Epidemiology of autoimmune and inflammatory diseases in a French nationwide HIV cohort : AIDS

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EPIDEMIOLOGY AND SOCIAL

Epidemiology of autoimmune and inflammatory diseases in a French nationwide HIV cohort

Lebrun, Delphinea,b; Hentzien, Maximea; Cuzin, Lisec; Rey, Davidd; Joly, Véroniquee; Cotte, Laurentf,g; Allavena, Clotildeh; Dellamonica, Pierrei; Servettaz, Améliea; Bani-Sadr, Firouzéa,j and the Dat’AIDS study group

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AIDS 31(15):p 2159-2166, September 24, 2017. | DOI: 10.1097/QAD.0000000000001603
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Abstract

Introduction

HIV infection and inflammatory and autoimmune diseases (IADs) are both related to immune dysfunction [1,2]. Combination antiretroviral therapy (cART) and immunodeficiency induced by HIV itself may favor or prevent the development of different IAD [1,2]. Indeed, the prevalence of some autoantibodies, such as antinuclear antibodies, is high and up to three times greater than in a healthy population [3]. In contrast, the frequency of autoantibodies is lower in patients on cART than in cART-naive patients [3]. Since the introduction of cART, patients living with HIV (PLHIV) have a higher life expectancy and develop more comorbidities [4,5]. Although the prevalence of comorbidities such as cardiovascular disease, non-HIV-related cancer, diabetes or chronic renal disease have been well described in the cART era, epidemiological data regarding IAD in PLHIV are scarce [2,6–13]. Furthermore, the role of immune restoration and HIV replication control following cART and hepatitis C virus (HCV) and/or hepatitis B virus (HBV) coinfection in the emergence of IAD is poorly known.

The aim of this study was thus to estimate the prevalence of IAD among PLHIV followed in a large French multicenter cohort in the cART era (from January 2000 to July 2013) and to describe the occurrence of IAD according to cART onset, the immunovirological status of the patients, and HCV and/or HBV coinfection.

Methods

Dat’AIDS is a French multicenter prospective cohort involving 12 large HIV reference centers in France [14]. Data are collected in real time during clinical visits and data collection is ongoing since 2000 using a computerized medical record. Dat’AIDS prospectively collects demographic, clinical and biological data, antiretroviral history, HIV viral load and CD4+ cell counts at regular 3–6-month intervals during routine clinical assessment [14]. The Dat’AIDS cohort is registered with clinicaltrials.gov under the identifier NCT02898987. All PLHIV followed up in the Dat’AIDS cohort from January 2000 to July 2013 were included.

Patients with IAD were identified by the presence of International Classification of Diseases, tenth revision (ICD-10) codes corresponding to these diseases in the database. These disorders included systemic lupus erythematosus (SLE), cutaneous lupus erythematosus, antiphospholipid syndrome, Sjögren's syndrome, systemic scleroderma, sarcoidosis, Takayasu arteritis, giant cell arteritis, Kawasaki's disease, periarteritis nodosa, granulomatosis with polyangeitis, IgA vasculitis, Goodpasture syndrome, Behcet's disease, polymyalgia rheumatica, rheumatoid arthritis (RA), ankylosing spondyloarthritis (SpA), psoriatic arthritis, psoriasis, autoimmune thyroiditis, Grave's disease, autoimmune hemolytic anemia, immune thrombocytopenia, celiac disease, chronic inflammatory bowel disease and multiple sclerosis (MS). A person was considered to have an IAD if one of these ICD-10 codes was identified or one of these disorders was cited as a medical history in the database.

The following data were collected for all patients: age, sex, duration of HIV infection, IAD diagnosis date. For patients whose IAD was diagnosed at the same time as, or after the HIV diagnosis, we recorded the following data, at the closest date to IAD diagnosis: antiretroviral treatment (yes/no), CD4+ and CD8+ lymphocyte counts, CD4+/CD8+ ratio, HIV viral load, hepatitis B surface antigen and hepatitis C antibodies positivity indicating current or previous HCV infection.

