Epidemiology and social: CONCISE COMMUNICATION
Delayed first consultation after diagnosis of HIV infection in Cameroon
Marcellin, Fabiennea,b,c; Abé, Clauded; Loubière, Sandrinea,b,c; Boyer, Sylviea,b,c; Blanche, Jérômea,b,c; Koulla-Shiro, Sinatae; Ongolo-Zogo, Pierref; Moatti, Jean-Paula,b,c; Spire, Brunoa,b,c; Carrieri, Maria Patriziaa,b,c; and the EVAL Study Group
aINSERM, U912 (SE4S), France
bUniversité Aix Marseille, IRD, UMR-S912, France
cORS PACA, Observatoire Régional de la Santé Provence Alpes Côte d'Azur, Marseille, France
dSocio-anthropological Research Institute (IRSA), Catholic University of Central African States
eMinistry of Public Health, Division of Health Operations Research, Cameroon
fMinistry of Public Health – CHU, Yaoundé, Cameroon.
* Members of the EVAL Study Group are listed in the Acknowledgements.
Received 10 December, 2008
Revised 5 February, 2009
Accepted 13 February, 2009
Correspondence to Fabienne Marcellin, INSERM U912/ORS PACA, 23 rue Stanislas Torrents, 13006 Marseille, France. Tel: +33 4 96 10 28 79; fax: +33 4 96 10 28 99; e-mail: email@example.com
Objectives: To study the impact of both decentralization of HIV care and individual factors on delayed first consultation (≥6 months) after HIV diagnosis in Cameroon, in the context of the national antiretroviral treatment scale-up program.
Design: The national cross-sectional multicenter survey EVAL (ANRS 12-116) was conducted from September 2006 to March 2007 in 27 HIV centers in Cameroon.
Methods: Logistic regression was used to characterize patients with delayed first consultation among 3151 HIV-infected adults.
Results: Fifteen percent of patients reported a delay of at least 6 months before their first consultation after HIV diagnosis. In the multivariate analysis adjusted for the frequency of visits to the HIV center, independent correlates of reporting a delay of at least 6 months before consulting included the characteristics of the HIV centers (created before 2005 and located in small or medium-size hospitals) and the following individual patient characteristics: sex and matrimonial status (women living in a couple), the circumstances of the HIV diagnosis (test not performed in the hospital providing HIV care, test performed during a voluntary screening campaign) and patient's negative perception of antiretroviral treatment toxicity.
Conclusion: Delays before first consultation for HIV care in Cameroon have been reduced, thanks to the full implementation of the national program of decentralization. Results underline the importance of coordinating diagnosis with treatment activities and the need to develop counseling actions, focusing on the balance between antiretroviral treatment effectiveness and its potential side effects. Counseling should also be part of patients' follow-up after diagnosis during voluntary screening campaigns.
Late diagnosis and entry into HIV care can result in early death among HIV-infected patients [1–3], notably because of the complexity of managing patients with advanced disease . On the contrary, earlier initiation of antiretroviral treatment (ART) is known to increase patients' life expectancy, with a faster resolution of opportunistic infections and a decreased risk of recurrence . In high-income countries, 10–40% of patients still consult with CD4 cell counts below 200 cells/μl or with symptomatic HIV disease [6–11]. Late presentation is even more frequent in resource-limited countries, where most individuals do not know their HIV status until they experience symptoms . To decrease the burden of HIV-related morbidity and mortality, there is an urgent need to develop improved strategies to initiate ART at the most appropriate time .
Cameroon is among those western and central African countries most affected by the AIDS epidemic . Since 2001, this country has been developing a large national program for access to ART, characterized by the progressive two-step decentralization of HIV care from the central level, in the economic and administrative capital cities of Yaoundé and Douala to an intermediate level in provincial hospitals (first step, between 2001 and 2003) and, finally, to the most decentralized level in district hospitals (second step, starting in 2005).
The aim of the present study was to investigate to what extent individuals' attributes and the characteristics of healthcare facilities could influence delay in patients consulting for HIV care after HIV diagnosis in Cameroon.
Patients and methods
Study design and patients
The national cross-sectional survey EVAL (ANRS 12-116) was conducted in Cameroon from September 2006 to March 2007 and enrolled a random sample of 3151 HIV-infected adults, representative of the population of HIV-infected outpatients in the country. Participants were recruited in 27 hospitals delivering HIV care located in six provinces around the country (Centre, Littoral, West, South–West, North–West and Far-North). Eligibility criteria for entry in the survey were as follows: being aged 21 years or older and having been diagnosed HIV positive for at least 3 months. Participation was proposed to all eligible patients who were present in the hospital at the time of the survey, according to a random selection procedure. Patients who agreed to participate gave written informed consent, and refusals to participate were recorded. Clinical data were obtained from medical records and were complemented with socioeconomic and psychosocial data collected using face-to-face interviews .
