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Preventing Mother-to-Child Transmission of HIV in Vietnam:

An Assessment of Progress and Future Directions


by Chinh T. Le,a Thanh Tung Vu,b Minh Chau Luu,b Thi Nhan Do,b Thu-Ha Dinh,c and Mary L. Kambc
a
This study was conducted while the author was contracted by the Global AIDS Program (GAP), Vietnam Office, Centers for
Disease Control and Prevention (CDC), Hanoi, Vietnam. Current affiliation: Benton County Department of Public Health,
OR 97333, USA
b
Ministry of Health, LIFE-GAP Office, Socialist Republic of Vietnam
c
GAP Vietnam Office, CDC, Hanoi, and currently with the Division of Sexually Transmitted Disease Prevention, CDC,
Atlanta, GA 30333, USA

Summary
Preliminary to the development a new program supporting perinatal HIV prevention, this assessment
was conducted to evaluate Vietnam’s national prevention of mother-to-child HIV transmission
(PMTCT) program by estimating HIV prevalence among prenatal women and analyzing the healthcare
system capacity to deliver services. In 2002–03, a technical team reviewed existing national and local
surveillance and program data and conducted on-site interviews and observations at maternal-child
health (MCH) programs in the seven provinces with highest HIV rates. The team found that despite
high (85%) prenatal service utilization and widespread availability of HIV testing and dissemination of
prevention protocols, few HIV-infected mothers were identified in time to allow effective perinatal HIV
prevention. Program deficits clustered around the general areas of provider misunderstanding of
occupational HIV risk and MTCT, impractical PMTCT policies, and practices hampering effective use
of prevention and treatment protocols. Existing problems were significant but modifiable, and will
require implementation of practical and appropriate guidelines, enhanced clinical and laboratory
capacity, and continued program management and monitoring.

Key words: Prevention of mother-to-child transmission of HIV, Vietnam, perinatal HIV testing and
prophylaxis.

Introduction
In 2005, 2.3 million children under 15 years of age
were infected with HIV worldwide, most perinatally
[1]. Global attention around perinatal HIV has
Acknowledgements
focused predominantly on sub-Saharan Africa,
This article was funded by U.S. Centers for Disease where the epidemic is most severe. However, Asian
Control, Global AIDS Program. The authors thank nations with low community HIV prevalence but
the clinical and public health staff at the provinces large populations contribute high numbers of global
visited and government officials who participated in infections [2, 3]. In Vietnam, by 2003 more than
the interviews and provided documents and reports. 245 000 persons were estimated to have been HIV
We thank Mr Patrick Chong for his assistance in the infected, including 2500 children infected perinatally
evaluation, and Drs Nathan Shaffer and Mitchell [4]. Initially driven by injection drug use (60–70% of
Wolfe, Mr Richard Noegel and Ms Jennifer Mark reported HIV cases) and sex trade, HIV was increas-
for their review of the manuscript and helpful
ingly observed to affect other population groups [5].
suggestions.
Accordingly, Vietnam’s national AIDS strategy
Correspondence: Mary L. Kamb, Centers for Disease recognized not only the importance of interventions
Control and Prevention (CDC), Division of STD for persons most vulnerable to HIV but also
Prevention, 1600 Clifton Rd., N.E. Mailstop E-02, promoted a program on preventing mother-to-child
Atlanta, GA 30333, USA. Tel.: þ404-639-8632;
Fax: þ404-639-8609. E-mail: <mkamb@cdc.gov>. transmission of HIV (PMTCT) integrated into the

The findings and conclusions in this paper and those of the existing maternal-child health (MCH) program [5–6].
authors do not necessarily represent the views of the Centers Despite a large population (82 million) of whom
for Disease Control and Prevention. 75% live in rural areas, Vietnam’s public health

ß Published by Oxford University Press, 2008. 225


doi:10.1093/tropej/fmm112 Advance Access Published on 22 January 2008

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TABLE 1 infants and is the focus of most PMTCT programs.


