Frequency, determinants and consequences of delayed access to care for HIV infection in France

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1 Antiviral Therapy 12:89 96 Frequency, determinants and consequences of delayed access to care for HIV infection in France Emilie Lanoy 1,2, Murielle Mary-Krause 1,2, Pierre Tattevin 3, Isabelle Perbost 4, Isabelle Poizot-Martin 5, Caroline Dupont 6, Dominique Costagliola 1,2 * on behalf of the ANRS CO04 French Hospital Database on HIV Clinical Epidemiological Group 1 INSERM, UMR S 720, Paris, France; 2 Université Pierre et Marie Curie-Paris 6, UMR S 720, Paris, France 3 CHU Pontchaillou, Service des Maladies Infectieuses et de Réanimation Médicale, Rennes, France 4 Hôpital Archet 1, Nice, France 5 Hôpital Sainte-Marguerite CHU Marseille, Marseille, France 6 Hôpital Ambroise Paré, Service de Médecine Interne, Boulogne, France See additional online file Clinical Epidemiology Group of the FHDH *Corresponding author: Tel: ; Fax: ; Dominique.Costagliola@ccde.chups.jussieu.fr Background and objectives: We analysed the frequency and predictors of delayed access to care (DAC) for HIV infection, and its influence on survival. Methods: We studied predictors of DAC among 18,721 patients enrolled between 1997 and 2002 in the French Hospital Database on HIV (FHDH), DAC being defined by a CD4 + T-cell count below 200 copies/mm 3 and/or AIDS at FHDH enrolment. The association of DAC with the initiation of combined antiretroviral therapy (cart) and of DAC with survival were analysed with Cox multivariable models. Results: The overall prevalence of DAC was 35.7%. Compared with patients under 30 years of age, patients over 60 were 3.5 times more likely to have DAC (P<10 4 ). Compared with non-migrant women, odds ratios (OR) of DAC were higher among migrant women (1.5), non-migrant men (1.6) and migrant men (1.9; all P<10 4 ). Compared with men who have sex with men, other transmission groups had an estimated OR for DAC of 1.6 (P<10 4 ). DAC was more frequent among patients with a recent diagnosis of HIV infection [OR=1.3, 95% confidence intervals (CI)=(1.2;1.4)]. Patients with DAC received cart earlier than other patients [hazard ratio (HR)=2.2, 95% CI=(2.1;2.3)]. The DAC/mortality HR was 13.9 in the first 6 months after enrolment in the FHDH, and remained significantly higher than 1 during the subsequent 4 years. Conclusion: DAC is common in France and was associated with a higher mortality, despite early initiation of cart. Earlier access to care and specific clinical management of patients with DAC should be considered. Introduction Since the advent of combined antiretroviral therapy (cart), the incidence of AIDS-defining illnesses has fallen [1] and HIV-infected patients are living longer [2]. Overall and AIDS-free survival both depend on the CD4 + T-cell count. The risk of developing AIDS-defining illnesses is increased among patients with a late diagnosis of HIV infection [3]. Patients with CD4 + T-cell counts below 200/mm 3 at diagnosis of HIV infection have a shorter life expectancy than other patients, and most guidelines recommend cart for all patients with CD4 + T-cell counts between 200 and 350/mm 3 [4 6]. Many patients in industrialized countries access care at an advanced stage of HIV disease, when they already have AIDS or a CD4 + T-cell count below 200/mm 3. Many factors can lead to delayed access to care (DAC). Here we investigated socio-demographic factors linked to DAC in the cart era, together with the association of DAC with the clinical outcome. Methods Description of the French Hospital Database on HIV (FHDH) Since 1992, the French Hospital Database on HIV (ANRS CO 04 FHDH) has been collecting demographic, clinical and therapeutic information on patients managed in the 62 hospitals belonging to 29 HIV/AIDS treatment and information centres (CISIH). This clinical epidemiological network has been described in detail elsewhere [7]. All HIV-infected patients who give their written informed consent and are managed in a participating centre are enrolled in 2007 International Medical Press

