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HIV-associated tuberculosis and immigration in a high-income country: incidence trends and risk factors in recent years

Abgrall, Sophiea,b,c; del Giudice, Pascald; Melica, Giovannae; Costagliola, Dominiquea,b,fon behalf of FHDH-ANRS CO4

doi: 10.1097/QAD.0b013e3283366747
Epidemiology and Social

Objective: To examine trends in tuberculosis incidence rates in France during the combination antiretroviral therapy (cART) period.

Methods: From the French Hospital Database on HIV, we selected 72 580 patients (including 14 491 migrants) with no history of tuberculosis, followed between 1 January 1997 and 31 December 2008. We then examined incidence rates of tuberculosis and its risk factors.

Results: A total of 2625 patients were diagnosed with tuberculosis either at enrolment (N = 932) or during follow-up (N = 1693). During follow-up, the incidence rate of tuberculosis was 0.40/100 patient-years overall, 0.20 among nonmigrants and 1.03 among migrants. Adjusted risk of tuberculosis was 2.01 [95% confidence interval (CI) 1.79–2.26] times higher in migrants than in nonmigrants. The adjusted incidence rate of tuberculosis significantly increased in both migrants and nonmigrants after 2000–2001, with adjusted risks of 2.50 (95% CI 1.54–4.06) and 1.85 (95% CI 1.27–2.69) in 2008 compared with that in 1997, respectively. Other factors independently associated with a higher incidence of tuberculosis were medical follow-up less than or equal to 6 months, no previous antiretroviral therapy, lower CD4 cell count and higher viral load. Nonmigrant patients belonging to HIV-transmission groups other than homosexual men, residing in the Paris area or in French West Indies or with AIDS status were at a supplementary risk.

Conclusion: The incidence of tuberculosis is increasing among both migrant and nonmigrant HIV-infected patients in France. This is partly because sub-Saharan African migrants represent an increasing fraction of the HIV-infected population in France and also because of late access to care. Co-prescribing tuberculosis preventive therapy with cART might benefit selected patients, such as migrants and patients with late access to care.

aINSERM U 943, France

bUPMC Univ Paris 06, UMR_S 943, Paris, France

cAP-HP, Hôpital Avicenne, Service de maladies infectieuses et tropicales, Bobigny, France

dCHI Frejus-Saint Raphael, Service des maladies infectieuses, Fréjus, France

eAP-HP, Hôpital Henri-Mondor, Service d'immunologie clinique, Créteil, France

fAP-HP, Groupe hospitalier Pitié-Salpétrière, Service des maladies infectieuses et Tropicales, Paris, France.

1Please see the Acknowledgements section for the complete list of contributors.

Received 21 September, 2009

Revised 1 December, 2009

Accepted 9 December, 2009

Correspondence to Sophie Abgrall, INSERM U943, BP 335, 56 boulevard Vincent Auriol, 75625 Paris Cedex 13, France. Tel: +33 1 42 16 42 60; fax: +33 1 42 16 42 61; e-mail:

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Since 1996, the incidence rates of most HIV-associated opportunistic infections has fallen drastically in industrialized countries, along with AIDS-related mortality, owing to extensive use of combination antiretroviral therapy (cART) [1]. However, analysis of pooled cohorts in Europe and North America showed a 35% increase in the risk of AIDS in 2002–2003 compared with that in 1998 (the early cART era) among patients starting a first cART regimen, partly owing to a three-fold increase in risk of tuberculosis (TB) during the same period [2]. In France, TB was the most frequent AIDS-defining illness in 2001–2003 [3]. Changes in the epidemiology of HIV/AIDS in industrialized countries, and particularly the increasing number of migrants from areas with a high incidence of TB, including sub-Saharan Africa, may have contributed to these trends [2–5]. Indeed, the incidence of TB has declined gradually in the last 15 years in the general French population, but the rate of decline has slowed since 1997 (16.5, 11.4, 10.6, 8.6 and 8.9 per 100 000 person-years in France in 1993, 1997, 2001, 2005 and 2007, respectively), owing to the consequences of HIV infection and immigration [6–8]. The incidence of TB varies widely across French regions, with the highest incidence in the Paris area and French Guyana, which have the highest immigration rates [6].

