Increasing HIV testing among male partners

Joanna Orne-Gliemanna,b, Eric Balestrea,b, Patrice Tchendjouc,j,

Marija Miricd, Shrinivas Darake,f, Maia Butsashvilig, Eddy Perez-Thend,
Fred Ebokoh, Melanie Plazya,b, Sanjeevani Kulkarnie,
Annabel Desgrees du Loui, Francois Dabisa,b,
for the Prenahtest ANRS 12127 Study Group
Objective: Couple-oriented posttest HIV counselling (COC) provides pregnant
women with tools and strategies to invite her partner to HIV counselling and testing.
We conducted a randomized trial of the efficacy of COC on partner HIV testing in
low/medium HIV prevalence settings (Cameroon, Dominican Republic, Georgia,
India).
Methods: Pregnant women were randomized to receive standard posttest HIV counselling or COC and followed until 6 months postpartum. Partner HIV testing events were
notified by site laboratories, self-reported by women or both combined. Impact of COC
on partner HIV testing was measured in intention-to-treat analysis. Socio-behavioural
factors associated with partner HIV testing were evaluated using multivariable logistic
regression.
Results: Among 1943 pregnant women enrolled, partner HIV testing rates (combined
indicator) were 24.7% among women from COC group versus 14.3% in standard
posttest HIV counselling group in Cameroon [odds ratio (OR) 2.0 95% CI (1.23.1)],
23.1 versus 20.3% in Dominican Republic [OR 1.2 (0.81.8)], 26.8 versus 1.2% in
Georgia [OR 29.6 (9.195.6)] and 35.4 versus 26.6% in India [OR 1.5 (1.02.2)].
Women having received COC did not report more conjugal violence or union breakups than in the standard posttest HIV counselling group. The main factors associated
with partner HIV testing were a history of HIV testing among men in Cameroon,
Dominican Republic and Georgia and the existence of couple communication around
HIV testing in Georgia and India.
Conclusion: A simple prenatal intervention taking into account the couple relationship
increases the uptake of HIV testing among men in different socio-cultural settings. COC
could contribute to the efforts towards eliminating mother-to-child transmission of HIV.
2013 Wolters Kluwer Health | Lippincott Williams & Wilkins

AIDS 2013, 27:11671177

Keywords: counselling, HIV, male, testing, trial, women

a
INSERM, Centre INSERM U897 Epidemiologie et Biostatistique, bUniversite Bordeaux Segalen, Institut de Sante Publique
Epidemiologie Developpement (ISPED), Bordeaux, France, cLaboratoire dEpidemiologie et de Sante Publique, Centre Pasteur du
Cameroun, Yaounde, Cameroun, dCentro Nacional de Investigaciones en Salud Materno Infantil, Santo Domingo, Dominican
Republic, ePrayas Health Group, Prayas, Pune, India, fFaculty of Spatial Sciences, Population Research Centre, University of
Groningen, The Netherlands, gMaternal and Child Care Union, Tbilisi, Georgia, hInstitut de Recherche pour le Developpement,
UMR 912 SESSTIM (INSERM-IRD-Universite dAix-Marseille/AMU), Marseille, iInstitut de Recherche pour le Developpement,
CEPED UMR Universite Paris Descartes- Sorbonne Paris Cite - INED - IRD, and jReseau International des Instituts Pasteurs, Paris,
France.
Correspondence to Joanna Orne-Gliemann, PhD, ISPED, Universite Bordeaux Segalen, Bordeaux, France.
Tel: +33 5 57 57 45 17; e-mail: Joanna.Orne-Gliemann@isped.u-bordeaux2.fr
Received: 28 September 2012; revised: 22 December 2012; accepted: 17 January 2013.

DOI:10.1097/QAD.0b013e32835f1d8c

ISSN 0269-9370 Q 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins

1167

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

1168

AIDS

2013, Vol 27 No 7

Introduction
HIV testing is the cornerstone of HIV prevention [1]. HIV
testing and more specifically knowledge of ones serostatus
allows individuals to adopt safer behaviours that can reduce
HIV transmission [2]. HIV testing is also a prerequisite for
accessing care and treatment when HIV-infected. Antiretroviral treatment (ART) may also in turn contribute to
overall HIV prevention [3]. Yet, although the expected
benefits of HIV testing are well known, its coverage
remains low worldwide. Population-based studies conducted between 2007 and 2009 in nine resource-limited
countries estimated that only 34% of women and 17% of
men were ever informed of their HIV status [4]. Further,
HIV counselling and testing services have largely been
organized on an individual and sex-specific basis. Women
are often tested during pregnancy, for the prevention of
mother-to-child transmission of HIV (PMTCT). The
estimated coverage of prenatal HIV testing increased from
13% in 2004 to 21% in 2007 [4]. Whereas men usually
access HIV testing in outpatients consultations for sexually
transmitted infections, at voluntary HIV counselling and
testing centres, before a medical intervention, and more
recently within male circumcision programmes. In the
context of antenatal care (ANC), less than 20% of male
partners of pregnant women themselves get tested for HIV
[57].
Yet, male partners HIV testing is consistently associated
with the acceptability of PMTCT interventions by
women at all levels [5,8,9]. A recent cohort study in
Kenya suggests that a mans attendance to ANC visits with
his female partner and being himself tested for HIV
reduces the risk of HIV transmission to their infant and
increases child survival [10]. Partner HIV testing is also
key for the prevention of sexual transmission of HIV
during pregnancy and after delivery [11,12], as it has been
shown that a large proportion of new HIV infections
occur within marriage and cohabitation [13]. These
observational findings have rarely been corroborated by
experiments data. Indeed, such data on interventions
aiming at increasing HIV testing among male partners in
the context of prenatal care are scarce [14].
The Prenahtest Study is a multicountry randomized
intervention trial evaluating the efficacy of an innovative
prenatal HIV counselling intervention called coupleoriented posttest HIV counselling (COC) [15]. The
present analysis describes the primary study outcome, that
is the impact of COC on partner HIV testing and
investigates the socio-behavioural factors associated with
partner HIV testing.