The chronology of onset of IAD in relation to HIV infection was determined as follows: If the time between the dates of diagnosis of these two disorders was less than 1 year, the chronology of the two conditions was considered concomitant. If the IAD diagnosis date was mentioned more than 1 year before the date of HIV diagnosis, the chronology of IAD was considered as before the HIV diagnosis. If the IAD diagnosis date was notified more than 1 year after the HIV diagnosis date, the chronology of IAD was considered as after HIV diagnosis.

Quantitative data were described as mean ± SD and qualitative data as number (percentage). Quantitative variables were compared using the Student t or Mann–Whitney U test, as appropriate and qualitative variables using the chi-square or Fisher's exact test. The prevalence of each IAD with 95% confidence intervals (CIs) was calculated among PLHIV actively followed in the cohort on 1 January 2012. All analyses were performed using SAS version 9.4 (SAS Institute Inc., Cary, North Carolina, USA).

Results

Between January 2000 and July 2013, 33 403 PLHIV were included in the Dat’AIDS cohort: 71% were men, and mean age at HIV-infection diagnosis was 33.7 ± 11.1 years; 16 and 7% had HCV coinfection and hepatitis B surface (HBs) antigen positivity, respectively. In total, 1381 patients (6%) with IAD were identified. The characteristics of the patients are presented in Table 1. Most IAD patients were men (78%). Hepatitis C coinfection was present in 292 IAD patients (21%) and HBs antigen positivity in 80 (6%). Only eight patients were infected with HIV-2. In addition, 52 patients presented two IAD.

T1-14
Table 1:
Characteristics of the study population and prevalence of inflammatory and autoimmune diseases on 1 January 2012.

The prevalence of the different IAD among the 18 431 PLHIV who were being actively followed-up as of 1 January 2012 is given in Table 1. The most prevalent IADs were psoriasis, sarcoidosis, RA, SpA, Grave's disease, autoimmune hemolytic anemia, immune thrombocytopenia and chronic inflammatory bowel disease. In contrast, the prevalence of SLE and MS was low. The chronology of onset of IAD in relation to HIV diagnosis and the immunological characteristics of the patients are presented in Table 2. IAD preceded HIV diagnosis in 220 patients (16%), was concomitant in 189 patients (14%), and developed more than 1 year after in 812 patients (59%). For 160 patients (12%), the chronology was unknown. When the IAD occurred after HIV diagnosis, the mean time between HIV infection and the IAD diagnosis was 10.6 ± 6.4 years.

T2-14
Table 2:
Chronology and immunological context at the time of diagnosis of inflammatory and autoimmune diseases.

Among the 1001 patients developing an IAD concomitantly or after HIV diagnosis, only 74 (7%) patients had a CD4+ cell count below 50 cells/μl, whereas 157 (16%) patients had a CD4+ cell count between 50 and 200 cells/μl. Data were unknown for 87 patients (9%).

Immunovirological status and antiretroviral coverage at IAD diagnosis for patients developing IAD after the diagnosis of HIV infection are presented in Table 3. A total of 572 (70%) were on antiretroviral therapy and 419 of them (73%) had undetectable HIV viral load. The mean CD4+ cell count was above 300 cells/μl for all IAD, except for Behcet's disease. The mean CD8+ cell count was above 830 cells/μl and the CD4+/CD8+ ratio below 1 for most IAD.

T3-14
Table 3:
Immunovirological context at the time of diagnosis of inflammatory and autoimmune diseases among patients whose inflammatory and autoimmune disease diagnosis was made after that of HIV.

