Download Comparative Evaluation of Adherence to Antiretroviral Therapy in

HIV/AIDS
BRIEF REPORT
Comparative Evaluation of Adherence
to Antiretroviral Therapy in SubSaharan African Native HIV-Infected
Patients in France and Africa
Pierre Sellier,1 Philippe Clevenbergh,1 Liliana Ljubicic,1 Guy Simoneau,1
John Evans,2 Véronique Delcey,1 Myriam Diemer,1 Marc Bendenoun,1
Stéphane Mouly,1 and Jean-François Bergmann1
Service de Médecine Interne A, Hôpital Lariboisière, Paris, and 2Département
de Médecine Interne et Maladies Infectieuses, Hôpital Paul Brousse, Villejuif,
France
1
Patients with human immunodeficiency virus (HIV) infection who were native to sub-Saharan Africa but lived in
France were less adherent to antiretroviral therapy during a
visit back to Africa, compared with their level of adherence
in France. This was mainly related to self-perceived insufficient support from family members and/or fear of the consequences of disclosure of their HIV infection status to their
family.
Over the past several years, immigration from sub-Saharan Africa to Europe has greatly increased [1]. In France, individuals
from sub-Saharan Africa represented 29% of all immigrants in
1994 and 43% in 2001. Because the prevalence of HIV-1 infection is high in these countries, the increase in immigration
has led to a substantial increase in the number of sub-Saharan
African natives receiving HIV care in France. Of nearly 6000
new HIV cases recorded in 2003 in France, 19% occurred in
women from sub-Saharan Africa, and 9% occurred in men
from sub-Saharan Africa [2]. A similar trend has been reported
in other industrialized countries [3].
Many African-born patients who reside in France later visit
their country of origin. This could modify their adherence to
antiretroviral therapy (ART), although adherence to ART is
essential to derive sustained clinical benefit from therapy [4].
The aim of this study is to describe the factors affecting
adherence to ART in HIV-infected patients born in sub-Saharan
Received 14 February 2006; accepted 28 May 2006; electronically published 26 July 2006.
Reprints or correspondence: Dr. Pierre Sellier, Hôpital Lariboisière Service de Médecine
Interne A, 2 Rue Ambroise Paré, 75475 Paris Cedex 10, France ([email protected]).
Clinical Infectious Diseases 2006; 43:654–7
2006 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2006/4305-0020$15.00
654 • CID 2006:43 (1 September) • HIV/AIDS
Africa when residing in France and during visits to Africa. The
second objective is to compare adherence in Africa and in
France for the same patients (with each patient being his or
her own control subject) and to explore the possible explanations for a difference in adherence in these 2 locations.
Patients and methods. This cross-sectional observational
study was conducted in 3 infectious diseases departments in
Paris between May and December 2004. Entry criteria for the
study included being a native of sub-Saharan Africa, having
HIV infection, receiving ART, and having travelled back to the
country of origin during the previous 12 months. Consecutive
patients attending the outpatient departments who met entry
criteria were invited to participate in the study after providing
written informed consent. The interviewer surveyed demographic characteristics of the patients, adherence to ART in
France, factors possibly influencing adherence to ART in
France, adherence to ART during the previous visit to Africa,
and factors possibly influencing adherence to ART in Africa
(using the same items that were used to determine adherence
to ART in France, with additional specific questions).
Patients were categorized into 3 groups according to their
adherence to ART in France and Africa. The first group (“never
missing doses”) included patients taking all doses of ART on
all days, with possible irregular timing of intake (within 2 h).
The second group (“rarely missing doses”) included patients
missing up to 4 doses or 1 full day of treatment during a month.
The third group (“frequently missing doses”) included patients
who reported any other irregular drug intake.
For quantitative data, we report the mean value and SD.
Qualitative results are reported as frequency counts. The comparison between adherence in France and in Africa was made
by crossing the data (either quantitative or qualitative). A comparison of the most frequently reported reasons for lack of
adherence was conducted for patients rarely or frequently missing doses of ART. Quantitative data were analyzed using analysis
of variance, and qualitative data were analyzed using the x2
test. For qualitative data with 2 variables and 2 classes, Fisher’s
exact test was used.
Results. A total of 61 patients were enrolled in this study.
The countries of origin were Ivory Coast (20 patients), Congo
(10), Cameroon (9), Central African Republic (9), Mali (8), Benin (2), The Gambia (2), and the Democratic Republic of Congo
(1). A total of 42 (69%) of the 61 patients had informed their
sexual partner(s) about their HIV-positive status. Demographic
characteristics for the patients are reported in table 1.