2 E Lanoy et al. the FHDH. A standardized data collection form includes baseline characteristics, values of usual biological markers such as CD4 + T-cell counts and plasma HIV RNA levels, and clinical manifestations, treatments, death and the cause of death. Data are recorded prospectively by trained research assistants, using DMI2 software (property of the French Ministry of Health). By the end of 2003, the database contained information on more than 93,954 HIV-infected patients having attended at least one follow-up visit between 1992 and 2003; mean follow-up was 55 months. Study population Patients who were enrolled in the database between 1 January 1997 and 31 December 2002 were included in this analysis. Exclusion criteria were as follows: no available CD4 + T-cell count within 90 days after the first visit to an FHDH centre, diagnosis of HIV infection more than 30 days after this visit, and AIDS at enrolment in FHDH without a known date for the first AIDSdefining event. We also excluded patients who were diagnosed with AIDS more than 90 days before their first visit to an FHDH centre and patients with viral load under 500 copies/ml at enrolment, as they had probably previously attended a non-fhdh centre in which they had received care for HIV infection. Among the 25,329 patients aged at least 15 years who were enrolled in the FHDH cohort between 1997 and 2002, 23,077 had at least one CD4 + T-cell count within 90 days after the first visit to an FHDH centre. Of these subjects, 23,007 had been diagnosed as HIV-seropositive less than 30 days after their first visit. Of these, 153 patients were not eligible because they had a diagnosis of AIDS with no dated AIDS-defining event. A further 562 patients were excluded because AIDS had been diagnosed more than 90 days before their enrolment in the FHDH and 3,571 patients with a viral load under 500 copies/ml at enrolment were also excluded, for the reasons given above. A total of 18,721 patients met the inclusion criteria. Definition of DAC Patients were defined as having DAC if, at enrolment in the FHDH, they had AIDS (Expanded European Definition [8]), and/or a CD4 + T-cell count below 200/mm 3. This definition was chosen because international guidelines recommend cart initiation in cases of AIDS or before the CD4 + T-cell count falls below 200/mm 3 [4,6]. We used the most recent available CD4 + T-cell count during the 90-day period straddling the date of FHDH enrolment. Statistical methods The impact of each of the variables listed below on the likelihood of DAC was analysed by backward multivariable logistic regression. The following demographic variables were studied for their association with DAC: sex, age, HIV transmission group, sub-saharan African migrant status, time since HIV diagnosis and period of enrolment (to take account of changes in HIV/AIDS management over time, the study period was divided into the periods and ). Age was divided into five groups: <30 years, years, years, years and >59 years. As nationality is not recorded in the FHDH, we used the surrogate variable stays in a foreign country for more than 6 months since By comparison with databases in which nationality is recorded, this variable provides a good approximation of migrant status [9]. On this basis, patients were divided into migrants from sub-saharan Africa and others [10]. HIV transmission groups were defined as follows: men who have sex with men (MSMs), intravenous drug users (IVDUs), heterosexuals and unknown/miscellaneous. The geographical regions in which patients were enrolled were grouped together into five areas, as follows: Paris area, Provence-Alpes-Côte d Azur, rest of metropolitan France, French Departments in the Americas (Martinique, Guadeloupe and Guyane) and the Reunion Islands. The time since HIV diagnosis at enrolment was divided into three categories: less than 1 year, 1 year or more, and not available. Interactions between migration from Sub-Saharan Africa and sex, the transmission group, and the time since HIV diagnosis were tested, and those with P-values below 0.10 were taken into account in the multivariable model. For each patient included in the analysis, time (in months) between enrolment in the FHDH and the first cart prescription was computed. Time (in months) between