Abstract
Background
It is unclear whether cancer risk among people with human immunodeficiency virus (HIV, PWH) has declined equally across all racial/ethnic and transmission risk groups.
Methods
We used data on PWH aged ≥20 years from the HIV/AIDS Cancer Match Study during 2001–2019. We used Poisson regression to assess time trends in incidence rates for each cancer site by racial/ethnicity and risk groups, adjusting for age, registry, and sex. We also estimated adjusted rate ratios across racial and ethnic and risk groups in 2001–2004 and 2015–2019.
Results
Trends in age-standardized rates differed across racial/ethnic groups and across risk groups for some cancers. For example, liver cancer rates declined 23% per 5-year period among White PWH, 11% among Black PWH, and 18% among Hispanic PWH. Anal cancer rates declined among men who have sex with men, were stable among people who inject drugs, and increased among other risk groups. Between 2001–2004 and 2015–2019, the relative difference in cancer incidence rates by race/ethnicity increased for Hodgkin lymphoma (HL) and liver cancer but decreased for non-Hodgkin lymphoma (NHL); by risk group, relative differences increased for NHL and liver cancer and decreased for HL and lung and anal cancers.
Conclusions
Among PWH in the United States during 2001–2019, HL, lung, liver, and cervical cancer rate trends were different across racial/ethnic groups. HL, lung, anal, and liver cancer rate trends were different across risk groups. Future work should examine underlying causes of the differences in trends.
Keywords: HIV, cancer, differences in trends, incidence rate ratio
Among people with HIV in the US, during 2001–2019, Hodgkin lymphoma (HL), lung, liver, and cervical cancer incidence trends were different across racial/ethnic groups. HL, lung, anal, and liver cancer incidence trends were different across risk groups.
People with human immunodeficiency virus (HIV, PWH) have an elevated risk of developing certain cancers, largely due to a combination of HIV-induced immune suppression and higher prevalence of coinfections due to shared mechanisms of transmission, as well as risk behaviors such as smoking [1]. Progression to AIDS represents greater immunosuppression and has been shown to increase the risk of virus-associated cancers in PWH. Since the mid-1990s, the overall cancer risk among PWH in the United States has declined substantially as a result of the improved efficacy, earlier initiation, and wider availability of antiretroviral therapy (ART), reflecting improvements in HIV treatment and subsequent HIV viral suppression [2–4]. There are known disparities in ART use and viral suppression by race and ethnicity and by HIV transmission categories (eg, men who have sex with men [MSM], people who inject drugs [PWID]) [5, 6], which raises the question of whether these disparities may have resulted in unequal progress in cancer incidence reductions over time by race and ethnicity and by transmission categories.
Data on differences in trends will help health professionals, researchers, and policymakers understand the extent to which the improvements in health outcomes in the ART era have extended across populations of PWH and monitor progress toward reducing disparities and inequities among PWH. Hence, we systematically compared cancer trends over time and recent cancer rates across racial/ethnic groups and HIV transmission risk groups.
METHODS
Study Population and Case Definition
We used data from the HIV/AIDS Cancer Match Study (HACM) [7], a record linkage study of population-based HIV and cancer registries in 14 US regions (Colorado, 2001–2015; Connecticut, 2002–2016; Washington, DC, 2007–2015; Florida, 2001–2019; Georgia, 2004–2012; Louisiana, 2001–2015; Maryland, 2008–2018; Massachusetts, 2007–2016; Michigan, 2001–2015; New Jersey, 2001–2012; New York, 2001–2019; North Carolina, 2001–2014; Puerto Rico, 2003–2017; and Texas, 2001–2019).
We restricted our analysis to PWH aged ≥20 years. Person-years of follow-up started at the latter of HIV report date or the beginning of registry coverage and ended at the first of death, end of registry coverage, or age 85 years. Cancer diagnoses were ascertained through linkage with cancer registries and restricted to the most common types of cancer among PWH: non-Hodgkin lymphoma (NHL); Kaposi sarcoma (KS); Hodgkin lymphoma (HL); and lung, anal, liver, colon, prostate, breast, and cervical cancers. Cancer sites were defined by International Classification of Diseases for Oncology, 3rd version, codes. Cancers were restricted to first malignant tumors of each type.
Statistical Analyses
We calculated age-standardized cancer rates by time period, race and ethnicity, and transmission category using the entire HACM population as the standard population. To assess time trends in incidence rates, we divided calendar years into 4 periods (2001–2004, 2005–2009, 2010–2014, and 2015–2019). We used Poisson regression to calculate incidence rate ratios (IRRs) and 95% confidence intervals to compare later periods to the first period (2001–2004) and to estimate the average change per 5-year calendar period using the calendar time variable with a trend (after assessing the linearity assumption). Then, we identified differences in trends across groups by including interaction terms between calendar period (in dummy coding) and either racial/ethnic group or HIV transmission group. We then estimated rate ratios across racial/ethnic or HIV risk groups separately for the first (2001–2004) and the latest time period (2015–2019). All Poisson regression models included terms for attained age (20–24, 25–29, …, 80–84), combined sex and risk group (MSM excluding PWID, PWID, heterosexual, and other), race and ethnicity (non-Hispanic Black, non-Hispanic White, Hispanic, all other racial/ethnic groups combined), and registry. Due to a smaller number of PWH and cancers in the “other racial/ethnic groups” category (approximately 6% of the total number of cancers, including 133 cancers of any type among Asian individuals, 31 among American Indian and Alaska Native individuals, and 11 among Pacific Islander individuals), we were underpowered to estimate trends of cancer rates over time in those groups and thus excluded them in our analyses. We then assessed whether the IRRs across racial/ethnic and risk groups increased or decreased over time, that is, whether the differences across groups have widened or narrowed, and tested for statistically significant changes with an interaction term between race and ethnicity (or risk group) and time period. All tests were 2-sided, and P values <.05 were considered to be statistically significant. Prostate cancer analyses were restricted to male sex. Breast and cervical cancer analyses were restricted to female sex.
