOGICAL ABSTRACTS/PsycINFO/PsycLIT, BIOSIS, e-psyche
ORIGINAL RESEARCH ARTICLE
Sharply rising prevalence of HIV infection in Bali: a critical
assessment of the surveillance data
P P Januraga MD MPH*§, L P L Wulandari MD MPH*, P Muliawan MD MSc*, S Sawitri
L Causer MD MPH‡, D N Wirawan MD MPH† and J M Kaldor PhD‡§
MD MPH†,
*School of Public Health; †Department of Community Medicine, Faculty of Medicine, Udayana University, Bali, Indonesia; ‡Kirby Institute,
Faculty of Medicine, University of New South Wales, Sydney, Australia
Summary: This study critically examines serological survey data for HIV infection in selected populations in Bali, Indonesia.
Sero-survey data reported by the Bali Health Office between 2000 and 2010 were collated, and provincial health staff were interviewed
to gain a detailed understanding of survey methods. Analysis of time series restricted to districts that have used the same sampling
methods and sites each year indicates that there has been a steady decline in HIV prevalence among prisoners, from 18.7% in 2000 to
4.3% in 2010. In contrast, HIV prevalence among women engaged in sex work increased sharply: from 0.62% in 2000 to 20.2% in
2010 (brothel based), and from 0% in 2000 to 7.2% in 2010 (non-brothel based). The highest prevalence was recorded among people
who injected drugs. Recent surveys of gay men and transvestites also found high prevalences, at 18.7% and 40.9%, respectively.
Review of the methodology used in the surveys identified inconsistencies in the sampling technique, sample numbers and sites over
time, and incomplete recording of individual information about survey participants. Attention to methodological aspects and
incorporation of additional information on behavioural factors will ensure that the surveillance system is in the best position to
support prevention activities.
Keywords: HIV, AIDS, Asia, epidemiology, high-risk behaviour, sex workers, transvestites, waria, Bali, seroprevalence
BACKGROUND
The epidemic of HIV infection is recognized as a major public
health threat in Indonesia. Even though the estimated national
HIV prevalence is relatively low, at 0.3% in 2011, the epidemic
is highly diverse, with considerable variation by geographic
area.1 While spread of infection was initially high among
people who inject drugs, sexual transmission has come to
represent an increasing proportion of cases detected.2 Among
the 33 Indonesian provinces, Bali has been one of the more
heavily affected, ranking fifth according to the absolute
number of reported diagnoses of infection over the past
10 years and second on a per capita basis, with a substantial
increase in the number of diagnoses reported each year over
this period.3
Recognising the limitations of HIV case reporting as a means
of public health surveillance, the Provincial Heath Office in Bali
has, since 2000, conducted serological surveys in populations
considered to be at higher risk for HIV infection. These
surveys have become the primary source of data for tracking
trends in the HIV epidemic in Bali, and results have been
made available on a regular basis in provincial and national
Correspondence to: P P Januraga
Email: januraga@sph.unud.ac.id
§These
authors contributed equally to this work.
surveillance reports. The surveys have provided a general indication that HIV prevalence is increasing in some populations,
particularly women involved in sex work.4 However, the
data from the surveys have generally been published only
as annual, province-wide prevalences, by broad population
group. Furthermore, the surveillance data have not been
subject to more detailed analyses that might provide insight
into their validity, nor has there been an assessment of the
extent to which observed trends and patterns may be due to
changes in sampling frames. We therefore conducted a study
that aimed to fill these gaps and have exposed the findings to
the scrutiny of peer-reviewed publication.
METHODS
We obtained copies of archival records and reports of HIV serological surveys from the Bali Provincial Health Office (BHO).
As the reports did not contain comprehensive descriptions of
survey procedures, we obtained further information on procedures from interviews undertaken by the first author (PPJ)
with staff from BHO who had been involved in the surveys.
The following summary of procedures is based on both the
reports and the interviews. HIV surveys were carried out
by staff from BHO using the ‘unlinked anonymous’ method.
Potential survey participants were approached and their
verbal informed consent sought for drawing blood to submit
to serological testing for hepatitis B and syphilis. Verbal
DOI: 10.1177/0956462413477556. International Journal of STD & AIDS 2013; 24: 633–637
634
International Journal of STD & AIDS
Volume 24
August 2013
................................................................................................................................................
Table 1 Annual sero-surveys for HIV in Bali: recruitment
strategies by population group
Population
Recruitment sites
Selection methods
Direct FSWs
Denpasar
Direct FSWs other
sites
Indirect FSWs
Denpasar
Indirect FSWs
other sites
Gay
Brothels
Simple random
Brothels
Consecutive sampling
Waria
IDU
Prisoners
Pregnant women
Registered massage
Whole population
parlours
Massage parlours, cafes and Consecutive sampling
karaoke bars
Community
Respondent-driven
sampling
Community
Respondent-driven
sampling
Community
Respondent-driven
sampling
Prisons
Cluster sampling
Health centres
Consecutive sampling
FSW ¼ female sex worker; IDU, intravenous drug user
Includes all subjects who were available and willing to participate during the
surveys until it reaches the number of samples needed
informed consent was used because, for many women involved
in sex work in Bali, signing forms could be perceived as threatening. Blood specimens from those who consented were then
divided into two aliquots. One portion was used for the hepatitis B and syphilis testing, and participants who were found to
have syphilis were advised to attend a clinic for treatment if
needed. The other portion was tested for HIV antibodies separate from all identifiers to ensure that there was no possibility
of associating the results with specific individuals. According
to BHO staff, the unlinked anonymous strategy was adopted
because it was believed to be consistent with World Health
Organization recommendations for HIV surveillance, and
because BHO assumed that many people would refuse to participate in the surveys if their primary purpose was presented
as HIV testing, even if unlinked. For the purposes of this
paper, we reviewed only the results of the HIV testing.
For each (annual) round of the survey, BHO recorded information on the dates when and locations (districts, as well as
specific locations within the districts) where specimens were
collected, the number of specimens tested and the number
found to be positive, broken down by population subgroup.
The subgroups selected for the surveys varied by district and
by year, and included intravenous drug users, prisoners,
female sex workers (both ‘indirect’, working in cafes, karaoke
bars and massage parlours, and ‘direct’, working in brothels),
self-identified gay men, waria (Indonesian term for transvestites2,5) and pregnant women. Table 1 summarizes the strategies
used to recruit each of these population groups.