Methods
Ethics statement
The Prenahtest study protocol V4 18 December
2006 received ethical clearance from Comite National

dEthique, 23 January 2007, in Cameroon; Comite de

Etica Indepediente, Fundacion Dominica de Insectoligia,
9 April 2007, in Dominican Republic; IRB 00006752
of Maternal and Child Care Union, 13 November
2008 in Georgia; Independent Ethics Committee for
Prayas Health Group, 27 March 2007, in India. The
Prenahtest study was registered on ClinicalTrials.gov as
NCT01494961.

Study setting
The study was carried out at four urban health centres
catering mainly for underprivileged populations and
located in four low/intermediate-resource countries with
low/medium HIV prevalence: Centre Me`re-Enfant de la
Fondation Chantal Biya in Yaounde, Cameroon (national
HIV prevalence in 2009 estimated at 5.3%), Hospital
Materno-Infantil San Lorenzo de los Mina in Santo
Domingo, Dominican Republic (HIV prevalence: 0.9%),
Sane Guruji Hospital in Pune, India (HIV prevalence:
0.3%) and Maternity Hospital N85 in Tbilisi, Georgia
(HIV prevalence: 0.1%) [16].
Study population and sampling
The study sample size was calculated so as to be able to
measure in each study site a minimum improvement of
10% of the proportion of tested partners among women
from the COC group (target: 15%) compared with
women from the standard posttest HIV counselling group
(baseline: under 5%), with an alpha type I error of 5%
(two-sided test) and a b type II risk of 10% (power of
90%). Considering a proportion of 15% of women lost
to follow-up and of noninterpretable observations, a
minimum of 242 women in each group, that is 484
women per site were to be included. Inclusion criteria
were: age at least 15 years, having a partner (defined as
regular by the woman) on the day of enrolment, and
accepting follow-up (including home visits if necessary)
by the study team until 6 months postpartum. Exclusion
criteria were: herself or her partner having been tested for
HIV during her current pregnancy, having a partner who
is absent for more than 6 months per year, being
unwilling/unable to provide contact information and
having a mental impairment at the moment of enrolment.
Enrolment and randomization
Between 26 February and 15 October 2009, all women
attending their first prenatal care visit in the four study
sites were informed about the study and, if interested to
participate, screened for eligibility. Eligible women were
offered participation and required to provide written
informed consent. Women were enrolled before HIV
testing, which was performed on the same day using rapid
tests, except in Georgia where ELISA testing was used.
Women were scheduled to receive posttest HIV
counselling as per each site protocol, either on the same
day of HIV testing (Dominican Republic), a few days
later (India) or at the next ANC visit (Cameroon
and Georgia). Women were individually randomized to

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Partner HIV testing Orne-Gliemann et al.

receive either standard posttest HIV counselling or the

COC intervention; women were blinded to the nature of
the counselling. Randomization was performed centrally
in Bordeaux and stratified according to trial centre.
Blocked randomization was drawn by the trial statistician
(in blocks of 10) to assign eligible women to one of the
two counselling groups.

Posttest HIV counselling

Standard posttest HIV counselling
Standard posttest HIV counselling was delivered in each
study site according to WHO [17] and local HIV
counselling guidelines. Observations conducted during
the pilot phase of the trial highlighted that the content
and quality of sessions varied across sites and within sites;
all sessions discussed HIV transmission and prevention
and PMTCT, however most poorly addressed partner
HIV testing and mens involvement within the prenatal
HIV counselling and testing process [18].
Intervention: couple-oriented posttest HIV counselling
COC was designed as a strengthened posttest HIV
counselling session, provided once to women and for
30 min on average. Through counselling, education and
role-play, COC aims to develop womens communication skills and self-efficacy, so as to empower women to
discuss HIVand sexual issues with their partner, including
partner HIV testing and couple HIV counselling. The
structure of the COC intervention was adapted from
WHO [17] and was described in a COC manual, which
was used to train the COC counsellors and could also be
used during the counselling session [19]. COC counsellors did not provide standard posttest VIH counselling
during the trial period. Tested during the pilot phase of
the trial, COC was shown to be feasible and acceptable in
the four study sites [18].

Data collection and follow-up

Three structured face-to-face quantitative questionnaires
were administered to participants: at baseline prior to
prenatal HIV testing (T0), 28 weeks after the posttest
HIV counselling (T1) and 6 months postpartum (T2).
Women were assigned identification numbers and all the
questionnaires, process forms and laboratory samples
were labelled with matching numbers to maintain confidentiality.
Adverse events, described as experience of violence
or union break-ups occurring among study participants
after randomization, were systematically documented
and their relatedness to the study and/or intervention
was assessed. Psychosocial services were available upon
request.
Partner HIV counselling was provided as per each site
protocol. All counsellors received refresher training on
couple HIV counselling prior to the trial.

1169

Women were provided incentives for follow-up: condoms, family planning visits, selected contraceptive
methods and selected sexually transmitted infections
screening were offered for free. Repeat HIV testing was
offered to all HIV-negative women at T2. All women and
partners tested HIV-positive within the study and their
exposed infants were referred to a local HIV care and
treatment programme.

Statistical analysis
All partner HIV testing events were computed from the
day the woman received posttest HIV counselling to
6 months postpartum. Partner HIV testing rates were
measured using three indicators: tests notified within site
laboratory logbooks, tests self-reported by women within
the questionnaires (reports of tests having occurred on site
or elsewhere) and tests notified by laboratory logbooks or
reported by women (combined indicator). To estimate
the effect of COC on these outcomes, an intention-totreat analysis was conducted on all randomized women.
In case of a missing value on our main outcome, we
considered that the partner was not tested for HIV. As the
four study sites present different epidemiological, sociodemographic and cultural contexts, the data were not
pooled a priori and all statistical analysis were stratified
according to study site. Odds ratios (OR) and confidence
intervals at 95% (CI) were estimated and Wald tests were
used. To estimate socio-behavioural factors associated with
the combined indicator for partner HIV testing, we first
conducted nonadjusted logistic regressions. Variables that
were statistically significant at 0.25 in univariable analysis
were included in the multivariable models. To select the
final adjusted models, a descending manual method was
performed and confounders were verified. The goodness
of fit of the final adjusted models was checked with the
Hosmer and Lemeshow test and the accuracy was checked
with the area under curve statistic. Data were processed and
analysed with the use of SAS software (version 9.2; SAS
Institute, Cary, North Carolina, USA).