the date of enrolment and the date of death or the date of the last visit to an FHDH participating centre was used to estimate Kaplan Meier survival. The association of the enrolment period and of DAC with cart prescription was analysed using multivariable Cox proportional hazards models, and the interaction between the enrolment period and DAC was taken into account. The association of DAC with survival was assessed in a multivariable Cox proportional hazards model adjusted for sex, age, the transmission group, the area of enrolment, sub-saharan African migrant status, the enrolment period, and the time since HIV diagnosis. Many AIDS-defining events occur in the first 6 months after enrolment in the cohort, especially in patients with DAC [11]. Thus, to determine how long DAC influenced survival, time since enrolment was divided into 6-month periods up to 24 months, then into 12- month periods up to 48 months. To take into account the multiplicity of tests, we used the Benjamini & Hochberg approach [12]. All analyses were done with SAS statistical software version 9.1 (SAS Institute, Inc., Cary, NC, USA) International Medical Press

3 Delayed access to care for HIV Results Among the 18,721 patients included in this analysis, 6,687 (35.7%) had DAC (Table 1). At enrolment in the FHDH, 313 patients with DAC (4.7%) had AIDS and a CD4 + T-cell count over 200/mm 3, 2,320 (34.7%) had AIDS and a CD4 + T-cell count below 200/mm 3, and other patients had only a CD4 + T-cell count below 200/mm 3. The five most frequent AIDS-defining events were Pneumocystis jiroveci pneumonia in 638 patients (24.2%), cerebral toxoplasmosis in 298 patients (11.3%), Kaposi s sarcoma in 234 patients (8.9%), oesophageal candidiasis in 216 patients (8.2%) and tuberculosis in 201 patients (7.6%). The prevalence of DAC rose from 35.0% in to 37.4% in but, after adjustment for other factors, the period of enrolment was not associated with DAC (P=0.10). An interaction between migration from sub- Saharan Africa and sex (P=0.02) was taken into account in the multivariable model. Compared with women who were not migrants from sub-saharan Africa, migrant women [odd ratio (OR)=1.5], non-migrant men (OR=1.6), and migrant men (OR=1.9) were more likely to have DAC. Compared with MSM, all other transmission groups were more likely to have DAC [OR=1.6, 95% confidence intervals (CI)=(1.5;1.7)]. The frequency of DAC increased with age, from an OR of 1.9 among patients aged between 30 and 40 years compared with patients younger than 30 years, to 3.5 among patients aged over 60 years (P<10 4 ). The region of recruitment was not significantly linked to DAC (P=0.10) although there was a tendency to more frequent DAC in French Departments of the Americas and the Reunion Island [OR=1.1, 95% CI=(1.0;1.3)]. DAC was also more frequent among patients diagnosed with HIV infection less than 1 year before FHDH recruitment than among patients with a longer or unknown time since HIV diagnosis [OR=1.3, 95% CI=(1.2;1.4)]. Table 1. Multivariable regression for predicting DAC Variable All patients Patients with DAC % OR 95% CI (OR) Sex and sub-saharan African migrant status Non-migrant women 4,259 1, Migrant women 1, [1.29;1.70] Non-migrant men 12,167 4, [1.45;1.73] Migrant men [1.62;2.17] Age, years <30 4,557 1, ,215 2, [1.74;2.06] ,833 1, [2.53;3.07] , [2.69;3.46] > [2.91;4.12] Transmission group MSM 5,773 1, IV drug users 2, [1.56;1.95] Heterosexuals 8,382 3, [1.42;1.69] Other or unknown 2, [1.46;1.80] Geographical area Rest of metropolitan France 5,377 1, Paris area 9,113 3, [0.99;1.15] Provence Alpes Côte d Azur 2, [0.97;1.19] French Departments of the Americas 1, [1.04;1.30] Reunion Island [0.88;1.50] Period of enrolment ,748 4, ,973 2, [0.99;1.13] Time since HIV diagnosis <1 year 11,818 4, year 6,438 2, [0.74;0.86] Not available [0.47;0.73] Total 18,721 6, % CI, 95% confidence intervals; DAC, delayed access to care; IV, intravenous; OR, odds ratio; MSM, men who have sex with men. Antiviral Therapy 12:1 91