We then used the criteria for second-generation HIV surveillance developed by the WHO/UNAIDS Working Group on
Global HIV/AIDS and STI Surveillance to assess whether the
surveillance data could be used to evaluate trends over time.6
The criteria included consideration of the frequency of data collection, the appropriateness of the population being surveyed,
the consistency over time of the surveillance sites and groups
and the coverage of the groups under surveillance.6,7 Data
obtained through procedures that met the criteria were then
analysed to determine HIV prevalence and analyse time
trends among subgroups by geographic location. We used
statistical tests for trends in proportions to assess the trends
by year.
The Institutional Review Board of the Kerti Praja Foundation
(YKP), which provides HIV prevention and clinical services to
people at risk of HIV in Denpasar, Bali, provided ethical
approval for this study. The Bali Health Office gave permission
to access, analyse and publish results of the surveys and to
conduct interviews with its surveillance staff.
RESULTS
Based on internal BHO records, serological surveys were conducted in all nine of Bali’s districts in the period 2000–2012.
Information retained in the Health Office was in tabular form,
with numbers tested and numbers found positive recorded by
year, district and population subgroup. Line records of individuals tested were not available, and there was no information on
age or any other characteristics of participants.
Table 2 shows the numbers of samples tested from all population subgroups in Bali between 2000 and 2010. The size of
samples per year and the frequency of sampling seem to be
appropriate. However, as shown in Table 3, the frequency, consistency of sites and representativeness of the samples varied
considerably by year and by district. In virtually all districts,
the serological surveillance focused on prisoners and female
sex workers. Data for a broader set of population subgroups
were available for only Denpasar, the district with the largest
population and the location of the Bali capital, and for only
the years 2009 and 2010. As shown in Figure 1, the prevalence
of HIV in Denpasar was highest in people who injected drugs
(55%, confidence interval [CI] +9.95), followed by waria and
then direct female sex workers. The lowest prevalence in
Denpasar was among pregnant women, with three infections
detected among 790 tests in 2009–2010.
Repeated annual surveys that covered most or all of the study
period with a reasonable annual sample size and that hence
could provide information on time trends were available for
only female sex workers, prisoners and, to a lesser extent,
people who injected drugs. The BHO reports demonstrated
that in Denpasar, samples for direct sex workers were obtained
each year at the same three brothel complexes, and that samples
for indirect workers were taken from all registered ‘traditional
massage parlours’. Similarly, in Tabanan, the same site was
used to obtain specimens from direct sex workers each year.
In other districts, the locations of the sampling of both direct
and indirect sex workers changed from year to year. The
authors sought information from the BHO about the rationale
for choosing specific sites in these districts each year, but
were not able to obtain an explanation.
Sample sizes in each district were determined by the BHO,
based on available budget. At virtually all of the sex work
sites, women were recruited on the basis of their presence at
the time of visit by BHO staff. All women present were
invited to participate until the intended sample size was
achieved (consecutive sampling). From 2006 on, and at only
the Denpasar sites, women were selected using the systematic
random sampling method, with YKP providing the sampling
list and assisting in the field recruitment after having compiled
a field census with the help of pimps and brothel owners prior
to the sero-survey implementation. This methodology was
reported by BHO to have been consistently applied over the
period of the surveys.4
Consistently sampled annual series results for prisoners were
available from most of the districts, with Lapas Kerobokan in
Januraga et al. Sharply rising prevalence of HIV infection in Bali
635
................................................................................................................................................
Table 2
Annual sero-surveys in Bali: numbers tested by population group (2000 –2010)
Year
Population group
0
1
2
3
4
5
6
7
8
9
10
Prisoners
IDU
Gay men
Waria
Indirect FSWs
Direct FSWs
Pregnant women
301
3
583
708
1
584
621
39
42
58
659
288
468
526
524
302
618
661
301
78
72
389
400
390
707
96
148
87
346
496
400
200
227
295
81
262
126
403
65
64
100
564
442
100
8
680
386
277
267
400
395
805
FSW ¼ female sex worker; IDU, intravenous drug user
Table 3
Annual sero-surveys in Bali: numbers tested by population group, district and year (2000 –2010)
Year
District
Population group
0
1
2
3
4
5
6
7
8
9
10
Buleleng
Prisoners
Waria
Direct FSWs
Prisoners
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
IDU
Gay men
Waria
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
IDU
Gay men
Waria
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
IDU
Indirect FSWs
Direct FSWs
Prisoners
IDU
Prisoners
Indirect FSWs
Direct FSWs
Prisoners
Direct FSWs
78
83
68
81
75
7
63
105
65
8
117
110
85
9
37
76
46
33
19
33
81
79
108
20
36
71
55
50
63
21
50
67
94
72
9
80
117
10
303
15
200
205
200
Jembrana
Tabanan
Badung
Denpasar
Gianyar
Bangli
Klungkung
Karangasem
18
10
3
58
14
2
76
20
43
27
33
43
45
187
353
392
300
55
1
200
96
200
100
100
15
200
19
6
64
200
134
200
100
141
109
150
235
401
218
250
247
250
245
600
46
36
48
45
77
66
59
53
100
149
67
37
33
41
10
31
26
40
12
60
60
8
37
262
403
29
31
25
52
21
400
24
42
51
292
181
295
12
210
202
96
96
66
209
400
400
68
150
100
78
72
231
400
390
66
101
158
48
54
35
68
48
26
17
30
25
37
39
29
40
57
137
11
42
14
24
1
19
11
4
6
18
22
8
3
22
36
FSW ¼ female sex worker; IDU, intravenous drug user
Highlighted data only used in subsequent analyses (see Results and Figure 1)
Badung, the biggest prison in Bali, providing the largest
number of samples. Kerobokan has also been the main prison
in Bali for people incarcerated for offences related to drug
use. Prisoners were recruited at each site on the basis of
random sampling: sample size each year was determined in
advance, after which cell blocks were selected by simple
random sampling and all inmates in each selected block
invited to participate. Again, the methodology was reported
to have been consistent over the period.
In Denpasar District, people who inject drugs were surveyed
during four years of the study period. Recruitment was assisted
by the local non-government organization, Yakeba Foundation,
and participants were recruited using respondent-driven
sampling. The recruitment methods were described by BHO
as being the same each year.
Based on the requirement for consistently collected surveillance data, we limited subsequent statistical analyses of time
trends to data on prisoners from all districts, sex workers
from Denpasar and Tabanan and people who inject drugs
from Denpasar. Figure 1 shows trends among prisoners in
Badung (Kerobokan) and in the other districts. The prevalence
has declined steadily in Kerobokan from 19 (CI +5.59) to 4.3%
636
International Journal of STD & AIDS
Volume 24
August 2013
................................................................................................................................................
