on behalf of the Swiss HIV Cohort Study,
Affiliations of authors: International Agency for Research on Cancer, Lyon, France (GMC, SF); Centro di Riferimento Oncologico, Aviano, Italy (JP, LDM); Coordination and Data Centre, Swiss HIV Cohort Study, Lausanne, Switzerland (MR, OK); Cancer Registry of the Canton of Zürich, Zürich, Switzerland (AK); 5Cancer Registry of the Canton of Geneva, Geneva, Switzerland (ER); Cancer Registry of the Canton of Vaud, Lausanne, Switzerland (FL); Cancer Registry of the Canton of Neuchâtel, Neuchâtel, Switzerland (FL); Cancer Registry of Basel, Basel, Switzerland (GJ); Cancer Registry of St. Gallen and Appenzell, St. Gallen, Switzerland (TF); Cancer Registry of the Canton of Ticino, Locarno, Switzerland (AB); Cancer Registry of the Canton of Valais, Sion, Switzerland (DDW)
Correspondence to: Gary M. Clifford, Ph.D., International Agency for Research on Cancer, 150 cours Albert Thomas, 69372 Lyon cedex 08, France (e-mail: clifford{at}iarc.fr).
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ABSTRACT |
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INTRODUCTION |
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Conversely, most clinical cohort studies of persons infected with HIV provide detailed individual information on behavioral risk factors, biologic markers, and treatment (5). However, cohort studies often lack the power to detect less frequent cancers and also include only selected groups of persons infected with HIV [e.g., homosexual and bisexual men (9) or hemophilic men (10)].
The Swiss HIV Cohort Study (SHCS) is a large prospective cohort that is representative of persons infected with HIV in Switzerland (11,12), with detailed follow-up information available that begins soon after diagnosis of HIV infection. Furthermore, the SHCS coverage areas largely overlap with popu-lation-based cancer registries that record comprehensive quality-checked information on cancer incidence (13). We used data from the SHCS and cancer registries to estimate excess cancer risk in persons infected with HIV and to investigate the modifying effects of HAART use and behavioral factors on cancer risk.
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SUBJECTS AND METHODS |
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Nine active cancer registries, covering 56% of the Swiss population, record population-based quality-checked epidemiologic data on cancer incidence in Switzerland (13). The cancer registries of Basel, Geneva, Ticino, St. Gallen and Appenzell, Vaud, and Zürich overlap directly with six of the seven regions covered by SHCS centers (all except the Bern SHCS center) (see Figure available at http://jncicancerspectrum.oupjournals.org/jnci/content/vol97/issue6). The Neuchâtel and Valais cancer registries do not directly overlap with SHCS centers, although some residents of these cantons are followed in a neighboring SHCS center (see Figure available at http://jncicancerspectrum.oupjournals.org/jnci/content/vol97/issue6). Records from the Glarus/Graubünden Cancer Registry were not available for linkage.
Swiss cancer registries vary greatly both in size and periods of cancer enrollment (Table 1). Routine indicators of data completeness and quality in the registries are good: only 1%3% of case patients are registered on the basis of death certificates only, and the proportion of histologic verification is greater than 90% (13).
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Each SHCS center held its own nominal participant records. Thus, each SHCS database was independently matched with the corresponding cantonal cancer registry. Furthermore, to account for intercantonal migration and health care mobility, cross-cantonal linkages within French-speaking Switzerland (Geneva, Lausanne, Neuchâtel, and Valais) and Italian/German-speaking Switzerland (Basel, St. Gallen, Zürich, and Ticino) were also conducted.