Mother-child health (MCH) performance indicators, As part of a needs assessment of PMTCT services,
Vietnam, 1997–2000 Vietnam Ministry of Health (MOH), with support
from the U.S. Centers for Disease Control and
% of pregnancies that received no prenatal care: Prevention, sought to estimate the extent of perinatal
National average: 28.3% (rural ¼ 31%, HIV infections and to evaluate the country’s capacity
urban ¼ 12.7%) to deliver PMTCT-specific services within the exist-
% of pregnancies that received three or more prenatal ing MCH system. This was the first assessment of its
visits:
National average: 34.5% (rural ¼ 29.2%,
kind in Vietnam, and serves as a baseline to evaluate
urban ¼ 66.6%) the subsequent, enhanced national PMTCT program
% of women who gave birth at home: under the MOH.
National average: 38.3% (rural ¼ 43%,
urban ¼ 8%) Methods
% of pregnant women with anemia: 30% In 2002–03 a team of pediatric and public health
Fetal and stillbirth deaths: 7 per 1000 researchers reviewed existing HIV-related reports
pregnancies from MOH including national HIV Sentinel
Infant mortality 36.7 per 1000 Surveillance (HIV SS) data (1994–2002), MCH
(age 1–12 months): live births statistics (1997–2002), and official documents and
% of newborns with 7.3%
birth weight <2500 gm:
policies [4–7, 10–17]. Team members visited public
Maternal mortality rate: 95 per 100 000 health offices and the main obstetrical hospitals
births (n ¼ 8) in the seven cities or provinces (Fig. 1) with
highest HIV case rates. At each site, the team
interviewed health officials, laboratory technicians,
counselors and obstetric and pediatric practitioners
system is well developed and extensive, reaching rural about local HIV trends, access and use of PMTCT
and urban areas in every province. Basic primary services, their own analysis of local issues (e.g., staff
health care services are delivered at the commune training, capacities, attitudes on HIV and PMTCT),
level, and an estimated 92% of villages have a health and HIV testing strategies used, whether routine (i.e.,
center [6–8]. By 1982, 85% of pregnant women had at ‘‘opt out’’ testing for all patients unless they explicitly
least one antenatal visit; and by 2000, 56% of refused), voluntary opt-in (i.e., testing those who
communes were served by a physician, 88% by an explicitly accepted), universal mandatory (i.e., testing
assistant or midwife, and 77% of communes had a for all patients and not involving consent), or
trained health worker delivering basic preventive selective (i.e., targeted testing based on perceived
interventions [6–9]. Most (96%) deliveries were patient risk). The investigators also directly observed
attended, at least by traditional birth assistants if not procedures at facilities. The eight provincial hospitals
midwives [8]. However, essential supplies were often visited served about a third of the total deliveries in
limited: In 2000, only 80% of commune health centers each province; another third took place in district or
had access to electricity, 50% to an infant scale, 41% commune health centers, and the remaining third
to a gynecological exam light, 15% to piped water, occurred at home (Table 1).
and 12% to a telephone [6–8]. The infrastructure and Team members also met with officials from the
human capacity were superior at the district and national institutions, local non-governmental orga-
provincial levels, although quality varied [7]. National nizations, and international agencies who currently
performance indicators for 1997–2001 (Table 1) or had participated in PMTCT projects in Vietnam
indicated that MCH care in Vietnam lagged behind (UNAIDS, WHO, and UNCEF) [18]. Relevant data
wealthier Thailand and Malaysia, but functioned were compiled, including current policies, practices
more effectively than other resource-limited countries and program effectiveness indicators (e.g., rates of
in Southeast Asia and elsewhere [6–8]. prenatal HIV testing and counseling; HIV screening
The World Health Organization (WHO) has at delivery; dose and frequency of HIV antiretroviral
recommended that national PMTCT programs (ARV) prophylaxis for infected women and their
include three concurrent strategies: (1) prevention infants, and follow-up care). Descriptive observa-
of primary HIV infection among childbearing tions were reported if providing valuable information
women; (2) prevention of unwanted pregnancy about access and quality of local PMTCT services.
among HIV-infected women; and (3) interventions
preventing HIV transmission from infected mothers Results
to infants [1, 4]. The first two strategies are typically In order to evaluate the nation’s MCH system
achieved through behavioral change and contra- capacity to provide effective PMTCT interventions,
ception approaches, while the third involves deliver- the assessment findings focused on two areas:
ing services for HIV-infected women and their (1) HIV case identification and completeness of