Figure 1 HIV prevalence among selected population groups, for Denpasar (2009–2010) and for
districts in which there was a consistently collected annual series
(CI +2.74) over 10 years (P , 0.05), and has been stable at
below 3% in other districts. In contrast, the HIV prevalence
among both direct and indirect female sex workers has
increased steadily. Among direct sex workers, the prevalence
in Denpasar and Tabanan rose from 1% (CI +1.21) to 20%
(CI +3.53) in the 10-year period, while among indirect
workers in Denpasar, in whom there had been no HIV detected
at the start of the period, the prevalence was 7% (CI +3.5) by
the end of 10 years (Figure 1) (P , 0.05). For people who
injected drugs, there was no indication of a change in prevalence over the four years for which surveys were conducted
(P ¼ 0.213).
DISCUSSION
This report is the first detailed epidemiological analysis of the
recent shift in the HIV epidemic in Bali from being predominantly linked to intravenous drug use to primarily affecting
female sex workers. People who inject drugs still have the
highest HIV prevalence in Bali, but it has remained stable
over the last decade. In addition, despite the strong association
between injecting drugs and incarceration,8 HIV prevalence
among prison inmates appears to be decreasing. This decline
may reflect a change in the prison population, the impact
of harm reduction programmes or both.8 In Denpasar and
Badung there are more than five centres implementing harm
reduction programmes, run by both government and nongovernment agencies. In Kerobokan prison itself, a harm
reduction programme began in 2001, with a VCT programme
commencing in 2004.8 Furthermore, there is evidence that the
population of people who inject is itself decreasing in size,
with a recent study estimating the number in Bali being
700 –800, compared with 2500 people in 2003.9,10 It is possible
that the stable level of HIV infection reflects sampling of an
ageing and diminishing cohort of people who inject drugs.
Based on the analyses reported in this paper, when restricting
time trend assessment to consistently sampled sites, it appears
that the increase of HIV prevalence among women engaged in
sex work is real and substantial. Rising rates of HIV in this
population are an important public health concern, for the
women themselves, for their male sexual partners and for
other women who are partners of these men.2,11,12 The Bali
AIDS Commission in 2007 reported almost 3000 direct female
sex workers working in brothel complexes in Bali, with most
in Denpasar.13 The Ministry of Health in 2006 estimated that
more than 82,000 men were clients of brothel-based sex
workers and 25,000 were clients of other sex workers in Bali.
Apart from the serological surveys, the only alternative information on HIV prevalence in populations at higher risk has
come from the Integrated Behavioural and Biological Survey
(IBBS) conducted in 2007 in 11 Indonesian provinces. This
survey, which included 250 brothel-based female sex workers
in Bali, found that the province had the second highest HIV
prevalence for this population, 14% (CI +4.3),14 a figure comparable with the estimate of 15% (CI +4.34) from the serological sero-survey in the same year based on Denpasar and
Tabanan sites. The IBBS 2007 report also showed that consistent
condom use among sex workers in Bali was low, and that the
Bali workers had the largest number of clients per week
among workers in the IBBS provinces.14,15
Based on sero-surveys conducted primarily in Denpasar
District, HIV sero-prevalence among waria and gay men in
Bali is already high. According to behavioural surveys, both
groups engage in sex work, with a higher percentage among
warias.2,14 – 16 In Bali, a recent study estimated that there were
between 430 and 900 waria and 12,000 gay men living in
Denpasar and Badung districts.17 As in many developing
countries, these populations can be hard to reach for prevention
programmes, which may be opposed by religious and other
social opinion leaders. In light of the results of our study,
more importance should be placed on interventions to
prevent HIV transmission in these groups.5
Under WHO-UNAIDS guidelines, if HIV prevalence among
at least one population group is consistently above 5% and
below 1% in the general adult population, the HIV epidemic
is ‘concentrated’, while if prevalence has reached 1% in the
general adult population, then the epidemic is considered to
be ‘generalized’.18 However, it is recognized that this classification should be applied with care, as in most countries HIV
Januraga et al. Sharply rising prevalence of HIV infection in Bali
637
................................................................................................................................................
prevalence among the general adult population is estimated
using HIV prevalence among pregnant women,19 which can
differ substantially from estimates derived from general adult
population surveys.20
In Denpasar, all pregnant women tested were seen at
primary health centres facilities operated by the government.
Since many pregnant women also seek antenatal care from
other facilities, mostly private, the sample of women surveyed
may not be representative.18,21 A PMTCT programme run by
a local NGO in the same years reported HIV infection in 1.2%
(CI +1.4) of pregnant women 2009 and in 0.87% (CI +.85)
of pregnant women in 201022 on the basis of 458 tested in 2010.
Our detailed examination of the sero-survey data indicates
several ways in which their quality could be improved. First,
survey results should be recorded and retained in line record
form, and consideration given to including age, at least, as
an additional field for each person in the survey. Having
sufficient numbers of participants at each site for each round,
and consistent sampling of sites over time, would ensure
the consistency and representativeness of survey results.
Increased numbers of participants would provide the possibility of analysing prevalence by age subgroups, supplying
information that would provide a better understanding of
epidemic dynamics.
To further inform and understand the epidemic, it would
also be helpful to add behavioural questions to the sero-surveys.
These would provide indicators that could be used to monitor
the impact of prevention programmes.18 – 20,23,24 The national
IBBS, run by the central government, has provided useful information regarding epidemic progress nationally, but it is undertaken with long time intervals between rounds and does not
specifically address the epidemic at the provincial level in
Indonesia. The IBBS could be adapted to meet local needs
and research questions. Ideally, the IBBS and local surveillance
system could be better integrated to prevent duplication of
effort and improve efficiency.
Since the surveillance findings indicate that the epidemic
is being driven by unsafe sexual behaviours, more research
on social and sexual networks is needed.25 Ethnographic
and qualitative studies can provide a better understanding of
network structures and how they relate to epidemic patterns,
and can assist in identifying which interventions are appropriate for each population.26
Finally, the quality and value of the surveillance system
would be enhanced by the provision of local human resources
to plan, implement and evaluate its activities. Capacity building in the methods of surveillance and allocation of human
resources with responsibility for design and analysis of
surveys are critical steps on this pathway.23
ACKNOWLEDGEMENTS
We would like to acknowledge our colleagues at the Bali
Health Office, especially Dr Nyoman Subrata and Dr Agus
Suryadinata, for trusting us with and sharing their data for
this study. We also offer our appreciation to the staff of
Badung and Denpasar Health Offices for their willingness
to help us validate the data. This project was carried out
with support from the Australian Agency for International
Development. JMK is a National Health and Medical
Research Council Senior Principal Research Fellow.
Competing interests: None declared.