The aim of this study was to examine trends in TB incidence rates in France during the cART period (up to 2008), as well as risk factors for TB, and the contribution of immigration from sub-Saharan Africa.

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The FHDH is a large prospective cohort study of HIV-infected patients aged at least 15 years and treated in 62 French university hospitals. The only enrollment criteria are documented HIV-1 or HIV-2 infection, being followed in one of the participating centers and written informed consent. Trained research assistants use French Ministry of Health DMI2 software to collect on standardized forms clinical and biological data prospectively at inclusion and at each visit or hospital admission for an HIV-related clinical event or a new treatment prescription, or at least every 6 months.

Patients aged at least 15 years with at least one follow-up visit in the FHDH after 1 January 1997 and at least one available CD4 cell count and one plasma viral load (pVL) value were selected for this study. The date of study entry was defined as the date of the first FHDH follow-up visit if the patient was enrolled on or after 1 January 1997 or as 1 January 1997 for patient enrolled before 1997. Patients were not eligible if a previous antiretroviral therapy or an AIDS-defining event was notified before their first FHDH follow-up visit and if they participated in a blinded clinical trial of antiretroviral therapy during their follow-up. Patients with a history of TB before 1 January 1997 or before inclusion in the FHDH were also excluded. The cutoff date for database analysis was 31 December 2008. TB was diagnosed on the basis of information recorded by physicians in each participating center, according to the 1993 CDC classification [9], differentiating pulmonary (i.e. intrathoracic TB, including tracheal, bronchial, pleural, mediastinal lymph node localizations) and extrapulmonary TB. All diagnosis of TB, both definite (bacteriological documentation yielding Mycobacterium tuberculosis) or presumptive (clinical and neuroradiological signs, including response to specific therapy) were considered for the study. Of the total 72 580 patients who met the inclusion criteria, 2625 were diagnosed with TB either at enrolment in the database or during follow-up.

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Statistical analysis

Patients who had TB at their first visit were compared with patients who were diagnosed with TB during follow-up (incident cases) by using the Mann–Whitney test, the Fisher's exact test or the χ 2-test, as appropriate.

We calculated the incidence rates of TB between study entry and 31 December 2008 and investigated associated risk factors. To take reporting delays into account, we used a censoring method recommended for cohort studies [10]. Surviving patients whose last follow-up data were obtained during the 6-month period before 31 December 2008 (last database update) were censored on 31 December 2008. Person-years of follow-up were calculated from the date of inclusion in the study to the date of the first episode of TB, death, the last follow-up visit or the end of the study, whichever occurred first.

Poisson regression models were used to identify risk factors for TB. Fixed variables (sex and HIV-transmission groups, place of birth, region of care) and time-updated variables (age, duration of follow-up, calendar period, antiretroviral treatment history, AIDS status, CD4 cell count, pVL) were considered for analysis. Regions of care were defined according to the epidemiology of HIV infection in France and included the Paris area, southern France, French West Indies (Martinique, Guadeloupe, French Guyana) and other regions of metropolitan France plus the Reunion Island. International migration was defined according to the United Nations and the national French definitions: anyone born and having lived outside France and now residing in France, whatever the nationality and the duration of stay in France [11]. On this basis regions of birth were divided into three groups: France, sub-Saharan Africa and ‘others’ (America, Asia and Europe). Risk factors were assessed separately for migrant and nonmigrant patients. Factors significantly associated with TB occurrence at the 10% level in univariate analyses were included in the multivariable model. The SAS statistical package version 9.1 was used for all analyses (SAS Institute, Cary, North Carolina, USA).

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Study population

From 1 January 1997 to 31 December 2008, 72 580 patients enrolled in the FHDH had at least one follow-up visit, with a CD4 cell count and a pVL assay and no previous history of TB. Their characteristics at study entry are shown in Table 1. Migrant patients represented 9.0% (n = 2593), 14.7% (n = 856), 29.0% (n = 2291), 33.3% (n = 2318) and 29.7% (n = 475) of all patients enrolled in the FHDH before 1 January 1997, in 1997, in 2000–2001, in 2004–2005 and in 2008, respectively. Patients originating from sub-Saharan Africa represented 4.2% (n = 1200), 8.1% (n = 472), 20.0% (n = 1584), 22.4% (n = 1558) and 21.4% (n = 343) of the patients, respectively.