Results
Recruitment and retention
Among the 4249 pregnant women informed about
the Prenahtest Study, 3366 (79.2%) were screened for
eligibility. One thousand and thirty-eight women
(30.8%) did not meet eligibility criteria, mainly because
women were not available for the planned follow-up
period (42.0%) or they had already been tested for HIV
during their current pregnancy (25.8%). Of the 2328
eligible women, 1943 (83.5%) consented to participate
and were randomized (484 in Cameroon, Dominican
Republic and India, respectively, and 491 in Georgia).
One thousand nine hundred and twenty-two women
(98.9%) completed the baseline T0 questionnaire and of
these, 1726 (89.8%) completed either the T1 or T2
questionnaire (Fig. 1). Overall lost to follow-up rates after

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

1170

AIDS

2013, Vol 27 No 7
Randomized women
Total N = 1943
Cameroon DR
Georgia India
n = 484 n = 484 n = 491 n = 484

Standard Counselling (SC)

Total N = 973

Couple-oriented Counselling (COC)

Total N = 970

Cameroon DR
Georgia India
n = 245 n = 242 n = 245 n = 241

Cameroon DR
Georgia India
n = 239 n = 242 n = 246 n = 243

Lost to follow-up
Not seen at T0
N=9

Lost to follow-up
Not seen at T0
N = 12

Seen at T0
Total N = 964

Seen at T0
Total N = 958

Cameroon DR
Georgia India
n = 241 n = 240 n = 245 n = 238

Cameroon DR
Georgia India
n = 236 n = 235 n = 246 n = 241

Lost to follow-up
SC not received
N = 18

Lost to follow-up
COC not received
N = 15

SC received
Total N = 946

COC received
Total N = 943

Cameroon DR
Georgia India
n = 228 n = 240 n = 243 n = 235

Cameroon DR
Georgia India
n = 225 n = 234 n = 245 n = 239

Lost to follow-up
Not seen at T1 and T2
N = 70

Lost to follow-up
Not seen at T1 and T2
N = 93

Seen at T1
Total N = 862

Seen at T1
Total N = 831

Cameroon DR
Georgia India
n = 215 n = 209 n = 228 n = 210

Cameroon DR
Georgia India
n = 204 n = 193 n = 231 n = 203

Seen at T2
Total N = 676

Seen at T2
Total N = 694

Cameroon DR
Georgia India
n = 179 n = 126 n = 175 n = 196

Cameroon DR
Georgia India
n = 182 n = 133 n = 194 n = 185

Fig. 1. Trial profile. Prenahtest ANRS 12127 trial (20092011). DR, Dominican Republic.

randimization were comparable between women from

standard posttest HIV counselling and COC groups
(11.0% in standard posttest HIV counselling and 11.3% in
COC in Cameroon, 6.9 and 6.1% in Georgia and 9.1 and
11.9% in India), except in Dominican Republic (12.8% in
standard posttest HIV counselling and 20.3% in COC
group, P 0.04).

Participant characteristics
Womens characteristics at enrolment and during followup are presented in Table 1. We found no baseline
differences between women assigned to standard posttest

HIV counselling or COC and very little differences

between women followed-up and those lost-to-followup. Womens median age at baseline varied between 21 in
Dominican Republic and 27 years in Cameroon. Women
were more likely to be primiparous in Georgia and India
(52.5 and 41.9%, respectively) than in Cameroon or
Dominican Republic (<30%). All or almost all women
were married in India (99.0%) and Georgia (83.7%),
whereas in Cameroon only 37.8% were formally married;
in Dominican Republic women were mostly in free
union (83.1%). More than 40% of women in Georgia and
India had been accompanied by their partner to their

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Median age in years (IQR)

Median education level, years (IQR)
Remunerated activity
Primiparous
Median gestational age (IQR)
Union
Free union
Married
Not in union (single, divorced,
widowed)
Median duration relationship, years (IQR)
Cohabitation with
Partner only
Partner and family/in-laws
Without partner (with
family/in-laws or alone)
See each other every day
Partner violence
Ever ignored
Ever insulted
Ever slapped, hurt
Partner alcohol consumption
Never
Occasionally
Frequently
Partner accompanied woman to ANC
Perception of partner involvement in
her pregnancy
None/Not enough
Normal
High
Ever discussed about HIV with
partner
Ever discussed about condoms
with partner
Perception of HIV risk
Yes
Don not know
No
Ever tested for HIV
Partner ever tested for HIV
Knowledge someone close tested for HIV
Wish to suggest HIV testing to partner

At enrolment (n 1943)
2331
1116
42.7
26.7
1220
32.4
35.7
32.0
27
34.0
34.0
32.0
71.7
50.4
44.0
29.5
22.9
62.1
15.0
18.3
3.5
33.0
63.5
86.7
83.0
59.6
16.7
23.8
84.6
71.4
86.3
92.5

78
86
77
4
82
82
77
172
121
106
71
55
149
36
44
8
76
146
209
200
143
40
57
204
172
207
223

N 245

27
14
103
64
16

SC

COC
%

150
42
44
204
165
192
225

193

12
88
131
216

57
148
31
45

111
106
76

181

86
85
64

71
97
68

63.6
17.8
18.6
86.4
69.9
81.7
95.3

81.8

5.2
38.1
56.7
91.5

24.2
62.7
13.1
19.1

47.0
44.9
32.2

77.0

36.6
36.2
27.2

28

30.1
41.1
28.8

2331
1116
46.2
19.7
1220

N 239
27
13
109
46
16

Cameroon

35
41
163
137
91
130
204

153

16
78
145
141

61
164
13
59

73
108
36

216

151
55
34

14.6
17.2
68.2
57.1
37.9
54.4
87.6

63.8

7.0
33.9
63.0
58.8

25.6
68.9
5.5
24.6

30.5
45.2
15.1

91.1

62.9
22.9
14.2

15

85.4
5.0
9.6

1926
812
18.3
28.0
919

N 242

2.5

204
12
23

22
10
44
67
13

SC

26
33
176
134
96
118
206

138

17
70
148
144

71
155
9
64

55
95
24

219

162
43
30

11.1
14.0
74.9
57.0
40.9
50.4
90.4

58.7

7.6
31.3
66.1
61.3

30.2
66.0
3.8
27.4

23.5
40.6
10.3

93.2

68.9
18.3
12.8

15

84.3
6.8
8.9

1927
812
23.8
29.4
1121

N 242

2.3

198
16
21

21
10
56
69
16

COC

Dominican Republic

Table 1. Characteristics of participating pregnant women. Prenahtest ANRS 12127 trial (20092011).