RESULTS
This study included 7.4 million person-years of follow-up among 822 543 PWH during 2001–2019. Non-Hispanic Black PWH accounted for 42% of the total person-years, non-Hispanic White PWH accounted for 26%, Hispanic PWH accounted for 26%, and 6% of person-time occurred among PWH in the “other” racial groups (Supplementary Table 1). By HIV transmission group, MSM accounted for the largest fraction of total person-years (40% of total), followed by males (23%) and females (22%) in other risk groups, and male PWID (10%) and female PWID (5%; Supplementary Table 1).
There were 34 661 cancers in our follow-up period, including 8130 NHLs, 4391 KSs, 1892 HLs, 5598 lung cancers, 3458 anal cancers, 2346 liver cancers, 1377 colon cancers, 4559 prostate cancers, 1943 breast cancers, and 967 cervical cancers (Supplementary Table 2). Cancer counts by race and ethnicity are presented in Supplementary Table 2. Cancer counts by transmission category are presented in Supplementary Table 3. Age-standardized cancer rates by time period, race and ethnicity, and transmission categories are presented in Supplementary Tables 4–6.
Overall Cancer Trends
During 2001–2019, the incidence of anal, cervical, and breast cancers remained stable among PWH, whereas the incidence of the remaining 7 cancers declined over time (P trend <.05). Per 5-year period, the largest declines in cancer rates were observed for NHL (23%), lung cancer (23%), KS (22%), followed by liver cancer (16%), HL (14%), colon cancer (9%), and prostate cancer (6%; Tables 1 and 2).
Table 1.
Trends in Incidence Rate Ratios (IRRs), Averaged IRRs, and P Heterogeneity by Race/Ethnicity
| Cancer Type | Overall | Black | White | Hispanic | P Heterogeneity | ||||
|---|---|---|---|---|---|---|---|---|---|
| Period IRR | (95% CI) | Period IRR | (95% CI) | Period IRR | (95% CI) | Period IRR | (95% CI) | ||
| Non-Hodgkin lymphoma | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.84 | (.78–.89) | 0.90 | (.82–1.00) | 0.81 | (.72–.92) | 0.73 | (.65–.83) | |
| Period 3: 2010–2014 | 0.64 | (.60–.69) | 0.72 | (.65–.79) | 0.60 | (.53–.68) | 0.56 | (.49–.64) | |
| Period 4: 2015–2019 | 0.47 | (.43–.50) | 0.52 | (.46–.59) | 0.46 | (.40–.54) | 0.40 | (.34–.45) | |
| Avg. IRR/5-year period | 0.77 | (.76–.79) | 0.81 | (.78–.83) | 0.77 | (.73–.80) | 0.74 | (.71–.77) | .0765 |
| Kaposi sarcoma | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.80 | (.73–.87) | 0.82 | (.71–.94) | 0.82 | (.70–.97) | 0.73 | (.62–.87) | |
| Period 3: 2010–2014 | 0.62 | (.57–.68) | 0.67 | (.58–.78) | 0.62 | (.53–.74) | 0.57 | (.48–.67) | |
| Period 4: 2015–2019 | 0.47 | (.42–.52) | 0.50 | (.42–.59) | 0.47 | (.39–.57) | 0.43 | (.36–.52) | |
| Avg. IRR/5-year period | 0.78 | (.75–.80) | 0.80 | (.76–.84) | 0.78 | (.73–.82) | 0.76 | (.72–.80) | .7935 |
| Hodgkin lymphoma | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.94 | (.82–1.09) | 0.92 | (.73–1.15) | 0.99 | (.74–1.34) | 0.94 | (.73–1.21) | |
| Period 3: 2010–2014 | 0.86 | (.74–.99) | 0.86 | (.69–1.07) | 0.87 | (.65–1.17) | 0.81 | (.63–1.05) | |
| Period 4: 2015–2019 | 0.64 | (.54–.74) | 0.81 | (.64–1.04) | 0.46 | (.32–.66) | 0.57 | (.43–.75) | |
| Avg. IRR/5-year period | 0.86 | (.82–.90) | 0.93 | (.87–1.01) | 0.80 | (.72–.88) | 0.82 | (.76–.89) | .0287 |
| Lung cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.74 | (.68–.81) | 0.74 | (.66–.82) | 0.80 | (.68–.95) | 0.62 | (.49–.78) | |