From January 1985 through January 2003, 12 490 persons infected with HIV were enrolled in the SHCS. Persons infected with HIV were excluded from the present study (in hierarchical order) if they 1) did not report a legal residence in a canton covered by a cancer registry with which their SHCS records were linked (4076 persons infected with HIV, principally those from the Bern SHCS center), 2) had no name available in the SHCS for linkage with cancer registries (80 persons infected with HIV), or 3) were not followed in the SHCS during periods with complete data at corresponding cantonal cancer registries (1030 persons infected with HIV, principally from the Zürich SHCS center, in which no cancer registry data were available after 1996). For each person infected with HIV included in the study, the relevant time period for the calculation of person-years at risk began 3 months after the date of SHCS enrollment and ended on the date of last SHCS information, date of cancer diagnosis, or death, whichever was earliest. Person-years at risk were censored for those younger than age 16 years (13 participants) and older than age 69 years (20 participants) and if no complete cancer registry data were available in the corresponding years (see Table 1 for complete data periods by registry) (126 participants left-censored, 2688 participants right-censored).
Observed cancers included only incident cases reported to cancer registries during the above-defined person-years at risk. Eighty-one KSs, 25 non-Hodgkin lymphomas, two invasive cervical cancers, and eight nonAIDS-defining cancers diagnosed between 0 and 3 months from SHCS enrollment were considered prevalent cases and were not included in standardized incidence ratio (SIR) calculations. Cancers were classified according to the International Classification of Diseases for Oncology, 2nd revision (ICD-O-2) (16) and according to the International Classification of Diseases and Related Health Problems, 10th revision (17). In situ carcinomas of the cervix (48 women) and other preneoplastic lesions (ICD-O-2 behavior codes 02) (16) were excluded from the present analysis because of incomplete reporting in cancer registries.
This study was approved by the ethics committees of the SHCS and the International Agency for Research on Cancer.
Statistical Methods
Expected numbers of incident cancers were computed from cancer registry, sex-, age- and period-specific incidence rates (13,18,19). Observed numbers of incident cancers in persons infected with HIV were compared with expected numbers by the SIR. Corresponding 95% confidence intervals (CIs) were computed using Poisson distribution (20). SIRs were calculated within strata of sex, HIV exposure category (with "injecting drug or sexual contacts" being attributed to "injecting drug use"), CD4+ cell count at SHCS enrollment (measured using flow cytometry), use (yes/no) of HAART (defined as prescription of at least three antiretroviral drugs, including a protease inhibitor or a non-nucleoside reverse transcriptase inhibitor), and period before or after AIDS diagnosis (14).
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RESULTS |
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Table 2 shows observed and expected numbers and corresponding SIRs for cancer sites or types with at least two cases observed. Statistically significantly elevated SIRs for persons infected with HIV compared with the general population were observed for KS (SIR = 192, 95% CI = 170 to 217), non-Hodgkin lymphoma (SIR = 76.4, 95% CI = 66.5 to 87.4), and invasive cervical cancer (SIR = 8.0, 95% CI = 2.9 to 17.4). Other statistically significantly elevated SIRs were observed for anal cancer (SIR = 33.4, 95% CI = 10.5 to 78.6); Hodgkin lymphoma (SIR = 17.3, 95% CI = 10.2 to 27.4); liver cancer (SIR = 7.0, 95% CI = 2.2 to 16.5); cancers of the lip, mouth, and pharynx (SIR = 4.1, 95% CI = 2.1 to 7.4); cancers of the trachea, lung, and bronchus (SIR = 3.2, 95% CI = 1.7 to 5.4); and nonmelanomatous skin cancer (SIR = 3.2, 95% CI = 2.2 to 4.5). Nonmelanomatous skin cancer included 26 basal cell carcinomas and five squamous cell carcinomas, and all lung cancers were histologically diagnosed as carcinomas. All nonAIDS-defining cancers combined showed a statistically significantly elevated SIR of 2.8 (95% CI = 2.3 to 3.3). The SIR for KS was much higher in women (SIR = 502, 95% CI = 239 to 927) than in men (SIR = 188, 95% CI = 166 to 212). No other relevant differences in SIRs between the sexes emerged, including SIRs for all nonAIDS-defining cancers combined (SIR = 2.9, 95% CI = 2.3 to 3.5 in men and SIR = 2.6, 95% CI = 1.7 to 3.7 in women) (Table 2).
