JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Social Science
Delayed Presentation and Late Testing for HIV: Demographic and Behavioral Risk Factors in a Multicenter Study in Italy
Girardi, Enrico MD*; Aloisi, Maria Stella BSc*; Arici, Claudio MD†; Pezzotti, Patrizio PhD‡; Serraino, Diego MD*; Balzano, Roberta BSc*; Vigevani, Gianmarco MD§; Alberici, Francesco MD¶; Ursitti, Maria MD**; D’Alessandro, Margherita MD††; Monforte, Antonella d’Arminio MD‡‡; Ippolito, Giuseppe MD*; for the ICoNA Behavioural Epidemiology Study Group
From *Dipartimento di Epidemiologia, INMI Lazzaro Spallanzani, Roma; †Divisione di Malattie Infettive, Ospedali Riuniti, Bergamo; ‡Reparto AIDS e MST, Istituto Superiore di Sanità, Roma; §I Divisione di Malattie Infettive, Ospedale Luigi Sacco, Milano; ¶Divisione di Malattie Infettive, Ospedale Civile, Piacenza; **Divisione di Malattie Infettive, Arcispedale Santa Maria Nuova, Reggio Emilia; † †Clinica Malattie Infettive, Università di Chieti; ‡ ‡Istituto di Malattie Infettive e Tropicali, Università di Milano, Italy.
Received for publication July 15, 2003; accepted November 26, 2003.
This work was partially supported by Ministero della Salute–Ricerca corrente degli IRCCS e Progetto AIDS Sociale–ISS.
The ICoNA network is supported by an unrestricted educational grant from Glaxo-SmithKline
Reprints: Enrico Girardi, Dipartimento di Epidemiologia, Istituto Nazionale per le Malattie Infettive, Lazzaro Spallanzani–IRCCS, Via Portuense, 292-00149 Roma, Italy (e-mail: firstname.lastname@example.org).
Summary: Ensuring timely access to care for persons with HIV is an important public health goal. To identify factors associated with delayed presentation to medical care after testing HIV-positive or with late HIV testing, we studied 968 patients at their first HIV care visit, enrolled in a multicenter study in Italy from 1997–2000. Patients completed a questionnaire on HIV-testing history, sexual behavior, and drug use behavior. Delayed presenters were patients with >6 months between their first HIV-positive test and presentation for HIV care; late testers were patients with CD4 count < 200 /mm3 or clinically defined AIDS at their first HIV-positive test. Among the study patients, 255 (26.3%) were delayed presenters, and 280 (28.9%) were late testers. In multinomial logistic regression analysis, injection drug use significantly increased (odds ratio [OR]= 5.04) the probability of delayed presentation but reduced (OR = 0.55) the chance of late testing. A previous HIV-negative test was associated with a reduced risk of both delayed presentation (OR = 0.39) and late testing (OR = 0.36). Unemployment was positively associated with delayed presentation and increasing age with late testing, whereas HIV counseling at the time of first positive HIV test strongly (OR = 0.42) reduced the odds of delayed presentation. Interventions aimed at promoting timely access to care of HIV-infected persons should consider differentiated programs for delayed presentation and late testing.
Ensuring timely access to care for persons with HIV is considered an important public health goal in industrialized countries, 1 as antiretroviral treatment, if given during the asymptomatic phase of the infection, may greatly delay progression to clinically symptomatic HIV disease. 2 Just as importantly, early entry into medical care may reduce the likelihood of further spread of infection, both by the decrease in viral replication that results from antiretroviral therapy 3 and by a higher probability that the person will adopt risk reduction behaviors. 4,5
However, late initiation of medical care after acquisition of HIV infection remains common. 1,6–8 This delay may occur because HIV-infected persons are not aware of their risk of infection and fail to seek testing, or, even if aware of their risk, do not seek testing or face significant barriers to access HIV testing. In addition, patients may not immediately seek—or be provided with access to—medical care upon receiving their first HIV-positive test result. 7,9
Identification of patient characteristics associated with late presentation to care is important to target interventions aimed at favoring early entrance into HIV care. However, our understanding of this problem is incomplete. Most of the studies that examined the issue of late presentation have focused on the delay in seeking HIV testing, 6,7 but relatively few have looked at the reasons for delay in presenting for care after testing HIV positive. 10–16 These studies were performed before highly active antiretroviral therapy (HAART) came into widespread use; most of them were conducted on groups of patients recruited in single clinics, and no study that we know of has analyzed the factors related to both these components of delay in the same group of patients.