Table 1

Table 1

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Characteristics of patients diagnosed with tuberculosis

TB was diagnosed in 2625 patients: 932 (35.5%) at FHDH enrolment (prevalent TB) and 1693 (64.5%) during follow-up (incident TB). Prevalent TB represented 31.2% of first TB diagnoses in 1997, 40.6% in 2000–2001, 30.4% in 2004–2005 and 16.5% in 2008 (Table 2). Compared with patients with incident TB, patients with prevalent TB were more likely to have disseminated forms (extrapulmonary or both pulmonary and extrapulmonary), to have contracted HIV infection through heterosexual intercourse, to originate from sub-Saharan Africa, to live in the Paris area and to have a low CD4 cell count and high viral load. Among prevalent TB, pulmonary TB was diagnosed in 47.1% of the nonmigrants (n = 179) and 47.5% of the migrants (n = 262) (P = 0.25) and in 55.6% of the nonmigrants (n = 564) and 48.6% of the migrants (n = 330) among incident TB (P = 0.03).

Table 2

Table 2

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Incidence of tuberculosis during follow-up

During a total follow-up of 427 957 person-years, the incidence rates of TB were 0.40/100 person-years [95% confidence interval (CI) 0.38–0.42] overall, 0.28/100 person-years (95% CI 0.26–0.30) among nonmigrant patients and 1.03/100 person-years (95% CI 0.95–1.11) among migrant patients. After adjustment on sex and HIV-transmission group, place of birth, region of care, time-updated age, duration of follow-up, antiretroviral treatment history, AIDS status, CD4 cell count and pVL, the incident rate of TB was 0.69/100 person-years in 1997, remained stable in 1998 and 1999 and then steadily increased from 2000 to 2008 (adjusted incidence rates 1.01 in 2000 up to 1.39 in 2008), with a significant increase in TB rate ratios in recent years (2000–2008), the risk of TB being multiplied by two in 2008 compared with 1997 (aRR, 2.01; 95%CI, 1.51–2.68) (Fig. 1).

Fig. 1

Fig. 1

When nonmigrant and migrant patients were analyzed separately, the adjusted incidence rates of TB were around two times lower in nonmigrant patients than in migrant patients (0.46/100 and 0.77/100 person-years in 1997, 0.57/100 and 1.60/100 person-years in 2000, 0.64/100 and 1.24/100 person-years in 2002 and 0.86/100 and 1.94/100 person-years in 2008, respectively). However, the adjusted incidence rates increased in both populations over time and the risk of TB increased significantly from 2000–2001 to 2008 compared with that in 1997 both among nonmigrant patients [+85% in 2008 compared with that in 1997; adjusted relative risk (aRR) 1.85; 95% CI 1.27–2.70] and migrant patients (+151% in 2008 compared with that in 1997; aRR 2.51; 95% CI 1.55–4.07). Among nonmigrant patients, the pattern of incidence trends over time was similar in the different groups of HIV transmission except for homosexual men for whom results showed steady rates over time (data not shown).

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Risk factors for tuberculosis

After adjustment on sex and HIV-transmission group, region of care, time-updated age, duration of follow-up, calendar period, antiretroviral treatment history, AIDS status, CD4 cell count and pVL, migrant patients were twice as likely as nonmigrant patients to be diagnosed with TB (aRR 2.01; 95% CI 1.79–2.26). Compared with patients born in France, the aRR of TB was 2.16 (95% CI 1.88–2.48) among patients originating from sub-Saharan Africa and 1.83 (95% CI 1.57–2.14) among other migrants.

In both migrant and nonmigrant patients, the risk of TB was associated with follow-up of less than 6 months, a low time-updated CD4 cell counts or high time-updated plasma viral load and the absence of antiretroviral therapy. However, among nonmigrant patients, the risk of TB was also higher in the Paris area and the French West Indies, in AIDS patients and homosexual men were the HIV-transmission group with the lowest risk of TB (Table 3).

Table 3

Table 3

Similar results were obtained when pulmonary TB and extrapulmonary TB were analyzed separately (data not shown).