Table 1. Evaluation of factors affecting adherence to antiretroviral therapy (ART) in France among patients
born in sub-Saharan Africa but living in France.
Variable
Percentage of total patients
Age, mean years SD
Sex
All patients
(n p 61)
Frequently
missing
doses group
(n p 16)
Rarely
missing
doses group
(n p 22)
Never
missing
doses group
(n p 23)
100
37.4 7.3
26
36.5 10.3
36
38.2 4.7
38
37.2 7.1
Male
23 (38)
3 (19)
11 (50)
9 (39)
Female
Education
58 (62)
13 (81)
11 (50)
14 (61)
22 (36)
39 (64)
10 (63)
6 (37)
8 (36)
14 (64)
4 (17)
19 (83)
24 (39)
37 (61)
13 (81)
3 (19)
7 (32)
15 (68)
4 (17)
19 (83)
37 (61)
24 (39)
6 (37)
10 (63)
15 (68)
7 (32)
16 (70)
7 (30)
62
4.4 2.9
6.3 2.7
4.1 3.7
5.3 3.0
5.6 2.7
6.1 3.2
3.4 2.0
42 (69)
13 (68)
16 (73)
13 (56)
19 (31)
3 (32)
6 (27)
10 (44)
None or primary school
Secondary school or university
Mean no. of pills per day SD
Duration of ART, mean years SD
Drug to be taken with/without food intake
Yes
No
.77
.14
.015
Employed
Yes
No
Marital status
Married/living together
Living alone
P
!.01
.09
.57
.03
.23
NOTE. Data are no. (%) of patients, unless otherwise indicated.
Adherence in France and the factors affecting it are described
in table 1, and adherence in Africa and the factors affecting it
are described in table 2. In France, the most frequently reported
reasons for a lack of adherence to therapy were “being busy”
(in 23 [61%] of the patients) and “simply forgot” (in 7 [18%])
(table 3).
A total of 38 (62%) of the 61 patients were accompanied
during the travel to Africa, and 30 (79%) of 38 had informed
their travel companions about their HIV-positive status. While
in Africa, the patients mainly stayed with relatives (in 57 [93%]
of 61 cases). Only 1 patient had to prolong his stay in Africa
longer than initially planned.
A statistically significant decrease in adherence was noted in
Africa. The proportion of patients frequently missing doses rose
from 16 (26%) of 61 patients in France to 30 (49%) of 61
patients in Africa (P p .015). The most frequently reported
reasons for lack of adherence to ART in France or Africa among
patients rarely or frequently missing their doses are shown in
table 3.
Distinct reasons were reported to explain a lack of adherence
to ART in Africa, compared with France. The answer “being
busy” was given by 12 (31%) of 38 of the patients in Africa,
compared with 23 (61%) of 38 patients in France (P p .02).
The answer “fear of social stigma” was given by 8 patients (21%)
in Africa, compared with only 2 patients (5%) in France. Although never invoked by patients to justify poor compliance
in France, the lack of a confidential place to store medications
was mentioned by 3 (8%) of the patients as a reason for poor
compliance in Africa.
Discussion. The adherence to ART of our cohort when
living in France is close to adherence levels previously reported
in industrialized countries [5–8]. Reduced adherence with increased duration of treatment has already been reported [9].
In accordance with the findings of others [6], we found a
relationship between degree of adherence and educational level
or occupation (both of which are clearly related to income
level). HIV-infected patients are less likely to be employed,
compared with the general population. In France, 28% of HIVpositive individuals are unemployed, and this percentage increases to 44% for immigrants [10].
The 2 most frequently reported reasons for lack of adherence
in our study (“being busy” and “simply forgot”) have also been
reported as reasons for lack of adherence elsewhere [11]. In
our study, adherence while in Africa is low, compared with the
findings of other series. In a cohort of Senegalese adults, 88%
of patients reported adherence to 180% of the prescribed doses
[12], with a long-term reported adherence rate of 180% [13].
Similar results have been reported for other cohorts [14, 15].
HIV/AIDS • CID 2006:43 (1 September) • 655
Table 2. Evaluation of factors affecting adherence to antiretroviral therapy (ART) in Africa among
patients born in sub-Saharan Africa but living in France.