This report is based on data collected on a large number of HIV-infected persons who enrolled in a multicenter cohort study of the natural history of HIV disease in the HAART era, the ICoNA cohort, in Italy in 1997–2000, and who were “naive” for antiretroviral therapy at the time that they enrolled in the study. We analyzed data from patients for whom study enrollment coincided with the first HIV care visit, i.e., those who had no prior CD4 cell count or plasma HIV RNA determinations. Among these patients, we aimed to quantify delayed presentation to medical care after testing HIV positive; identify patient factors associated with such delay; and verify whether these factors differed from those associated with late HIV testing (i.e., being tested for the first time when an AIDS-defining illness has occurred or CD4 count is <200/mm3).
PATIENTS AND METHODS
Study Design and Patient Selection
This study was part of a larger multicenter, longitudinal observational study of the natural history of HIV infection, “The Italian Cohort Naive Antiretrovirals—ICoNA,” that was conducted in 67 hospital infectious diseases units throughout Italy. 17 HIV-infected patients, aged ≥18 years, were enrolled in this study either between 1997 and 1998 (first enrollment period) or during 2000 (second enrollment period). Criteria for inclusion were identical in the 2 periods: consecutive antiretroviral-naive patients presenting to each participating clinical center were enrolled, independently of the reason for attending the clinic. Among 67 ICoNA centers, 59 agreed to participate in a behavioral epidemiology study. In these centers, HIV-infected individuals were offered a self-administered, pre-coded questionnaire upon enrollment that included questions on sociodemographic characteristics, health profile, including HIV testing history and personal behavior history, including sexual and drug using behaviors. 18 Clinical and therapeutic data were abstracted from patients’ records.
Patients who completed the questionnaire at study enrollment and answered the question on the date of their first HIV-positive test were included in the analysis if their first HIV-positive test was in the 6 months preceding their enrollment or, if their first positive HIV test was >6 months before enrollment, they had not had a previous CD4 cell count or plasma HIV RNA determination, as determined by medical record review and patient interview.
Patients were defined as “delayed presenters” if >6 months had elapsed between the date of their first HIV-positive test and their presentation for HIV care.
Patients were defined as “late testers” if they had a first HIV-positive test in the 6 months preceding study enrollment and they had a CD4 count < 200 /mm3 or clinically defined AIDS at enrollment.
Univariate analysis was used to assess the associations between delayed presentation for HIV care and sociodemographic, HIV testing, and behavioral factors and to assess the association of the same factors with late HIV testing among patients who had a first HIV-positive test in the 6 months preceding enrollment (i.e., among those who were not delayed presenters). To identify factors independently associated with being either a delayed presenter or a late tester, factors significantly associated with delayed presentation for care or late HIV testing in univariate analysis were entered in a multinomial logistic regression model. In this latter analysis, we included all the patients who had no missing data in any of the variables considered. Data analysis was performed using SPSS version 11.0 for Windows.
In 1997–2000, 4453 HIV-infected antiretroviral-naive individuals were enrolled into the ICoNA Cohort at 59 clinical centers. Of the enrolled individuals 2900 (65.1%) completed the enrollment questionnaire. HIV-infected persons who completed the questionnaire had a higher median CD4 cell count compared with those who did not (435 cells/mm3 vs. 389.5 cells/mm3; P < 0.01) and were less likely to have clinically defined AIDS (315/2900, 10.9% vs. 220/1553, 14.2%; P < 0.01) and to be born outside Italy (155/2900, 5.3% vs. 137/1553, 8.8%; P < 0.01). Among the individuals who completed the questionnaire, 968 (33.4%) met the criteria for inclusion in this analysis. Of the 1932 patients who were not eligible, 1928 had already received medical care for their HIV infection, and only 4 did not report the date of their first positive HIV test.
Characteristics of the 968 patients included in the present analysis are summarized in Table 1. The group was primarily male (740, 76.4%) aged between 30–39 years (488, 50.4%), and most of the patients were born in Italy (898, 92.8%). The median CD4 cell count was 306/mm3 and 37.2% of patients had a CD4 count < 200/mm3; 190 patients (19.6%) had clinically defined AIDS.
The median time since the first HIV-positive test was 1.64 months, and 255 (26.3%) tested positive at least 6 months before the first visit and were, therefore, classified as delayed presenters. In this group of patients, 237 (92.9%) had had a first HIV-positive test >1 year before enrollment and 222 (87.1%) >2 years.