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TABLE 2
HIV prevalence among pregnant women screened
during antenatal visits as part of National HIV
Sentinel Surveillance, Vietnam, 1994–2002

Year No. No. HIV()/ Prevalence


provincesa No. screened (range)

1994 10 2/12 542 0.02 (0–0.13)


1995 10 9/13 586 0.07 (0–0.38)
1996 12 8/21 500 0.04 (0–0.19)
1997 20 22/18 119 0.12 (0–1.22)
1998 20 13/15 655 0.08 (0–0.96)
1999 20 13/16 172 0.08 (0–0.38)
2000 20 31/15 853 0.20 (0–1.00)
2001 31 80/22 310 0.36 (0–1.92)
2002 31 72/21 486 0.30 (0–1.00)
a
Number of Vietnam’s 61 provinces or urban areas
participating in National HIV Sentinel Surveillance
activities during that year.

among women receiving antenatal services increased


from 0.02% (range, 0–0.13%) in 1994 to 0.30%
(range, 0–1.0%) in 2002, with some provinces
reporting near 1% prevalence (Table 2). Antenatal
HIV SS prevalence ranged from 0.38 to 0.88% in the
seven provinces covered in the evaluation. With an
estimated of 1.5–2 million births per year, national
prevalence data suggested up to 6000 infants may
have been exposed to HIV at birth in 2002, although
this estimate would be skewed high if participating
provinces had higher HIV prevalence than non-
participating provinces.
FIG. 1. Map of Vietnam, showing the provinces and Six of the eight major hospitals visited conducted
cities where PMTCT programs were assessed in 2002: universal mandatory HIV testing at time of delivery.
Ho Chi Minh City (population 8.5 million and Seropositivity rates at those facilities ranging from
largest urban area), Ha Noi (capital city; 3.5 million), 0.34 to 1.1% in 2002 (Table 3), generally consistent
Hai Phong city (1.5 million), Quang Ninh province with provincial HIV SS estimates, suggesting identi-
(1.1 million), An Giang province (2.1 million), Can fication of most HIV cases among pregnant women
Tho province (2.5 million), and Kien Giang province delivering at these facilities. The other two of the
(1.6 million). hospitals used alternative testing strategies during
prenatal visits: An Giang employed a selective
strategy, and Can Tho routinely offered voluntary
reporting of HIV infection among pregnant women, opt-in testing using a voluntary counseling and
and (2) adequacy of the existing program at testing (VCT) approach. At these two sites, compar-
preventing perinatal HIV transmission. At the time ison of antenatal infection estimates by provincial
of the assessment, highly active ARV therapy HIV SS estimates and by facilities suggested that
(HAART) was not yet available in Vietnam, and their testing strategies may have missed many
thus although referrals for clinical evaluation and infected mothers.
follow-up were addressed, provision of HIV therapy Interviewed healthcare workers reported that
was not evaluated. although shortages of testing commodities sometimes
occurred, HIV testing services were generally avail-
Case identification and reporting of perinatal HIV able at all antenatal and delivery sites (confirmed by
Established in 1994, Vietnam’s HIV SS collects site visits). Typically, HIV Enzyme Immunoassay
seroprevalence data for subpopulations of varying (EIA) tests were performed locally, with positive
HIV risk, one such group being antenatal women. results forwarded to specific regional laboratories
By 2001, 31 of all 61 provinces participated in licensed for confirmatory tests. Test costs varied
HIV SS activities. Nationwide, HIV prevalence among the sites, and were typically charged to the