REFERENCES
1 MOH of Indonesia. Mathematic Model of HIV Epidemic in Indonesia 2008 –2014.
Jakarta: Ministry of Health Of Indonesia, 2008
2 Riono P, Jazant S. The current situation of the HIV/AIDS epidemic in
Indonesia. AIDS Educ Prev 2004;16(Suppl. A):78 –90
3 MOH of Indonesia. HIV-AIDS Data Update; Second Quater 2012. Jakarta:
Ministry of Health of Indonesia, 2012
4 Bali Health Office. Laporan Hasil Pelaksanaan Serosurvei STS dan HIV di Provinsi
Bali tahun 2000 –2009 (Report of Bali Province’s sero-surveys results, year
2000–2009). Denpasar: Bali Health office, 2009
5 Pisani E, Girault P, Gultom M, et al. HIV, syphilis infection, and sexual
practices among transgenders, male sex workers, and other men who have sex
with men in Jakarta, Indonesia. Sex Transm Infect 2004;80:536
6 UNAIDS/WHO Working Group on global HIV/AIDS and STI surveillance.
Guidelines for Second Generation HIV Surveillance. Geneva: UNAIDS/WHO,
2000
7 Garcia-Calleja J, Zaniewski E, Ghys P, Stanecki K, Walker N. A global analysis
of trends in the quality of HIV sero-surveillance. Sex Transm Infect
2004;80(Suppl. 1):i25
8 Hartawan A, Sawitri A, Septarini W. Survei Perilaku Berisiko dan Perilaku
Pencegahan Tertular HIV di Lapas Kerobokan, Denpasar, Bali. Denpasar: Lapas
Kerobokan, 2009
9 Sawitri AAS, Blogg J, Angela R. Estimating the number of the people who
inject drugs in Bali, 2010. Drug Alcohol Rev 2012;31:813 –7
10 Sumantera I, Wirawan DN, Masmini N, Gerong L. Estimasi jumlah pemakai
narkoba suntik atau IDU (injecting drug users) di propinsi Bali [An estimation of
number of injecting drug users in Bali]. Jakarta: Indonesia HIV/AIDS Prevention
and Care Project, 2003
11 Alary M, Lowndes CM. The central role of clients of female sex workers in the
dynamics of heterosexual HIV transmission in sub-Saharan Africa. AIDS
2004;18:945– 7
12 Hesketh T, Zhang J, Qiang DJ. HIV knowledge and risk behaviour of female
sex workers in Yunnan Province, China: potential as bridging groups to the
general population. AIDS Care 2005;17:958– 66
13 KPAD Bali. Estmisasi Jumlah ODHA di Bali. Denpasar: KPAD Bali, 2007
14 MOH of Indonesia. Integrated Biological - Behavioral Surveillance of
Most-at-Risk-Groups (MARG). Jakarta: Ministry of Health Republic Indonesia,
2007
15 Prabawanti C, Bollen L, Palupy R, et al. HIV, Sexually transmitted infections,
and sexual risk behavior among transgenders in Indonesia. AIDS Behav
2010:1 –11
16 Joesoef M, Gultom M, Irana I, et al. High rates of sexually transmitted diseases
among male transvestites in Jakarta, Indonesia. Int J STD AIDS 2003;14:609
17 MOH of Indonesia. Estimasi Jumlah Populasi Kunci di Indonesia tahun 2012
(Estimation of Key Populations Numbers in Indonesia 2012). Jakarta: Ministry of
Health of Indonesia, 2012
18 WHO/UNAIDS. Guidelines for second generation HIV Surveillance. 2000
19 Lyerla R, Gouws E, Garcia-Calleja JM. The quality of sero-surveillance in
low- and middle-income countries: status and trends through 2007. Sex Transm
Infect 2008;84(Suppl. 1):i85 – 91
20 Rehle T, Lazzari S, Dallabetta G, Asamoah-Odei E. Second-generation HIV
surveillance: better data for decision-making. Bull World Health Organ
2004;82:121– 7
21 CDC. Program Operations Guidelines for STD Prevention Surveillance and Data
Management. 2010. See http://www.cdc.gov/STD/Program/surveillance/
4-PGsurveillance.htm#sentinel (last checked 15 March 2010)
22 Wulandari LPL, Lubis D, Wirawan A. HIV prevalence among pregnant
mother in Bali, are we sitting on a time bomb. In: ICAAP 10, Busan, 2011
23 Diaz T, De Cock K, Brown T, Ghys PD, Boerma J. New strategies for HIV
surveillance in resource-constrained settings: an overview. AIDS 2005;19:S1
24 Garnett G, Garcia-Calleja J, Rehle T, Gregson S. Behavioural data as an adjunct
to HIV surveillance data. Sex Transm Infect 2006;82(Suppl 1):i57
25 Rothenberg R, Narramore J. Commentary: The relevance of social network
concepts to sexually transmitted disease control. Sex Transm Dis 1996;23:24
26 Ward H. Prevention strategies for sexually transmitted infections: importance
of sexual network structure and epidemic phase. Sex Transm Infect
2007;83(Suppl. 1):i43
(Accepted 14 January 2013)
Number 8
August 2013
Guidelines
2013 UK National Guideline for the management of
lymphogranuloma venereum: Clinical Effectiveness Group of the
British Association for Sexual Health and HIV (CEG/BASHH)
Guideline development group . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 593
J White, N O’Farrell and D Daniels
Sexual risk and HIV prevention behaviours among
African-American and Latino MSM social networking users . . . . . . 643
S D Young, G Szekeres and T Coates
Are teachers at higher risk of HIV infection than the general
population in Burkina Faso? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 651
F Kirakoya-Samadoulougou, N Nagot, S Yaro et al.
Review
Endocrine and metabolic abnormalities among HIV-infected
patients: A current review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 603
D Kibirige and R Ssekitoleko
Audit reports
Audit of the effect of electronic patient records on uptake
of HIV testing in a level 3 genitourinary medicine service . . . . . . . . 661
E Clarke, S Bhatt, R Patel and S Samraj
Original research articles
Increasing screening frequency in men who have sex with men:
impact of guidance on risk profiling on workload and earlier
diagnosis of sexually transmitted infection and HIV . . . . . . . . . . . . . . 613
A Baker, C Fleury, E Clarke et al.
Population-based prevalence of hepatitis B and C virus, HIV,
syphilis, gonorrhoea and chlamydia in male injection drug
users in Lagos, Nigeria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619
W Tun, L Vu, S B Adebajo et al.
Factors associated with asymptomatic non-chlamydial
non-gonococcal urethritis in heterosexual men: findings from
a case-control study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 627
J M Saunders, C H Mercer, L J Sutcliffe et al.