| Period 3: 2010–2014 | 0.55 | (.50–.60) | 0.52 | (.47–.59) | 0.62 | (.53–.74) | 0.48 | (.39–.60) | |
| Period 4: 2015–2019 | 0.47 | (.43–.51) | 0.44 | (.39–.50) | 0.51 | (.43–.61) | 0.45 | (.36–.56) | |
| Avg. IRR/5-year period | 0.77 | (.75–.80) | 0.75 | (.72–.78) | 0.80 | (.75–.84) | 0.79 | (.74–.85) | .0169 |
| Anal cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.98 | (.87–1.10) | 1.02 | (.83–1.24) | 0.91 | (.76–1.08) | 1.13 | (.85–1.50) | |
| Period 3: 2010–2014 | 0.95 | (.85–1.07) | 0.99 | (.81–1.20) | 0.88 | (.74–1.05) | 1.01 | (.76–1.33) | |
| Period 4: 2015–2019 | 0.96 | (.85–1.09) | 1.16 | (.93–1.43) | 0.83 | (.69–1.00) | 0.98 | (.74–1.30) | |
| Avg. IRR/5-year period | 0.99 | (.95–1.02) | 1.04 | (.98–1.11) | 0.95 | (.89–1.00) | 0.97 | (.89–1.05) | .3378 |
| Liver cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.97 | (.84–1.11) | 1.04 | (.84–1.29) | 0.77 | (.58–1.01) | 0.97 | (.74–1.28) | |
| Period 3: 2010–2014 | 0.80 | (.70–.92) | 0.93 | (.75–1.15) | 0.64 | (.48–.84) | 0.72 | (.55–.95) | |
| Period 4: 2015–2019 | 0.62 | (.53–.72) | 0.73 | (.58–.92) | 0.43 | (.32–.59) | 0.60 | (.46–.79) | |
| Avg. IRR/5-year period | 0.84 | (.80–.88) | 0.89 | (.83–.95) | 0.77 | (.70–.84) | 0.82 | (.76–.89) | .0004 |
| Colon cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 1.03 | (.84–1.26) | 1.06 | (.79–1.42) | 0.92 | (.61–1.40) | 1.03 | (.68–1.57) | |
| Period 3: 2010–2014 | 0.86 | (.71–1.05) | 0.98 | (.73–1.30) | 0.75 | (.50–1.13) | 0.80 | (.53–1.21) | |
| Period 4: 2015–2019 | 0.80 | (.65–.98) | 0.81 | (.60–1.10) | 0.85 | (.56–1.28) | 0.73 | (.48–1.10) | |
| Avg. IRR/5-year period | 0.91 | (.86–.96) | 0.92 | (.84–1.00) | 0.95 | (.84–1.07) | 0.87 | (.78–.98) | .5608 |
| Prostate cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 1.11 | (.98–1.26) | 1.19 | (1.01–1.41) | 1.13 | (.87–1.46) | 1.22 | (.88–1.69) | |
| Period 3: 2010–2014 | 0.95 | (.85–1.07) | 0.99 | (.84–1.16) | 1.06 | (.83–1.36) | 1.03 | (.75–1.40) | |
| Period 4: 2015–2019 | 0.90 | (.80–1.02) | 0.97 | (.82–1.15) | 0.93 | (.72–1.19) | 0.94 | (.69–1.28) | |
| Avg. IRR/5-year period | 0.94 | (.91–.97) | 0.95 | (.91–.99) | 0.94 | (.88–1.01) | 0.93 | (.86–1.00) | .9689 |
| Cervical cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.81 | (.67–.99) | 0.93 | (.72–1.20) | 0.8 | (.42–1.51) | 0.64 | (.44–.93) | |
| Period 3: 2010–2014 | 0.78 | (.64–.95) | 0.88 | (.68–1.14) | 0.77 | (.40–1.47) | 0.52 | (.35–.76) | |
| Period 4: 2015–2019 | 0.84 | (.68–1.04) | 0.97 | (.73–1.27) | 1.06 | (.54–2.07) | 0.56 | (.37–.84) | |
| Avg. IRR/5-year period | 0.95 | (.89–1.02) | 0.99 | (.90–1.08) | 1.02 | (.82–1.28) | 0.83 | (.72–.94) | .0316 |
| Breast cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.85 | (.72–1.01) | 0.90 | (.73–1.12) | 0.60 | (.38–.94) | 1.04 | (.68–1.58) | |
| Period 3: 2010–2014 | 0.99 | (.84–1.16) | 0.98 | (.80–1.21) | 0.97 | (.65–1.47) | 1.11 | (.74–1.66) | |
| Period 4: 2015–2019 | 0.95 | (.80–1.13) | 0.99 | (.80–1.24) | 0.80 | (.51–1.25) | 1.19 | (.79–1.79) | |
| Avg. IRR/5-year period | 1.02 | (.97–1.07) | 1.02 | (.95–1.09) | 1.01 | (.88–1.17) | 1.06 | (.95–1.19) | .9463 |
Poisson regression models adjusted for time periods, attained age, sex and risk group, and registry.
Abbreviations: CI, confidence interval; IRR, incidence rate ratio.
Table 2.
