Open Access

HIV sero-discordance among married HIV patients initiating anti-retroviral therapy in northern Vietnam

AIDS Research and Therapy201613:39

DOI: 10.1186/s12981-016-0124-9

Received: 7 June 2016

Accepted: 1 November 2016

Published: 15 November 2016

Abstract

Background

In many countries in Asia, the HIV epidemic is in a concentrated phase, with high prevalence in certain risk groups, such as men who inject drugs. There is also a rapid increase of HIV among women. The latter might be due to high levels of sero-discordant couples and increasing transmission from male to female partners over time.

Methods

All adult married patients initiating antiretroviral treatment at four out-patient clinics in Quang Ninh province in north-eastern Vietnam between 2007 and 2009 were asked to participate in the study. Clinical information was extracted from patients’ records, and a structured questionnaire was used to collect social, demographic and economic data.

Results

Two hundred eighty-eight married patients for whom information on the HIV status of their spouse was available were included in the study. Overall, the sero-discordance rate was 58%. The sero-discordance rate was significantly higher among married males, 71% had spouses not infected, than married females, of whom 18% had spouses not infected. Other factors associated with a high rate of sero-discordance were injection drug use (IDU) history, tuberculosis (TB) history and the availability of voluntary counselling and testing (VCT) in residential locations. High sero-concordance was associated with college/university education.

Conclusion

The sero-discordance was significantly higher among married males than married females. Other factors also related to high sero-discordance were history of IDU, history of TB and the availability of VCT in residential locations. In contrast, college/university education and female sex were significantly related to low sero-discordance. To contain the increasing HIV prevalence among women, measures should be taken to prevent transmission among sero-discordant couples.

Trial registration NCT01433601

Keywords

HIV ART Gender Late presentation Sero-discordance Vietnam

Background

In couples where one person is living with HIV and the other is HIV negative, the HIV-negative partner is at continuous risk for infection. Sexual behaviour, viral load and sexually transmitted disease influence the risk for transmission between partners. In most Asian countries, including Vietnam, the HIV epidemic is in a concentrated stage, with the highest HIV prevalence among certain risk groups, such as people who inject drugs (PWID), of whom the majority are men [1]. In areas with a generalised HIV epidemic, as in many sub-Saharan African countries, the HIV prevalence is higher among women than men [2, 3]. However, increasing numbers of women are contracting HIV also in settings with concentrated HIV epidemics [2]. In Vietnam, the first HIV case was detected in 1990. By March 2010, the HIV prevalence among adults aged 15–49 years was estimated to be 0.53%, with 209,424 HIV+ cases reported, of whom 45,227 had died [4]. Since late 2005, antiretroviral therapy (ART) programs have been scaled up, with funding coming mostly from the U.S. President’s Emergency Plan for AIDS Relief and the Global Fund to Fight AIDS, Tuberculosis and Malaria.

The aim of this project was to study sero-concordance and discordance rates in a cohort of people living with HIV initiating ART who were recruited from 2007 to 2009. A further aim was to study factors influencing discordance and concordance, including gender.

Methods

Study setting

The study was carried out at 4 out-patient clinics (OPCs) in Quang Ninh, a province in north-eastern Vietnam with a population of 1.1 million. Quang Ninh’s economy is growing rapidly, based mainly on industries such as coal mining, cement manufacturing and harbours, as well as tourism associated with the famous Ha Long Bay. Quang Ninh is also among the areas hardest hit by the HIV epidemic in Vietnam, with an estimated HIV prevalence of slightly above 1% among those aged 15–49 years [5].

Study participants

Of 660 naïve HIV positive patients eligible for ART who were registered continuously from July 2007 to November 2009 at 4 OPCs in Quang Ninh, Vietnam, 640 patients (97%) gave their consent to participate in a Randomized Controlled Trail (RCT) to assess the effect of peer support on virological treatment failure rates. Of the patients 288 (46%) were married. For the purpose of this study, we included only married patients whose partners were willing to provide their HIV test results. Among these 452 were male (70.6%) and 188 female (29.4%).

