Siriwasin W, Shaffer N, Roongpisuthipong A, Bhiraleus P, Chinayon P, Wasi C, Singhanati S, Chotpitayasunondh T, Chearskul S, Pokapanichwong W, Mock P, Weniger BG, Mastro TD, for the Bangkok Collaborative Perinatal HIV Transmission Study Group . HIV Prevalence, Risk, and Partner Serodiscordance Among Pregnant Women in Bangkok. JAMA. 1998;280(1):49-54. doi:10.1001/jama.280.1.49
From Rajavithi Hospital, Department of Medical Services, Ministry of Public Health, Bangkok, Thailand (Drs Siriwasin and Chinayon and Ms Singhanati); The HIV/AIDS Collaboration, Nonthaburi, Thailand (Drs Shaffer, Weniger, and Mastro, Ms Pokapanichwong, and Mr Mock); Centers for Disease Control and Prevention, Atlanta, Ga (Drs Shaffer, Weniger, and Mastro); Siriraj Hospital Faculty of Medicine, Mahidol University, Bangkok (Drs Roongpisuthipong, Bhiraleus, Wasi, and Chearskul); and Children's Hospital, Department of Medical Services, Ministry of Public Health, Bangkok (Dr Chotpitayasunondh).
Context.— Most prior studies of the human immunodeficiency virus (HIV) epidemic
in Thailand have focused on commercial sex encounters; however, because the
epidemic increasingly concerns stable heterosexual relationships, determining
risk factors for this form of transmission is warranted.
Objectives.— To determine temporal trends in HIV prevalence, risk factors for HIV
seropositivity, and rates of partner serodiscordance for pregnant women in
Design.— Retrospective review of hospital antenatal clinic HIV test results from
1991 through 1996. Baseline demographic and behavioral risk factors for HIV
were assessed for subjects enrolled from November 1992 through March 1994.
Setting.— Two Bangkok hospitals with routine antenatal clinic HIV counseling and
Participants.— The HIV-positive pregnant women enrolled in a perinatal HIV transmission
study and their partners and HIV-negative pregnant controls.
Results.— From 1991 through 1996, antenatal clinic HIV seroprevalence increased
from 1.0% to 2.3%. On multivariate analysis of data from 342 HIV-positive
and 344 HIV-negative pregnant women, more than 1 lifetime sex partner, history
of a sexually transmitted disease, and a high-risk sex partner were the most
important factors for seropositivity (all P<.001).
Twenty-six percent of partners of HIV-positive women were HIV negative. Women
reporting more than 1 lifetime sex partner were more likely to have an HIV-negative
partner than women reporting only 1 (45% vs 8%; relative risk, 5.5; 95% confidence
interval, 3.2-9.5; P<.001); women reporting no
high-risk behaviors were less likely to have an HIV-negative partner (10%
vs 44%; relative risk, 0.2; 95% confidence interval, 0.1-0.4; P <.001).
Conclusions.— Prevalence of HIV in pregnant women has increased steadily in Bangkok
from 1991 through 1996. Sex with current partners was the only identified
risk exposure for about half (52%) of the HIV-positive women. Although few
HIV-positive pregnant women reported high-risk behaviors, more than 1 lifetime
partner and a partner with high-risk behavior were strong risk factors for
seropositivity. Together with the unexpected finding that one fourth of partners
of seropositive pregnant women were seronegative, these data emphasize that
women in the general population are at risk for HIV because of the risk behavior
of both current and previous partners.
OUTSIDE the United States and western Europe, the human immunodeficiency
virus (HIV) epidemic is largely heterosexual and is growing. The largest percentage
increase in new cases is occurring in Asia and in women of childbearing age.
Within 3 to 4 years, Asia may have the largest number of persons with HIV
In Asia, Thailand has had a relatively well-characterized epidemic.
After an explosive increase in 1988 in HIV seroprevalence in persons who inject
drugs, HIV seroprevalence increased rapidly in female sex workers (FSWs) and
their male clients, and then spread into the general population of women of
childbearing age.4,5 Based on
national sentinel surveillance data, it is estimated that there are 23000
births (2.3%) to HIV-positive women of 1 million annual births in a total
population of 60 million (C. Kunanusont, MD, PhD, Ministry of Public Health
[MOPH], Thailand, oral communication, May 1997). Although data have shown
a decline in HIV seroprevalence in male military recruits6,7
due to behavior changes such as increased condom use and decreased FSW patronage,7- 9 sentinel seroprevalence
data for antenatal women are less clear.10,11
Epidemiologic studies in Thailand have shown that FSW patronage is the
leading HIV risk behavior for men.12- 15
It is widely presumed that most transmission to non-FSW women is from a husband
or a partner and that women are at risk because of the risk behavior of their
partners.16 However, preliminary data from
our study hospitals suggested a higher-than-expected serodiscordance among
male partners of pregnant seropositive women. We thus investigated whether
independent risk factors for infection could be identified in antenatal women
in the general population, and how these risks were related to HIV serodiscordance
among current partners.