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TABLE 3
HIV positivity ratesa among pregnant women delivering at eight major hospitals, Vietnam, 2000–2002

Location (time period) Testing # women HIV


strategyb tested positive (%)

Quang Ninh General Hospital


(Jan–Dec 2000) Selective 642 2.3
(Jan–Dec 2001) Universal mandatory 2080 1.2
(Jan–mid-Oct 2002) Universal mandatory 2090 1.1
Hai Phong Obstetrics and Gynecology Hospital
(Jan–Dec 2000) Universal mandatory 8750 0.18
(Jan–Dec 2001) Universal mandatory 8543 0.32
(Jan–Sept 2002) Universal mandatory 9531 0.34
Ho Chi Minh City (two largest obstetrical hospitals)
Hung Vuong (Jan–Dec 2000) Universal mandatory 23 568 0.35
Hung Vuong (Jan–Dec 2001) Universal mandatory 22 109 0.68
Hung Vuong (Jan–Aug 2002) Universal mandatory 13 690 1.06
Tu Du (Jan–Dec 2000) Universal mandatory 37 530 0.31
Tu Du (Jan–Dec 2001) Universal mandatory 35 390 0.43
Tu Du (Jan–Sept 2002) Universal mandatory 28 842 0.51
Ha Noi, Maternity C Hospital
(Jan–Dec 2002) Universal mandatory 10 171 0.43
Kien Giang, Rach Gia General Hospital
(Jan–Dec 2001) Universal mandatory 4431 0.45
(Jan–Oct 2002) Universal mandatory 3637 0.60
An Giang General Hospital
(Jan 2000–Oct 2002) Selective NAc NAc
Can Tho Provincial Hospital
(Jan 2002–Oct 2002) Voluntary opt-in 4679 0.1
a
HIV-positive test at either a prenatal visit or delivery.
b
See text for definition of testing strategies. Hospitals that conducted ‘‘universal mandatory’’ testing obtained HIV test at the
time of labor and delivery.
c
Data not available on total number tested. Thirty-three HIV-positive pregnant women were identified at this site by selective
testing.

patients. Cost and patients’ refusal were cited by indicating substantial underreporting of identified
providers as the main reasons for low prenatal testing cases to the national HIV program.
rate, although patients generally paid out-of-pocket
for mandatory testing done at delivery. Of note, any PMTCT program
HIV testing was primarily done to ‘‘protect health Review of policies and protocols indicated the HIV
workers’’ rather than for perinatal HIV prevention, national program focused primarily on delivering
and mothers screening positive were commonly basic information-education-communication (IEC)
isolated along with their infants away from other messages [11], which reached 80% of the population,
patients. In fact, in most hospitals, women were not reportedly [7]. MOH had developed handbooks and
informed of positive test results by hospital staff as protocols for counseling, prevention [11–15], and
this responsibility fell to local health departments clinical protocols based on those of other countries
where confirmatory test results were performed. [16] (e.g., use of CD4 cell counts, viral load mea-
MOH statistics indicated that from 1996 to 1999, surements, and antimicrobial and ARV agents
of the expected several thousand cases, a total of unavailable in most of Vietnam). One of the goals
217 pregnant women nationwide were reported as of the national AIDS program was to implement an
HIV-infected. For the years 2000 and 2001, there effective PMTCT program using VCT, and zidovu-
were, respectively, 108 and 182 HIV-positive mothers dine and nevirapine prophylaxis [12, 13]. The team
reported to the MOH nationwide [5, 6]. Yet for the found widespread dissemination of protocols but
same 2-year period, local data indicated 605 HIV- observed that the understanding of these varied
positive women had delivered at the 6 hospitals among patients and even among health providers.
visited that provided universal testing at delivery, Monitoring implementation of the national

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TABLE 4
Prenatal HIV testing and ARV administration to positive mothers and infants at eight major hospitals,
Vietnam, 2000–2002

Facility/Location (time period) No. mothers given ARVs/No. No. infants given
HIV mothers delivering ARVc/No. HIV mothers