Patients in the intervention group received enhanced adherence support from peer supporters and the control group had conventional support. According to the Vietnamese National HIV Guidelines (2005), HIV-infected individuals were eligible to be registered for free at an ART clinic if they: (1) were confirmed HIV positive, (2) possessed valid civil registration information (home address and telephone), (3) had a family member who can act as a supporter, and (4) agreed to enroll and to be followed up in the ART program. Each clinic was staffed with two medical doctors, one adherence counselor, one reception nurse, one phlebotomy nurse, one pharmacist, and one volunteer who was a person living with HIV (PLHIV). The staff were trained on basic and advanced HIV care and treatment and certified by Ministry of Health.

Data collection

Before initiating ART, each patient was interviewed by a trained interviewer using a structured questionnaire. The questionnaire was designed to collect information about family structure, socioeconomic situation, mode of HIV transmission, history of HIV diagnosis, TB and ART, as well as alcohol and heroin use. The partners of married patients were encouraged to take a HIV test provided free under the OPC’s VCT program. Clinical staging and baseline laboratory tests (including a full blood count, alanine aminotransferase, hepatitis coinfection, CD4+ T cell count and plasma HIV viral load) were collected from the participants’ medical records. The viral load was determined using a method based on the enzyme-linked immunosorbent assay (Exavir™ Load) [6]).

Statistical analysis

The characteristics of the enrolled patients were described and grouped first in relation to the HIV status of their wife/husband. Univariate and multivariate analyses were carried out to study the effect of occupation, education level, resident’s area and gender on the HIV sero-status of the patient’s spouse or partner. Other indicators assessed included the following: CD4 count, clinical staging history of TB infection and injecting heroin and known duration of HIV infection between HIV diagnosis and initiating ART.

The collected data were analysed using SPSS version 20. Chi Square tests were performed to examine the difference between proportions, with 95% confidence intervals (CI) used in the comparisons. Odds ratios (ORs) were calculated with 95% CI to compare risks between the two patient groups. Multiple logistic regression equations were used to compute the ORs of each factor adjusted for other factors presented in given models (aORs). In all the tests and the regression models, p values less than 5% were considered significant.

Ethical considerations

The study was approved by the Institutional Review Boards of Hanoi Medical University, Ministry of Health, Vietnam (numbers 26/IRB, 66/HMURB, 59/HMURB and 98/HMURB) of Hanoi Medical University) and the Regional Board for Ethics Review from Karolinska Institutet in Stockholm, Sweden (number 2006/1367-31/4). Before conducting the study, written informed consent was obtained and all identifying information (names, initials, etc.) were then omitted to ensure the confidentiality. Patients in the intervention group were informed about the study and that they would be visited by a peer supporter and that the home visits might disclose their HIV status. In order to avoid unintentional disclose of HIV status through study participation efforts were made. The peer supporters where instructed to act in a manner that would not evoke suspicion in the study participants neighborhood. In advance of each visit the peer supporters called the study participants to decide when and where to meet. The study participants could at any time cancel a meeting or decide not to participate in the intervention or study. Biological samples were collected and used only after written consent. All blood samples were coded to protect the identity of patients and to ensure confidentiality.

Both intervention and control groups received equal care and treatment and those who did not fulfill the inclusion criteria’s for the study were managed with a set standard of care and treatment according to the National HIV Treatment Guidelines. Peer-supporters received ART at the study clinics and were treated in the same way as other HIV patients according to the National Guidelines. Moreover, peer-supporters’ viral load (ExaVirTM Load) were also measured every 6 months, and they received a salary and transportation fees each month. Data were accessible only to research team, data manager and coordinator of the project.