Trends in Incidence Rate Ratios (IRRs), Averaged IRRs, and P Heterogeneity by Risk Group
| Cancer Type | Overall | Men Who Have Sex With Men | People Who Inject Drugs | Other | P Heterogeneity | ||||
|---|---|---|---|---|---|---|---|---|---|
| Period IRR | (95% CI) | Period IRR | (95% CI) | Period IRR | (95% CI) | Period IRR | (95% CI) | ||
| Non-Hodgkin lymphoma | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.84 | (.78–.89) | 0.80 | (.71–.89) | 0.77 | (.66–.90) | 0.91 | (.83–1.00) | |
| Period 3: 2010–2014 | 0.64 | (.60–.69) | 0.59 | (.53–.66) | 0.68 | (.58–.80) | 0.70 | (.64–.77) | |
| Period 4: 2015–2019 | 0.47 | (.43–.50) | 0.42 | (.37–.47) | 0.47 | (.38–.58) | 0.53 | (.48–.60) | |
| Avg. IRR/5-year period | 0.77 | (.76–.79) | 0.75 | (.72–.77) | 0.80 | (.75–.85) | 0.80 | (.78–.83) | .1037 |
| Kaposi sarcoma | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.80 | (.73–.87) | 0.78 | (.70–.87) | 0.8 | (.60–1.06) | 0.85 | (.72–1.01) | |
| Period 3: 2010–2014 | 0.62 | (.57–.68) | 0.62 | (.55–.69) | 0.60 | (.43–.83) | 0.65 | (.54–.77) | |
| Period 4: 2015–2019 | 0.47 | (.42–.52) | 0.45 | (.40–.51) | 0.45 | (.30–.69) | 0.55 | (.45–.67) | |
| Avg. IRR/5-year period | 0.78 | (.75–.80) | 0.77 | (.74–.80) | 0.77 | (.68–.87) | 0.81 | (.76–.86) | .2457 |
| Hodgkin lymphoma | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.94 | (.82–1.09) | 0.94 | (.76–1.16) | 1.18 | (.81–1.73) | 0.87 | (.69–1.10) | |
| Period 3: 2010–2014 | 0.86 | (.74–.99) | 0.77 | (.62–.95) | 1.35 | (.91–1.99) | 0.87 | (.69–1.09) | |
| Period 4: 2015–2019 | 0.64 | (.54–.74) | 0.52 | (.42–.66) | 1.12 | (.70–1.78) | 0.71 | (.55–.90) | |
| Avg. IRR/5-year period | 0.86 | (.82–.90) | 0.80 | (.75–.86) | 1.06 | (.92–1.22) | 0.90 | (.84–.97) | .0009 |
| Lung cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.74 | (.68–.81) | 0.83 | (.69–1.00) | 0.69 | (.59–.80) | 0.76 | (.67–.86) | |
| Period 3: 2010–2014 | 0.55 | (.50–.60) | 0.61 | (.50–.73) | 0.58 | (.50–.67) | 0.52 | (.46–.59) | |
| Period 4: 2015–2019 | 0.47 | (.43–.51) | 0.51 | (.42–.62) | 0.48 | (.41–.57) | 0.46 | (.40–.52) | |
| Avg. IRR/5-year period | 0.77 | (.75–.80) | 0.79 | (.75–.84) | 0.79 | (.75–.84) | 0.76 | (.73–.79) | .1018 |
| Anal cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.98 | (.87–1.10) | 0.89 | (.77–1.04) | 1.33 | (.95–1.85) | 1.04 | (.83–1.32) | |
| Period 3: 2010–2014 | 0.95 | (.85–1.07) | 0.84 | (.73–.97) | 1.30 | (.92–1.83) | 1.07 | (.85–1.34) | |
| Period 4: 2015–2019 | 0.96 | (.85–1.09) | 0.81 | (.69–.94) | 1.44 | (.99–2.11) | 1.23 | (.97–1.55) | |
| Avg. IRR/5-year period | 0.99 | (.95–1.02) | 0.94 | (.89–.98) | 1.10 | (.98–1.23) | 1.07 | (1.00–1.15) | .0056 |
| Liver cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.97 | (.84–1.11) | 0.79 | (.58–1.06) | 0.97 | (.79–1.18) | 1.05 | (.81–1.37) | |
| Period 3: 2010–2014 | 0.80 | (.70–.92) | 0.65 | (.49–.86) | 0.78 | (.63–.96) | 0.89 | (.69–1.15) | |
| Period 4: 2015–2019 | 0.62 | (.53–.72) | 0.49 | (.36–.66) | 0.64 | (.51–.80) | 0.65 | (.50–.85) | |
| Avg. IRR/5-year period | 0.84 | (.80–.88) | 0.79 | (.72–.87) | 0.85 | (.79–.91) | 0.84 | (.78–.91) | .0061 |
| Colon cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 1.03 | (.84–1.26) | 0.94 | (.64–1.37) | 1.25 | (.78–2.00) | 1.00 | (.76–1.33) | |
| Period 3: 2010–2014 | 0.86 | (.71–1.05) | 0.83 | (.58–1.19) | 1.09 | (.68–1.76) | 0.80 | (.61–1.06) | |
| Period 4: 2015–2019 | 0.80 | (.65–.98) | 0.83 | (.58–1.20) | 0.87 | (.52–1.47) | 0.74 | (.56–.98) | |
| Avg. IRR/5-year period | 0.91 | (.86–.96) | 0.94 | (.85–1.04) | 0.92 | (.79–1.07) | 0.88 | (.81–.96) | .4323 |
| Prostate cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 1.11 | (.98–1.26) | 1.17 | (.96–1.41) | 1.23 | (.92–1.65) | 1.01 | (.84–1.23) | |
| Period 3: 2010–2014 | 0.95 | (.85–1.07) | 0.91 | (.76–1.09) | 1.19 | (.90–1.59) | 0.93 | (.78–1.12) | |
| Period 4: 2015–2019 | 0.90 | (.80–1.02) | 0.91 | (.76–1.10) | 1.05 | (.77–1.42) | 0.85 | (.70–1.02) | |
| Avg. IRR/5-year period | 0.94 | (.91–.97) | 0.93 | (.88–.97) | 0.98 | (.90–1.07) | 0.93 | (.88–.98) | .6912 |
| Cervical cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.81 | (.67–.99) | 0.78 | (.55–1.11) | 0.82 | (.65–1.04) | |||
| Period 3: 2010–2014 | 0.78 | (.64–.95) | 0.66 | (.45–.97) | 0.81 | (.64–1.02) | |||
| Period 4: 2015–2019 | 0.84 | (.68–1.04) | 0.85 | (.55–1.31) | 0.83 | (.65–1.06) | |||
| Avg. IRR/5-year period | 0.95 | (.89–1.02) | 0.92 | (.80–1.06) | 0.95 | (.88–1.03) | .7754 | ||
| Breast cancer | |||||||||
| Period 1: 2001–2004 | Ref | Ref | Ref | Ref | |||||
| Period 2: 2005–2009 | 0.85 | (.72–1.01) | 0.86 | (.60–1.22) | 0.85 | (.70–1.03) | |||
| Period 3: 2010–2014 | 0.99 | (.84–1.16) | 0.91 | (.65–1.29) | 1.00 | (.84–1.21) | |||
| Period 4: 2015–2019 | 0.95 | (.80–1.13) | 1.02 | (.70–1.47) | 0.94 | (.78–1.14) | |||
| Avg. IRR/5-year period | 1.02 | (.97–1.07) | 1.03 | (.91–1.15) | 1.01 | (.96–1.07) | .4151 | ||
Poisson regression models adjusted for time periods, attained age, sex, race and ethnicity group, and registry.