Patients with psoriasis, Grave's disease, immune thrombocytopenia and autoimmune hemolytic anemia were significantly more often HCV coinfected compared with the entire cohort (24, 34, 38 and 41%, respectively versus 16%) (P < 0.001 each). As these IAD have also been observed as side-effects during or after interferon treatment, we compared HCV coinfection in the subset of patients who were interferon-therapy-naive or in whom IAD diagnosis was present before interferon therapy. Among HIV/HCV coinfected patients with a history of interferon therapy, the diagnosis of psoriasis, Grave's disease, immune thrombocytopenia and autoimmune hemolytic anemia were present after interferon therapy in 45 (n = 35/78), 73 (n = 8/11), 31 (n = 8/26) and 86% (n = 12/14), respectively. After excluding these patients and all patients without IAD who received interferon, only patients with psoriasis, Grave's disease and immune thrombocytopenia remained significantly more often HCV coinfected compared with the entire cohort (P < 0.001 for psoriasis and immune thrombocytopenia and P = 0.008 for Grave's disease).

Patients with immune thrombocytopenia and autoimmune hemolytic anemia more often had HBs antigen positivity compared with the entire cohort (13 and 15 versus 7%; P < 0.01 and <0.05, respectively). After excluding patients who received interferon therapy for HBV and HCV coinfection (present in 1.2% of patients), the results remained similar: 13 and 19 versus 6.4%; P = 0.046 and 0.01, respectively.

Discussion

To the best of our knowledge, this is the first study to estimate the prevalence of 26 IAD in a large western multicenter cohort of PLHIV, representative of PLHIV living in France, as well as the first to analyze the chronology and the immunovirological context at the time of IAD diagnosis, and the frequency of HCV and/or HBV coinfection. The most prevalent IAD (>100/100 000 persons) were psoriasis, sarcoidosis, RA, SpA, Grave's disease, autoimmune hemolytic anemia, immune thrombocytopenia and chronic inflammatory bowel disease. In contrast, the prevalence of SLE and MS were low. Most patients (59%) developed IAD more than 1 year after HIV infection with a mean time from HIV diagnosis to IAD of 10.6 ± 6.4 years. The CD4+ cell counts were most often above 200 cells/μl at the time of diagnosis of IAD. HCV coinfection was significantly more frequent in patients with psoriasis, Grave's disease and immune thrombocytopenia, whereas chronic hepatitis B was more common in patients with immune thrombocytopenia and autoimmune hemolytic anemia.

Among the most prevalent IADs, psoriasis and sarcoidosis are those for which the CD4+ response plays a notable role [12,15]. Psoriasis is a common disease with an adult prevalence ranging from 0.51 to 11.43% in different countries [15]. In our cohort, psoriasis had the highest prevalence of the IADs (2295.0/100 000 persons). In line with our study, psoriasis also had the highest incidence density with 101.8/100 000 person-years among PLHIV followed in a Taiwanese cohort from 2000 to 2012 [6]. Psoriasis can be the presenting feature of HIV infection and can be cleared with antiretroviral therapy [15]. However, severe exacerbation of psoriasis during cART-associated immune reconstitution has been reported [15]. The main mechanisms postulated to explain the development of this IAD in HIV-infected patients are a T-cell imbalance characterized by decreased CD4+ T cells and a relative increase in CD8+ memory T cells [15]. Of note, more than half the patients (67%) in our cohort developed psoriasis after HIV diagnosis with a mean delay of 10.2 ± 6.5 years and had mean CD4+ and CD8+ cell counts of 426 ± 301 and 890 ± 467 cells/μl, respectively. The prevalence of HCV coinfection was higher in patients with psoriasis before any interferon therapy than in the subset of cohort who did not receive interferon (19 versus 11%; P < 0.001). Higher prevalence of HCV infection in patients with psoriasis has also been observed in epidemiological studies [16,17]. In one study, HCV-infected patients were twice as likely to have psoriasis than uninfected patients [16].

Sarcoidosis is an immune-mediated disease characterized by the accumulation of CD4+ T lymphocytes in active granulomas [12]. Since the introduction of cART, cases of sarcoidosis have been reported during the period of immunological recovery [18,19]. In contrast, in our cohort, 84% of patients developed sarcoidosis with a mean delay of 11.2 ± 7.6 years after HIV diagnosis. In line with our study, a series of 11 HIV-infected patients developing sarcoidosis with a mean interval of 92 ± 46 months after the diagnosis of HIV infection has also been reported [12]. Furthermore, the mean CD4+ cell count was high in this series, and comparable with that of our patients (447 ± 245 and 418 ± 234 cells/μl, respectively) [12].