Results

Social, demographic and economic characteristics

Among the 288 married patients who were ART-naive and where information on the HIV status of their spouses was available, the majority were HIV-infected men (75%), and the mean age was 32 (SD = 5.5) years (Table 1). The mode of HIV transmission reported among men was mainly sharing needles during heroin use (58%), whereas sexual transmission was reported in 94% of women (p < 0.01). IDU, past or present, was reported by half of the patients, significantly higher among males (63%) than females (4.2%) (p < 0.01). Of these patients, 18% reported active heroin use in the last 6 months.
Table 1

Patients’ socio-economic and clinical-laboratory characteristics at enrolment

Characteristics

Sub-character

Females (n = 72)

Males (n = 216)

p value*

(%)

95% CI

(%)

95% CI

Education

Secondary or less

51

39–63

48

41–55

>0.05

High school

36

25–48

42

35–49

College/university

13

6–22

11

7–16

Occupation

Unemployed

12

8–17

27

23–32

<0.05

Employed

88

80–95

73

68–77

Known PLHIV in family

Yes

65

59–72

27

23–31

<0.01

No

35

28–42

73

69–78

Mode of HIV infection

Sexual intercourse

94

89–98

29

24–33

<0.001

IDU

4

2–8

64

59–68

<0.001

Do not know

2

0–5

7

5–10

Disclosure of HIV status

Yes

92

88–95

92

91–96

>0.05

No

8

4–11

8

5–10

 

History of IDU

Yes

5

2–8

73

69–78

<0.001

No

95

92–96

27

23–31

Clinical stage

Stage 3 or 4

33

28–39

61

58–64

<0.05

Stage 1 or 2

67

62–70

39

35–44

Duration of known HIV infection

≥2 years

36

30–41

45

40–49

>0.05

<2 year

64

57–70

55

50–60

CD4 cell count

≥100/µl

65

58–71

45

39–51

<0.01

<100/µl

35

29–41

159

159

55

50–60

99

60

CD4 cell count by group (cells/µl)

0–49

50–99

100–149

150–199

≥200

Mean

Median

18.1

12.5

16.7

22.2

30.6

159

159

 

46.8

18.1

9.7

11.6

13.9

 

<0.0001

Viral load by group

<400

400–3499

3500–9999

10000–49999

≥50000

0

16.2

6.5

25

52.3

 

0

20.8

12.5

26.4

40.3

 

>0.05

* Chi square test comparison between proportions of males and females

A large majority of the patients (92%) had disclosed their HIV+ status to other people (spouse, parents, siblings).

Clinical characteristics

Clinical stage 3 or 4 (AIDS defining Opportunistic Infections) at diagnosis was significantly (p < 0.01) more common among males than females (61 vs. 34%). Males were significantly (p < 0.001) more immunosuppressed than females, and the average CD4 counts was (104/µl) and (152/µl), respectively.

Sero-discordance

Overall, the sero-discordance rate was 58%. Men had a significantly (p < 0.01) higher rate of sero-discordance compared to women, 71 and 18%, respectively. Males reporting IDU had significantly higher sero-discordance (p < 0.001) compared to males not reporting IDU (79 vs. 58%). Among women reporting IDU compared to women not reporting IDU the observed effect size was lager then among men (33 vs. 17%), however, however no significant difference in sero-discordance.

Discussion

There was a high sero-discordance rate among the married couples in our study, and it was higher among men than among women. The sero-discordance rate shown in this study is higher than that reported in other countries, e.g. Thailand (58%) [7] or Nigeria (25%) [8].