Abbreviations: CI, confidence interval; IRR, incidence rate ratio.
Differences in Cancer Trends Across Racial/Ethnic Groups
There were significant differences in cancer trends across racial/ethnic groups for HL and lung, liver, and cervical cancers during 2001–2019. Among Black, White, and Hispanic PWH, respectively, HL rates declined 7%, 20%, and 18% per 5-year period (P interaction = .03; Table 1, Figure 1); lung cancer rates declined 25%, 20%, and 21% per 5-year period (P interaction = .02); and liver cancer rates declined 11%, 23%, and 18% per 5-year period (P interaction = .0004). Cervical cancer rates declined 17% per 5-year period among Hispanic PWH but did not change among Black and White PWH (P interaction = .03). Even though it did not reach statistical significance (P interaction = .08), NHL rates declined 19%, 23%, and 26% per 5-year period among Black, White, and Hispanic PWH, respectively. Trends for the remaining cancer types did not differ significantly across racial/ethnic groups (Table 1, Figure 1).
Figure 1.
Incidence rate ratios comparing recent time periods (2005–2009, 2010–2014, 2015–2019) to the first time period (2001–2004) for 4 cancers that showed differences in trends between race and ethnicity groups.
Rate Comparisons and Changes in Cancer Rate Ratios Across Racial/Ethnic Groups Over Time
We presented side-by-side comparisons of IRRs between racial/ethnic groups in the first and latest time periods and assessed whether the IRRs differed significantly between 2 time periods: 2001–2004 and 2015–2019 (Table 3). The relative difference in cancer rates among White PWH compared with Black PWH changed significantly between the 2 time periods for HL and lung and liver cancers. Between 2001–2004 and 2015–2019, differences in relative cancer rates between White and Black PWH increased for HL (White vs Black: IRR2001–2004 = 0.67, IRR2015–2019 = 0.47, P interaction = .023) and liver cancer (IRR2001–2004 = 1.23, IRR2015–2019 = 0.68, P interaction = .001) and changed significantly for lung cancer (IRR2001–2004 = 0.94, IRR2015–2019 = 1.05, P interaction = .036).
Table 3.
Incidence Rate Ratios (IRRs) Between Racial and Ethnic Groups Within Calendar Periods and Statistical Significance for Differences in IRRs Between Periods
| White vs Black (ref) | Hispanic vs Black (ref) | Hispanic vs White (ref) | |||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Cancer Type | 2001–2004 | 2015–2019 | Change | 2001–2004 | 2015–2019 | Change | 2001–2004 | 2015–2019 | Change | ||||||
| IRR | (95% CI) | IRR | (95% CI) | P Value | IRR | (95% CI) | IRR | (95% CI) | P Value | IRR | (95% CI) | IRR | (95% CI) | P Value | |
| Non-Hodgkin lymphoma | 1.03 | (.90–1.18) | 1.02 | (.89–1.17) | .605 | 1.28 | (1.12–1.46) | 1.10 | (.97–1.25) | .027 | 1.24 | (1.07–1.43) | 1.08 | (.94–1.24) | .257 |
| Kaposi sarcoma | 0.74 | (.62–.88) | 0.87 | (.72–1.04) | .655 | 1.08 | (.90–1.29) | 1.11 | (.94–1.31) | .725 | 1.46 | (1.21–1.77) | 1.28 | (1.06–1.54) | .602 |
| Hodgkin lymphoma | 0.67 | (.48–.92) | 0.47 | (.35–.63) | .023 | 1.31 | (.98–1.76) | 1.02 | (.81–1.29) | .097 | 1.97 | (1.41–2.76) | 2.18 | (1.60–2.97) | .446 |
| Lung cancer | 0.94 | (.79–1.13) | 1.05 | (.91–1.20) | .036 | 0.58 | (.47–.71) | 0.72 | (.62–.83) | .137 | 0.61 | (.48–.77) | 0.69 | (.59–.80) | .885 |
| Anal cancer | 1.30 | (1.02–1.65) | 1.17 | (1.00–1.38) | .184 | 0.82 | (.60–1.12) | 0.83 | (.70–.99) | .629 | 0.63 | (.46–.85) | 0.71 | (.60–.84) | .416 |
| Liver cancer | 1.23 | (.90–1.67) | 0.68 | (.53–.87) | .001 | 1.07 | (.79–1.45) | 1.12 | (.92–1.36) | .54 | 0.88 | (.62–1.23) | 1.64 | (1.28–2.11) | .005 |
| Colon cancer | 0.91 | (.57–1.44) | 0.90 | (.69–1.15) | .693 | 1.09 | (.69–1.71) | 0.96 | (.75–1.23) | .779 | 1.20 | (.71–2.02) | 1.07 | (.82–1.40) | .775 |
| Prostate cancer | 0.46 | (.34–.62) | 0.43 | (.38–.49) | .927 | 0.49 | (.35–.69) | 0.44 | (.39–.51) | .921 | 1.07 | (.73–1.57) | 1.03 | (.88–1.20) | .976 |
| Cervical cancer | 0.70 | (.42–1.18) | 0.68 | (.43–1.06) | .97 | 1.10 | (.74–1.63) | 0.80 | (.56–1.13) | .021 | 1.57 | (.87–2.82) | 1.18 | (.70–1.97) | .133 |
| Breast cancer | 1.07 | (.72–1.58) | 0.86 | (.67–1.12) | .485 | 0.69 | (.45–1.04) | 0.79 | (.64–.97) | .559 | 0.64 | (.38–1.08) | 0.91 | (.68–1.23) | .365 |
Poisson regression models were also adjusted for sex and risk group, registry, and an interaction between race and ethnicity with calendar period.