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One-third of the cases of TB were diagnosed at enrolment in the FHDH cohort, mainly in migrant patients. During follow-up, the incidence of TB was 0.40/100 person-years overall, with an adjusted risk of TB 2.01-fold higher in migrant than in nonmigrants. The incidence of TB increased significantly in both migrant and nonmigrant patients from 2000–2001 to 2008 compared with that in 1997. Other adjusted factors associated with the risk of TB were medical follow-up of less than 6 months, no previous antiretroviral therapy, a low CD4 cell count and a high viral load; nonmigrant patients belonging to HIV-transmission groups other than homosexual men, residing in the Paris area or the French West Indies or with AIDS status were at a higher risk.

The objective of our study was to examine trends in TB incidence rates and risk factors since 1997 among patients enrolled in the database in 1997 or before and who had no previous history of TB. Patients with a diagnosis of TB before the start date were, therefore, excluded. However, analyses restricted to patients included in the database after 1 January 1997 gave similar results, although with slightly larger confidence intervals (data not shown). Cases of TB were diagnosed by local infectious diseases physicians and were not validated by a validation committee. It is, thus, possible that some presumptive diagnosis were incorrect, resulting in misclassification. As diagnosis of pulmonary TB was added to the AIDS cases definition in 1993 long before this study [9], such misclassifications were probably balanced in the different groups and would lead only to an underestimation of the link between risk factors and TB. It should be noted that we did not include TB relapses, for which a prior history of TB is a strong risk factor. However, the large size of the FHDH population allows us to investigate events such as TB that are rare in industrialized countries.

The incidence rates of TB among HIV-infected patients in this study were 40 times higher than those reported among the general population in France and 20 times higher than those reported in the Paris area, which has the highest prevalence of TB in France with French Guyana [6], confirming that HIV in itself is a risk factor for TB. Of note, these incidence rates were as high as incidence rates reported for the HIV-seronegative population in a country with high incidence of TB, such as South Africa [12]. Overall incidence rates of TB in our study, which combines patients receiving and not receiving cART, were also higher than those reported after cART initiation in high-income countries, probably partly due to the high percentage of untreated patients in the study [13].

One-fifth to one-third of the patients with TB in our cohort had TB occurrence at the same time that HIV infection was diagnosed and recorded in the database, suggesting that TB continues to reveal HIV infection in industrialized countries. Cases of TB diagnosed at enrolment in the database mainly involved patients originating from sub-Saharan Africa, mainly infected through heterosexual intercourse and living in the Paris area, and patients with a higher level of immunodeficiency, all of which are associated with delayed access to care [14].

As in other studies, the increase in the incidence of TB in the periods 2000–2008 compared with that in 1997 was at least partly due to an increase in the number of HIV-infected patients originating from sub-Saharan Africa [15]. However, the risk of TB increased in migrants over time, whereas the proportion of migrants in the study population stabilized in the last periods. The incidence of TB also increased in nonmigrant HIV-infected patients over time, whereas it declined or stabilized in the general nonmigrant population, showing that the increased incidence of TB is not due solely to migration or to changes in the epidemiology of HIV infection [6,16]. The place of TB among first AIDS-defining events has remained stable in France since 2003, at about 22% [16]. Among migrant patients, TB was the first AIDS-defining event in 32% of cases in 1997, rising to 49% in 2003 and declining thereafter [16]. Nevertheless, the incidence of TB increased, not only in migrants but also in nonmigrant patients, in regions such as the Paris area and Guyana, where there is a high level of migration from countries endemic for TB, highlighting the probable interaction between different populations in these regions.

In addition to immunodeficiency (low CD4 cell count and AIDS), factors predictive of the response on cART (pVL) and migration status, the risk of TB was increased by factors known to be related to TB in both HIV-seropositive and HIV-seronegative populations, such as intravenous drug use [17–20]. Social deprivation is another known risk factor for TB. We had no information in the database on factors such as homelessness and incarceration that are associated with the risk of TB [18], and no information was available either on current drug use. Homosexuals, who tend to have higher socioeconomic status, had a lower incidence of TB in this study. Contrary to studies conducted in regions with poor access to antiretroviral therapy, the risk for TB fell with the length of follow-up in our database, probably owing to better access to care, rapid case identification at the beginning of follow-up and the use of antiretroviral therapy [12].