The study was conducted in Bangkok at the 2 largest maternity services
in Thailand. Siriraj Hospital is a 2000-bed university teaching hospital and
Rajavithi Hospital is a leading MOPH hospital. At each hospital, about 20000
women register for antenatal care each year and both serve predominantly lower-income
populations in the surrounding communities.
At both study hospitals, as in most hospitals in Thailand, HIV testing
of pregnant women is a routine part of antenatal sexually transmitted disease
(STD) control. Most women are tested for HIV, syphilis, and hepatitis B infection
at first antenatal clinic (ANC) visit and at third trimester. About 85% of
women delivering at the study hospitals register for antenatal care before
their third trimester. The ANC HIV testing was introduced in 1991. Since 1992,
all women registering for antenatal care are offered group HIV pretest counseling
and asked for written consent for confidential HIV testing as part of routine
hospital procedures (routine antenatal testing is offered throughout most
of the country). The HIV testing is performed using enzyme immunoassay, and
positive results are confirmed by particle agglutination or Western blot testing.
Women testing HIV positive are offered individual, confidential posttest counseling.
For enrolled women (below), hospital HIV test results were confirmed by enzyme
immunoassay and Western blot testing at The HIV/AIDS Collaboration laboratory.
After posttest counseling, HIV-positive pregnant women were offered
enrollment (about 45% of all seropositive pregnant women) in a prospective
perinatal transmission study17 if they registered
for antenatal care before their third trimester, resided in the Bangkok area,
had a Thailand national identification card, intended to continue the pregnancy,
planned to deliver at the study hospital, and were planning to have follow-up
care for themselves and their children at the hospital. At enrollment, a pretested
baseline questionnaire was administered covering demographic, obstetric, and
behavioral information for the women and their perception of current partner
risk behavior. After enrollment of a seropositive woman, the next consenting
HIV-negative woman attending the ANC, matched by trimester, was offered enrollment
as a control. Control women were given the same questionnaire but not followed.
At study hospitals, current partners of women testing positive for HIV
or other STD tests are routinely asked to visit the hospital for confidential
counseling and STD testing. Separate or joint confidential counseling by hospital
and study staff is offered to the woman and her partner. Confirmed partner
HIV test results were used for analysis of partner HIV status and serodiscordance.
We considered couples married if they reported themselves as married
according to legal or traditional criteria. Because 99% of both HIV-positive
and HIV-negative women reported being married or having a regular partner, current partner denotes the husband or regular partner
of the woman at enrollment. Sexual partner was defined
as a male partner with whom the woman had had sexual intercourse. Lifetime sex partners was defined as the sum of different men with
whom a woman had had sexual intercourse. Commercial sex
work was defined as exchange of sex for money, and women were considered
as FSWs if they had engaged in commercial sex work. History of STD was based
on reported diagnosis of any STD (unspecified) or syphilis or gonorrhea, specifically.
Hospital HIV test results for first ANC visits were summarized to evaluate
temporal trends. Associations with HIV seropositivity of demographic, obstetric,
and behavioral risk factors were determined by χ2, χ2 for trend, and Fisher exact test (SAS Version 6, SAS Institute Inc,
Cary, NC, and Epi Info Version 6, Centers for Disease Control and Prevention
[CDC], Atlanta, Ga). Continuous data were compared with the Wilcoxon rank
sum test. All factors associated with HIV infection on univariate analysis
at P <.1 were included in unconditional, stepwise
multivariate logistic regression analysis. Continuous variables were dichotomized
for logistic analysis. Two final models were generated to predict women's
seropositivity: the first model included women's behavioral factors; the second
model also included women's reported behaviors of their current partner. In
a separate analysis of seropositive women whose partners' HIV status was known,
relative risk for partner serodiscordance was calculated on the basis of women's
The study protocol was approved by the Thailand MOPH Ethical Review
Committee and the CDC Institutional Review Board. Voluntary, written, informed
consent was obtained from all study participants (except as described).
Nearly complete (>98%) ANC seroprevalence data were available for 1991
through 1996, representing about 20000 antenatal registrants per hospital
per year (1 hospital started routine testing in July 1991). Seroprevalence
was similar at the hospitals (Table 1).
For the 2 hospitals combined, ANC HIV prevalence increased from 1.0% to 2.3%
during 1991 to 1996 (P<.001), an increase from
about 400 to 800 HIV-positive women among those registering for ANC annually.