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More than half of enrolled persons infected with HIV (3878 [53.1%]) never developed AIDS during the study follow-up period. However, 1415 (19.4%) were enrolled at/after AIDS diagnosis and 2011 persons infected with HIV (27.5%) were diagnosed with AIDS during follow-up. To compare the results with those of other population-based linkage studies based on AIDS diagnosis, we estimated and compared SIRs for nonAIDS-defining cancers before and after AIDS diagnosis (Table 3). For Hodgkin lymphoma, the SIR after AIDS diagnosis (SIR = 25.7, 95% CI = 9.2 to 56.2) was higher than that before diagnosis (SIR = 14.9, 95% CI = 7.7 to 26.1), although 95% confidence intervals were broad and overlapped. For all nonAIDS-defining cancers combined, SIRs before and after AIDS diagnosis were similar (SIR = 2.6, 95% CI = 2.1 to 3.2 and SIR = 3.3, 95% CI = 2.4 to 4.5, respectively).
SIRs were investigated by risk category to evaluate the influence of behavioral factors (Table 4). Thirty-two percent of persons infected with HIV were homosexual or bisexual men, 37% were intravenous drug users, and 31% belonged to other exposure categories (mostly heterosexuals, 28%). The SIR for KS was higher in homo/bisexual men (SIR = 346, 95% CI = 302 to 395) than in intravenous drug users (SIR = 33.6, 95% CI = 19.9 to 53.2), whereas heterosexuals/others had an intermediate risk (SIR = 130, 95% CI = 87.6 to 186). SIRs for non-Hodgkin lymphoma and invasive cervical cancer, where applicable, varied less across the risk categories than that of KS. SIRs for all nonAIDS-defining cancers combined were higher for intravenous drug users (SIR = 4.3, 95% CI = 3.2 to 5.7) than for homo/bisexual men (SIR = 2.6, 95% CI = 1.9 to 3.4) or heterosexuals/others (SIR = 2.0, 95% CI = 1.3 to 2.8), largely because SIRs of intravenous drug users for cancer of the trachea, lung, and bronchus (SIR = 12.6, 95% CI = 5.0 to 26.1; SIR = 1.2, 95% CI = 0.2 to 3.5; and SIR = 3.0, 95% CI = 0.8 to 7.9, respectively) and liver cancer (SIR = 50.5, 95% CI = 15.9 to 119 versus 0 in other risk categories) were higher than those in the other groups.
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DISCUSSION |
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Association of HAART With Cancer Risks
In this study, the impact of HAART on cancer risk, based on individual treatment data, was evaluated in persons with a median follow-up of 4.8 years post-HAART. By mid-1997, 70% of SHCS participants with a history of CD4+ cell count less than 200 cells/mm3 were receiving HAART (6). Decreases in KS and non-Hodgkin lymphoma risks in HAART users were evident, confirming findings from previous studies (5,21,22).
A statistically significant decline in KS, but not yet in non-Hodgkin lymphoma, had emerged in an earlier evaluation of the SHCS among which the 19921994 and 19971998 periods were compared (6). There was no evidence from the present study that HAART was associated with a reduced SIR ofcancers other than KS or non-Hodgkin lymphoma (5), but rather that the SIR of certain nonAIDS-defining cancers may have actually increased in the post-HAART era. A possible explanation for this observation is that the improvement in life expectancy made possible by new antiretroviral treatment, along with an only partial reconstitution of immune status, may allow a larger number of cancers with long latent periods to manifest clinically.
Hodgkin Lymphoma
In the present study, persons infected with HIV showed a 17-fold increased risk for Hodgkin lymphoma compared with that of the general population, which is slightly higher than in previous studies (1,2,4). For the first time to our knowledge, however, the SIR for Hodgkin lymphoma showed a tendency to increase in the post-HAART era. Although the change was similar in both men and women, 95% confidence intervals on the estimates for HAART users and nonusers were broad and overlapped, and so random variation cannot be ruled out. The association between HAART and Hodgkin lymphoma incidence requires confirmation in other studies with longer follow-up after HAART.