Sharply rising prevalence of HIV infection in Bali: a critical
assessment of the surveillance data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 633
P P Januraga, L P L Wulandari, P Muliawan et al.
A glimmer of hope? Evaluation of time for non-genitourinary
medicine physicians to diagnose HIV infection in patients
presenting with HIV-related illness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 639
E Clarke, O Drew, S Sundaram et al.
Case reports
Dilated common bile duct and deranged liver function tests
associated with ketamine use in two HIV-positive MSM . . . . . . . . . 667
J Zhou, S G Shaw and Y Gilleece
Testicular and kidney masses in a HIV-infected man . . . . . . . . . . . . . 671
R Liang and S Chaudhry
Raltegravir-induced Drug Reaction with Eosinophilia and
Systemic Symptoms (DRESS) syndrome – implications for
clinical practice and patient safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 675
M E O Perry, N Almaani, N Desai et al.
Letter to the Editor
Predictors of long-term HIV RNA suppression on
darunavir/ritonavir monotherapy in the MONET trial . . . . . . . . . . . . . . 679
J Arribas, F Pulido, A Hill et al.
Corrigendum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 683
This journal is abstracted/indexed in: MEDLINE, EMBASE/Excerpta Medica, ADONIS, AIDS ABSTRACTS, Global Health, CAB ABSTRACTS, Elsevier
BIOBASE/Current Awareness in Biological Sciences, PAPILLOMAVIRUS REPORT, CURRENT CONTENTSÕ , CLINICAL MEDICINE, SCISEARCHÕ , RESEARCH
ALERTÕ , CURRENT AIDS LITERATURE, VIROLOGY & AIDS ABSTRACTS, PSYCHOLOGICAL ABSTRACTS/PsycINFO/PsycLIT, BIOSIS, e-psyche
ORIGINAL RESEARCH ARTICLE
Sharply rising prevalence of HIV infection in Bali: a critical
assessment of the surveillance data
P P Januraga MD MPH*§, L P L Wulandari MD MPH*, P Muliawan MD MSc*, S Sawitri
L Causer MD MPH‡, D N Wirawan MD MPH† and J M Kaldor PhD‡§
MD MPH†,
*School of Public Health; †Department of Community Medicine, Faculty of Medicine, Udayana University, Bali, Indonesia; ‡Kirby Institute,
Faculty of Medicine, University of New South Wales, Sydney, Australia
Summary: This study critically examines serological survey data for HIV infection in selected populations in Bali, Indonesia.
Sero-survey data reported by the Bali Health Office between 2000 and 2010 were collated, and provincial health staff were interviewed
to gain a detailed understanding of survey methods. Analysis of time series restricted to districts that have used the same sampling
methods and sites each year indicates that there has been a steady decline in HIV prevalence among prisoners, from 18.7% in 2000 to
4.3% in 2010. In contrast, HIV prevalence among women engaged in sex work increased sharply: from 0.62% in 2000 to 20.2% in
2010 (brothel based), and from 0% in 2000 to 7.2% in 2010 (non-brothel based). The highest prevalence was recorded among people
who injected drugs. Recent surveys of gay men and transvestites also found high prevalences, at 18.7% and 40.9%, respectively.
Review of the methodology used in the surveys identified inconsistencies in the sampling technique, sample numbers and sites over
time, and incomplete recording of individual information about survey participants. Attention to methodological aspects and
incorporation of additional information on behavioural factors will ensure that the surveillance system is in the best position to
support prevention activities.
Keywords: HIV, AIDS, Asia, epidemiology, high-risk behaviour, sex workers, transvestites, waria, Bali, seroprevalence
BACKGROUND
The epidemic of HIV infection is recognized as a major public
health threat in Indonesia. Even though the estimated national
HIV prevalence is relatively low, at 0.3% in 2011, the epidemic
is highly diverse, with considerable variation by geographic
area.1 While spread of infection was initially high among
people who inject drugs, sexual transmission has come to
represent an increasing proportion of cases detected.2 Among
the 33 Indonesian provinces, Bali has been one of the more
heavily affected, ranking fifth according to the absolute
number of reported diagnoses of infection over the past
10 years and second on a per capita basis, with a substantial
increase in the number of diagnoses reported each year over
this period.3
Recognising the limitations of HIV case reporting as a means
of public health surveillance, the Provincial Heath Office in Bali
has, since 2000, conducted serological surveys in populations
considered to be at higher risk for HIV infection. These
surveys have become the primary source of data for tracking
trends in the HIV epidemic in Bali, and results have been
made available on a regular basis in provincial and national
Correspondence to: P P Januraga
Email: januraga@sph.unud.ac.id
§These
authors contributed equally to this work.
surveillance reports. The surveys have provided a general indication that HIV prevalence is increasing in some populations,
particularly women involved in sex work.4 However, the
data from the surveys have generally been published only
as annual, province-wide prevalences, by broad population
group. Furthermore, the surveillance data have not been
subject to more detailed analyses that might provide insight
into their validity, nor has there been an assessment of the
extent to which observed trends and patterns may be due to
changes in sampling frames. We therefore conducted a study
that aimed to fill these gaps and have exposed the findings to
the scrutiny of peer-reviewed publication.
METHODS
We obtained copies of archival records and reports of HIV serological surveys from the Bali Provincial Health Office (BHO).
As the reports did not contain comprehensive descriptions of
survey procedures, we obtained further information on procedures from interviews undertaken by the first author (PPJ)
with staff from BHO who had been involved in the surveys.
The following summary of procedures is based on both the
reports and the interviews. HIV surveys were carried out
by staff from BHO using the ‘unlinked anonymous’ method.
Potential survey participants were approached and their
verbal informed consent sought for drawing blood to submit
to serological testing for hepatitis B and syphilis. Verbal
DOI: 10.1177/0956462413477556. International Journal of STD & AIDS 2013; 24: 633–637
634
International Journal of STD & AIDS
Volume 24
August 2013
................................................................................................................................................
Table 1 Annual sero-surveys for HIV in Bali: recruitment
strategies by population group
Population
Recruitment sites
Selection methods
Direct FSWs
Denpasar
Direct FSWs other
sites
Indirect FSWs
Denpasar
Indirect FSWs
other sites
Gay
Brothels
Simple random
Brothels
Consecutive sampling
Waria
IDU
Prisoners
Pregnant women
Registered massage
Whole population
parlours
Massage parlours, cafes and Consecutive sampling
karaoke bars
Community
Respondent-driven
sampling
Community
Respondent-driven
sampling
Community
Respondent-driven
sampling
Prisons
Cluster sampling
Health centres
Consecutive sampling
FSW ¼ female sex worker; IDU, intravenous drug user
Includes all subjects who were available and willing to participate during the
surveys until it reaches the number of samples needed
informed consent was used because, for many women involved
in sex work in Bali, signing forms could be perceived as threatening. Blood specimens from those who consented were then
divided into two aliquots. One portion was used for the hepatitis B and syphilis testing, and participants who were found to
have syphilis were advised to attend a clinic for treatment if
needed. The other portion was tested for HIV antibodies separate from all identifiers to ensure that there was no possibility
of associating the results with specific individuals. According
to BHO staff, the unlinked anonymous strategy was adopted
because it was believed to be consistent with World Health
Organization recommendations for HIV surveillance, and
because BHO assumed that many people would refuse to participate in the surveys if their primary purpose was presented
as HIV testing, even if unlinked. For the purposes of this
paper, we reviewed only the results of the HIV testing.