95% confidence interval in paratheses.
Abbreviations: CI, confidence interval; IRR, incidence rate ratio.
The relative difference in cancer rates between Hispanic and Black PWH narrowed across time periods for NHL (Hispanic vs Black: IRR2001–2004 = 1.28, IRR2015–2019 = 1.10, P interaction = .027) and changed significantly for cervical cancer (IRR2001–2004 = 1.10, IRR2015–2019 = 0.80, P interaction = .021).
The relative difference in cancer rates comparing Hispanic to White PWH increased significantly between the 2 time periods for liver cancer (Hispanic vs White: IRR2001–2004 = 0.88, IRR2015–2019 = 1.64, P interaction = .005).
There were also differences in cancer rates by race and ethnicity for some of the remaining cancer types in the 2 time periods where P interaction was not significant. Notably, anal cancer rates were highest among White PWH (White vs Black: IRR2015–2019 = 1.17; Hispanic vs White: IRR2015–2019 = 0.71); prostate (White vs Black: IRR2015–2019 = 0.43; Hispanic vs Black: IRR2015–2019 = 0.44) and breast cancer (White vs Black: IRR2015–2019 = 0.86; Hispanic vs Black: IRR2015–2019 = 0.79) rates were highest among Black PWH, and HL rates were lowest among White PWH (White vs Black: IRR2015–2019 = 0.47; Hispanic vs White: IRR2015–2019 = 2.18).
Differences in Cancer Trends Across Risk Groups
There were significant differences in incidence trends across risk groups for HL and anal and liver cancers during 2001–2019. HL rates declined 20% per 5-year period in MSM, 10% in other risk groups, and remained unchanged among PWID (P interaction = .0009; Table 3, Figure 2). Anal cancer rates declined among MSM (6% per 5-year period), were stable among PWID, and increased among other risk groups (7% per 5-year period; P interaction = .0056). Liver cancer rates declined 21% among MSM, 15% among PWID, and 16% among other risk groups per 5-year period (P interaction = .0061; Table 3, Figure 2).
Figure 2.
Incidence rate ratios comparing recent time periods (2005–2009, 2010–2014, 2015–2019) to the first time period (2001–2004) for 3 cancers that showed differences in trends between 3 risk groups. Abbreviations: MSM, men who have sex with men; PWID, people who inject drugs.
Rate Comparisons and Changes in Cancer Rate Ratios Across Risk Groups Over Time
Rate ratios between risk groups in 2001–2004 and 2015–2019 are presented in Table 4. When MSM were compared to PWID, the relative difference in cancer rates decreased between 2001–2004 and 2015–2019 for HL (MSM vs PWID: IRR2001–2004 = 2.08, IRR2015–2019 = 1.14, P interaction = .025), lung cancer (IRR2001–2004 = 0.44, IRR2015–2019 = 0.51, P interaction = .030), and anal cancer (MSM vs PWID: IRR2001–2004 = 3.23, IRR2015–2019 = 2.04, P interaction = .010). Meanwhile, the relative difference in liver cancer rates increased (MSM vs PWID: IRR2001–2004 = 0.34, IRR2015–2019 = 0.22, P interaction = .007). There was no change in cancer rate gaps between other risk groups vs PWID from 2001–2004 to 2015–2019 for any cancer.
Table 4.
Incidence Rate Ratios (IRRs) Between Risk Groups Within Calendar Periods and Statistical Significance for Differences in IRRs Between Periods
| MSM vs PWID | Other vs PWID | Other vs MSM | |||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Cancer Type | 2001–2004 | 2015–2019 | Change | 2001–2004 | 2015–2019 | Change | 2001–2004 | 2015–2019 | Change | ||||||
| IRR | (95% CI) | IRR | (95% CI) | P Value | IRR | (95% CI) | IRR | (95% CI) | P Value | IRR | (95% CI) | IRR | (95% CI) | P Value | |
| Non-Hodgkin lymphoma | 1.10 | (.94–1.28) | 0.93 | (.77–1.11) | .961 | 1.15 | (1.01–1.32) | 1.20 | (1.00–1.43) | .242 | 1.05 | (.92–1.19) | 1.29 | (1.14–1.47) | .043 |
| Kaposi sarcoma | 2.70 | (2.13–3.33) | 2.22 | (1.56–3.23) | .745 | 1.19 | (.93–1.52) | 1.38 | (.95–2.01) | .353 | 0.44 | (.37–.53) | 0.62 | (.52–.74) | .084 |
| Hodgkin lymphoma | 2.08 | (1.45–3.03) | 1.14 | (.78–1.64) | .025 | 1.55 | (1.09–2.22) | 1.22 | (.85–1.74) | .423 | 0.74 | (.55–.99) | 1.08 | (.85–1.37) | .016 |
| Lung cancer | 0.44 | (.36–.55) | 0.51 | (.44–.6) | .030 | 0.69 | (.59–.80) | 0.67 | (.59–.77) | .931 | 1.55 | (1.26–1.92) | 1.32 | (1.14–1.52) | .054 |
| Anal cancer | 3.23 | (2.33–4.55) | 2.04 | (1.59–2.56) | .010 | 1.24 | (.88–1.74) | 0.99 | (.77–1.26) | .474 | 0.38 | (.29–.50) | 0.49 | (.41–.58) | .027 |
| Liver cancer | 0.34 | (.25–.47) | 0.22 | (.18–.28) | .007 | 0.40 | (.30–.54) | 0.34 | (.28–.41) | .999 | 1.18 | (.83–1.69) | 1.54 | (1.22–1.95) | .015 |
| Colon cancer | 1.37 | (.79–2.38) | 1.28 | (.91–1.79) | .760 | 1.54 | (.96–2.49) | 1.29 | (.95–1.75) | .691 | 1.12 | (.70–1.78) | 1.01 | (.79–1.29) | .545 |
| Prostate cancer (male only) | 1.82 | (1.32–2.50) | 1.72 | (1.47–2.04) | .768 | 1.46 | (1.07–1.98) | 1.30 | (1.10–1.53) | .224 | 0.80 | (.62–1.04) | 0.75 | (.67–.85) | .425 |
| Cervical cancer (female only) | 0.80 | (.57–1.10) | 0.71 | (.51–.99) | .875 | ||||||||||
| Breast cancer (female only) | 1.31 | (.95–1.81) | 1.06 | (.86–1.32) | .270 | ||||||||||
Poisson regression models were also adjusted for race and ethnicity group, registry, and an interaction between risk group with calendar period.