As a consequence of changes in opposite directions, however, HAART users seem to have a similar SIR for Hodgkin lymphoma and non-Hodgkin lymphoma (although absolute numbers remain higher for non-Hodgkin lymphoma). The relationship we observed is different from past findings up to 1998, where SIRs for Hodgkin lymphoma were more than 10-fold lower than those for non-Hodgkin lymphoma (1,4). A "threshold effect" of immunity on the risk of different cancers may account for the present and previous findings. Mbulaiteye et al. (23) reported an increased non-Hodgkin lymphoma risk with each decline of 100 CD4+ cells/mm3, whereas Hodgkin lymphoma risk was similar for individuals in the greater than or equal to 200, 100199, and 5099 CD4+ cells/mm3 categories but much lower for individuals with less than 50 CD4+ cells/mm3. Furthermore, although organ transplant recipients are at greatly elevated risk for non-Hodgkin lymphoma, they have little excess risk for Hodgkin lymphoma (24), suggesting important differences in their relationship to immunodeficiency. Misclassification of the type of lymphoma is unlikely to account for our findings, because all Hodgkin lymphomas were histologically confirmed, and only eight cases (3%) of non-Hodgkin lymphoma were reported as lymphomas not otherwise specified.
Contribution of Smoking to Cancer Risk
Although the information on smoking history was missing for the earliest part of the cohort, it is worth noting that no lung cancers were observed in persons infected with HIV who were nonsmokers, and excess risks were insensitive to CD4+ counts. Thus, a threefold excess risk of cancers of the trachea, lung, and bronchus in all persons infected with HIV, consistent with previous studies (15,25), seems to be directly attributable to high smoking levels of persons infected with HIV (26), particularly intravenous drug users (27). The fact that all lung cancers were histologically diagnosed carcinomas excludes, however, misclassification with masses of non-neoplastic origin or non-Hodgkin lymphoma in our study. Cancers of the lip, mouth, and pharynx showed a risk pattern similar to that of cancer of the lung, with a predominance among intravenous drug users and a lack of case patients among nonsmokers.
We observed a high prevalence of smoking in the SHCS (72% overall, 96% in intravenous drug users). This observation illustrates the great importance, especially after the introduction of HAART, of planning active smoking cessation programs for persons infected with HIV (7).
Human PapillomavirusRelated Cancers
Immunity is important for the clearance of human papillomavirus (HPV) infection and of preneoplastic lesions of the anogenital tract (28), and our present study confirmed the fact that persons infected with HIV are at excess risk for HPV-related cancers (i.e., cervical and anal cancer). The excess risk of invasive cervical cancer found in women in the SHCS (SIR = 8.0) confirms reports from record linkage studies from the United States and Italy (1,4). As reported previously (1,2,4), the SIR for anal cancer (31.9) was much more elevated than that of invasive cervical cancer, but anal cancer was nearly restricted to homosexual and bisexual men (four of five anal cancer cases). Increased exposure to HPV through anal intercourse may therefore contribute substantially, along with impaired immunity, to the strength of the observed association. SIRs for invasive cervical cancer and anal cancer were not clearly affected by the CD4+ count or HAART use.
At least two additional types of cancer may be associated with HPV. Mucosal HPV types are associated with a fraction of cancers of the mouth and pharynx (29). HPV may thus contribute, along with smoking, to the fourfold increased risk of cancer of the lip, mouth, and pharynx observed in the SHCS. Finally, nonmelanomatous skin cancer, which is associated with cutaneous HPV types (30), was found to be increased by threefold in the SHCS. This increase is in agreement with the SIR reported in Australia (4.2) (2) and Scotland (2.8) (3), and slightly higher than the SIR from Italy (1.5) (4). Although the SIR is statistically significant, the excess of this tumor in persons infected with HIV is still approximately 10-fold less than that among organ transplant recipients (24). Furthermore, the squamous/basal cell cancer ratio in this study was low (5/26), at variance with what is reported among organ transplant recipients (30). Misclassification with KS appears unlikely because all skin cancers in our study were histologically confirmed.