Among the 255 delayed presenters, 99 (38.8%) had <200 CD4/mm3 or clinically defined AIDS at their first visit; these patients represented 26.1% of the 379 patients with <200 CD4 cells/mm3 or clinically defined AIDS upon enrollment.
As shown in Table 1, the proportion of delayed presenters declined significantly over time from 31.0% in 1997 to 16.0% in 2000. Table 1 also shows the univariate association between delayed presentation to care and patient factors. Significant differences in proportion of delayed presenters were recorded among patients enrolled in different parts of Italy. A higher proportion of delayed presenters was observed among less educated and unemployed patients, among those reporting no negative HIV test before the first positive one and no counseling at the time of the first positive test, and among those reporting use of drugs, either injecting or noninjecting. Older patients and those reporting same gender sex had lower proportion of delayed presenters.
Among the 713 patients who presented for HIV care within 6 months from the first HIV-positive test, 280 (39.3%) had a CD4 count <200 cells/mm3 or clinically defined AIDS at enrollment and thus were classified as late testers. These patients had a first HIV-positive test a median of 30 days before enrollment. Table 2 shows the univariate association between late testing and patient factors. Most of these associations differed from those recorded for delayed presentation. No significant association was found between education and employment status and late testing, and the proportion of late testers tended to be lower among those reporting drug use, those reporting one or no partner in the previous 6 months, and among younger and male patients. A higher proportion of late testers was observed among those who had no negative HIV tests prior to the first positive one, while no association was found with receiving counseling.
Table 3 shows the results of multinomial logistic regression analysis performed to identify patient factors independently associated with delayed presentation and late testing. In this analysis we found that use of injecting drugs (odds ratio [OR] 5.04) or unemployment (OR 2.75) were significantly associated with a higher probability of delayed presentation to care after testing positive, while having at least one negative test before the first positive one (OR 0.39), and counseling when first testing positive (OR 0.42), were associated with a decreased probability of delayed presentation. Conversely, use of injected drugs (OR 0.55) was associated with a decreased probability of testing late, as were female gender (OR 0.38), having 1 (OR 0.68) or >1 (OR 0.21) sexual partner in the previous 6 months, and having at least 1 negative test before the first positive (OR 0.36), while older patients had a higher probability of being late testers (OR 2.90, 4.05, and 2.60, for patients aged 30–39 years, 40–49 years, and ≥50 years, respectively, compared with those aged <30 years).
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.
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Antimicrobial Agents and ChemotherapyIntensification of Antiretroviral Therapy through Addition of Enfuvirtide in Naive HIV-1-Infected Patients with Severe Immunosuppression Does Not Improve Immunological Response: Results of a Randomized Multicenter Trial (ANRS 130 Apollo)Antimicrobial Agents and Chemotherapy
Plos OneEstimation of HIV-Testing Rates to Maximize Early Diagnosis-Derived Benefits at the Individual and Population LevelPlos One
MycosesDisseminated histoplasmosis and aids: relapse and late mortality in endemic area in north-eastern BrazilMycoses
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivChronic illness burden and quality of life in an aging HIV populationAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
European Journal of Public HealthAIDS patients with tuberculosis: characteristics and trend of cases reported to the National AIDS Registry in Italy-1993-2010European Journal of Public Health
Plos OneHIV and Hepatitis C Virus Testing Delays at Methadone Clinics in Guangdong Province, ChinaPlos One
Current Opinion in Infectious DiseasesLate diagnosis of HIV infection: major consequences and missed opportunitiesCurrent Opinion in Infectious Diseases
JAIDS Journal of Acquired Immune Deficiency SyndromesLate-Disease Stage at Presentation to an HIV Clinic in the Era of Free Antiretroviral Therapy in Sub-Saharan AfricaJAIDS Journal of Acquired Immune Deficiency Syndromes
JAIDS Journal of Acquired Immune Deficiency SyndromesLate Presenters in an HIV Surveillance System in Italy During the Period 1992-2006JAIDS Journal of Acquired Immune Deficiency Syndromes
Sexually Transmitted DiseasesAuthors’ ResponseSexually Transmitted Diseases
HIV testing; HIV care; delay; intravenous drug use; behavioral survey
© 2004 Lippincott Williams & Wilkins, Inc.
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