4 E Lanoy et al. Figure 1. Probability of receiving cart among patients with and without DAC Proportion of patients with antiretroviral treatment CD4 + T-cells or AIDS in CD4 + T-cells or AIDS in >200 CD4 + T-cells without AIDS in >200 CD4 + T-cells without AIDS in Number of patients at risk ,857 Time since inclusion in FHDH, months ,777 2,364 1,590 All CD4 values are in copies/mm 3. cart, combined antiviral therapy; DAC, delayed access to care; FHDH, French Hospital Database on HIV. Among the 18,721 patients, 14,160 received at least one prescription of cart. Patients with DAC received cart earlier than patients without DAC (91.3% versus 62.4% at 6 months during the two periods, Figure 1). Compared with patients without DAC enrolled in , cart prescription was more rapid in patients with DAC enrolled either in [hazard ratio (HR)=2.1, 95% CI=(2.0;2.2)] or in [HR=1.8, 95% CI=(1.7;1.9)], and it was less rapid in patients without DAC enrolled in [HR=0.7, 95% CI=(0.6;0.7)], Figure 1). A total of 737 patients died, including 568 patients with DAC (77.1%). Among the patients with DAC who died, 282 (49.6%) died of AIDS, 281 (49.5%) from other causes, and five (0.9%) from unknown causes. The corresponding figures in patients without DAC were 40 (23.7%), 128 (75.7%) and one (0.6%). Survival was significantly better among patients without DAC. Overall, the mortality rate was 0.3% [95% CI=(0.2%;0.4%)] at 6 months among patients without DAC and 4.9% [95% CI=(4.4%;5.5%)] among patients with DAC (Figure 2A); the corresponding values at 4 years were 3.0% [95% CI=(2.5%;3.5%)] and 13.9% [95% CI=(12.7%;15.2%)], Figure 2B). The risk of death linked to DAC was very high in the first 6 months after enrolment, with an HR of The HR then fell slowly to 2.6, 2 years after enrolment, and remained significantly higher than 1, 4 years after enrolment (Figure 3). Discussion The proportion of patients with DAC at enrolment in the FHDH database was 35.7%. We found that older patients, patients who were recently diagnosed with HIV infection, and patients belonging to transmission groups other than MSM were more likely to have DAC. Compared with non-migrant women, the risk of DAC was increased in migrant women, then nonmigrant men, with migrant men having the greatest risk. Although patients with DAC received cart promptly after enrolment in the FHDH, their mortality rate remained higher than that of other patients during the first 4 years of follow-up. Our study has some limitations. Variables such as education, marital status and employment status have been shown to influence the risk of DAC [13 17], but these are not recorded in the FHDH database and could therefore not be studied. Mortality may have been underestimated in our study because of losses to follow-up. Indeed, in a previous study, we showed that the prevalence of loss to follow-up was 8.5% at 1 year, and that patients with advanced HIV disease were at an increased risk of loss to follow-up [18]. It is therefore possible that we underestimated the negative prognostic value of DAC. Two strengths of this study are the large number of patients enrolled in a national cohort and the fact that hospital cohorts are representative of access to hospital care International Medical Press

5 Delayed access to care for HIV Figure 2. Survival curves for patients with and without DAC A 1.00 >200 CD4 + T-cells without AIDS in >200 CD4 + T-cells without AIDS in CD4 + T-cells or AIDS in Survival CD4 + T-cells or AIDS in B 0.90 Number of patients at risk Time since inclusion in FHDH, months 18,721 16,312 15,809 15,302 14,819 14,417 14,007 >200 CD4 + T-cells without AIDS in >200 CD4 + T-cells without AIDS in Survival CD4 + T-cells or AIDS in CD4 + T-cells or AIDS in Number of patients at risk Time since inclusion in FHDH, months 14,007 11,849 9,979 8,263 6,719 5,138 3,732 2,424 (A) First 6 months and (B) after 6 months. DAC, delayed access to care; FHDH, French Hospital Database on HIV. All CD4 values are in copies/mm 3. Antiviral Therapy 12:1 93