Isoniazid preventive therapy and cART have each been reported to reduce the risk of TB [17,19,21–23]. We had no information in the database on isoniazid prophylaxis, but isoniazid preventive therapy is currently rarely given in France in HIV-infected patients, except in cases of contact with patients with pulmonary TB. More stringent diagnosis and treatment of latent TB, together with the use of newer screening tests, such as those based on interferon release, could help to reduce the incidence of TB in such regions [24–30]. WHO recommendations of isoniazid-preventive therapy for all people living with HIV in areas where the prevalence of latent TB exceeds 30% [25–27] might be extended to selected populations in regions with a lower TB burden. Indeed, antiretroviral therapy was independently associated with a lower rate ratio of TB in our study, but the continuing increase in incidence rates and risks of TB in recent years despite the widespread use of cART calls for the co-prescription of TB-preventive therapy and cART for severely immunodepressed high-risk patients such as migrants and socially excluded patients [31].

In conclusion, the incidence of TB has been increasing in recent years among HIV-infected patients in France among both migrant and nonmigrant populations. This is partly related to the higher proportion, among the HIV-infected population, of sub-Saharan Africa migrants, who tend to be younger heterosexual men or women living in the Paris area; delayed access to care with short medical follow-up, poorer immune status, infrequent antiretroviral therapy; and other known risk factors for TB such as intravenous drug use. Selected patients, such as migrants from highly endemic regions and patients with delayed access to care in selected parts of France, might, therefore, benefit from co-prescription of TB-preventive therapy and cART.

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FHDH is supported by Institut National de la Santé et de la Recherche Médicale (INSERM), Agence Nationale de la Recherche sur le SIDA (ANRS) and the French Ministry of Health. We thank all the participants of the French Hospital Database on HIV, and especially the research assistants, without whom this work would not have been possible.

Clinical Epidemiology Group of the FHDH. Scientific committee: S. Abgrall, F. Barin, M. Bentata, E. Billaud, F. Boué, C. Burty, A. Cabié, D. Costagliola, L. Cotte, P. De Truchis, X. Duval, C. Duvivier, P. Enel, L. Fredouille-Heripret, J. Gasnault, C. Gaud, J. Gilquin, S. Grabar, C. Katlama, M.A. Khuong, J.M. Lang, A.S. Lascaux, O. Launay, A. Mahamat, M. Mary-Krause, S. Matheron, J.L. Meynard, J. Pavie, G. Pialoux, F. Pilorgé, I. Poizot-Martin, C. Pradier, J. Reynes, E. Rouveix, A. Simon, P. Tattevin, H. Tissot-Dupont, J.P. Viard, N. Viget.

DMI2 coordinating center: French Ministry of Health (Valérie Salomon), Technical Hospitalization Information Agency, ATIH (N. Jacquemet).

Statistical analysis center: INSERM U943 (S. Abgrall, D. Costagliola, S. Grabar, M. Guiguet, E. Lanoy, L. Lièvre, M. Mary-Krause, H. Selinger-Leneman), INSERM Transfert (J.M. Lacombe, V. Potard).

COREVIH: Paris area: Corevih Ile de France Centre (GH Pitié-Salpétrière: F. Bricaire, S. Herson, C. Katlama, A. Simon; Hôpital Saint-Antoine: N. Desplanque, P.M. Girard, J.L. Meynard, M.C. Meyohas, O. Picard; Hôpital Tenon: J. Cadranel, C. Mayaud, G. Pialoux), Corevih Ile de France Est (Hôpital Saint-Louis: J.P. Clauvel, J.M. Decazes, L. Gerard, J.M. Molina; GH Lariboisière-Fernand Widal: M. Diemer, P. Sellier; Hôpital Avicenne: M. Bentata, P. Honoré; Hôpital Jean Verdier: V. Jeantils, S. Tassi; Hôpital Delafontaine: D. Mechali, B. Taverne), Corevih Ile de France Nord (Hôpital Bichat-Claude Bernard: E. Bouvet, B. Crickx, J.L. Ecobichon, S. Matheron, C. Picard-Dahan, P. Yeni), Corevih Ile de France Ouest (Hôpital Ambroise Paré: H. Berthé, C. Dupont; Hôpital Louis Mourier: C. Chandemerle, E. Mortier; Hôpital Raymond Poincaré: P. de Truchis), Corevih Ile de France Sud (Hôpital Européen Georges Pompidou: D. Tisne-Dessus, L. Weiss; GH Tarnier-Cochin: D. Salmon; Hôpital Saint-Joseph: I. Auperin, J. Gilquin; Hôpital Necker adultes: L. Roudière, J.P. Viard; Hôpital Antoine Béclère: F. Boué, R Fior; Hôpital de Bicêtre: J.F. Delfraissy, C. Goujard; Hôpital Henri Mondor: C. Jung, Ph. Lesprit; Hôpital Paul Brousse: D. Vittecoq).