61
45
139
93
37
70
120

86

25
94
123
109

35
191
19
104

49
24
8

222

81
157
7

26
215
4

24.9
18.4
56.7
38.0
15.1
28.6
49.2

35.1

10.8
40.5
53.0
44.5

14.3
78.0
7.8
42.4

20.0
9.8
3.3

90.6

33.1
64.1
2.9

0.85

10.6
87.8
1.6

2230
1115
30.2
53.5
913

N 245
26
15
74
131
11

SC

COC
%

51
32
163
95
22
62
125

110

28
124
94
101

25
202
17
94

59
29
4

214

87
142
17

43
196
7

20.7
13.0
66.3
38.6
8.9
25.2
51.2

44.7

12.0
52.0
40.2
41.1

10.2
82.8
7.0
38.2

24.2
11.9
1.6

87.3

35.4
57.7
6.9

0.75

17.5
79.7
2.8

2230
1116
29.3
51.6
913

N 246
25
15
72
127
12

Georgia

17
35
186
95
23
31
192

113

19
61
158
111

170
60
8
98

27
36
45

227

109
113
16

2.4

0
238
0

7.1
14.7
78.2
39.9
9.7
13.0
81.0

47.5

8.2
26.3
68.1
46.6

71.4
25.2
3.4
41.2

11.3
15.1
18.9

95.4

45.8
47.5
6.7

1.14.6

0
100
0

2024
712
24.8
41.2
1625

N 241
21.5
10
59
98
20

SC

India

17
26
198
81
21
29
182

124

24
51
166
110

166
57
16
107

29
36
39

224

94
128
19

0
241
0

7.1
10.8
82.2
33.6
8.7
12.0
76.2

51.5

10.2
21.6
70.3
45.6

69.5
23.8
6.7
44.4

12.0
14.9
16.2

92.9

39.0
53.1
7.9

14.1

0
100
0

2023
710
20.7
43.6
1627

N 243
21
10
50
105
20

COC

Partner HIV testing Orne-Gliemann et al.

1171

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

0.9
99.1
65.4
91.1M
90.7
2
211
140
195
194
2
216
124
166
191
0.4
94.8M
91.8M
71.0M
91.8M
1
219
212
164
212
0
78.5
39.0
33.3
50.9
0
179
89
76
116
2
188
156
162
164
0.5
98.1
74.4
74.4
68.6

1.0
97.4
80.8
83.9M
85.0M

N 228
N 193

Woman identified as HIV-infected

HIV status disclosure to partner
Discussed about HIV with partner
Discussed about condoms with partner
Suggested HIV to testing to partner

22
209
170
173
179

10.1
95.9
78.0
79.4
82.1

28
203
171
163
180

13.3
96.7
80.7
76.9
84.9

1
207
157
157
144

N 211
N 212
N 218
During follow-up (n 1726)

% among available responses; ANC, Antenatal care; COC, couple-oriented posttest HIV counselling; IQR, interquartile range; SC, standard posttest HIV counselling.
M
P < 0.05.

N 214
N 219
N 231

N 245
N 242
N 242
N 239
At enrolment (n 1943)

SC

n
N 245

n
%
COC
Cameroon

0.9
99.5
56.6
75.8
87.2

N 243
N 246

n
i
%

COC
SC

Dominican Republic

SC

Georgia

COC

SC

India

COC

N 241

2013, Vol 27 No 7
%

AIDS

Table 1 (continued )

1172

ANC visit, much less so in the two other sites (18.4% in

Cameroun and 25.4% in Dominican Republic). Women
in Cameroon reported a history of couple communication on HIV (87.8%), whereas HIV had been little
discussed within couples in India (45.7%) and Georgia
(42.8%). Most women in Cameroon reported a history of
HIV testing (84.3%) compared with 38.3% in Georgia
and 36.4% in India. Women reported that their partner
had been previously tested for HIV in 69.6% of cases in
Cameroon, 38.6% in Dominican Republic, 12.0% in
Georgia and 9.1% in India.
HIV prevalence in the study sample was 11.6% in
Cameroon and below 1% in the three other sites. More
than 95% of women disclosed their HIV status to their
partner, with comparable rates in both study groups,
except in Georgia where disclosure was significantly more
likely within the COC group (94.8 versus 78.5%,
P < 0.0001). In Georgia, couple communication regarding HIV and condoms during the follow-up period was
poor among women from standard posttest HIV counselling group (<40%) and significantly higher among
women from COC group (>70%, P < 0.0001). Women
in Dominican Republic and Georgia were significantly
more likely to have suggested HIV testing to their partner
than women from standard posttest HIV counselling
group; no difference according to group was observed in
Cameroon and India.

Partner HIV testing rates and effect of coupleoriented posttest HIV counselling
Overall, COC resulted in an absolute gain in partner
HIV testing rates, which varied between study sites.
According to the combined indicator integrating both
laboratory and womans self-reported data on partner HIV
testing, 59 partners (24.7%) in Cameroon were tested for
HIV in COC group versus 35 (14.3%) in standard posttest
HIV counselling group [OR 1.97; CI (1.243.13)];
in Dominican Republic, 56 partners (23.1%) versus
49 (20.3%) [OR 1.19; CI (0.771.83)]; in Georgia,
66 partners (26.8%) versus three (1.2%) [OR 29.57;
CI (9.1595.56)]; and in India, 86 partners (35.4%)
versus 64 (26.6%) [OR 1.51; CI (1.032.23)]
(Table 2).
When looking only at the data notified by the laboratory,
the effect of COC on partner HIV testing rates remained
highly significant in Cameroon, Georgia and in India
(P < 0.01) and became significant in Dominican Republic, with a significantly higher proportion of partners
tested from COC group compared with standard posttest
HIV counselling group [8.3 versus 2.5%, OR 3.54;
CI (1.408.98)].