Liver Cancer in Persons Infected With HIV
Liver cancer is etiologically linked with infection with HBV and HCV, but the influence of immune status on the development of chronic hepatitis, cirrhosis, and hepatocellular carcinoma is not well understood. No clear excess of liver cancer in people with HIV or AIDS emerged in early studies (31). The sevenfold excess risk of liver cancer in the SHCS is consistent with an eightfold risk identified in people with AIDS in the United States (1) but greater than those found in Italy (4) (1.9) and Australia (2) (2.7).
Although the excess of hepatocellular carcinoma in Swiss persons infected with HIV was primarily due to co-infection with HBV and/or HCV in intravenous drug users, it remains difficult to disentangle the direct interaction of HIV and HBV/HCV from the effect of their common transmission route. Nevertheless, co-infection with HIV and HCV or HBV, respectively, led to higher mortality from liver cancer than did HCV or HBV infection alone in a study of British hemophilic men and boys (10) and of homosexual men in the United States (9).
Study Strengths and Limitations
The SHCS has many strengths, including a large cohort size, length, and completeness of follow-up and availability of information, at least for a proportion of persons infected with HIV, on cancer risk factors. Approximately half of persons infected with HIV as well as the majority of AIDS patients in Switzerland have been enrolled in the SHCS, and both sexes and different risk categories are well represented. Another major strength of the present methodology was the access to follow-up of persons infected with HIV soon after HIV diagnosis, many of whom (53%) never developed AIDS. To identify cancers influenced by HIV-induced immunosuppression, most previous studies compared cancer risks in persons with AIDS before and after AIDS (1), as well as by CD4+ counts at AIDS diagnosis (4,8,32) but could not evaluate risks in persons infected with HIV who never developed AIDS before cancer or death.
This study also has some limitations. Sixty KS, 34 non-Hodgkin lymphoma, five invasive cervical cancer, and four Hodgkin lymphoma cases recorded in the SHCS during the relevant person-years at risk could not be identified in corresponding cancer registries and are not included in SIR calculations. Although these missed incident cases may simply have turned out not to be malignancies on histologic confirmation, they may also have resulted from undermatching due to inaccuracies in personal identifiers and self-reported legal residence in the SHCS. Conversely, some KS cases may not have been biopsied, resulting in under-reporting to cancer registries. Both undermatching and under-reporting would result in an underestimation of SIRs. Although the inverse problem of overmatching may also have occurred, resulting in an overestimation of SIRs, we expect it to have been minimal, given the high specificity of the linkage procedure (15). The potential for overestimation of person-years under surveillance and ascertainment bias associated with AIDS diagnosis (inherent in previous linkage studies using AIDS registries) should also be small, given that all persons infected with HIV were under close active follow-up and that the majority were not diagnosed with AIDS during this period.
In conclusion, HAART treatment may prevent excess risk of KS and non-Hodgkin lymphoma, but not that of Hodgkin lymphoma or other nonAIDS-defining cancers. Focusing on ways to encourage persons infected with HIV to quit smoking would be effective in reducing lung cancer in these persons.
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NOTES |
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This study was performed within the framework of the Swiss HIV Cohort Study, supported by the Swiss National Science Foundation (Grant 3347-069366) and was funded by grants from OncoSuisse (ICP OCS 01355-03-2003) and Grant 20 F.3, from the Istituto Superiore di Sanità, Rome, Italy.
The authors thank Dr. Claudia Braga for updating the software used for linkage, Ms. Trudy Perdrix-Thoma for technical assistance, Bruno Ledergerber (Zürich), Cedric Bandelier (Geneva), Jose Oliveira (Vaud), Pedram Sandi (Basel), Stefano Bachmann and Pietro Vernazza (St. Gallen), Enos Bernasconi (Ticino), Nicole Probst (Zürich), Gerald Fioretta and Christine Bouchardy (Geneva), Lalao Randimbison (Vaud), Marc Wirdam (Basel), and Fabio Montanaro (Ticino) for assisting with the linkage procedures.
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Manuscript received September 10, 2004; revised January 5, 2005; accepted January 20, 2005.
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