Fifty-three of the 132 patients died, 34 (64.2%) of anal cancer. The survival curve with anal cancer is shown in Fig. 2. The 2-year survival rates in the cART and the precART period were 79.8% [95% confidence interval (CI), 72.2–87.4] and 45.5% (95% CI, 16.0–74.9), respectively. In a multivariable Cox model, patients diagnosed with anal cancer in the precART period had a higher risk of death than those diagnosed in the cART period [hazard ratio, 14.1; 95% CI, 5.2–38.6].
The main characteristics of the patients in the groups with and without anal cancer are shown in Table 2. In addition, patients with anal cancer were exposed to cART for a median duration of 37.1 months before the diagnosis of anal cancer (IQR, 4.5–59.8)) and patients without anal cancer for a median duration of 14.5 months (IQR, 0.0–59.6) before death or the end of follow-up. Whatever the multivariable model (Table 2), anal cancer was more likely to occur in older patients, in MSM, in patients with a prior AIDS diagnosis and in patients with lower nadir CD4 cell counts. For example, in model 1 adjusted on the period, men had a higher risk of anal cancer than women (hazard ratio, 7.7 and 2.6 for MSM and non-MSM, respectively). MSM were more at risk of anal cancer than were non-MSM (hazard ratio, 3.0; 95% CI, 2.0–4.5). No relationship between sex, the HIV transmission group and the study period was found. A significant increase in the incidence of anal cancer was observed in the recent cART era as compared with the precART period, with adjusted hazards ratios of 2.9 (95% CI, 1.3–6.3), 2.1 (95% CI, 0.9–4.9) and 2.2 (95% CI, 1.0–5.3), respectively. Compared with the period of 1999–2000, hazard ratio was 0.8 (95% CI, 0.5–1.2) in the years 2001–2002 and 0.8 (95% CI, 0.5–1.3) in the years 2003–2004, indicating no significant increase in the incidence of anal cancer in the three sub-periods of the recent cART era. In the model 2 adjusted on cART, exposure to cART was associated with a higher risk of anal cancer (hazard ratio, 1.7; 95% CI, 1.1–2.8). When the analysis was restricted to the years 1998–2004, the hazard ratio associated with the exposure to cART was similar (hazard ratio, 1.7; 95% CI, 0.9–3.2).
The overall incidence of anal cancer per 100 000 person-years increased between the precART and the cART period (Fig. 3). In the precART, the early cART and the three sub-periods of the recent cART era (1999–2000, 2000–2001 and 2002–2003), the incidences of anal cancer were 10.5 (95% CI, 4.3–16.7), 18.4 (95% CI, 10.1–26.6), 43.1 (95% CI, 29.2–57.0), 36.3 (95% CI, 23.8–48.9) and 39.3 (95% CI, 25.9–52.7) per 100 000 person-years, respectively. The increase was noted in all HIV transmission groups with a hazard ratio of 2.5 (95% CI, 1.2–5.3) between 1999 and 2004 and between 1992 and March 1996, even if absolute risk was higher in MSM than in the other transmission groups. The incidence of anal cancer in MSM was 18.2 per 100 000 (95% CI, 4.7–31.7) in the precART period, 45.0 (95% CI, 23.6–66.4) in the early cART period and 75.1 (95% CI, 57.4–92.8) between 1999 and 2004. Among other men and among women, the incidence of anal cancer in the recent cART era was 28.6 and 9.4 per 100 000 person-years, respectively.
All cases of anal cancer were validated, and 93.9% of diagnoses were histologically confirmed. The primary analysis included both confirmed and presumptive diagnoses, but the results were similar when presumptive cases were excluded. For instance, as compared with the precART period, the adjusted hazard ratio was 2.5 (95% CI, 1.2–5.3) in the years 1999–2004 in the analysis, which included presumptive diagnoses and hazard ratio was 2.5 (95% CI, 1.1–5.6) in the analysis, which only included confirmed diagnoses.
The present study shows that anal cancer in HIV-infected patients occurred in MSM and at around 40 years of age, with an increase in the incidence since the introduction of cART in France. This increase affected all HIV transmission groups, although the absolute risk was higher in MSM.