High sero-discordance rate was associated with male sex, history of IDU and diagnosis of TB. Patients with a history of IDU might be less sexually active, hence posing less of a risk of transmitting the virus to their spouse, also shown in an earlier study [9]. Patients with a history of IDU were commonly diagnosed early as part of the on-going sentinel surveillance program among risks groups. This may explain the counterintuitive result that patients with known HIV infection for more than 2 years had a higher sero-discordance rate than patients with known infection less than 2 years. Early HIV detection through sentinel surveillance or VCT before development of severe immunosuppression or indication for ART might sensitise the patients to preventive measures such as condom use or abstinence, as shown in a study from Ethiopia [10]. In Dong Trieu, where no sentinel surveillance activities or VCT were available until 2002 compared to 1995 in Ha Long City, the sero-concordance rate was significantly higher.

As shown, patients with higher education had a significantly lower sero-discordance rate. This could be due to a more favourable social status in the community, making the individual more socially vulnerable to accidental disclosure and stigmatisation. This factor may be a strong disincentive to HIV testing [11, 12], thereby delaying diagnosis and increasing the duration of exposure and risk for HIV transmission to the partner. In Vietnam, a high proportion of men have visited female sex workers [13]. As the latter are a vulnerable group with a high prevalence of HIV and Sexually Transmitted Diseases (STDs) [14], the male partners may have been infected not only with HIV, but also STDs such as syphilis, herpes type 2 and gonorrhoea, all of which increase the risk for HIV transmission [15].

There was a much higher rate of sero-discordance among male married patients than female married patients. A study in Italy concluded that the efficiency of male-to-female transmission was 2.3 times greater than that of female-to-male transmission [16]. Thus, a higher discordance rate would be expected among married male patients with an equal sex distribution of index patients. This factor, combined with the finding that men were more severely immunosuppressed than women, indicating a longer duration of HIV infection, may lead to the conclusion that the male partner was the index case in most cases and infected their female partner. This idea is also supported by the high proportion of widows (40%) in the study population.

High plasma viral load that may increase the risk of transmitting HIV to their sexual partners [17]. This idea is supported by the general trend of increasing HIV prevalence among women, particularly those who live in areas with a high prevalence of male PWID [18, 19]. In our cohort we could not find a significant correlation between high baseline viral load and level of sero-discordance (Table 2).
Table 2

Factors related to HIV sero-discordant/concordant status

Characteristics

Variable

Concordance N = 121

Discordance N = 167

Adjusted odds ratio

N (%)

95% CI

N (%)

95% CI

(95% CI)

p value

Sex

Male

62 (29%)

23–35

154 (71%)

65–77

1

 

Female

59 (82%)

71–90

13 (18%)

10–29

4.8 (2.0–11.4)

<0.001

Education

Secondary or less

56 (40%)

32–49

84 (60%)

51–68

1

 

High school

45 (39%)

30–48

71 (61%)

52–70

1.2 (0.6–2.3)

NS

College/university

20 (63%)

44–78

12 (37%)

22–56

3.2 (1.2–8.7)

0.025

Occupation

Unemployed

14 (27%)

16–41

38 (73%)

59–84

0.8 (0.3–1.9)

NS

Employed

107 (45%)

39–52

129 (55%)

48–61

1

 

Having children

Yes

89 (40%)

34–47

132 (60%)

53–66

1

 

No

32 (48%)

36–60

35 (52%)

40–64

1.3 (0.6–2.7)

NS

Resident’s area

Dong Trieu

25 (68%)

50–81

12 (32%)

19–49

5.2 (1.7–15.4)

0.003

Uong Bi

20 (47%)

31–62

23 (53%)

38–69

2.5 (0.997–6.5)

0.051

Yen Hung

16 (46%)

29–63

19 (54%)

37–71

2.4 (0.9–6.8)

NS

Ha Long

60 (35%)

28–42

113 (65%)

58–72

1

 

Mode of HIV infection

Sexual intercourse

85 (60%)

51–68

57 (40%)

32–48

1

 

IDU

26 (21%)

14–29

100 (79%)

71–86

0.4 (0.2–1.1)

NS

Do not know

10 (42%)

23–63

14 (58%)

37–77

0.6 (0.2–2.0)

NS

Hepatitis coinfection

Yes

29 (32%)