95% confidence interval in paratheses.
Abbreviations: CI, confidence interval; IRR, incidence rate ratio; MSM, men who have sex with men; PWID, people who inject drugs.
When cancer rates were compared between other risk groups and MSM PWH, relative difference increased for NHL (other risk groups vs MSM: IRR2001–2004 = 1.05, IRR2015–2019 = 1.29, P interaction = .043) and liver cancer (IRR2001–2004 = 1.18, IRR2015–2019 = 1.54, P interaction = .015). In contrast, the relative difference in rates of HL (other risk groups vs MSM: IRR2001–2004 = 0.74, IRR2015–2019 = 1.08, P interaction = .016) and anal cancer (IRR2001–2004 = 0.38, IRR2015–2019 = 0.49, P interaction = .027) decreased over time. Among those cancers with no significant difference in trends in rates, KS and prostate cancer rates were highest among MSM.
DISCUSSION
During 2001–2019, cancer rates among PWH declined for all cancer types except anal, cervical, and female breast cancers. However, cancer incidence trends were not uniform across racial/ethnic groups for HL and lung, liver, and cervical cancers and not uniform across transmission risk groups for HL and anal and liver cancers. In addition, comparing 2015–2019 to 2001–2004 for race and ethnicity subgroups, relative differences in cancer rates increased for HL and liver cancer and decreased for NHL. Relative differences in cancer rates for HIV transmission subgroups increased for NHL and liver cancer and decreased for HL and lung and anal cancers.
There were substantial declines in NHL incidence over time overall, averaging 23% per 5-year period, and large declines were observed across racial/ethnic (19%–26%) and risk groups (20%–25%). NHL rates were highest among Hispanic PWH in 2001–2004, but the difference in NHL rates between Hispanic and Black PWH narrowed from 2001–2004 to 2015–2019. NHL rates declined more rapidly among MSM than other risk groups, resulting in larger differences across risk groups in the most recent time period. Timely initiation of ART was associated with lowering the risk of systemic NHL, given the association between HIV-related immunosuppression and NHL risk [8]. Though the declines in NHL rates among Black PWH, as well as among PWID, and in other risk groups were slightly attenuated compared with other groups, each group experienced substantial declines in incidence rates. These findings, along with declines in KS, a cancer strongly associated with immunosuppression, show the benefits of ART across racial/ethnic and HIV transmission risk groups.
HL rates declined over time, averaging 14% per 5-year period, with significant differences in trends across racial/ethnic groups and risk groups. HL rates declined rapidly among White and Hispanic PWH but remained stable among Black PWH. HL rates declined rapidly among MSM and other risk groups but remained stable among PWID. HL rates were lowest among White PWH in 2001–2004. The relative differences in HL rates between White and Black PWH widened from 2001–2004 to 2015–2019. HL rates were highest among MSM PWH, but differences between MSM and other risk groups declined over time.
Lung cancer rates declined substantially over time, averaging 23% per 5-year period. There were differences in trends across racial/ethnic groups but no differences in trends across risk groups. Lung cancer rates were lowest among Hispanic PWH. The relative difference in lung cancer rates between White and Black PWH changed from 2001–2004 to 2015–2019. Lung cancer rates were highest among PWID; however, the relative difference in rates between risk groups decreased over time. The notably higher lung cancer rates among PWID are likely because of a higher prevalence of smoking in this group [9–11]. These downward trends might be due to, in addition to ART and improved immune functions, a reduction in smoking, but we did not have individual smoking information.
Anal cancer rates overall were stable across racial/ethnic groups. Anal cancer rates were highest among White PWH and among MSM PWH. Anal cancer trends were different across risk groups. They declined among MSM (6% per 5-year period), resulting in narrowing differences between MSM and other risk groups. The reasons why anal cancer declined only among White and only among MSM merits further investigation. For example, this might reflect differences in the timing of HIV treatment, including timely initiation at high nadir CD4 counts, which would reduce persistence of high-risk anal human papillomavirus (HPV) and subsequent anal cancer risk, as those with a prior AIDS diagnosis are more likely to develop invasive anal cancer [12]. It might also reflect disparities in access to and use of anoscopy or screening tests [13, 14]. There is a lack of consensus recommendations for anal cancer screening [15, 16]. Recently, however, the International Anal Neoplasia Society developed guidelines on anal cancer screening use among various high-risk groups, which will provide a foundation to inform risk-targeted anal cancer screening [17].