6 E Lanoy et al. Figure 3. Adjusted hazard ratios for mortality linked to DAC Hazard ratio (95% CI) P= P= P= P= and after Months from enrollment in FHDH The analysis was adjusted on sex, age, transmission group, area of enrolment, sub-saharan African migrant status, enrolment period and time since HIV diagnosis. The levels of significance were computed with the Benjamini & Hochberg approach [12]. DAC, delayed access to care; FHDH, French Hospital Database on HIV. 2.6 P= P= P= Many previous studies have focused on either late HIV testing or late diagnosis or DAC. However, predictors of late testing, late diagnosis or DAC are different. Moreover, the definitions used in these studies were sometimes different. The most common clinical definition of late diagnosis of HIV infection was diagnosis of AIDS within 1, 3, 6, 9 or 12 months [13,14,19 23]. This definition may be useful when the analysis is based on AIDS surveillance and when follow-up data are lacking. However, when follow-up data are available, a definition based on symptoms or immunological parameters is more accurate. An immunological criterion a CD4 + T- cell count below 200/mm 3 at diagnosis has also been used to define late diagnosis [15,24,25]. We used both clinical and immunological criteria to define DAC, as in a study by the ICONA cohort group [15], because they correspond to recommendations of systematic antiretroviral treatment in all available guidelines [4 6]. Almost one-third of patients who were enrolled in the FHDH between 1997 and 2002 had late access to care, a proportion very similar to that observed in other studies during the cart era: 30.3% in a French hospital [20], 28% based on Spanish AIDS surveillance data [13], 28.9% in an Italian multicentre study [15] and 33.7% in an Italian tertiary care centre [21]. In the FHDH database, the overall prevalence of DAC was 35.7% in and 41.7% in (data not shown). An increase in the frequency of DAC during the cart era has also been observed in Australia (18% in , 33.1% in 1997) [22], and in a tertiary care centre in Rome (20.5% in 1996, 33.7% in 1997) [21]. It should be noted that these latter two studies focused only on AIDS cases. Recent diagnosis of HIV infection is linked to DAC, but the proportion of patients with DAC diagnosed with HIV infection more than 1 year before FHDH enrolment was 28.7%. In the ICONA cohort, 26.3% of patients did not seek primary care for more than 6 months after their first test for HIV infection [15]. In two American urban hospitals, the estimated proportions of patients who delayed seeking primary care for more than 1 and 2 years after HIV diagnosis were 39% and 32%, respectively [26]. The risk of late access to care rose strongly with age in our study, in keeping with other reports showing a significantly increased risk after age 45 years. Published odds ratios for DAC in older age groups range from 3 to 6.5 [13,15,21,22,24,26]. Late diagnosis of HIV infection in patients over 50 years has a very serious impact, as these patients generally have a slower immunological response to cart and experience more rapid clinical progression [27]. In addition, they are more likely to have comorbidities, complicating the management of HIV infection [28]. We found that, relative to non-migrant women, DAC was more frequent among men and among migrants from sub-saharan Africa, with an interaction between gender and migrant status. Migrants in general are at a higher risk of DAC [13,21,22,29], possibly because access to HIV testing and treatment is more difficult in sub-saharan Africa. The observation that non-migrant International Medical Press

7 Delayed access to care for HIV men were more likely than migrant women to have DAC in our study may be related to the fact that all pregnant women in France are offered HIV screening. For other pathologies detected during pregnancy, access to care is also earlier among women [30]. This link between late access to care (or late diagnosis) and male gender is found in most studies [13,14,21,24,26]. A lower prevalence of DAC among MSM has also been described elsewhere [20,25], possibly owing to better HIV/AIDS awareness, relative to heterosexual populations [14,19,23,26]. Some studies have also shown a lower prevalence of DAC among intravenous drug users [13,21], while others suggest the opposite [15,26]. The median interval between diagnosis and enrolment in the FHDH database was 53 months among intravenous drug users, compared with 17 months overall. The frequency of DAC showed regional disparities