23–42

62 (68%)

54–77

0.6 (0.3–1.3)

NS

No

92 (47%)

40–54

105 (53%)

46–60

1

 

History of IDU

Yes

31 (22%)

16–30

109 (78%)

70–84

0.6 (0.3–1.3)

NS

No

90 (61%)

52–69

58 (39%)

31–48

1

 

Clinical stage

Stage 3 or 4

68 (49%)

40–57

71 (51%)

43–59

1

 

Stage 1 or 2

53 (36%)

28–44

96 (64%)

56–72

0.9 (0.4–1.7)

NS

Duration of known HIV infection

≥2 years

80 (46%)

39–54

93 (54%)

46–61

1

NS

<2 year

41 (36%)

27–45

74 (64%)

55–73

0.6 (0.3–1.3)

NS

History of TB

Yes

10 (25%)

13–41

30 (75%)

58–87

1

 

No

111 (45%)

39–51

137 (55%)

49–61

0.2 (0.05–0.8)

0.026

CD4 cell count

≥100/µl

73 (52%)

43–60

68 (48%)

40–57

1

 

<100/µl

48 (33%)

25–41

99 (67%)

59–75

1.1 (0.6–2.2)

NS

Viral load

≥100,000 copies/ml

40 (39%)

29–49

63 (61%)

51–70

1.1 (0.5–2.1)

NS

<100,000 copies/ml

81 (44%)

37–51

104 (56%)

49–63

1

 

As all the patients were included in the study at the start of ART, the effect of viral suppression on transmission rates is not a likely cause of the high sero-discordance rate, although this has been shown to be the case in other studies [20]. TB may occur at a modest level of immunosuppression, and individuals diagnosed with TB are tested for HIV. These factors might have led to earlier diagnosis and hence a reduction in the exposure time for the spouses. The deterioration in health, as well as common stigmatisation of TB, may have decreased the sexual activity and hence the exposure of the spouse [9].

The high sero-discordance rates of the HIV+ married men may indicate that a large part of the population was aware of preventive measures, especially in the areas where VCT has been carried out for a longer duration. However, the high number of female spouses at risk of exposure emphasises the need for continued and increased measures to prevent transmission such as Information, Education and Communication programs and provision of condoms in the community to prevent HIV transmission among couples [21, 22]. In Zambia, it has been reported that the ideological stance in the U.S. President’s Emergency Plan for AIDS Relief to promote abstinence and faithfulness before condoms (the ‘ABC’ approach) might have deterred the organisations involved in the implementation of the program from giving information and providing condoms to at-risk populations [23]. The ABC approach has not been so influential in Vietnam where condoms have been promoted as a core part of the prevention program. This may have influenced the comparably high rates of sero-discordance reported, in combination with other factors such as the prevalence of IDU and the rate of sexual HIV transmission.

Early initiation of ART reduce sexual transmission, especially among sero-discordant couples, the incidence of Opportunistic Infections (OIs) and death [2431]. The risk for transmission is proportional to the viral load in combination with other factors that increase the risk for blood to blood contact as STD’s, genital lesions and anal intercourse. Hence viral load monitoring is important to assess both the effect of treatment as well early detection of increased risk for HIV transmission, especially among sero-discordant couples (27). In seen in Table 2 there were no significant difference in viral load between sero-concordant and discordant or male and females. In many low-income countries, patients are generally diagnosed at a late stage of the disease and the ART coverage is in many places still low [28]. As seen in our study, there was limited access to ART, even for those patients who were severely immunosuppressed and with high viral load. The lack of access was mainly due to the program’s regulation, under which the number of patients started on ART each month was limited to avoid overloading health staff.