RA and SpA can develop in PLHIV at any time, independently of cART [20,21]. In our cohort, 45% of patients with SpA were diagnosed before HIV diagnosis, whereas 64% of patients with RA were diagnosed after HIV diagnosis with a mean delay 13.0 ± 6.9 years. The prevalence of RA and SpA were 211.6/100 000 persons and 265.9/100 000 persons, respectively, higher than the overall prevalence rate of 62/100 000 persons (95% CI 33–91) and 47/100 000 persons (95% CI 22–72) found for RA and SpA, respectively, in France in 1997, although the prevalence of IAD reported in our study was not standardized, due to the low number of patients, and therefore, no direct comparison can be made with other studies [22]. In contrast, PLHIV followed in the Taiwanese cohort and who received cART had a lower risk of RA and SpA than the general population [6].

The prevalence of chronic inflammatory bowel diseases was 596.8/100 000 persons in our cohort. A potential pathophysiological relationship between chronic inflammatory bowel disease and HIV infection remains controversial, with a paucity of data to support or reject the hypothesis that CD4+ cell count depletion may induce remission of bowel inflammation in PLHIV [23]. Indeed, no formal epidemiological studies in the cART era have been published [24]. In our cohort, most patients (58%) who developed chronic inflammatory bowel disease did so after HIV diagnosis with a mean delay of 10.0 ± 5.2 years and a mean CD4+ cell count of 488 ± 313 cells/μl. They received antiretroviral therapy in 68% of cases and had undetectable HIV viral load in 44% of cases. A diagnosis of chronic inflammatory bowel in patients with low CD4+ cell count (<200 cells/μl) was observed in only 21% of patients, suggesting a possible protective role of low CD4+ cell count.

PLHIV have a higher risk of presenting autoimmune cytopenia than the general population [6]. Indeed, the prevalence of immune thrombocytopenia was 325.5/100 000 (95% CI: 243.3–407.8) in our cohort, whereas the unadjusted, overall 18-year period (1992–2009) prevalence of immune thrombocytopenia was found to be 50.29/100 000 (95% CI: 48.51–52.06) in the adult population in United Kingdom [25]. Both immune thrombocytopenia and autoimmune hemolytic anemia could be the first manifestations of HIV infection and may resolve with antiretroviral therapy, with a direct correlation with the decrease in HIV viral load below the detectable limit [2]. In our cohort, most of the cases occurred after HIV diagnosis, but 45% of patients with immune thrombocytopenia, and 70% of patients with autoimmune hemolytic anemia had an undetectable HIV viral load. Severe autoimmune cytopenias have been also described in treatment-naive HCV infection, with complete resolution observed with HCV treatment in some cases, and as a complication of interferon therapy [26–28]. In our cohort, after excluding patients with a diagnosis of immune thrombocytopenia and autoimmune hemolytic anemia after interferon therapy, both HCV coinfection and chronic hepatitis B were significantly more frequent in patients with immune thrombocytopenia (29 and 13%), whereas chronic hepatitis B was more common in patients with autoimmune hemolytic anemia (19%) compared the entire cohort who did not receive interferon (11 and 6.4%), underlining the possible role of HCV and/or HBV coinfection in their pathogenesis.

HCV coinfection was also significantly more frequent in patients with Grave's disease before any interferon therapy in our cohort as compared with the subset of cohort who did not receive interferon (21 versus 11%). Grave's disease is the leading cause of hyperthyroidism in the general population, in PLHIV and in HCV mono-infected patients and is most commonly diagnosed 12–36 months after cART-associated immune reconstitution [29–31]. In line with other studies, Grave's disease developed in most of cases after HIV diagnosis (83%) and in patients receiving cART (94%) [29]. In contrast, the mean delay from initiation of ART to the diagnosis of Graves's disease was high (8.9 ± 5.0 years), which is not in favor of cART-associated immune reconstitution as the likely pathogenesis of Graves’ disease in these patients [31].