Adverse events
In total, 77 women reported separating from their partner
during the follow-up period, most in Dominican
Republic (n 51). There was no significant difference

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Partner HIV testing Orne-Gliemann et al.

1173

Table 2. Effect of prenatal couple-oriented HIV counselling on partner HIV testing rates (n U 1943). Prenahtest ANRS 12127 trial (20092011).
Laboratory logbooks
N
Cameroon
SC (n 245)
COC (n 239)
Dominican Republic
SC (n 242)
COC (n 242)
Georgia
SC (n 245)
COC (n 246)
India
SC (n 241)
COC (n 243)

OR

95% CI

Combined indicatora

Self-reported by women
p

OR

95% CI

OR

95% CI

14 5.7
35 14.6

ref
2.83 1.485.41

35 14.3
<0.01 56 23.4

ref
1.84 1.152.93

35 14.3
0.01 59 24.7

ref
1.97 1.243.13

<0.01

6
20

ref
3.54 1.408.98

45 18.6
<0.01 48 19.8

ref
1.08 0.691.70

49 20.3
0.73 56 23.1

ref
1.19 0.771.83

0.44

2.5
8.3

3 1.2
ref
3 1.2
ref
3 1.2
ref
65 26.4 28.97 8.9693.63 <0.01 64 26.0 28.36 8.7791.72 <0.01 66 26.8 29.57 9.1595.56 <0.01
31 12.9
68 28.0

ref
2.63 1.654.21

62 25.7
<0.01 81 33.3

ref
1.44 0.972.14

64 26.6
0.07 86 35.4

ref
1.51 1.032.23

0.04

COC, couple-oriented posttest HIV counselling; OR, unadjusted odds ratios; SC, standard posttest HIV counselling. Intention-to-treat analysis.
a
Notified within laboratory logbooks AND/OR self-reported by women.

in union break-ups between women from standard

posttest HIV counselling and COC groups in all sites
(Table 3). Less than 16% of women reported emotional
violence from their partner during the follow-up period.
Verbal violence was very rarely reported in Georgia
(<3%), however, it was more frequent in Dominican
Republic (>17%). Physical violence was reported by less
than 7% of women overall. Women from COC group
were less likely to report emotional violence than women
from standard posttest HIV counselling group in Georgia
and India (3.5 versus 11.8% and 9.4 versus 16.0%,
respectively), and less likely to report physical violence in
Cameroon and India (1.9 versus 6.4% and 6.5 versus
12.8%, respectively) (Table 3).

Factors associated with partner HIV testing

Factors associated with partner HIV testing were
documented among women followed-up at least once
and for whom all variables of interest were documented
(n 1607). The adjusted models are presented Table 4.
In Cameroon, among the factors significantly associated
with partner HIV testing (combined indicator) was
the fact that the woman had received COC [Adjusted
OR (AOR) 2.4; CI (1.44.0), P < 0.01], was

HIV-infected [AOR 2.4; CI (1.15.0), P 0.02],

reported having ever discussed condoms with her
partner [AOR 2.4; CI (1.15.3), P 0.03] and that
her partner had been previously tested for HIV
[AOR 2.3; CI (1.34.2), P < 0.01]. In Dominican
Republic, partners were more likely to have been tested
for HIV when the woman perceived her partner
as very involved in her pregnancy [AOR 2.3;
CI (1.34.1), P 0.02, compared with normally
involved] and when her partner had been previously
tested for HIV [AOR 3.8; CI (2.17.2), P < 0.01].
In Georgia, partner HIV testing was more likely
when the woman had received COC [AOR 20.5;
CI (5.970.5), P < 0.01], when her partner had been
previously tested for HIV [AOR 4.2; CI (1.4
13.2), P 0.03] and when she wished to suggest HIV
testing to her partner [AOR 1.9; CI (1.13.7),
P 0.03]. Finally in India, among the factors significantly associated with partner HIV testing were
that the woman had received COC [AOR 1.7;
CI (1.12.5), P 0.01], had been accompanied by
her partner to ANC [AOR 2.0; CI (1.33.1),
P < 0.01] and had suggested HIV testing to her partner
[AOR 2.3; CI (1.15.1), P 0.03].

Table 3. Conjugal violence and union break-ups reported during the follow-up period (n U 1726). Prenahtest ANRS 12127 trial (20092011).
Cameroon
(n 430)

Union break-up (%)

Violence (%)
Emotional violence
Verbal violence
Physical violence

Dominican Republic
(n 404)

Georgia
(n 459)

India
(n 433)

SC
(n 218)

COC
(n 212)

SC
(n 211)

COC
(n 193)

SC
(n 228)

COC
(n 231)

14 (6.4)

8 (3.8)

0.22

23 (10.9)

27 (14.0)

0.35

2 (0.9)

1 (0.4)

0.62

29 (13.3)
36 (16.5)
14 (6.4)

24 (11.4)
25 (11.9)
4 (1.9)

0.54
0.17
0.02

27 (12.8)
44 (20.9)
8 (3.8)

21 (10.9)
36 (18.7)
6 (3.1)

0.55
0.58
0.71

27 (11.8)
6 (2.6)
0

8 (3.5)
2 (0.9)
0

<0.01
0.15

SC
(n 219)

COC
(n 214)

1 (0.5)

1 (0.5)

1.00

35 (16.0)
44 (20.1)
30 (13.7)

20 (9.4)
30 (14.0)
14 (6.5)

