In this study we investigated the delay between HIV testing and receipt of HIV-related care in a large population of patients enrolled throughout Italy in 1997–2000 in a multi-center cohort study. Overall, we found that a quarter of all patients did not receive HIV-related care until at least 6 months after their first positive HIV test, and that use of intravenous drugs, unemployment, having no negative tests before the first positive one, and having no counseling at the time of first positive test were associated with a higher probability of delayed presentation to care. We also found that patients that delayed presentation for HIV-related care after testing HIV positive differed from those who were first HIV tested late in the course of their infection.
These findings may be of both clinical and public health relevance: in our study, most of those classified as delayed presenters had a first HIV-positive test >2 years before their first clinical visit, and almost 40% presented with advanced HIV infection. However, delayed presenters represented at most a quarter of patients in our study who presented for care only when already severely immunosuppressed or symptomatic; the other three-quarters were late testers. This suggests that late testing, rather than delay in seeking care after testing HIV positive, may be the main determinant of late presentation for care.
Our estimate of 26% for delayed presentation to care in this cohort of Italian patients is similar to those from studies conducted in a variety of settings in the United States before HAART became widely available, where estimates ranged from 21–47%. 10–14 European data are relatively sparse. The CD4 count surveillance system in England and Wales has shown that, in 1996 and 1997, for newly reported cases of HIV infection, a CD4 count within 6 months of the HIV diagnosis was traceable for only 57% of cases, suggesting a possible delay in entry into care for a substantial proportion of patients. 19
The association of a history of intravenous drug use and unemployment with delayed presentation to care may primarily reflect a difficulty for drug users and other persons with disadvantaged socioeconomic status to access primary care services, as suggested from previous studies from the United States. 13,20 In Italy, where HIV care is provided free of charge in the context of a universal health care system, most HIV infections in drug users are diagnosed in drug treatment centers, 21 which provide HIV testing but not treatment. The delay in presenting for care may thus be also due to delays in onward referral to HIV treatment centers for specialized care and appropriate antiretroviral therapy and may reflect at least in part the concern of caregivers to initiate therapy in patients with an unstable lifestyle. 22–25
Testing HIV positive at the first HIV test and not receiving counseling was also associated with delay in entry into care. This finding lends support to the suggestion that the circumstances of testing and the quality of counseling services may be important in determining whether those who test HIV positive present early for medical care. 7,16
Among >700 patients who presented for care within 6 months of their first HIV-positive test, almost 40% already had advanced HIV infection. Our data concur with results of other studies conducted on patients with newly diagnosed HIV infection in the United States and in Europe in the HAART era 8,26–28 and underscore the continuing importance of the problem of late HIV testing.
Factors associated with late testing in the present study do not differ from those reported in previous studies conducted in Italy and in other European countries. 29–31 Greater recognition of risk could explain, at least in part, the finding of a lower proportion of late testers among patients reporting a higher number of sexual partners in the previous 6 months and among younger patients. Differing responses to recognition of the risk of being infected could also partly explain the lower proportion of late testers found among women, as suggested by the fact that, among AIDS patients infected through heterosexual contacts reported to the Italian National Registry, more than half of women reported sexual contact with a person with known HIV infection compared with approximately 15% of men. 32 The finding that those who had a previous negative test were less likely to be late testers may be explained on the basis of studies suggesting that repeat testers may be more aware of a higher risk of acquiring HIV infection and willing to seek early treatment of HIV infection. 33
Conversely, a lower probability of being late testers could also reflect a higher probability of being actively offered HIV testing. In fact, women are frequently offered testing at the time of pregnancy, 34 and intravenous drug users, among whom there was a low proportion of late testers, as in other European and US studies, 8,29–31 are actively offered testing in drug treatment centers or other medical services. Again it should be noted that, at least for drug users, early testing does not necessarily imply early access to care.
This study has several limitations. First, among patients enrolled in this study the proportion of foreign-born persons was lower that that expected on the basis of data showing that, in most recent years, approximately 15% of AIDS cases in Italy were reported among the foreign born. 32 The small number of foreign-born participants in this study, probably due to the fact that we used an Italian language questionnaire, precluded any meaningful analysis of the association between ethnic group and access to HIV testing and care. Second, the date of the first positive HIV test, used to define patients as delayed presenters, was self-reported and therefore subject to recall bias. However, we found a good agreement between the classification of patients as delayed presenters based on date of first HIV test reported in the questionnaire or reported in the medical history (kappa 0.78, standard error 0.023). Third, the group of patients we analyzed, although quite large and recruited in several clinical centers in Italy, was not a probability sample of HIV-infected patients entering into care in the country, and thus selection bias could not be entirely prevented. Moreover, patients considered for the present analysis had a less advanced stage of HIV disease and were less likely to be foreign born compared with patients who were enrolled in this cohort but did not complete the enrollment questionnaire. Finally, information on other factors that might be associated with either late testing or delayed presentation to care, such as psychologic function or social and community support, was not collected in this study.
This study show that factors associated with delay to presentation to medical care after testing HIV positive differ from those associated with testing late in the course of HIV infection. Therefore, interventions aimed at promoting timely access to care of persons with HIV infections should include differentiated programs that specifically address these 2 aspects. In particular, interventions for drug users are urgently needed. Studies conducted in the early 1990s have shown that difficulties in linking drug users to HIV treatment services may be at least in part overcome by providing on-site medical services in drug treatment centers. 35,36 Preliminary evidence suggests that, using strategies such those involving direct administration of drugs, complex therapeutic interventions such as HAART could also be transferred outside of specialized care services. 37 Finally, strategies to promote early diagnosis of HIV infection need to be devised. These strategies may include increasing the availability of testing in different settings and actively offering testing as a part of routine medical care. 8
We wish to thank Dr. Julia Heptonstall for critical reading of an earlier version of the manuscript and Dr. Douglas Horejsh for editing the final version of the manuscript.
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Members of the ICoNA Behavioural Epidemiology study group who contributed to this study are:
Ancona: M. Montoni, G. Scalise; Aviano (PN): U. Ti-relli; Bari: G. Angarano, G. Pastore; Bergamo: F. Suter, C. Arici; Bologna: F. Chiodo, F. Ghinelli; Brescia: G. Carosi, C. Minardi, G. Cadeo; Busto Arsizio (VA): G. Rizzardini; Cagliari: P.E. Manconi; Chieti: E. Pizzigallo; Como: E. Rinaldi, Ferrara: F. Ghinelli; Galatina (LE): P. Grima; Genova: N. Pier-santelli; Grosseto: M. Toti; Latina: F. Soscia; Lecco: A. Orani; Mantova: A. Scalzini; Lucca: G. Pagano; Milano: M. Moroni, A. Cargnel, A. Lazzarin, A. d’Arminio Monforte, A. Cargnel, G. Filice, L. Caggese; Modena: R. Esposito; Naples: A. Chirianni, C. Izzo; Pavia: G. Filice, L. Minoli; Perugia: S. Pauluzzi; Piacenza: F. Alberici; Pisa: F. Menichetti; Potenza: C. de Stefano; Ravenna: T. Zauli; Reggio Emilia: L. Bonazzi, G. Magnani; Rimini (FO): M. Arlotti; Rome: L. Ortona, M.S. Aloisi, A. Antinori, G. Antonucci, R. Balzano, S. D’Elia, G. Ippolito (study coordinator), P. Narciso, N. Petrosillo, G. Rezza, V. Vullo, D. Serraino, P. Pezzotti; Turin: P. Caramello, M.L. Soranzo; Varese: P. Grossi.