Outside Paris area: Corevih Alsace (CHRU de Strasbourg: P. Fraisse, J.M. Lang, D. Rey; CH de Mulhouse: G. Beck-Wirth), Corevih de l'Arc Alpin (CHU de Grenoble: J.P. Stahl, P. Lecercq), Corevih Auvergne-Loire (CHU de Clermont-Ferrand: F. Gourdon, H. Laurichesse; CHRU de Saint-Etienne: A. Fresard, F. Lucht); Corevih Basse-Normandie (CHRU de Caen: C. Bazin, R. Verdon), Corevih Bourgogne (CHRU de Dijon: P. Chavanet), Corevih Bretagne (CHU de Rennes: C. Arvieux, C. Michelet), Corevih Centre (CHRU de Tours: P. Choutet, A. Goudeau, M.F. Maître), Corevih Franche-Comté (CHRU de Besançon: B. Hoen; CH de Belfort: P. Eglinger, J.P. Faller); Corevih Haute-Normandie (CHRU de Rouen: F Borsa-Lebas, F Caron), Corevih Languedoc-Roussillon (CHU de Montpellier: J. Reynes; CHG de Nîmes: J.P. Daures), Corevih Lorraine (Nancy Hôpital de Brabois: T. May, C. Rabaud; CHRU de Reims: J.L. Berger, G. Rémy), Corevih de Midi-Pyrénées (Toulouse CHU Purpan: E. Arlet-Suau, L. Cuzin, P. Massip, M.F. Thiercelin Legrand; Toulouse Hôpital la Grave: G. Pontonnier; Toulouse CHU Rangueil), Corevih Nord-Pas de Calais (CH de Tourcoing: N. Viget, Y. Yasdanpanah), Corevih PACA Est (Nice Hôpital Archet 1: P. Dellamonica, C. Pradier, P. Pugliese; CHG Antibes-Juan les Pins: K. Aleksandrowicz, D. Quinsat), Corevih PACA Ouest (Marseille Hôpital de la Conception: I. Ravaux, H. Tissot-Dupont; Marseille Hôpital Nord: J.P. Delmont, J. Moreau; Marseille Institut Paoli Calmettes: J.A. Gastaut; Marseille Hôpital Sainte-Marguerite: I. Poizot-Martin, F. Retornaz, J. Soubeyrand; Marseille Centre pénitentiaire des Baumettes: A. Galinier, J.M. Ruiz; CHG d'Aix-En-Provence: T. Allegre, P.A. Blanc; CH d'Arles: D. Bonnet-Montchardon; CH d'Avignon: G. Lepeu; CH de Digne Les Bains: P. Granet-Brunello; CH de Gap: J.P. Esterni, L. Pelissier; CH de Martigues: R. Cohen-Valensi, M. Nezri; CHI de Toulon: S. Chadapaud, A. Laffeuillade), Corevih Pays de la Loire (CHRU de Nantes: E. Billaud, F. Raffi), Corevih de la Vallée du Rhône (Lyon Hôpital de la Croix-Rousse: A. Boibieux, D. Peyramond; Lyon Hôpital Edouard Herriot: J.M. Livrozet, J.L. Touraine; Lyon Hôtel-Dieu: L. Cotte, C. Trepo).

Corevih Guadeloupe (CHRU de Pointe-à-Pitre: M. Strobel; CH Saint-Martin: F. Bissuel), Corevih Guyane (CHG de Cayenne: R. Pradinaud, M. Sobesky), Corevih Martinique (CHRU de Fort-de-France: A. Cabié), Corevih de La Réunion (CHD Félix Guyon: C. Gaud, M. Contant).

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epidemiology; HIV/AIDS; immigration; industrialized country; tuberculosis

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