A total of 342 HIV-positive and 344 HIV-negative pregnant women were
enrolled from November 1992 through March 1994. Most (75%) were enrolled before
their third trimester. Of eligible women asked to enroll, 95% of 360 HIV-positive
and 97% of 355 HIV-negative women participated. One additional HIV-positive
woman did not complete enrollment and one was later excluded because seropositivity
could not be confirmed. For HIV-positive women, reasons for participation
included counseling support, expedited medical care for study visits, and
reimbursement for transportation and medical expenses; reasons for nonparticipation
included not wanting to be part of an HIV study, to sign a consent form, or
to answer personal questions.
As seen in Table 2, compared
with HIV-negative controls, HIV-positive women were younger at time of first
pregnancy, had been with their partner for less time, and were more likely
from a rural area, to have separated from a prior partner, and to be primigravida
and nulliparous. Most women (>95%) were literate, and duration of time in
Bangkok was similar. Most were married and nearly all (except 2 HIV-positive
women) were living with the current partner. Family income was comparable
and consistent with salaries for unskilled work.
Seropositive women had a higher sexual-risk profile than seronegative
women (Table 3). The HIV-positive
women were younger at first sexual intercourse and more likely to have had
more than 1 lifetime sex partner (50% vs 23%), to have been pregnant by more
than 1 partner (among multigravida, 53% vs 27%), and to have an STD history
(22% vs 5%). Commercial sex work, although uncommon (10% vs 2%), was strongly
associated with seropositivity. Injection drug use was rare (1% in HIV-positive
women), but having a sex partner who used injection drugs was associated with
More than 1 lifetime sex partner was associated with seropositivity,
and for greater analytic precision, partner number was categorized as 1, 2,
or more than 2 partners (Table 3).
Odds ratios for seropositivity increased from 2.7 with 2 lifetime sex partners
to 6.9 with more than 2. Excluding FSWs, odds ratios increased from 2.6 for
2 lifetime partners to 4.5 for more than 2.
Past contraceptive use was similar for HIV-positive and HIV-negative
women (Table 3). About two thirds
reported use of oral contraceptives, and one fifth, injectable contraception
and condoms as contraception. According to women's perceptions, partners of
HIV-positive women were more likely to have behavioral risks for HIV (eg,
sex with an FSW in past 5 years, STD history, and sex with an FSW while married).
Factors associated with HIV seropositivity on univariate analysis were
analyzed by multivariate logistic regression (Table 4). Model 1 includes women's behavioral risk factors; model
2 also includes behavioral risk factors of male partners (reported by the
women). In both models, more than 2 lifetime sex partners for the women was
most strongly associated with seropositivity, while 2 lifetime sex partners
was also an independent risk factor. In model 2, several women's behavioral
factors dropped out (STD history, partner who uses injection drugs, and with
partner less than 1.5 years), and were replaced by 2 partner behavioral risk
factors: STD history and sex with FSWs in past 5 years. Nulliparity and migration
from rural area were also statistically significant in both models. Commercial
sex work and younger age did not change final models.
Of 307 HIV-positive women (90%) with current partners tested at the
study hospitals, 81 partners (26.4%) were HIV negative. Concordant couples
were together longer than discordant couples (mean, 2.2 vs 1.9 years, P=.04). Partner serodiscordance was evaluated by women's
risk exposure (Table 5). Women
reporting more than 1 lifetime sex partner were more likely to have a serodiscordant
partner than those reporting 1 (45% vs 8%; relative risk, 5.47). The same
association was found when excluding FSWs, with slightly lower relative risk.
Female sex workers were more likely than non-FSWs to have a serodiscordant
partner. About half (52%) of women did not report any risk apart from sex
with current partners. For these women, only 10% of partners were HIV negative
vs 44% of partners of women reporting 1 or more risk behaviors.
Seroprevalence of HIV has increased steadily in pregnant women in Bangkok
and sex with current or previous partner is the only identified HIV risk for
most HIV-positive women in ANCs. This study confirms the common assumption
that most Thai women with HIV infection are infected by their husbands, who
bring HIV infection into the home after FSW contact.4,16
However, more women than previously thought have had more than 1 sexual partner,
and multiple partners is a strong risk factor for infection in pregnant women
in the general population.
The hospital prevalence data described herein are based on routine counseling
and testing of about 40000 pregnant women each year. We believe they are a
reliable indicator of HIV prevalence for the general antenatal population.