We focused our interest on the delay between HIV diagnosis and the first consecutive medical consultation for HIV care. This delay was estimated using patients' answers to the following question: ‘After knowing that you were HIV positive, how much time passed before you went to consult health personnel for the treatment of your illness?’.
We used binary logistic regression to identify correlates of reporting a delay of at least 6 months before first consultation after HIV diagnosis. Factors with a P value of less than 0.25 in univariate analyses were considered eligible for entering the multivariate model. A forward stepwise selection procedure based on the likelihood ratio test was used to determine the final model (entry threshold at P = 0.05). In order to take into account the heterogeneity of patients' follow-up, analyses were adjusted for the frequency of visits to the HIV care center. In a sensitivity analysis, we performed a second regression model to explore correlates of reporting a delay of at least 1 month before consulting after HIV diagnosis. The significance level was fixed at α is equal to 0.05. The SPSS version 14.0 (SPSS Inc., Chicago, Illinois, USA) and SAS version 9.1 (SAS Institute Inc., Cary, North Carolina, USA) for Windows software were used for the analyses.
Seven patients out of 10 were women (n = 2239, 71%), mean age (SD) was 38 (9) years and 78% of patients were living in urban or semi-urban areas. Forty-eight percent of patients (69% of men and 39% of women) reported living in a couple, and 82% reported having children in their household. Three quarters of the patients were living under the poverty line of 20 000 F CFA (Francs of the Financial Cooperation in central Africa) per equivalent adult per month . Most patients (94%) had disclosed their HIV status to at least one person apart from medical staff. Nineteen percent of patients reported the presence of other HIV-positive persons in their household. Median time since HIV diagnosis [interquartile range (IQR) 25–75%] was 21 (10–36) months. Most patients (n = 2631, 84%) had been diagnosed for medically related reasons (during hospitalization for 420 patients, after showing symptoms for 1537 patients, following a medical consultation for 396 patients and during pregnancy follow-up for 278 patients), whereas the remaining 16% of patients had been diagnosed during a voluntary screening campaign. Thirty-six percent of patients had decided on their own to be tested, and 55% had been tested in their hospital of follow-up. Most patients (n = 2466, 78%) were receiving ART at the time of the survey. For these patients, median (IQR) delay between HIV diagnosis and ART initiation was 1.9 (0.2–10.1) months. Thirteen percent of patients perceived ART as being associated with many side effects, whereas 88% perceived ART as a therapy, which decreases the risk of falling ill. Median (IQR) CD4 cell count at last assessment was 336 (208–448) cells/μl, with 24% of patients having less than 200 CD4 cells/μl.
Most patients (98.7%) were being followed up for HIV, whereas a small percentage (1.3%) did not usually go to a hospital or health center for the follow-up of their illness. Nineteen percent of patients were being followed up in HIV centers created in district hospitals after 2005, and 41% of patients were being followed up in HIV centers located in large hospitals (of which 81% were hospitals from the central and provincial levels of decentralization).
A total of 477 patients (15%) reported a delay of at least 6 months between HIV diagnosis and their first medical consultation for HIV care. A delay of less than 1 month was reported by 1787 patients (57%), whereas 887 patients (28%) reported delays between 1 and 6 months. The multivariate analysis (Table 1) showed that, after adjusting for the frequency of visits to the HIV center, patients who were followed up in a HIV center located in a large hospital consulted significantly earlier than those who were followed up in a HIV center located in a small or medium-size hospital. Furthermore, after adjusting for the size of the hospital, patients who were followed up in a HIV center created in the second step of decentralization, which corresponds to centers located in district hospitals, consulted significantly earlier than the other patients. The only sociodemographic correlate of delayed consultation in the multivariate analysis was the combination of sex and matrimonial status. Women living in a couple were at significantly higher risk of reporting a delay of at least 6 months than men and other women living alone. Factors related to the circumstances of HIV diagnosis included not having been diagnosed in the same hospital providing HIV care and having been diagnosed during a HIV screening campaign as opposed to screening for medically related reasons. Finally, perceiving ART as a therapy associated with many side effects significantly prolonged the delay before first consultation.
A sensitivity analysis performed using a cutoff point of 1 month for the delay before consulting resulted in the same pattern of correlates, but with lower values for odds ratios' estimates (data not shown).