Variable
All patients
(n p 61)
Frequently
missing
doses group
(n p 30)
Rarely
missing
doses group
(n p 8)
Never
missing
doses group
(n p 23)
Percentage of total patients
Time since most recent visit to Africa
!6 months
⭓6 months
100
49
13
38
29 (47)
32 (53)
13 (43)
17 (57)
3 (37)
5 (63)
13 (56)
10 (44)
Settlement
Urban area
43 (70)
20 (66)
5 (63)
18 (78)
18 (30)
5.5 3.8
10 (44)
7.0 3.9
3 (37)
5.1 3.3
5 (22)
3.6 2.9
Other
Duration of visit, mean weeks SD
Knowledge of HIV infection status
and/or support from family
No knowledge of status and/or
insufficient support
.53
.57
.004
.007
29 (47)
19 (63)
5 (63)
5 (22)
32 (53)
11 (37)
3 (37)
18 (78)
17 (28)
44 (72)
13 (43)
17 (57)
2 (25)
6 (75)
2 (9)
21 (91)
Frequently missing doses
16 (26)
8 (27)
2 (25)
6 (26)
Rarely missing doses
22 (36)
14 (46)
2 (25)
6 (26)
Never missing doses
23 (38)
8 (27)
4 (50)
11 (48)
Knowledge of status and/or
sufficient support
Knowledge of HIV infection status by
household members
None
Some or all
P
Adherence category in France
.02
.004
NOTE. Data are no. (%) of patients, unless otherwise indicated.
The relationship between adherence and educational level and/
or occupation has not been clearly observed for African cohorts
[15]. However, most available data about adherence to ART in
Africa come from clinical trials or selected cohorts, and their
implications are difficult to extrapolate to other patients.
The most relevant factor affecting adherence in our study is
self-perceived family support and/or the family’s and the household’s knowledge of the patient’s HIV infection status. This
confirms the findings of previously published studies conducted
for other populations [4, 6, 8]. In France, among individuals
from sub-Saharan Africa, 24% of men and 12% of women kept
their HIV infection status secret (F. Lert, personal communication). In cohorts of patients living in Africa, the rate of nondisclosure of HIV infection status to a current sexual partner
has been found to vary from 38% to 66% [16, 17]. Social or
familial stigmatization and/or fear of the consequences of revealing HIV infection status to sexual partners, in particular,
are closely related to poor adherence [14].
Among the various reasons reported, “avoiding stigma” and
“lack of a confidential place to store medications” were cited
more frequently to explain lack of adherence during the stay
in Africa than to explain lack of adherence in France. The
656 • CID 2006:43 (1 September) • HIV/AIDS
patients declared that the support by their family members was
notably stronger in France than in Africa and that more relatives
and/or members of the household were aware of their HIV
infection status in France than in Africa. The poorer adherence
observed among patients during their stay in Africa was not
related to an insufficient stock of medication, because all patients received an adequate quantity of drugs before leaving
France.
There are some limitations to our study because of its crosssectional design and the convenience sample used. The patients
included in this study received ART for several years and had
sufficient resources and an administrative situation allowing
them to travel. Whether our findings can be extrapolated to
the general population of HIV-infected individuals born in Africa but residing in France would require replication of the
study in a more controlled setting. We only assessed adherence
to therapy at a single time point. Therefore, it is impossible to
evaluate variations in adherence over time for a single individual. Some factors associated with a better adherence to therapy,
such as disclosure of HIV infection status to partners, could
either be the cause or the consequence of an adequate drug
intake. Communication bias, recall bias, and the desire to satisfy
Table 3. Comparisons of the reasons reported for irregular drug
intake in France and Africa among HIV-infected patients born in
sub-Saharan Africa but living in France.
No. (%) of patients
Reported reason
for missing a dose
Busy
Forgotten
Stigma
Adverse effects
In France
(n p 38)
23
7
2
2
(61)
(18)
(5)
(5)
In Africa
(n p 38)
12
8
8
3
(31)
(21)
(21)
(8)
Out of stock
Feeling well
2 (5)
1 (3)
1 (3)
0
Feeling bad
Inconvenient storage
1 (3)
0
3 (8)
3 (8)
physicians should have affected the answers about adherence
in France and in Africa equally and, therefore, should not have
affected the findings.