During the past 6 years, ANC HIV seroprevalence at the 2 largest maternity
services in Bangkok has increased from 1% to 2.3%. Our findings are consistent
with national surveillance data showing increases in ANC seroprevalence in
most regions; 1995 median prevalence rates were estimated at 2.7% in central
Thailand and 2.3% nationwide, double 1992 estimates.10,11
Seroprevalence rates for antenatal women and male military recruits are thought
to reflect most closely the rates in the general population. In Bangkok, prevalence
rates for 21-year-old military recruits were 2.9% in 1992 and 2.6% in 1994.6- 8 However, our data show
that prevalence in antenatal women continues to rise in Bangkok. One explanation,
suggested by our study, is that young women may have partners several years
older than themselves. Thus, prevalence in antenatal women may increase for
several years before reflecting falling prevalence rates in young men.
Few study women could be classified as practicing high-risk behaviors,
such as drug use, commercial sex, or having many partners. Although most were
infected via sex with partners, more women than commonly thought were likely
infected by a previous partner. Demographic and behavioral risk profiles of
most HIV-positive antenatal women were modest: young, recently married, nulliparous,
and with 1 or 2 previous partners. Despite the lack of high-risk behavior
according to traditional criteria, we show that even modestly increased sexual
exposure was a risk factor for infection. In the Bangkok setting of seroprevalence
rates of 2% to 5% in young men, women who are monogamous but who have had
1 or more previous partners are at demonstrably increased risk for infection.
In our multivariate analysis of women's risk factors, having 2 lifetime partners
(1 previous partner) increased the odds ratio for HIV infection to almost
3, and having more than 2 increased the odds ratio to nearly 6. This risk
persisted even when we tried to account for the current partner's risk behavior.
Although traditional Thai cultural values emphasize premarital abstinence
for women, 23% of HIV-negative and 50% of HIV-positive women in our sample
reported more than 1 lifetime partner. This is much higher than reported in
a national survey done in 1990 (less than 5% reported more than 1 partner),16 and in a recent MOPH survey (6% to 8% reported more
than 1 partner),18 indicating that the number
of sex partners may be commonly underreported.16
In addition, there may be differences in urban areas with large in-migrations.
Traditional sexual patterns in women may be changing rapidly while the HIV
epidemic is spreading. Although our study involved HIV-positive antenatal
women enrolled in a prospective perinatal transmission study, we believe the
study population is representative of the hospital catchment area because
enrollment criteria were largely geographic, registration rates were high,
and controls were drawn systematically from the clinic.
Elsewhere, in Kigali, Rwanda, in 1988, where HIV prevalence in women
of childbearing age was 32%, one third of women reported more than 1 lifetime
partner and were at increased infection risk.19
In Belle Glade, Fla, during 1989 to 1991, where antenatal seroprevalence was
5%, two thirds of women reported more than 1 lifetime partner and also were
at increased risk.20
One fourth of the HIV-positive pregnant women in this study had an HIV-negative
partner. This continues to be a consistent finding at the study hospitals.
Despite many reports on HIV testing of pregnant women worldwide, there have
been few reports of HIV test results of their partners. In Thailand, it is
commonly assumed that in a given relationship men are the index cases. However,
the male serodiscordance data indicate that even in an epidemic largely characterized
by transmission from FSWs to male clients to regular partners, it cannot be
assumed the male partner is the index case, even when both partners are seropositive.
In terms of biological risk, it is not surprising that some male partners
in this study were HIV negative. Female-to-male HIV transmission is relatively
Apart from biologic issues, our finding of a 26% male serodiscordance
rate for antenatal women with HIV infection raises complex counseling issues
and indicates additional stresses of HIV on the family unit.26
At these study hospitals, women with HIV infection and their partners were
counseled separately and were offered joint counseling; both concordant and
serodiscordant couples were encouraged to discuss results with each other.
Although partner testing provides important information to the individual
and to the family, a better understanding of the impact of this testing27 and how best to provide counseling support is needed.
Although the 100% condom campaign in Thailand has been remarkably successful
in increasing condom use in commercial sex encounters,28
preventing HIV transmission between partners will be more challenging,9 especially in young couples desiring children. Sexually
active persons, including adolescents, should be educated about HIV risks,
encouraged to know their partner's and their own HIV status, and encouraged
to avoid high-risk sex and to use condoms as a primary form of STD and birth
control. These precautions should not be limited to commercial sex exchanges.
Indeed, commercial sex interventions must not inadvertently encourage increased
noncommercial casual, unprotected sex.16 General
intervention strategies must acknowledge that young women in rapidly changing
cultures such as in Thailand are likely to be more sexually active than reported.
Although raising complex social issues, antenatal HIV counseling and testing
programs, along with partner counseling and testing, are valuable for patient
care, preventive education, and monitoring of the heterosexual HIV epidemic
in the general population.