0.04
0.09
0.01

COC, couple-oriented posttest HIV counselling; Emotional violence, woman reported that her partner ignored her or refused to listen/talk to her;
Physical violence, woman report that her partner slapped her, thrown anything at her or hurt her physically; SC, standard posttest HIV counselling;
Verbal violence, woman reported that her partner insulted her or talked to her badly.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

1.414.02
1.596.20
Ref
0.893.35
1.123.47
1.394.55

1.145.04
Ref
1.2511.74
0.678.13
1.105.33

1.6010.18

2.38
3.14
1
1.73
1.97
2.52

2.40
1
3.84
2.33
2.42

4.04

CI

<0.01

0.03

0.02
0.03

0.02
<0.01

<0.01
<0.01

P-value

1.20
3.85
1

1
2.04
2.28

2.51

1.43

AOR

0.582.50
2.077.16
Ref

Ref
0.459.16
1.274.10

1.404.51

0.862.36

CI

<0.01

0.02

<0.01

0.17

P-value

1.053.66
1.3481.19

10.43

Ref
1.3713.17
1.115.29

1.537.32
0.784.32
Ref

5.9670.48

CI

1.96

1
4.25
2.42

3.35
1.83
1

20.50

AOR

Georgia
(N 435)

0.03

0.03

0.03

<0.01
0.01

P-value

2.35

1.65
2.04

1.67

AOR

1.085.14

1.012.69
1.343.10

1.102.54

CI

India
(N 407)

0.03

0.04
<0.01

0.02

P-value

Adjusted logistic regressions, stratified on study site (Final model). ANC, antenatal care; AOR, adjusted odds ratio; CI, 95% confidence interval; COC, couple-oriented posttest HIV counselling; SC,
standard posttest HIV counselling. The analysis of the factors associated with partner HIV testing was conducted among a sub-sample of women enrolled in the trial for which there was no missing data
in the variables of interest. Four separate models were conducted for each study site.

COC versus SC
Age (in years)
<25
[2530]

30
Relationship duration (<1 versus
1 year)
Women remunerated activity (yes versus no)
Partner alcohol consumption (never versusfreq/occas)
Partner accompanied woman to ANC (yes versus no)
Perception partner involvement
Normal
Not/not enough
High
HIV status (HIV versus HIV)
Partner ever HIV tested
Do not know
Yes
No
Ever discussed condom use with partner (yes versus
no/do not know condoms)
Wishes to suggest HIV testing to partner (yes versus
no/not sure)
Discussed HIV with partner during follow-up
(yes versus no)
Had suggested HIV testing to partner during
follow-up (yes versus no)

AOR

Dominican Republic
(N 363)

AIDS

Cameroon
(N 402)

Table 4. Factors associated with partner HIV testing (combined indicator) in Cameroon, Dominican Republic, Georgia and India (n U 1607). Prenahtest ANRS 12127 trial (20092011).

1174
2013, Vol 27 No 7

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Partner HIV testing Orne-Gliemann et al.

Discussion
Our primary result is that, as hypothesized, a behavioural
intervention delivered to pregnant women, which takes
into account their couple relationship, can increase the
uptake of HIV testing among men in the context of
ANC. In the context of increased investments towards
the elimination of mother-to-child transmission of HIV,
COC, integrated within ANC and PMTCT services in
replacement of standard posttest HIV counselling, could
contribute to improve the coverage of mens HIV testing
worldwide. In low HIV prevalence settings, valorising
such a beneficial effect of prenatal HIV counselling and
testing is all the more so relevant that the number
of paediatric HIV infections avoided by PTMCT are a
priori limited.
We observed different effects of COC across study
sites, rather limited in Dominican Republic and very
important in Georgia. This suggests that the level of
HIV prevalence may not be a key determinant of the
acceptability of partner HIV testing. The analysis of the
socio-behavioural factors associated with partner HIV
testing provides further insight on why and how COC
may have influenced womens attitudes and their partners
behaviour. In India and Georgia, mens presence in ANC
is relatively frequent and in our study was used as an
opportunity for partner HIV testing (significant association in Georgia in univariate analysis only). However,
partner HIV testing in ANC may be challenging in
certain settings [20]. Qualitative results from our pretrial
pilot study [18] showed that, in the Cameroon and
Dominican Republic study sites, the attitudes of
healthcare workers towards men were often harsh,
ANC wards were too crowded, and thus men felt
ill-at-place, as reported by others in Uganda [21]. Partners
in these two sites may have preferred to be tested for HIV
in non-ANC laboratories or free-standing HIV counselling and testing centres. And this is why, although the
laboratory logbooks provide verifiable data, they may also
underestimate the rates of partner HIV testing. Further,
the fact that overall fewer partner HIV tests were
performed at the site laboratories, as compared to those
self-reported by women, may to some extent reflect a
social desirability bias, whereby women over-reported
partner HIV testing to please the interviewer, which
could also explain the absence of difference in selfreported partner HIV testing rates among women from
standard posttest HIV counselling and COC groups.
We observed that in Cameroon, Dominican Republic
and Georgia, men were more likely to be tested for HIV
during their partners pregnancy when they had already
been tested once. Understanding mens motivation and
perceptions of the benefits of HIV testing, both as
individuals and within their couple, is thus crucial to
further improve uptake [2226]. In addition, partners
were more likely to have been tested when women had