Although SLE has rarely been reported among PLHIV, the Taiwanese cohort reported an incidence density of 17.7/100 000 person-years, corresponding to a standardized incidence rate of SLE that was twice as high in PLHIV as in the general population [6]. In our study, the prevalence of SLE was low (16.3/100 000) and seemed lower than the crude 2010 prevalence of SLE observed in France (47.0/100 000) [32]. As in other reports [2,7], all the cases of our cohort received antiretroviral therapy and had good immunovirological control at the time of SLE diagnosis.

HIV infection has been associated with a significantly lower risk of developing MS [33,34]. The incidence rate ratio of MS in Denmark in a cohort of 5018 patients with newly diagnosed HIV infection and 50 149 controls (1994–2011), matched for age and sex was 0.3 (95% CI 0.04–2.2) [33]. In a comparative cohort study in England between 1999 and 2011, in a cohort of 21 207 PLHIV and 5298 496 controls stratified by age and sex, the incidence rate ratio of developing MS in PLHIV relative to those without HIV was 0.38 (95% CI 0.15–0.79) [34]. In the Taiwanese cohort study, the incidence density of MS between 2000 and 2012 was also low, at 2.93/100 000 person-years [6]. In line with these results, we observed a low prevalence of MS (38.0/100 000). Of note, the prevalence of MS in 2004 in France was 94.7/100 000 population [35]. The physiopathogenesis of this possible protective association could be related to immunosuppression or to antiretroviral therapy, as it has been hypothesized that the pathogenesis of MS could be linked to several human endogenous retroviruses [34]. In our cohort, eight out of 20 patients (40%) developed MS after HIV diagnosis and all of them had undetectable HIV viral load, with a mean CD4+ cell count of 716 ± 378 cells/μl.

During HIV infection, CD8+ cell counts are elevated and do not normalize, despite long-term cART [36]. The exact role of CD8+ cells in autoimmune disease is poorly understood, apart from psoriasis, in which intraepidermal T cells are predominantly CD8+ and represent key effector cells [37]. Furthermore, the role of CD8+ cells and the CD4+/CD8+ ratio in HIV patients with IAD is unknown. In our cohort, no particular profile of CD8+ cell count or CD4+/CD8+ ratio was observed according to the different IAD. The mean CD8+ was above 830 cells/μl and the CD4+/CD8+ ratio below 1 for most of them.

The major strength of this study is that it provides data from a large nationwide prospectively collected cohort of over 33 000 PLHIV followed in routine practice in France. However, some limitations deserve to be mentioned. The major limitation concerns the identification of patients with IAD. These patients were identified by the presence of ICD-10 codes, assuming that the diagnoses were correctly established by clinicians. These diagnoses were not verified, and we could not assess whether the diagnoses met the criteria for diagnostic classifications commonly used in clinical research. However, our findings are in line with other published data [6]. The second limitation is the high level of missing data on ethnicity, precluding evaluation of this variable. Indeed, the prevalence of some IADs, such as SLE or MS, differs according to ethnicity [32,34]. Finally, we assumed HCV and HBV coinfection were present before IAD. This assumption may not be valid if patients had acquired them after IAD. However, previous studies have shown that these coinfections are present most of time at the time of HIV diagnosis [38]. Furthermore, the higher prevalence of HCV and HBV coinfection observed in some IAD in our cohort is in line with the literature [16,17,27,30].