There are some methodological considerations in this study. Non-naïve was an exclusion criteria, hence patients that had used ART prior to enrolment were not asked to join the RCT. Therefore, this cohort might not be representative of HIV patients in Vietnam. Indicators such as IDU and history of TB were self-reported, and this might have caused an underestimation. Information regarding number of years married, number of sex partners or sexual intercourse behaviour was not collected. Thus, the data might not represent the magnitude of all predictors of sero-discordance among married patients. As the study included only patients who registered at OPCs, information on patients who have not yet registered is lacking. Thus, the study does not fully reflect the entire characteristics of People Living with HIV in Vietnam.

Conclusions

There was a high sero-discordance rate among the married patients. Being a female, having education at college/university level and living in an area with late initiation of VCT were predictors of higher HIV sero-concordance, whereas being male, having a history of IDU and TB and living in an area with earlier VCT initiation were predictors of the HIV sero-discordance of the partner. To contain the increasing HIV prevalence among women and prevent transmission among sero-discordant couples, measures should be taken to reduce the HIV viral load and exposure. These include providing increased information, as well as condoms and ART to the HIV-positive partner, regardless of their immune status. Pre-Exposure Prophylaxis (PrEP) might in some cases also be an option to reduce transmission. Viral load monitoring is important to assess the effect of treatment, early detection treatment failure or poor adherence, as well as of increased risk for HIV transmission, especially among sero-discordant couples.

Abbreviations

HIV: 

human immunodeficiency virus

PWID: 

people who inject drugs

IDU: 

injection drug use

TB: 

tuberculosis

VCT: 

voluntary counselling and testing

ART: 

antiretroviral therapy

OPCs: 

out-patient clinics

CI: 

confidence intervals

ORs: 

odds ratios

STDs: 

sexually transmitted diseases

ABC: 

abstinence, be faithful, condoms

PLHIV: 

people living with HIV

Declarations

Authors’ contributions

VVT: study design, data collection, data analysis, manuscript writing; DDC: study design, data collection, manuscript writing; NPH: study design, data collection, manuscript writing; TA: study design, manuscript writing; NTKC: study design, data collection, manuscript writing; HDP: data analysis, manuscript writing; VD: data analysis, manuscript writing; ML: study design, data collection, data analysis, manuscript writing. All authors read and approved the final manuscript.

Acknowledgements

This study was funded by the Swedish International Development Cooperation Agency (Grant No. SWE2007404) and the European Union Framework Program 7 (Project No: 222946). We wish to acknowledge support and contributions from the directorial board and our colleagues at Uong Bi hospital. We also acknowledge the teams’ work at the OPC of the provincial hospital in Quang Ninh, the Health Centre in Ha Long and Yen Hung district hospital. A special thanks to the study participants, as well as to their families, for their valuable contribution to the study.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

All data can be obtained from the first author and corresponding author on request.

Ethics approval and consent to participate

Consent to publish: has been obtained from all authors and participants.

Funding

Swedish International Development Cooperation Agency (SIDA) and the CHAIN EU FP7. Trial registration: NCT01433601.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Division of Global Health, Department of Public Health Sciences, Karolinska Institute
(2)
Health System Research Project, Ha Noi Medical University
(3)
Oxford University Clinical Research Unit
(4)
Department of Probability and Mathematical Statistics, Institute of Mathematics