Quang Ninh Provincial Hospital


(Jan–Dec 2000) 8/8 8/8 (100%)
(Jan 2001–Oct 2002) 34/42 (81.0%) 1/42 (2.4%)
Hai Phong City Maternity Hospital
(Jan 2000–Oct 2002) 32/58 (55.2%) 13/58 (22.4%)
Ho Chi Minh City, Hung Vuong Maternity Hospital
(Jan 2000–Oct 2002) 53/241 (22.0%) 10/241 (4.1%)
Ho Chi Minh City, Tu Du Maternity Hospital
(Jan 2000–Oct 2002) 89/425 (20.9%) 5/425 (1.2%)
Ha Noi, Maternity Hospital C
(Jan–Oct 2002) 37/44 (84.1%) NAa/44
Kien Giang, Rach Gia Provincial Hospital
(2001–2002) 0/39 0/39
An Giang General Hospital
(Jan 2000–Oct 2002) 0/33 0/33
Can Tho Provincial Hospital
(Jan 2002–Oct 2002) 0/5 0/5
Total 253/895 (28.3%) 37/851 (4.3%)b
a
NA: data not available.
b
Excludes denominator data from Ha Noi as numerator data were not available.
c
Per national guidelines.

guidelines was limited because accountability pro- identified several barriers to effective prophylaxis:
cesses for the provincial and national systems were Zidovudine was unavailable for infants in oral
not clearly documented [18]. syrup form. Supplies of nevirapine were often limited
National goals were ambitious given available and hard to access quickly. But most importantly,
resources. The national budget for PMTCT activities per MOH policy, provision of ARV prophylaxis
ranged from 120 to 810 million VN Dong (USD required a positive HIV test be confirmed by desig-
8000–54 000) annually. During 2000, the budget was nated laboratories (35 were available by 2002,
500 million VN Dong, (USD 34 000), mainly spent nationwide) and confirmatory test results generally
on IEC activities [9]. Although international donors took at least a week (and sometimes several weeks) to
provided support to some aspects of the national return. Consequently, very few women identified as
AIDS program, few were involved in PMTCT HIV-positive during late pregnancy (and none during
projects. An ‘‘Action Plan’’ developed in 2000 by labor and delivery) were eligible for therapy. Thus,
MOH, with international support, outlined a com- even where ARV prophylactic drugs were available,
prehensive PMTCT program but did not define they were often not provided.
resources to support it [17]. Under this collaborative Postpartum, HIV-positive mothers were advised
international effort, only two PMTCT projects were not to breastfeed their infants [13], who were given
conducted: UNAIDS donated a limited supply formula feeding, but only for the duration of hospital
of ARV drugs, and UNICEF assisted in a survey stay. Formula was unaffordable for most families,
among pregnant women, community leaders, considering its cost of the equivalent of USD 20 per
and health providers on PMTCT knowledge and month in 2002, and the average monthly income
attitudes [7]. of USD 35 [9, 10]. Furthermore, most mother–child
Our survey revealed that for HIV positive mothers, pairs screening HIV positive did not receive
provision of prenatal or intrapartum ARV prophy- follow-up care for a variety of reasons: about 20%
laxis was sporadic despite its recommendation in of families gave an incorrect address, possibly for
protocols available at all facilities visited (Table 4). fear of discrimination; many returned to distant
During 2000–02, at the 8 hospitals visited, 253 districts or communes where few health workers were
(28.3%) of 895 pregnant women identified as trained in HIV care; some HIV-positive mothers
HIV-positive and 37 (4.1%) infants born to these abandoned their newborns infants, who then
mothers received any ARV drugs. The on-site visits remained in isolation wards without specific