Epidemiological data could be useful to identify risk factors and pathogenic mechanisms of IAD in the HIV population, as well as in the overall population, and could prompt researchers to consider more investigations into the possible relationship between HIV and IAD. Our study shows that some IAD are not rare among PLHIV, and occur mostly in patients with immunovirological control under cART. Furthermore, the role of HCV or HBV coinfection in some IAD is also confirmed. As the HIV population is ageing and cART therapy is now recommended for all HIV patients, follow-up of trends in the prevalence of IAD in patients with long-term cART therapy and immunovirological control is mandatory to evaluate the long-term impact of cART on the epidemiology of IAD in this population.

Acknowledgements

Dat’AIDS scientific committee: Dellamonica P., Pugliese P., Poizot-Martin I., Cuzin L., Yazdanpanah Y., Raffi F., Cabié A., Garraffo R., Delpierre C., Allavena C., Katlama C., Valantin M.A., Duvivier C., Hoen B., Peytavin G., Jacomet C., Rey D., Delobel P., Cheret A., Chidiac C., Isnard-Bagnis C., Cotte L., Peyramond D., Bani-Sadr F., Joly V., Jovelin T., Saune K., Roger P.M., Chirouze C., May T.

Dat’AIDS Study Group: P. Enel, V. Obry-Roguet, O. Faucher, S. Bregigeon, A. Ménard, I. Poizot-Martin, (Marseille); Alvarez M, Biezunski N, Cuzin L, Debard A, Delobel P, Delpierre C, Fourcade C, Marchou B, Martin-Blondel G, Porte L, Mularczyk M, Garipuy D, Saune K, Lepain I, Marcel M, Metsu D, Puntis E (Toulouse); P. Pugliese, L. Bentz, C. Ceppi, E. Cua, J. Cottalorda, J. Durant, S. Ferrando, JG Fuzibet, R. Garraffo, V. Mondain, A. Naqvi, I. Perbost, S. Pillet, B. Prouvost-Keller, C. Pradier, S. Wehrlen-Pugliese, P.-M. Roger, E. Rosenthal, P. Dellamonica (Nice); F. Raffi, C. Allavena, E. Billaud, C. Biron, B. Bonnet, S. Bouchez, D. Boutoille, L. Khatchatourian C. Brunet, T. Jovelin, N. Hall, C. Bernaud, P. Morineau, V. Reliquet, O. Aubry, P. Point, M. Besnier, H. Hüe, M. Cavellec, A. Soria, S. Sécher, E. André-Garnier, A. Rodallec, V. Ferré, L. Leguen, M. Lefebvre, O. Grossi (Nantes); A Cheret, P. Choisy (Tourcoing); C. Duvivier (Pasteur Necker), M.A. Valantin, R. Agher, C. Katlama (Paris Pitié Salpétriere); A. Cabié, S. Abel, S. Pierre-François, B. Liautaud (Fort de France); D. Rey, P. Fischer, M. Partisani, C. Cheneau, M. Priester, C. Bernard-Henry, M.L. Batard, E. de Mautort (Strasbourg); C. Chirouze, Q. Gardiennet (Besançon); F. Bani-Sadr, J.L. Berger, Y. N’Guyen, D. Lambert, M. Hentzien, D. Lebrun, C. Migault, I. Kmiec, V. Brodard (Reims), L. Cotte, C. Chidiac, T. Ferry, F. Ader, F. Biron, A. Boibieux, P. Miailhes, T. Perpoint, I. Schlienger, J. Lippmann, E. Braun, J. Koffi, C. Longuet, V. Guéripel, C. Augustin-Normand, C. Brochier, S. Degroodt (Lyon).

The Nadis EMR is developed and maintained by Fedialis Medica.

Authors contributions: All authors participated in the design of the study protocol and data collection. D.L. and M.H. performed the data management and statistical analyses. D.L., A.S. and F.B.-S. wrote the first article draft. All authors participated in interpretation of the data and writing of the final article and all authors approved the final article. F.B.-S. was responsible for the overall supervision of the study.

Conflicts of interest

There are no conflicts of interest.

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Keywords:

autoimmunity; Dat’AIDS cohort; HIV; multiple sclerosis; psoriasis; sarcoidosis

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