1175

suggested HIV testing to their partner in Cameroon and

India. Partner HIV testing was not associated with
verbal couple communication on HIV in Dominican
Republic where local gender roles may not place
women as the best initiators of partner HIV testing. A
medical prescription from health workers could be
helpful to encourage partners to be tested [27], however,
the efficacy of such a strategy was not confirmed in a
recent trial [14]; invitations distributed by influential
people may be another intervention successful in
prompting couples to seek joint HIV testing as shown
in Rwanda [28]. Finally in Cameroon, partner HIV
testing was associated with couple communication on
condom. These results suggest that COC may have
supported women who had already initiated a conjugal
discussion around HIV prevention to suggest HIV
testing to their partner. They also confirm that HIV
testing remains a key entry point for the prevention of
sexual risks within the couple.
Another important result of our trial is that not only was
COC shown to be safe but it also seemed to have potential
benefits in reducing partner violence in Georgia and
India. The counselling, education and role play activities
conducted during COC are likely to have helped women
in finding the right moment and the right words to
discuss sensitive topics with their partner, such as HIV
prevention and specifically partner HIV testing.
In spite of the positive impact of COC, partner HIV
testing rates remained low in the four study sites, with
overall less that a third of men tested for HIV during their
partners pregnancy. With the scaling-up of treatment
programmes, HIV testing will be increasingly available
in primary healthcare centres, within mobile clinics,
through door-to-door programmes or even maybe
within community sites such as bars [29]. Multiplying
HIV testing options for men and mainstreaming HIV
counselling and testing services in community development and health programmes will be critical to promote
partner HIV testing as a culturally acceptable behaviour
and increase the acceptability of HIV prevention
initiatives targeting couples.
This study has certain limitations. First, COC is a brief,
single-session counselling intervention and, as such, was
certainly limited in the amount of individualized skill
building it could provide. Second, because of the large
socio-cultural differences and variations in participant
characteristics according to the country, we conducted
four separate explanatory models to assess the factors
associated with partner HIV testing, which means that
we could not directly compare results across sites. Finally,
because a large proportion of men tested for HIV in
Cameroon were tested outside the study site, their
HIV status could not be confirmed, and thus we were
unable to investigate sero-discordance as an explanatory
variable.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

1176

AIDS

2013, Vol 27 No 7

Overall, however, this trial is the first to show the efficacy

of a counselling intervention in increasing partner HIV
testing rates in low-resource settings. Further, the
multisite design allowed documenting the impact of
COC according to diverse socio-cultural backgrounds
and in different epidemiological contexts. Investing in
couple-oriented prenatal HIV counselling and integrating a couple approach to HIV prevention within routine
mother and child health services, at the health centre level
as well as within the community, could be a simple public
health strategy contributing to the elimination of motherto-child transmission of HIV and to improve the
management of sexual risks in a conjugal context.

Acknowledgements
We thank our fieldwork team for their efforts and the
counsellors dedicated to providing women with the
best service possible. Special thanks to Brigitte Bazin,
Claire Rekacewicz and Laurence Quinty (ANRS), and
Catherine Wilfert (EGPAF) for encouraging the study
team throughout the trial. We would like to thank also
Karen Malateste for her involvement in the early stages of
the analysis.
J.O.G. wrote the study proposal, was the overall trial
coordinator and led the process of data analysis,
interpretation, and paper writing. All authors participated
in designing the study and the questionnaires. P.T., M.M.,
E.P-T, S.D., M.B. were the local site coordinators,
provided advice during study design and managed the
fieldwork. F.D., P.T. and A.D.L. were the study
investigators and provided advice during study design
and fieldwork. All authors cointerpreted the data and
co-wrote the article. E.B. and M.P. conducted the
statistical analysis. S.K. and F.E. provided advice during
fieldwork, data analysis, data interpretation, and writing.
This research was sponsored and primarily funded by the
Agence Nationale de Recherches sur le SIDA et les
hepatites virales (French Nationale Agency on AIDS
Research) (grant ANRS 12127). Complementary funding was provided by the Elizabeth Glaser Pediatric AIDS
Foundation (Sub-agreement 35407).
No funding bodies had any role in study design, data
collection and analysis, decision to publish, or preparation
of the manuscript.
ClinicalTrials.gov: NCT01494961.
Members of the Prenahtest ANRS 12127 Study Group
Principal investigators: Francois Dabis, Patrice Tchendjou
Trial coordinator: Joanna Orne-Gliemann

Site coordinators: Maia Butsashvili (Georgia), Shrinivas

Darak (India), Marija Miric (Dominican Republic), Eddy
Perez-Then (Dominican Republic - Investigator), Patrice
Tchendjou (Cameroon)
Methodology, biostatistics, data management (Bordeaux): Eric
Balestre, Karen Malateste, Melanie Plazy
Data collection: Denise Amassana (Cameroun), Tatiana
Etounou (Cameroon), Mukta Gadgil (India), Maia Kajaia
(Georgia), Maitreyi Kulkarni (India), Mildred Martinez
(Dominican Republic), Angeline Ngo Essounga (Cameroon), Laura Nunez (Dominican Republic), Lucia Santos
(Dominican Republic), Marina Topuridze (Georgia)
Social sciences expertise: Annabel Desgrees du Lou, Fred
Eboko
Public health expertise: Sanjeevani Kulkarni, Vinay
Kulkarni, Eddy Perez-Then

Conflicts of interest
There are no conflicts of interest.

References
1. Coates TJ, Richter L, Caceres C. HIV Prevention 3 behavioural
strategies to reduce HIV transmission: how to make them work
better. Lancet 2008; 372:669684.
2. The Voluntary HIV-1 Counseling and Testing Efficacy Study
Group. Efficacy of voluntary HIV-1 counselling and testing in
individuals and couples in Kenya, Tanzania, and Trinidad: a
randomised trial. Lancet 2000; 356:103112.
3. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour
MC, Kumarasamy N, et al. Prevention of HIV-1 infection with
early antiretroviral therapy. N Engl J Med 2011; 365:493505.
4. World Health Organisation. Towards universal access. Scaling
up priority HIV/AIDS interventions in the health sector. Progress
report 2010. Geneva: World Health Organisation 2010.
Available from: http://whqlibdoc.who.int/publications/2010/
9789241500395_eng.pdf. [Accessed 8 November 2011].
5. Farquhar C, Kiarie JN, Richardson BA, Kabura MN, John FN,
Nduati RW, et al. Antenatal couple counseling increases
uptake of interventions to prevent HIV-1 transmission. J Acquir
Immune Defic Syndr 2004; 37:16201626.
6. Msuya SE, Mbizvo EM, Hussain A, Uriyo J, Sam NE, StrayPedersen B. Low male partner participation in antenatal HIV
counselling and testing in northern Tanzania: implications for
preventive programs. AIDS Care 2008; 20:700709.
7. Kakimoto K, Kanal K, Mukoyama Y, Chheng TV, Chou TL,
Sedtha C. Influence of the involvement of partners in the
mother class with voluntary confidential counselling and testing acceptance for prevention of mother to child transmission
of HIV programme (PMTCT programme) in Cambodia. AIDS
Care 2007; 19:381384.
8. Kiarie JN, Kreiss JK, Richardson BA, JohnStewart GC. Compliance with antiretroviral regimens to prevent perinatal HIV-1
transmission in Kenya. AIDS 2003; 17:6571.
9. Sarker M, Sanou A, Snow R, Ganame J, Gondos A. Determinants of HIV counselling and testing participation in a Prevention of Mother-to-Child Transmission programme in rural
Burkina Faso. Trop Med Int Health 2007; 12:14751483.
10. Aluisio A, Richardson BA, Bosire R, John-Stewart G, MboriNgacha D, Farquhar C. Male antenatal attendance and HIV
testing are associated with decreased infant HIV infection and
increased HIV-free survival. J Acquir Immune Defic Syndr
2011; 56:7682.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Partner HIV testing Orne-Gliemann et al.