References

  1. Government of Socialist Republic of Vietnam (GSRV). The Third Country Report on Following up the Implementation to the Declaration of Commitment on HIV and AIDS: Reporting Period January 2006–December 2007. Hanoi, Vietnam: Vietnamese Government; 2008. http://www.unaids.org.vn.
  2. Global report: UNAIDS report on the global AIDS epidemic 2010. UNAIDS/10.11E | JC1958E. ISBN: 978-92-9173-871-7.
  3. AIDS epidemic update: November 2009. UNAIDS/09.36E/JC1700E. ISBN: 978-92-9173-832-8.
  4. Viet Nam Hiv/Aids Estimates And Projections. Ministry Of Health—Vietnam Administration Of Hiv/Aids Control. Ha Noi 4/209. http://www.ilo.org/wcmsp5/groups/public/---ed_protect/---protrav/---ilo_aids/documents/legaldocument/wcms_174609.pdf.
  5. Hiv/Aids Estimates And Projections 2005–2010. Ministry of Health, Vietnam. http://www.aidsdatahub.org/sites/default/files/documents/HIVAIDS_Estimates_and_Projections_2005_2010.pdf.pdf.
  6. Labbett W, Garcia-Diaz A, Fox Z, Clewley GS, Fernandez T, Johnson M, Geretti AM. Comparative evaluation of the ExaVir Load version 3 reverse transcriptase assay for measurement of human immunodeficiency virus type 1 plasma load. J Clin Microbiol. 2009;47(10):3266–70.View ArticlePubMedPubMed CentralGoogle Scholar
  7. Rojanawiwat A, Ariyoshi K, Pathipvanich P, Tsuchiya N, Auwanit W, et al. Substantially exposed but HIV-negative individuals are accumulated in HIV-serology-discordant couples diagnosed in a referral hospital in Thailand. Jpn J Infect Dis. 2009;62:32–6.PubMedGoogle Scholar
  8. Ikechebelu J, Mbamara SU, Joe-Ikechebebelu NN, Ezenwabachili AO. Sexual practices of people living with HIV in South Eastern Nigeria. Niger J Clin Pract. 2009;12:416–20.PubMedGoogle Scholar
  9. Nguyen NT, Keithly SC. A qualitative study on the sexual behaviour of people living with HIV in Vietnam. AIDS Care. 2012;24(7):921–8.View ArticlePubMedGoogle Scholar
  10. Bonnenfant YT, Hindin MJ, Gillespie D. HIV diagnosis and sexual risk behavior intentions among couple VCT clients in Ethiopia. AIDS Care. 2012;24(9):1078–86.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Khuat TH, Nguyen TVA, Odgen J. Understanding HIV and AIDS related stigma and discrimination in Vietnam. Washington: International Center for Research on Women; 2004.Google Scholar
  12. Gaudine A, Gien L, Thuan TT, Dung do V. Perspectives of HIV-related stigma in a community in Vietnam: a qualitative study. Int J Nurs Stud. 2009;47:38–48.View ArticlePubMedGoogle Scholar
  13. Duong CT, Nguyen TH, Hoang TT, Nguyen VV, Do TM, et al. Sexual risk and bridging behaviors among young people in Hai Phong, Vietnam. AIDS Behav. 2008;12:643–51.View ArticlePubMedGoogle Scholar
  14. Vu Thuong N, Van Nghia K, Phuc Hau T, Thanh Long N, Van Thi Bao C, et al. Impact of a community sexually transmitted infection/HIV intervention project on female sex workers in five border provinces of Vietnam. Sex Transm Infect. 2007;83:376–82.View ArticlePubMedGoogle Scholar
  15. Otten MW Jr, Zaidi AA, Peterman TA, Rolfs RT, Witte JJ. High rate of HIV seroconversion among patients attending urban sexually transmitted disease clinics. AIDS. 1994;8:549–53.View ArticlePubMedGoogle Scholar
  16. Nicolosi A, Correa Leite ML, Musicco M, Arici C, Gavazzeni G, et al. The efficiency of male-to-female and female-to-male sexual transmission of the human immunodeficiency virus: a study of 730 stable couples. Italian Study Group on HIV heterosexual transmission. Epidemiology. 1994;5:570–5.View ArticlePubMedGoogle Scholar