For each (annual) round of the survey, BHO recorded information on the dates when and locations (districts, as well as
specific locations within the districts) where specimens were
collected, the number of specimens tested and the number
found to be positive, broken down by population subgroup.
The subgroups selected for the surveys varied by district and
by year, and included intravenous drug users, prisoners,
female sex workers (both ‘indirect’, working in cafes, karaoke
bars and massage parlours, and ‘direct’, working in brothels),
self-identified gay men, waria (Indonesian term for transvestites2,5) and pregnant women. Table 1 summarizes the strategies
used to recruit each of these population groups.
We then used the criteria for second-generation HIV surveillance developed by the WHO/UNAIDS Working Group on
Global HIV/AIDS and STI Surveillance to assess whether the
surveillance data could be used to evaluate trends over time.6
The criteria included consideration of the frequency of data collection, the appropriateness of the population being surveyed,
the consistency over time of the surveillance sites and groups
and the coverage of the groups under surveillance.6,7 Data
obtained through procedures that met the criteria were then
analysed to determine HIV prevalence and analyse time
trends among subgroups by geographic location. We used
statistical tests for trends in proportions to assess the trends
by year.
The Institutional Review Board of the Kerti Praja Foundation
(YKP), which provides HIV prevention and clinical services to
people at risk of HIV in Denpasar, Bali, provided ethical
approval for this study. The Bali Health Office gave permission
to access, analyse and publish results of the surveys and to
conduct interviews with its surveillance staff.
RESULTS
Based on internal BHO records, serological surveys were conducted in all nine of Bali’s districts in the period 2000–2012.
Information retained in the Health Office was in tabular form,
with numbers tested and numbers found positive recorded by
year, district and population subgroup. Line records of individuals tested were not available, and there was no information on
age or any other characteristics of participants.
Table 2 shows the numbers of samples tested from all population subgroups in Bali between 2000 and 2010. The size of
samples per year and the frequency of sampling seem to be
appropriate. However, as shown in Table 3, the frequency, consistency of sites and representativeness of the samples varied
considerably by year and by district. In virtually all districts,
the serological surveillance focused on prisoners and female
sex workers. Data for a broader set of population subgroups
were available for only Denpasar, the district with the largest
population and the location of the Bali capital, and for only
the years 2009 and 2010. As shown in Figure 1, the prevalence
of HIV in Denpasar was highest in people who injected drugs
(55%, confidence interval [CI] +9.95), followed by waria and
then direct female sex workers. The lowest prevalence in
Denpasar was among pregnant women, with three infections
detected among 790 tests in 2009–2010.
Repeated annual surveys that covered most or all of the study
period with a reasonable annual sample size and that hence
could provide information on time trends were available for
only female sex workers, prisoners and, to a lesser extent,
people who injected drugs. The BHO reports demonstrated
that in Denpasar, samples for direct sex workers were obtained
each year at the same three brothel complexes, and that samples
for indirect workers were taken from all registered ‘traditional
massage parlours’. Similarly, in Tabanan, the same site was
used to obtain specimens from direct sex workers each year.
In other districts, the locations of the sampling of both direct
and indirect sex workers changed from year to year. The
authors sought information from the BHO about the rationale
for choosing specific sites in these districts each year, but
were not able to obtain an explanation.
Sample sizes in each district were determined by the BHO,
based on available budget. At virtually all of the sex work
sites, women were recruited on the basis of their presence at
the time of visit by BHO staff. All women present were
invited to participate until the intended sample size was
achieved (consecutive sampling). From 2006 on, and at only
the Denpasar sites, women were selected using the systematic
random sampling method, with YKP providing the sampling
list and assisting in the field recruitment after having compiled
a field census with the help of pimps and brothel owners prior
to the sero-survey implementation. This methodology was
reported by BHO to have been consistently applied over the
period of the surveys.4
Consistently sampled annual series results for prisoners were
available from most of the districts, with Lapas Kerobokan in
Januraga et al. Sharply rising prevalence of HIV infection in Bali
635
................................................................................................................................................
Table 2
Annual sero-surveys in Bali: numbers tested by population group (2000 –2010)
Year
Population group
0
1
2
3
4
5
6
7
8
9
10
Prisoners
IDU
Gay men
Waria
Indirect FSWs
Direct FSWs
Pregnant women
301
3
583
708
1
584
621
39
42
58
659
288
468
526
524
302
618
661
301
78
72
389
400
390
707
96
148
87
346
496
400
200
227
295
81
262
126
403
65
64
100
564
442
100
8
680
386
277
267
400
395
805
FSW ¼ female sex worker; IDU, intravenous drug user
Table 3
Annual sero-surveys in Bali: numbers tested by population group, district and year (2000 –2010)
Year
District
Population group
0
1
2
3
4
5
6
7
8
9
10
Buleleng
Prisoners
Waria
Direct FSWs
Prisoners
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
IDU
Gay men
Waria
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
IDU
Gay men
Waria
Indirect FSWs
Direct FSWs
Pregnant women
Prisoners
IDU
Indirect FSWs
Direct FSWs
Prisoners
IDU
Prisoners
Indirect FSWs
Direct FSWs
Prisoners
Direct FSWs
78
83
68
81
75
7
63
105
65
8
117
110
85
9
37
76
46
33
19
33
81
79
108
20
36
71
55
50
63
21
50
67
94
72
9
80
117
10
303
15
200
205
200
Jembrana
Tabanan
Badung
Denpasar
Gianyar
Bangli
Klungkung
Karangasem
18
10
3
58
14
2
76
20
43
27
33
43
45
187
353
392
300
55
1
200
96
200
100
100
15
200
19
6
64
200
134
200
100
141
109
150
235
401
218
250
247
250
245
600
46
36
48
45
77
66
59
53
100
149
67
37
33
41
10
31
26
40
12
60
60
8
37
262
403
29
31
25
52
21
400
24
42
51
292
181
295
12
210
202
96
96
66
209
400
400
68
150
100
78
72
231
400
390
66
101
158
48
54
35
68
48
26
17
30
25
37
39
29
40
57
137
11
42
14
24
1
19
11
4
6
18
22
8
3
22
36
FSW ¼ female sex worker; IDU, intravenous drug user
Highlighted data only used in subsequent analyses (see Results and Figure 1)
Badung, the biggest prison in Bali, providing the largest
number of samples. Kerobokan has also been the main prison
in Bali for people incarcerated for offences related to drug
use. Prisoners were recruited at each site on the basis of
random sampling: sample size each year was determined in
advance, after which cell blocks were selected by simple
random sampling and all inmates in each selected block
invited to participate. Again, the methodology was reported
to have been consistent over the period.
