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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. 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