Two important strengths of the present study are the inclusion of a large population from a nationwide study, which included prospectively studied individuals from various transmission groups both before and after the advent of cART, and the large number of person-years of follow-up (465 872 person-years).
As anal cancer is not an AIDS-defining illness, it is likely that some cases, especially of micro-invasive cancer, were not recorded in the database. However, this possible undernotification should have been fairly stable with time. Even if several studies documented an increased risk of anal cancer in HIV-infected patients in the precART era [2–4], national recommendations on AIN screening were introduced in France in 2002 , possibly resulting in over-reporting in the later period of the study. If this ascertainment bias was major, however, one would have expected the risk of anal cancer to increase more markedly after 2003. This was not the case; the increase was observed after 1996 in MSM and after the years 1999–2000 in non-MSM and women. In addition, the small number of cases observed between 1992 and April 1996 could be explained by a weak survival of HIV-infected patients and, therefore, insufficient time for anal cancer to develop.
Several studies showed an increased risk of anal cancer among HIV-infected patients in the precART era [2–4]. In contrast, few data on the incidence of anal cancer have been published since cART became widely available in industrialized countries. Moreover, comparisons between studies are difficult because the incidence depends upon age, immunodepression, AIDS, ethnicity, sex and the HIV transmission group. Nevertheless, it is possible to compare incidence trends over time. The AIDS and cancer registries for San Diego County were recently matched from 1988 to 2000 . The average annual incidence of invasive anal cancer precART was 49 per 100 000 men aged 25–64 years, compared with 144 per 100 000 post-cART. In this latter study, the high proportion of MSM and the restriction of the study population to patients with AIDS probably explain the much higher incidence rates of invasive anal cancer than found in our study (roughly 40/100 000 in the cART period). However, the incidence increased 2.9 fold between the two periods of this study, which is similar to what we observed. Similar increased ratios were found in two European cohorts  and a US registry . In contrast, the recently published study by Engels et al.  did not report such an increase.
Most of these studies examined two calendar periods (precART era compared with cART era) in order to indirectly measure the potential effect of cART on the incidence of anal cancer. In our study, cART was associated with an increase in the incidence of anal cancer. However, it is difficult to separate the effect of cART itself (individual effect) from that of the calendar period (population effect). As pointed out by Palefsky , several mechanisms may account for the increased frequency of HPV-associated diseases in HIV-seropositive individuals. One is the modulation of the immune response to HPV. Despite increasing the CD4 T-cell count and restoring immunity to several opportunistic pathogens [24–26], cART does not appear to enhance the control of HPV and has been associated with the progression of HPV-related AIN, the precursor of anal cancer [11–13]. Thus, the cART-induced increase in the survival of HIV-infected patients may allow sufficient time for AIN to progress to invasive anal cancer. The observed difference in the incidence between the precART and the cART periods could be due to differences in survival times between these two periods. Prior to cART, survival time was so short that it was insufficient for progression to anal cancer, whereas after the use of cART, the survival increased and the cancers became manifest. The incidence of anal cancer in our study remained stable during the recent cART period, likely because after an initial improvement in the survival associated with the advent of cART in the HIV-infected population, there has been no improvement in most recent periods .
One possible reason for heterosexual men having anal cancer would be the under-reporting of men-men sex. Nevertheless, recent data suggest that opportunistic HPV infection and AIN may occur in the anal canal of immunocompromized patients who have not practiced receptive anal intercourse [28,29]. This is in line with the increase in invasive anal cancer in nonhomosexual patients in our study.
Anal cancer shares many biological characteristics with cervical cancer, including a similar histopathologic appearance and association with HPV infection. The incidence of cervical cancer in HIV-infected patients is much lower than that of anal cancer  and its incidence remained unchanged or tended to increase slightly since the introduction of cART [15,30,31]. One may speculate that this different pattern could be explained by the fact that HIV-infected women undergo a regular cervical cancer screening program.