In Denpasar District, people who inject drugs were surveyed
during four years of the study period. Recruitment was assisted
by the local non-government organization, Yakeba Foundation,
and participants were recruited using respondent-driven
sampling. The recruitment methods were described by BHO
as being the same each year.
Based on the requirement for consistently collected surveillance data, we limited subsequent statistical analyses of time
trends to data on prisoners from all districts, sex workers
from Denpasar and Tabanan and people who inject drugs
from Denpasar. Figure 1 shows trends among prisoners in
Badung (Kerobokan) and in the other districts. The prevalence
has declined steadily in Kerobokan from 19 (CI +5.59) to 4.3%
636
International Journal of STD & AIDS
Volume 24
August 2013
................................................................................................................................................
Figure 1 HIV prevalence among selected population groups, for Denpasar (2009–2010) and for
districts in which there was a consistently collected annual series
(CI +2.74) over 10 years (P , 0.05), and has been stable at
below 3% in other districts. In contrast, the HIV prevalence
among both direct and indirect female sex workers has
increased steadily. Among direct sex workers, the prevalence
in Denpasar and Tabanan rose from 1% (CI +1.21) to 20%
(CI +3.53) in the 10-year period, while among indirect
workers in Denpasar, in whom there had been no HIV detected
at the start of the period, the prevalence was 7% (CI +3.5) by
the end of 10 years (Figure 1) (P , 0.05). For people who
injected drugs, there was no indication of a change in prevalence over the four years for which surveys were conducted
(P ¼ 0.213).
DISCUSSION
This report is the first detailed epidemiological analysis of the
recent shift in the HIV epidemic in Bali from being predominantly linked to intravenous drug use to primarily affecting
female sex workers. People who inject drugs still have the
highest HIV prevalence in Bali, but it has remained stable
over the last decade. In addition, despite the strong association
between injecting drugs and incarceration,8 HIV prevalence
among prison inmates appears to be decreasing. This decline
may reflect a change in the prison population, the impact
of harm reduction programmes or both.8 In Denpasar and
Badung there are more than five centres implementing harm
reduction programmes, run by both government and nongovernment agencies. In Kerobokan prison itself, a harm
reduction programme began in 2001, with a VCT programme
commencing in 2004.8 Furthermore, there is evidence that the
population of people who inject is itself decreasing in size,
with a recent study estimating the number in Bali being
700 –800, compared with 2500 people in 2003.9,10 It is possible
that the stable level of HIV infection reflects sampling of an
ageing and diminishing cohort of people who inject drugs.
Based on the analyses reported in this paper, when restricting
time trend assessment to consistently sampled sites, it appears
that the increase of HIV prevalence among women engaged in
sex work is real and substantial. Rising rates of HIV in this
population are an important public health concern, for the
women themselves, for their male sexual partners and for
other women who are partners of these men.2,11,12 The Bali
AIDS Commission in 2007 reported almost 3000 direct female
sex workers working in brothel complexes in Bali, with most
in Denpasar.13 The Ministry of Health in 2006 estimated that
more than 82,000 men were clients of brothel-based sex
workers and 25,000 were clients of other sex workers in Bali.
Apart from the serological surveys, the only alternative information on HIV prevalence in populations at higher risk has
come from the Integrated Behavioural and Biological Survey
(IBBS) conducted in 2007 in 11 Indonesian provinces. This
survey, which included 250 brothel-based female sex workers
in Bali, found that the province had the second highest HIV
prevalence for this population, 14% (CI +4.3),14 a figure comparable with the estimate of 15% (CI +4.34) from the serological sero-survey in the same year based on Denpasar and
Tabanan sites. The IBBS 2007 report also showed that consistent
condom use among sex workers in Bali was low, and that the
Bali workers had the largest number of clients per week
among workers in the IBBS provinces.14,15
Based on sero-surveys conducted primarily in Denpasar
District, HIV sero-prevalence among waria and gay men in
Bali is already high. According to behavioural surveys, both
groups engage in sex work, with a higher percentage among
warias.2,14 – 16 In Bali, a recent study estimated that there were
between 430 and 900 waria and 12,000 gay men living in
Denpasar and Badung districts.17 As in many developing
countries, these populations can be hard to reach for prevention
programmes, which may be opposed by religious and other
social opinion leaders. In light of the results of our study,
more importance should be placed on interventions to
prevent HIV transmission in these groups.5
Under WHO-UNAIDS guidelines, if HIV prevalence among
at least one population group is consistently above 5% and
below 1% in the general adult population, the HIV epidemic
is ‘concentrated’, while if prevalence has reached 1% in the
general adult population, then the epidemic is considered to
be ‘generalized’.18 However, it is recognized that this classification should be applied with care, as in most countries HIV
Januraga et al. Sharply rising prevalence of HIV infection in Bali
637
................................................................................................................................................
prevalence among the general adult population is estimated
using HIV prevalence among pregnant women,19 which can
differ substantially from estimates derived from general adult
population surveys.20
In Denpasar, all pregnant women tested were seen at
primary health centres facilities operated by the government.
Since many pregnant women also seek antenatal care from
other facilities, mostly private, the sample of women surveyed
may not be representative.18,21 A PMTCT programme run by
a local NGO in the same years reported HIV infection in 1.2%
(CI +1.4) of pregnant women 2009 and in 0.87% (CI +.85)
of pregnant women in 201022 on the basis of 458 tested in 2010.
Our detailed examination of the sero-survey data indicates
several ways in which their quality could be improved. First,
survey results should be recorded and retained in line record
form, and consideration given to including age, at least, as
an additional field for each person in the survey. Having
sufficient numbers of participants at each site for each round,
and consistent sampling of sites over time, would ensure
the consistency and representativeness of survey results.
Increased numbers of participants would provide the possibility of analysing prevalence by age subgroups, supplying
information that would provide a better understanding of
epidemic dynamics.