even after adjustment for other variables. The high prevalences of DAC in French overseas territories might be linked to specificities of the HIV/AIDS epidemic, as noted by the National AIDS Council for French Guyana and Guadeloupe [31]. Regarding the association of DAC with survival, patients with DAC received cart more rapidly after enrolment than patients without DAC. Higher mortality among patients with DAC was therefore not explained by lower access to cart. Moreover, patients without DAC received cart later during the period than This may be related to a desire to postpone the risk of cart adverse effects in patients with good clinical and immunological status. Even when cart was prescribed as recommended, patients with DAC were at a higher risk of death than patients without DAC, especially in the first 6 months after FHDH enrolment. The ART cohort collaboration and EuroSIDA papers showed that clinical progression and survival were poorer when cart was initiated at CD4 + T-cell counts below 200/mm 3 [3,32]. Moreover, the proportion of AIDS-related deaths was twice as high in patients with DAC in our study. Immunodepression induced by HIV infection impacts both on AIDS-related events and non-aids related events such as cancer, and hepatic diseases in hepatitis B or C virus-infected patients [5,33]. Since cart has been available, both AIDS-related mortality and non-aids-related mortality have decreased. Higher short-term mortality among AIDS patients doesn t seem to be a worse follow-up consequence. Comparison of mortality between lowincome and high-income countries, in a ART-LINC and ART-CC study [34], showed that mortality was much higher in low-income countries with active follow-up. Nevertheless, this study showed that in low-income and high-income countries, mortality was higher in the first 6 months after cart initiation. Baseline CD4 + T-cell count was strongly prognostic both in low-income and high-income settings: the lower the baseline CD4 + T-cell count, the higher the mortality rate [34]. This suggests that cart may not act rapidly enough in such patients, who are at a high risk of AIDS-defining illnesses and death. Patients with DAC therefore appear to warrant very close clinical supervision [5]. Overall, these data show that HIV testing must be improved in specific populations, and that primary care linkage should be facilitated at the time of diagnosis of HIV infection. Patients presenting late may qualify for intensified cart, interleukin-2 adjunction [35], and prophylactic treatment of opportunistic infections [36] to help improve their prognosis. Conclusions In France, DAC remains frequent, even in the cart era. We found that one-third of patients first sought care when they already had AIDS and/or a CD4 + T-cell count below 200/mm 3. DAC is particularly frequent among older patients, in whom it also has more serious implications. Although late access to care was more frequent among patients with a recent diagnosis of HIV infection, the proportion of patients who delayed seeking hospital care after their diagnosis was also high. This implies that HIV testing should be better targeted, and that patient management immediately after diagnosis should be improved, especially when HIV infection is diagnosed at an advanced stage. DAC is associated with a markedly higher risk of death, and clinical trials are needed to evaluate specific management approaches. Sponsorship Institut National de la Santé et de la Recherche Médicale (INSERM), Agence Nationale de Recherches sur le SIDA (ANRS), and Fondation pour la Recherche Médicale. Acknowledgements We are indebted to all the participants in the cohort, and especially the local research assistants, without whom this work would not have been possible. We are also grateful to ANRS, INSERM, Fondation pour la Recherche Médicale and the French Health Ministry for their financial support. Additional files The additional file Clinical Epidemiology Group of the FHDH can be accessed via the Volume 12 Issue 1 contents page, which can be found at (by clicking on Antiviral Therapy then Journal PDFs ). Antiviral Therapy 12:1 95

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