Immunosuppression may accelerate the progression from high-grade AIN to invasive anal cancer as CD4 cell nadir and AIDS onset, which are markers of immunosuppression, were independent risk factors for anal cancer in our study. However, Frisch et al.  did not found any association between anal malignancies and levels of immunosuppression in a study of HPV-associated cancers among 309 365 patients with HIV infection in the US.
The overall 2-year survival rate with anal cancer in the cART period was 79%, in keeping with the results of Biggar et al.  or Chiao et al.  who found no difference with the general population. Some other studies have suggested a lower survival rate than in the general population [5,33–36] but this concerns a very small number of cases, and some of them did not have a long period under cART. So, it seems that cART improved survival which became similar to that in HIV-negative individuals as showed by Chiao et al. .
In conclusion, given the cost-effectiveness of screening for anal AIN in HIV-infected MSM , our findings strongly suggest that screening for AIN should be implemented in HIV-infected MSM, whether or not they are using cART. Taking into account the lower level of incidence among other men and women, we recommend making such a cost-effectiveness evaluation before implementing screening in these groups.
The French Hospital Database on HIV is supported by the Agence Nationale de Recherches sur le SIDA et les hépatites (ANRS), INSERM and the French Ministry of Health.
The authors are grateful to all participants and research assistants of the French Hospital Database on HIV. Author contribution: Conception and design: C. Piketty, S. Grabar, M. Mary-Krause, D. Costagliola. Analysis and interpretation of the data: H. Selinger-Leneman, C. Piketty, S. Grabar, M. Mary-Krause, D. Costagliola. Drafting of the manuscript: C. Piketty, S. Grabar, M. Mary-Krause, D. Costagliola. Critical revision of the article for important intellectual content: C. Piketty, S. Grabar, M. Mary-Krause, D. Costagliola, C. Duvivier, M. Bonmarchand, L. Abramowitz. Final approval of the article: C. Piketty, H. Selinger-Leneman, S. Grabar, M. Mary-Krause, D. Costagliola, C. Duvivier, M. Bonmarchand, L. Abramowitz. Provision of study materials or patients: H. Selinger-Leneman, S. Grabar, M. Mary-Krause, D Costagliola. Statistical expertise: S. Grabar, M. Mary-Krause, D. Costagliola. Administrative, technical or logistic support: H. Selinger-Leneman. M. Mary-Krause, D. Costagliola. Collection and assembly of data: H. Selinger-Leneman, C. Piketty.
Clinical epidemiology group of the French hospital database on HIV.
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, 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 (E. Aronica, A. Pariente-Khayat), Technical Hospitalisation Information Agency, ATIH (N. Jacquemet, A. Rivet).
Statistical analysis center: INSERM U720 (S. Abgrall, D. Costagliola, S. Grabar, M. Guiguet, E. Lanoy, H. Selinger-Leneman, L. Lièvre, M. Mary-Krause, V. Potard)
CISIH: Paris area: CISIH de Bichat-Claude Bernard (Hôpital Bichat-Claude Bernard: E. Bouvet, B. Crickx, J.L. Ecobichon, C. Leport, S. Matheron, C. Picard-Dahan, P. Yeni), CISIH de Paris-Centre Ouest (Hôpital Européen Georges Pompidou: D. Tisne-Dessus, L. Weiss; G.H. Tarnier-Cochin: D. Salmon, D. Sicard; Hôpital Saint-Joseph: I. Auperin, J. Gilquin; Hôpital Necker adultes: L. Roudière, J.P. Viard), CISIH de Paris-Sud (Hôpital Antoine Béclère: F. Boué, R. Fior; Hôpital de Bicêtre: J.F. Delfraissy, C. Goujard; Hôpital Henri Mondor: C. Jung, P.H. Lesprit; Hôpital Paul Brousse), CISIH de Paris-Est (Hôpital Saint-Antoine: N. Desplanque, J.L. Meynard, M.C. Meyohas, O. Picard; Hôpital Tenon: J. Cadranel, C. Mayaud, G. Pialoux), CISIH de Pitié-Salpétrière (G.H. Pitié-Salpétrière: F. Bricaire, S. Herson, C. Katlama, A. Simon), CISIH de Saint-Louis (Hôpital Saint-Louis: J.P. Clauvel, J.M. Decazes, L. Gerard, J.M. Molina; G.H. Lariboisière-Fernand Widal: M. Diemer, P. Sellier), CISIH 92 (Hôpital Ambroise Paré: H. Berthé, C. Dupont; Hôpital Louis Mourier: C. Chandemerle, E. Mortier; Hôpital Raymond Poincaré: P. de Truchis), CISIH 93 (Hôpital Avicenne: M. Bentata, P. Honoré; Hôpital Jean Verdier: V. Jeantils, S. Tassi; Hôpital Delafontaine: D. Mechali, B. Taverne).