To further inform and understand the epidemic, it would
also be helpful to add behavioural questions to the sero-surveys.
These would provide indicators that could be used to monitor
the impact of prevention programmes.18 – 20,23,24 The national
IBBS, run by the central government, has provided useful information regarding epidemic progress nationally, but it is undertaken with long time intervals between rounds and does not
specifically address the epidemic at the provincial level in
Indonesia. The IBBS could be adapted to meet local needs
and research questions. Ideally, the IBBS and local surveillance
system could be better integrated to prevent duplication of
effort and improve efficiency.
Since the surveillance findings indicate that the epidemic
is being driven by unsafe sexual behaviours, more research
on social and sexual networks is needed.25 Ethnographic
and qualitative studies can provide a better understanding of
network structures and how they relate to epidemic patterns,
and can assist in identifying which interventions are appropriate for each population.26
Finally, the quality and value of the surveillance system
would be enhanced by the provision of local human resources
to plan, implement and evaluate its activities. Capacity building in the methods of surveillance and allocation of human
resources with responsibility for design and analysis of
surveys are critical steps on this pathway.23
ACKNOWLEDGEMENTS
We would like to acknowledge our colleagues at the Bali
Health Office, especially Dr Nyoman Subrata and Dr Agus
Suryadinata, for trusting us with and sharing their data for
this study. We also offer our appreciation to the staff of
Badung and Denpasar Health Offices for their willingness
to help us validate the data. This project was carried out
with support from the Australian Agency for International
Development. JMK is a National Health and Medical
Research Council Senior Principal Research Fellow.
Competing interests: None declared.
REFERENCES
1 MOH of Indonesia. Mathematic Model of HIV Epidemic in Indonesia 2008 –2014.
Jakarta: Ministry of Health Of Indonesia, 2008
2 Riono P, Jazant S. The current situation of the HIV/AIDS epidemic in
Indonesia. AIDS Educ Prev 2004;16(Suppl. A):78 –90
3 MOH of Indonesia. HIV-AIDS Data Update; Second Quater 2012. Jakarta:
Ministry of Health of Indonesia, 2012
4 Bali Health Office. Laporan Hasil Pelaksanaan Serosurvei STS dan HIV di Provinsi
Bali tahun 2000 –2009 (Report of Bali Province’s sero-surveys results, year
2000–2009). Denpasar: Bali Health office, 2009
5 Pisani E, Girault P, Gultom M, et al. HIV, syphilis infection, and sexual
practices among transgenders, male sex workers, and other men who have sex
with men in Jakarta, Indonesia. Sex Transm Infect 2004;80:536
6 UNAIDS/WHO Working Group on global HIV/AIDS and STI surveillance.
Guidelines for Second Generation HIV Surveillance. Geneva: UNAIDS/WHO,
2000
7 Garcia-Calleja J, Zaniewski E, Ghys P, Stanecki K, Walker N. A global analysis
of trends in the quality of HIV sero-surveillance. Sex Transm Infect
2004;80(Suppl. 1):i25
8 Hartawan A, Sawitri A, Septarini W. Survei Perilaku Berisiko dan Perilaku
Pencegahan Tertular HIV di Lapas Kerobokan, Denpasar, Bali. Denpasar: Lapas
Kerobokan, 2009
9 Sawitri AAS, Blogg J, Angela R. Estimating the number of the people who
inject drugs in Bali, 2010. Drug Alcohol Rev 2012;31:813 –7
10 Sumantera I, Wirawan DN, Masmini N, Gerong L. Estimasi jumlah pemakai
narkoba suntik atau IDU (injecting drug users) di propinsi Bali [An estimation of
number of injecting drug users in Bali]. Jakarta: Indonesia HIV/AIDS Prevention
and Care Project, 2003
11 Alary M, Lowndes CM. The central role of clients of female sex workers in the
dynamics of heterosexual HIV transmission in sub-Saharan Africa. AIDS
2004;18:945– 7
12 Hesketh T, Zhang J, Qiang DJ. HIV knowledge and risk behaviour of female
sex workers in Yunnan Province, China: potential as bridging groups to the
general population. AIDS Care 2005;17:958– 66
13 KPAD Bali. Estmisasi Jumlah ODHA di Bali. Denpasar: KPAD Bali, 2007
14 MOH of Indonesia. Integrated Biological - Behavioral Surveillance of
Most-at-Risk-Groups (MARG). Jakarta: Ministry of Health Republic Indonesia,
2007
15 Prabawanti C, Bollen L, Palupy R, et al. HIV, Sexually transmitted infections,
and sexual risk behavior among transgenders in Indonesia. AIDS Behav
2010:1 –11
16 Joesoef M, Gultom M, Irana I, et al. High rates of sexually transmitted diseases
among male transvestites in Jakarta, Indonesia. Int J STD AIDS 2003;14:609
17 MOH of Indonesia. Estimasi Jumlah Populasi Kunci di Indonesia tahun 2012
(Estimation of Key Populations Numbers in Indonesia 2012). Jakarta: Ministry of
Health of Indonesia, 2012
18 WHO/UNAIDS. Guidelines for second generation HIV Surveillance. 2000
19 Lyerla R, Gouws E, Garcia-Calleja JM. The quality of sero-surveillance in
low- and middle-income countries: status and trends through 2007. Sex Transm
Infect 2008;84(Suppl. 1):i85 – 91
20 Rehle T, Lazzari S, Dallabetta G, Asamoah-Odei E. Second-generation HIV
surveillance: better data for decision-making. Bull World Health Organ
2004;82:121– 7
21 CDC. Program Operations Guidelines for STD Prevention Surveillance and Data
Management. 2010. See http://www.cdc.gov/STD/Program/surveillance/
4-PGsurveillance.htm#sentinel (last checked 15 March 2010)
22 Wulandari LPL, Lubis D, Wirawan A. HIV prevalence among pregnant
mother in Bali, are we sitting on a time bomb. In: ICAAP 10, Busan, 2011
23 Diaz T, De Cock K, Brown T, Ghys PD, Boerma J. New strategies for HIV
surveillance in resource-constrained settings: an overview. AIDS 2005;19:S1
24 Garnett G, Garcia-Calleja J, Rehle T, Gregson S. Behavioural data as an adjunct
to HIV surveillance data. Sex Transm Infect 2006;82(Suppl 1):i57
25 Rothenberg R, Narramore J. Commentary: The relevance of social network
concepts to sexually transmitted disease control. Sex Transm Dis 1996;23:24
26 Ward H. Prevention strategies for sexually transmitted infections: importance
of sexual network structure and epidemic phase. Sex Transm Infect
2007;83(Suppl. 1):i43
(Accepted 14 January 2013)