  17. Cohen MS, Gay CL. Treatment to prevent transmission of HIV-1. Clin Infect Dis. 2010;50(Suppl 3):S85–95.View ArticlePubMedPubMed CentralGoogle Scholar
  18. Nguyen TA, Oosterhoff P, Hardon A, Tran HN, Coutinho RA, et al. A hidden HIV epidemic among women in Vietnam. BMC Public Health. 2008;8:37.View ArticlePubMedPubMed CentralGoogle Scholar
  19. Phinney HM. “Rice is essential but tiresome; you should get some noodles”: Doi Moi and the political economy of men’s extramarital sexual relations and marital HIV risk in Hanoi, Vietnam. Am J Public Health. 2008;98:650–60.View ArticlePubMedPubMed CentralGoogle Scholar
  20. Kumarasamy N, Venkatesh KK, Srikrishnan AK, Prasad L, Balakrishnan P, et al. Risk factors for HIV transmission among heterosexual discordant couples in South India. HIV Med. 2010;11:178–86.View ArticlePubMedGoogle Scholar
  21. Wingood GM, DiClemente RJ, Mikhail I, Lang DL, McCree DH, et al. A randomized controlled trial to reduce HIV transmission risk behaviors and sexually transmitted diseases among women living with HIV: the WiLLOW Program. J Acquir Immune Defic Syndr. 2004;37(Suppl 2):S58–67.View ArticlePubMedGoogle Scholar
  22. Kumarasamy N, Venkatesh KK, Srikrishnan AK, Prasad L, Balakrishnan P, et al. Risk factors for HIV transmission among heterosexual discordant couples in South India. HIV Med. 2010;11:178–86.View ArticlePubMedGoogle Scholar
  23. Gordon G, Mwale V. Preventing HIV with young people: a case study from Zambia. Reprod Health Matters. 2006;14:68–79.View ArticlePubMedGoogle Scholar
  24. World Health Organization. WHO clinical staging of HIV/AIDS for adults and adolescents. Geneva: World Health Organization; 2011. p. 2011.Google Scholar
  25. Sterne JA, May M, Costagliola D, de Wolf F, Phillips AN, et al. Timing of initiation of antiretroviral therapy in AIDS-free HIV-1-infected patients: a collaborative analysis of 18 HIV cohort studies. Lancet. 2009;373:1352–63.View ArticlePubMedGoogle Scholar
  26. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med. 2011;365(4):493–505.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Eshleman SH, Hudelson SE, Redd AD, Swanstrom R, Ouuu SS, Zhang XC, Ping LH, Piwowar-Manning E, Porcella SF, Sievers MF, Martens CA, Bruno D, Dukhovlinova E, McCauley M, Gamble T, Fogel JM, Sabin D, Quinn TC, Gunde L, Maliwichi M, Nhando N, Akelo V, Moyo S, Panchia R, Kumarasamy N, Chotirosniramit N, GonçalvesdeMelo M, Pilotto J, Grinsztejn B, Mayer K, Chen YQ, Hughes JP, Cohen MS. Treatment as prevention: characterization of partner infections in the HIV prevention trials network 052 trial. J Acquir Immune Defic Syndr. 2016;375:830–9.Google Scholar
  28. Damalie Nakanjako RC, Coutinho Alex G, Kamya Moses R. Strategies to optimize HIV treatment outcomes in resource-limited settings. AIDS Rev. 2009;11:179–89.PubMedGoogle Scholar
  29. Srikantiah P, Ghidinelli M, Bachani D, Chasombat S, Daoni E, et al. Scale-up of national antiretroviral therapy programs: progress and challenges in the Asia Pacific region. AIDS. 2010;24(Suppl 3):S62–71.View ArticlePubMedGoogle Scholar
  30. Anglemyer A, Rutherford GW, Baggaley RC, Egger M, Siegfried N. Antiretroviral therapy for prevention of HIV transmission in HIV-discordant couples. Cochrane Database Syst Rev. 2011;10(8):009153.Google Scholar
  31. World Health Organization. Guidance on couples HIV testing and counselling, including antiretroviral therapy for treatment and prevention in serodiscordant couples. Geneva: World Health Organization; 2012.Google Scholar

Copyright

© The Author(s) 2016

Advertisement