Outside Paris area: CISIH Auvergne-Loire (CHU de Clermont-Ferrand: F. Gourdon, H. Laurichesse; CHRU de Saint-Etienne: A. Fresard, F. Lucht); CISIH de Bourgogne-Franche Comté (CHRU de Besançon; CHRU de Dijon; CH de Belfort: P Eglinger, JP Faller; CHRU de Reims); CISIH de Caen (CHRU de Caen: C. Bazin, R. Verdon), CISIH de Grenoble (CHU de Grenoble), CISIH de Lyon (Hôpital de la Croix-Rousse: A. Boibieux, D. Peyramond; Hôpital Edouard Herriot: J.M. Livrozet, J.L. Touraine; Hôtel-Dieu: L. Cotte, C. Trepo), CISIH de Marseille (Hôpital de la Conception: I. Ravaux, H. Tissot-Dupont; Hôpital Nord: J.P. Delmont, J. Moreau; Institut Paoli Calmettes: J.A. Gastaut; Hôpital Sainte-Marguerite: I. Poizot-Martin, F. Retornaz, J. Soubeyrand; CHG d'Aix-En-Provence: T. Allegre, P.A. Blanc; Centre pénitentiaire des Baumettes: A. Galinier, J.M. Ruiz; C.H. d'Arles; C.H. d'Avignon: G. Lepeu; C.H. de Digne Les Bains: P. Granet-Brunello; C.H. de Gap: J.P. Esterni, L. Pelissier; C.H. de Martigues: R. Cohen-Valensi, M. Nezri; CHI de Toulon: S. Chadapaud, A. Laffeuillade), CISIH de Montpellier (CHU de Montpellier: J. Reynes; CHG de Nîmes), CISIH de Nancy (Hôpital de Brabois: T. May, C. Rabaud), CISIH de Nantes (CHRU de Nantes: E. Billaud, F. Raffi), CISIH de Nice (Hôpital Archet 1: P. Pugliese, C. Pradier; CHG Antibes Juan les Pins), CISIH de Rennes (CHU de Rennes: C Arvieux, C Michelet), CISIH de Rouen (CHRU de Rouen: F Borsa-Lebas, F Caron), CISIH de Strasbourg (CHRU de Strasbourg: P Fraisse, JM Lang, D Rey; CH de Mulhouse), CISIH de Toulouse (CHU Purpan: E. Arlet-Suau, L. Cuzin, P. Massip, M.F. Thiercelin Legrand; Hôpital la Grave; CHU Rangueil), CISIH de Tourcoing-Lille (C.H. Gustave Dron; C.H. de Tourcoing: Y. Yasdanpanah), CISIH de Tours (CHRU de Tours; CHU Trousseau).
Overseas: CISIH de Guadeloupe (CHRU de Pointe-à-Pitre), CISIH de Guyane (CHG de Cayenne: R. Pradinaud, M. Sobesky), CISIH de Martinique (CHRU de Fort-de-France), CISIH de La Réunion (CHD Félix Guyon: C. Gaud, M. Contant).
This work has been presented in part at the 16th International AIDS Conference, Toronto, Canada in August 2006.
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Keywords:© 2008 Lippincott Williams & Wilkins, Inc.
anal cancer; cancer; combination antiretroviral therapy; HIV infection; human papillomavirus infection; immune restoration; papillomavirus