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treatment due to lack of capacity for follow-up Testing accounted for the largest cost of any
testing or available ARVs in infant formulations. PMTCT program, and could be consider too
As a result, actual data on mother-to-child HIV costly in this low prevalence epidemic. However,
transmission were neither available at any sites pregnant women in Vietnam were already paying
visited nor nationwide. Provincial public health for a HIV test within the existing system of
officials readily acknowledged deficiencies in the universal mandatory screening at delivery, but
system in several areas [9, 10, 17]. were not receiving personal benefits. The observed
situation suggested that test costs could be
Discussion supported by individual payments when afford-
This assessment of the HIV perinatal situation and able, and subsidized by the government for
PMTCT efforts in Vietnam found that by 2003: (1) families living at or below poverty levels.
perinatal HIV infection was increasing with several 3. Optimizing preventive treatment and follow-up.
provinces nearing 1% antenatal prevalence; (2) HIV A strategy based on confirmation of any initial
testing was widely available, but testing strategies positive test is important in a low prevalence
primarily identified infections at delivery rather than epidemic, but lack of prompt confirmation
during pregnancy; (3) if identified, HIV-positive impaired timely PMTCT. Use of rapid testing
women generally did not receive effective prophylaxis assays in perinatal settings [19–21] would allow
as laboratory capacity and protocols did not allow identification of HIV infections on-site, and
provision of test results quickly enough for interven- rapid initiation of ARV prophylaxis. Routine
tion; and (4) most women identified as HIV-positive provision of test results with counseling, along
and their infants did not receive the clinical and with provision of effective prophylaxis and sup-
supportive follow up needed to ensure adequate care. port for follow-up HIV care is needed to inform
Almost all of these issues were related to systems- women of their HIV status, ensure they receive
level problems amenable to modification. appropriate care, and importantly to help edu-
In Vietnam and elsewhere, failure of PMTCT has cate them on how to minimize risk for HIV
been viewed as fundamentally caused by lack of ARV transmission to their infants and sex partners.
drugs needed for effective intervention. However, Additionally, positive women and infants should
provision of ARVs without effective testing strate- be offered care (and if appropriate, treatment) to
gies, public health system capacity or operational ensure their own health. This would require
support for delivering practical interventions could ensuring adequate supplies of appropriate pro-
waste resources. Four areas were identified, with phylactic drugs and infant formula supplementa-
recommendations made to address to ensure a more tion at central and birthing centers, developing
effective PMTCT program: appropriate delivery protocols and referral sys-
tems, and effective communication with women
1. Educating health care providers about HIV and and between hospitals and local commune
PMTCT. Training and education programs for health centers to reduce stigma around HIV and
providers about HIV transmission and preven- ensure continuity of care. Safe infant-feeding
tion, including ways to (i) reduce discrimination,
options are an area of urgent need for develop-
(ii) prevent occupational exposure through use of
ing world settings, and counseling on the variety
universal precautions and post-exposure prophy-
of possible options and their potential conse-
laxis, and (iii) prevent mother-to-child transmis-
quences should be discussed and options chosen
sion of HIV through prompt case identification
fully supported [22–24]. These options include
and timely prophylactic interventions were iden-
formula feeding when affordable, practice of
tified as priority areas to address.
exclusive breastfeeding for at least 6 months, or
2. Adopting affordable, routine prenatal HIV screen-
provision of HAART during the breastfeeding
ing approaches. For greatest PMTCT impact, HIV
period.
screening strategies would ideally occur during
4. Ongoing program monitoring. The use of standar-
prenatal care (rather than at delivery) and would
dized reporting forms in patient case manage-
use voluntary, routine (opt-out) testing and
ment and drug delivery, with consistent
counseling as a strategy [19]. Such antenatal
monitoring of key indicators such as rates and
screening could start with higher prevalence
timing of prenatal testing, HIV positivity, ade-
areas and be phased in elsewhere based on local
quate and timely prophylaxis, post-partum
or regional epidemiology. Practical approaches
follow-up and perinatal transmission were recom-
(e.g., group counseling, video-based models) that
mended as important for measuring program
explicitly describe the benefits of testing for
quality and effectiveness.
pregnant women and infants are available in
other parts of the world, and could be adapted to This assessment had some limitations. National
Vietnamese culture and healthcare systems. HIV SS covered only half of provinces and

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C. T. LE ET AL.

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