Delayed presentation after HIV diagnosis is a major issue among people living with HIV and AIDS (PLWHA), especially in resource-limited settings, in which individuals often enter into care at a late disease stage . This national representative study of HIV outpatients in Cameroon clearly shows the major benefits of decentralization in terms of prompt access to care of PLWHA.
Results also underline the problems of delayed first consultation when HIV screening facilities are not well coordinated with centers providing HIV care. The characteristics of the referral system between screening and treatment facilities are known to be correlated with access to HIV care after diagnosis . In addition, findings confirm the social vulnerability of HIV-infected women in the African setting , especially in the context of couple relationships. Finally, they underline the need for improved pretreatment counseling  in order to balance the negative impact of treatment side effects with treatment benefits.
The present study is limited by the fact that the outcome of interest is based on patients' self-reports, which may have been subject to social desirability bias. As a consequence, the length of time patients waited before seeking HIV care after diagnosis may be underestimated. Another limitation is that the population analyzed consisted almost completely of patients who had quite regular contacts with healthcare structures, leading to a probable underestimation of the number of patients with delayed access to HIV care. In addition, the cross-sectional study design prevented us from evaluating the number of patients who were diagnosed HIV positive and subsequently lost to follow-up. However, results highlighted the existence of a common pattern of determinants for delayed access to HIV care whatever the delay considered (1 or 6 months), and we may hypothesize that these determinants also predict dropout from the HIV care system.
It is important to note that most studies carried out to date in poor-resource settings have focused on the determinants of late presentation for HIV treatment . In contrast, the two major components of the causal process leading to late access to ART (late HIV diagnosis and delay before first consultation after diagnosis) have been poorly addressed until now. To our knowledge, our study is the first to explore this issue in the context of a large national program of ART scale-up in Sub-Saharan Africa.
As a conclusion, our study stresses that patients' delays before consulting for HIV care in Cameroon depend on both individual and supply-side characteristics. Although decentralization may improve access to HIV care, better strategies for timely engaging patients in a follow-up process should be thoroughly studied and implemented. Findings underline the need for improved coordination between HIV screening and care facilities. Counseling actions should be developed at the time of HIV diagnosis and before ART initiation, notably regarding the potential side effects of ART and the available means to manage them. Such actions should also be part of the follow-up of patients diagnosed during voluntary screening campaigns. The results underline the need to design interventions tailored to the African sociocultural context in order to engage women in a more complete way in HIV care. Finally, results clearly show the benefits of the national program of decentralization of HIV care in Cameroon and are very encouraging for any country engaged in a vast scale-up program.
The French National Agency for Research on AIDS and viral hepatitis (ANRS) funded the EVAL survey (ANRS 12-116) research program and the Cameroonian Ministry of Public Health supported its execution. The authors would like to thank the six hospitals that participated in the survey and their medical teams as well as all the patients who agreed to take part in the study. The authors would also like to thank Jude Sweeney for the English revision and editing of the manuscript.
F.M. and S.L. performed statistical analyses and participated in the writing of the manuscript. S.B. participated in the writing of the manuscript. J.B. was in charge of the management of the database and the recoding of variables. P.O.-Z. and S.K.-S. participated in the planning of the EVAL survey and supervised all the research projects in this survey as members of the Cameroonian Ministry of Public Health. C.A. revised the manuscript before submission and complemented it with contextual data as a member of the Socio-anthropological Research Institute of Yaoundé. J.-P.M., B.S. and M.P.C. were involved in the design of the EVAL survey. They chose the main directions for data analysis (research projects and objectives of the analyses) and participated in the interpretation of results.
The EVAL Study Group: S. Koulla-Shiro (Ministry of Public Health, Division of Health Operations Research, Yaoundé, Cameroon), P. Ongolo-Zogo (Ministry of Public Health, CHU, Yaoundé, Cameroon), J. Blanche, A-D. Bouhnik, S. Boyer, M-P. Carrieri, A. Dia, F. Eboko, S. Loubière, F. Marcellin, J-P. Moatti, Y. Obadia, C. Protopopescu, B. Spire (INSERM, IRD, University of the Mediterranean UMR 912, Marseilles, France), S-C. Abega, C. Abé, P.C. Bilé, C. Bios, R-C. Bonono, Y. Mehe, M.T. Mengue, H. Mimcheu, F. Mounsade, L.M. Ngaba, J. Ngo Mbog, S. Ngo Yebga, H. Nkwidjan (IRSA, Catholic University of Central Africa, Yaoundé, Cameroon), R. Nantchouang (GERCIS, catholic University of Central Africa, Yaoundé, Cameroon).