Conclusions. In our study, the degree of adherence to ART
among HIV-infected patients born in sub-Saharan African but
living in France was clearly reduced during their visit to their
country of origin. Sociodemographic and psychological variables identified as influencing adherence include occupation,
education, duration of ART, and overall self-perception of
knowledge of HIV infection status and/or support among family and household members. In Africa, the duration of the visit
and knowledge of HIV infection status and/or support by family and household members appear to alter adherence. The
reported reasons for nonadherence specific to Africa include
fear of social stigma and problems with confidential storage of
drugs; in contrast, “being busy” was mentioned more often as
a reason for nonadherence when living in France. Further studies are needed to evaluate the impact of travelling on adherence
to therapy. As adherence to therapy evolves in response to life
events, strategies have to be adapted to individual situations,
particularly during periods in which adherence to therapy is
critical.
Acknowledgments
Additional study sites and participants included S. Matheron (Hôpital
Bichat-Claude Bernard, Paris, France) and J. M. Troisvallets (Hôpital de
Gonesse, Gonesse, France).
Potential conflicts of interest. All authors: no conflicts.
References
1. Thierry X. Les entrées d’étrangers en France de 1994 à 1999 [in French].
Population 2001; 56:423–50.
2. Institut de veill sanitaire. Maladies à déclaration obligatoire: infection
à VIH et sida. Available at: http://www.invs.sante.fr/surveillance/vih
-sida/default.htm. Accessed 25 July 2006.
3. AIDS and HIV in Scotland, 1996: a summary. SCIEH Wkly Rep
1997; 31:33.
4. Paterson DL, Swindells S, Mohr J, et al. Adherence to protease inhibitor
therapy and outcomes in patients with HIV infection. Ann Intern Med
2000; 133:21–30.
5. Lopez-Suarez A, Fernandez-Guttierez del Alamo C, Perez-Guzman E,
Giron-Gonzalez JA. Adherence to the antiretroviral treatment in
asymptomatic HIV-infected patients. AIDS 1998; 12:685–6.
6. Gordillo V, Del Amo J, Soriano V, Gonzalez-Lahoz J. Sociodemographic
and psychological variables influencing adherence to antiretroviral
therapy. AIDS 1999; 13:1763–9.
7. Wenger N, Gifford A, Liu H, et al. Prevalence and predictors of HAART
use in patients with HIV infection in the United States. J Acquir Immune Defic Syndr 2000; 25:115–23.
8. Spire B, Duran S, Souville M, Leport C, Raffi F, Moatti JP. Adherence
to highly active antiretroviral therapies (HAART) in HIV-infected patients: from a predictive to a dynamic approach. APROCO Cohort
Study Group. Soc Sci Med 2002; 54:1481–96.
9. Carrieri P, Cailleton V, Le Moing V, et al. The dynamic of adherence
to highly active antiretroviral therapy: results from the French National
APROCO cohort. J Acquir Immune Defic Syndr 2001; 28:232–9.
10. Dray-Spira R, Lert F, Marimoutou C, Bouhnik AD, Obadia Y. Socioeconomic conditions, health status and employment among persons
living with HIV/AIDS in France in 2001. AIDS Care 2003; 15:739–48.
11. Weidle PJ, Ganea CE, Irwin KL, et al. Adherence to antiretroviral
medication in an inner city population. J Acquir Immune Defic Syndr
1999; 22:498–505.
12. Laurent C, Diakhate N, Ngom Gueye NF, et al. The Senegalese government’s highly active antiretroviral therapy initiative: an 18-month
follow-up study. AIDS 2002; 16:1363–70.
13. Laurent C, Ngom Gueye NF, Ndour CT, et al. Long-term benefits of
highly active antiretroviral therapy in Senegalese HIV-1–infected adults.
J Acquir Immune Defic Syndr 2005; 38:14–7.
14. Nachega JB, Stein DM, Lehman DA, et al. Adherence to antiretroviral
therapy in HIV-infected adults in Soweto, South Africa. AIDS Res Hum
Retroviruses 2004; 20:1053–6.
15. Orrell C, Bangsberg DR, Badri M, Wood R. Adherence is not a barrier
to successful antiretroviral therapy in South Africa. AIDS 2003; 17:
1369–75.
16. Nachega JB, Lehman DA, Hlatshwayo D, Mothopeng R, Chaisson RE,
Karstaedt AS. HIV/AIDS and antiretroviral treatment knowledge, attitudes, beliefs, and practices in HIV-infected adults in Soweto, South
Africa. J Acquir Immune Defic Syndr 2005; 38:196–201.
17. Degefa A, Sanders EJ, Mekonnen Y, et al. Knowledge and attitudes
towards antiretroviral therapy among factory workers participating in
a cohort on HIV and AIDS, Addis Ababa, Ethiopia. Ethiop Med J
2003; 41:75–87.
HIV/AIDS • CID 2006:43 (1 September) • 657