11. Allen S, Meinzen-Derr J, Kautzman M, Zulu I, Trask S, Fideli U,
et al. Sexual behavior of HIV discordant couples after HIV
counseling and testing. AIDS 2003; 17:733740.
12. Roth DL, Stewart KE, Clay OJ, van Der Straten A, Karita E, Allen
S. Sexual practices of HIV discordant and concordant couples
in Rwanda: effects of a testing and counselling programme for
men. Int J STD AIDS 2001; 12:181188.
13. Dunkle KL, Stephenson R, Karita E, Chomba E, Kayitenkore K,
Vwalika C, et al. New heterosexually transmitted HIV infections in married or cohabiting couples in urban Zambia and
Rwanda: an analysis of survey and clinical data. Lancet 2008;
371:21832191.
14. Byamugisha R, Astrom AN, Ndeezi G, Karamagi CA, Tylleskar
T, Tumwine JK. Male partner antenatal attendance and HIV
testing in eastern Uganda: a randomized facility-based intervention trial. J Int AIDS Soc 2011; 14:43.
15. Prenahtest ANRS 12127 Protocol. 18 December 2008. Available from: http://etudes.isped.u-bordeaux2.fr/PRENAHTEST/
PRENAHTEST_Protocol.pdf. [Accessed 8 November 2011].
16. UNAIDS. Report on the Global AIDS Epidemic. Geneva:
UNAIDS 2010. Available from: http://www.unaids.org/en/
media/unaids/contentassets/documents/unaidspublication/2010/
20101123_globalreport_en.pdf. [Accessed 8 November 2011].
17. World Health Organisation, Centres for Disease Control and
Prevention. Prevention of mother-to-child transmission of HIV
infection generic training package. Participant manual. Geneva:
World Health Organisation 2008. Available from: http://
www.womenchildrenhiv.org/pdf/p03-pi/gtp-01-08/
GTP_PB_2008_final.pdf. [Accessed 8 November 2011].
18. Orne-Gliemann J, Tchendjou PT, Miric M, Gadgil M, Butsashvili M, Eboko F, et al. Couple-oriented prenatal HIV counseling
for HIV primary prevention: an acceptability study. BMC
Public Health 2010; 10:197.
19. Orne Gliemann J, For the Prenahtest ANRS 12127 Study Group.
Couple-oriented posttest HIV counselling. Manual for conducting the intervention 2009. Available from: http://etudes.isped.
u-bordeaux2.fr/PRENAHTEST/PrenahtestInterventionManual_
6May09.pdf. [Accessed 8 November 2011].

1177

20. Ditekemena J, Matendo R, Koole O, Colebunders R, Kashamuka

M, Tshefu A, et al. Male partner voluntary counselling and
testing associated with the antenatal services in Kinshasa,
Democratic Republic of Congo: a randomized controlled trial.
Int J STD AIDS 2011; 22:165170.
21. Byamugisha R, Tumwine JK, Semiyaga N, Tylleskar T.
Determinants of male involvement in the prevention of
mother-to-child transmission of HIV programme in Eastern
Uganda: a cross-sectional survey. Reprod Health 2010; 7:12.
22. Larsson EC, Thorson A, Nsabagasani X, Namusoko S, Popenoe
R, Ekstrom AM. Mistrust in marriagereasons why men do not
accept couple HIV testing during antenatal care- a qualitative
study in eastern Uganda. BMC Public Health 2010; 10:769.
23. Theuring S, Mbezi P, Luvanda H, Jordan-Harder B, Kunz A,
Harms G. Male involvement in PMTCT services in Mbeya
Region, Tanzania. AIDS Behav 2009; 13 (Suppl 1):92102.
24. Katz DA, Kiarie JN, John-Stewart GC, Richardson BA, John FN,
Farquhar C. Male perspectives on incorporating men into
antenatal HIV counseling and testing. PLoS One 2009; 4:e7602.
25. Aarnio P, Olsson P, Chimbiri A, Kulmala T. Male involvement in
antenatal HIV counseling and testing: exploring mens perceptions in rural Malawi. AIDS Care 2009; 21:15371546.
26. Tchendjou P, Koki Ndombo P, Eboko F, Malateste K, Ngo
Essounga A, Amassana, et al. Factors associated with history
of HIV testing among pregnant women and their partners in
Cameroon. Baseline data from a behavioural intervention trial
(ANRS 12127 Prenahtest). J Acq Immune Defic Syndr 2011;
57(Suppl 1):915.
27. Mlay R, Lugina H, Becker S. Couple counselling and testing for
HIV at antenatal clinics: views from men, women and counsellors. AIDS Care 2008; 20:356360.
28. Wall K, Karita E, Nizam A, Bekan B, Sardar G, Casanova D, et al.
Influence network effectiveness in promoting couples HIV
voluntary counseling and testing in Kigali, Rwanda. AIDS
2012; 26:217227.
29. Menzies N, Abang B, Wanyenze R, Nuwaha F, Mugisha B,
Coutinho A, et al. The costs and effectiveness of four HIV counseling and testing strategies in Uganda. AIDS 2009; 23:395401.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.