There are no conflicts of interest.
Data presented previously at the XVIIe International AIDS Conference in Mexico City (3–8 August 2008) and published as abstract n°TUAB0206 in the Conference abstracts book.
1. Late diagnosis/entry into HIV care can result in early deaths among infected. Study highlights human year toll
. AIDS Alert
2. Lanoy E, Mary-Krause M, Tattevin P, Perbost I, Poizot-Martin I, Dupont C, Costagliola D. Frequency, determinants and consequences of delayed access to care for HIV infection in France. Antivir Ther 2007; 12:89–96.
3. Smit C, Hallett TB, Lange J, Garnett G, de Wolf F. Late entry to HIV care limits the impact of antiretroviral therapy in the Netherlands. PLoS ONE 2008; 3:e1949.
4. Boffito M, Pillay D, Wilkins E. Management of advanced HIV disease: resistance, antiretroviral brain penetration and malignancies. Int J Clin Pract 2006; 60:1098–1106.
5. Battegay M, Fluckiger U, Hirschel B, Furrer H. Late presentation of HIV-infected individuals. Antivir Ther 2007; 12:841–851.
6. Battegay M, Fehr J, Fluckiger U, Elzi L. Antiretroviral therapy of late presenters with advanced HIV disease. J Antimicrob Chemother 2008; 62:41–44.
7. Gay CL, Napravnik S, Eron JJ Jr. Advanced immunosuppression at entry to HIV care in the southeastern United States and associated risk factors. AIDS 2006; 20:775–778.
8. Borghi V, Girardi E, Bellelli S, Angeletti C, Mussini C, Porter K, Esposito R. Late presenters in an HIV surveillance system in Italy during the period 19*92-20*06. J Acquir Immune Defic Syndr 2008; 49:282–286.
9. Delpierre C, Dray-Spira R, Cuzin L, Marchou B, Massip P, Lang T, Lert F. Correlates of late HIV diagnosis: implications for testing policy. Int J STD AIDS 2007; 18:312–317.
10. Girardi E, Aloisi MS, Arici C, Pezzotti P, Serraino D, Balzano R, et al
. Delayed presentation and late testing for HIV: demographic and behavioral risk factors in a multicenter study in Italy. J Acquir Immune Defic Syndr 2004; 36:951–959.
11. Wolbers M, Bucher HC, Furrer H, Rickenbach M, Cavassini M, Weber R, et al
. Delayed diagnosis of HIV infection and late initiation of antiretroviral therapy in the Swiss HIV Cohort Study. HIV Med 2008; 9:397–405.
12. Girardi E, Sabin CA, Monforte AD. Late diagnosis of HIV infection: epidemiological features, consequences and strategies to encourage earlier testing. J Acquir Immune Defic Syndr 2007; 46(Suppl 1):S3–S8.
13. Person AK, Ramadhani HO, Thielman NM. Antiretroviral treatment strategies in resource-limited settings. Curr HIV/AIDS Rep 2007; 4:73–79.
14. UNAIDS. Report on the global AIDS epidemic
In: WHO-UNAIDS 2008; 2008.
15. Marcellin F, Boyer S, Protopopescu C, Dia A, Ongolo-Zogo P, Koulla-Shiro S, et al
. Determinants of unplanned antiretroviral treatment interruptions among people living with HIV in Yaounde, Cameroon (EVAL survey, ANRS 12-116). Trop Med Int Health 2008; 13:1470–1478.
16. DSCN. Second survey among Cameroonian households in 2001 (ECAM II 2001): living conditions and poverty profiles in Cameroon in 2001 – main survey report. In: Yaoundé: Direction de la Statistique et de la Comptabilité Nationale, Ministère de l'Economie et des Finances, République du Cameroun; 2002.
17. Valdiserri RO, Holtgrave DR, West GR. Promoting early HIV diagnosis and entry into care. AIDS 1999; 13:2317–2330.
18. Vidal L, Lou AD. AIDS and social situations of women in Africa: from notions to research methods. Sante 2001; 11:265–272.
19. Stenson AL, Charalambous S, Dwadwa T, Pemba L, Du Toit JD, Baggaley R, et al
. Evaluation of antiretroviral therapy (ART)-related counselling in a workplace-based ART implementation programme, South Africa. AIDS Care 2005; 17:949–957.
This article has been cited 3 time(s).
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Africa; delayed access to care; scale-up
© 2009 Lippincott Williams & Wilkins, Inc.
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