Liver cancer rates declined substantially over time, averaging 16% per 5-year period. Trends differed across racial/ethnic groups and risk groups. The difference in liver cancer rates across racial/ethnic and risk groups widened due to steeper declines among White PWH and among MSM. Hepatitis B virus (HBV) and hepatitis C virus (HCV) are highly associated with liver cancer [18–20], and 60%–75% of PWH with liver cancer also have coinfection with HCV [21, 22]. Even though curative HCV management and treatment, which was introduced in 2014, are highly efficacious for patients with HIV/HCV coinfection [23], barriers to treatment access and differential prescribing by race exist [24–26], which may contribute to the differences in liver cancer trends observed. In addition, the faster declines in liver cancer rates among MSM might be explained by better HBV vaccination coverage and control in that group.
Possible causes for differences in cancer trends and incidence rates include differential medical care and HIV treatments [27, 28] and differential access to and uptake of public health measures, such as vaccination, screening, smoking cessation, and harm reduction, by race and ethnicity and by risk group [29–33]. For example, by racial/ethnic group, Black and Hispanic PWH are less likely than White PWH to have their HIV diagnosed, to have access to high-quality care, and to be virally suppressed, which may have resulted in higher KS rates, as shown in our study [28]. By risk group, PWID are most likely to have their HIV infection diagnosed, while MSM are slightly more likely than others to have viral suppression through HIV treatment [28]. However, we were limited by the available data from the registry-based linkage study to investigate the specific role of combination ART, immunosuppression, viral suppression, and other risk factors on disparities in cancer rates. We also do not have information on access to care, insurance coverage, healthcare engagement patterns, and common comorbidities and causal agents for some of the cancer types discussed (eg, HPV, HBV, HCV, smoking status). Another limitation is that we were unable to conduct more granular analyses for racial/ethnic subgroups such as American Indians/Alaska natives, Asians, and Native Hawaiians/Other Pacific Islanders because of lower number of PWH and cancers in those subgroups.
Using a large linkage study of HIV and cancer surveillance systems, we found declines in incidence rates of 7 cancers, as well as differences in trends by racial/ethnic groups for HL and lung, liver, and cervical cancers and by risk groups for HL and lung, anal, and liver cancers. We observed growing disparities in incidence by race and ethnicity for HL and lung, liver, and cervical cancers. We also observed increased disparities in liver cancer rates by risk group and decreasing disparities in HL and lung cancer, and anal cancer rates. This study illustrates how racial differences in access, prescribing, and success of highly effective combination ART have important downstream consequences on cancer incidence. Future work should examine causes for the differences in trends, especially as they relate to disparate trends of anal and liver cancer across racial/ethnic groups and risk groups.
Supplementary Material
Contributor Information
Qianlai Luo, National Cancer Institute, Bethesda, Maryland, USA.
Marie-Josèphe Horner, National Cancer Institute, Bethesda, Maryland, USA.
Cameron B Haas, National Cancer Institute, Bethesda, Maryland, USA.
Jennifer K McGee-Avila, National Cancer Institute, Bethesda, Maryland, USA.
Ruth M Pfeiffer, National Cancer Institute, Bethesda, Maryland, USA.
Eric A Engels, National Cancer Institute, Bethesda, Maryland, USA.
Karen Pawlish, New Jersey State Department of Health, Trenton, New Jersey, USA.
Analise Monterosso, Texas Department of State Health Services, Austin, Texas, USA.
David J Riedel, University of Maryland, Baltimore, Maryland, USA.
Xiao-Cheng Wu, Louisiana State University Health Sciences Center New Orleans, New Orleans, Louisiana, USA.
Lou Gonsalves, State of Connecticut Department of Public Health, Hartford, Connecticut, USA.
Suzanne Speers, State of Connecticut Department of Public Health, Hartford, Connecticut, USA.
Colby Cohen, Florida Department of Health, Tallahassee, Florida, USA.
Meredith S Shiels, National Cancer Institute, Bethesda, Maryland, USA.
Supplementary Data
Supplementary materials are available at Clinical Infectious Diseases online. Consisting of data provided by the authors to benefit the reader, the posted materials are not copyedited and are the sole responsibility of the authors, so questions or comments should be addressed to the corresponding author.
Notes
Acknowledgments. The authors gratefully acknowledge the support and assistance provided by individuals at the following state human immunodeficiency virus (HIV)/AIDS and cancer registries: Colorado, Connecticut, District of Columbia, Florida, Georgia, Louisiana, Maryland, Massachusetts, Michigan, New Jersey, New York, North Carolina, Puerto Rico, and Texas. We also thank Timothy McNeel at Information Management Services for programming support.
The following cancer registries were supported by the cooperative agreement funded by the Centers for Disease Control and Prevention (CDC), National Program of Cancer Registries: Colorado (NU58DP006347–01), Georgia (5U58DP003875-01), Florida (NU58DP007161), Louisiana (NU58DP006332-03-00), Maryland (NU58DP006333NU58DP007114), Massachusetts (NU58DP006271-04-00), Michigan (17NU58DP006334), New Jersey (NU58/DP003931-05-00), New York (6NU58/DP006309), North Carolina (1NU58DP006281), and Texas (1NU58DP0063085NU58DP006308-04-00). The District of Columbia is supported by CDC cooperative agreement DP006302.
The following cancer registries were supported by the Surveillance, Epidemiology, and End Results Program Program of the National Cancer Institute: Connecticut (HHSN261201300019I), Louisiana (HHSN261201800007I/ HHSN26100002), Massachusetts (HHSN261201800008l), New Jersey (HHSN261201300021I, N01-PC-2013-00021), and New York (HHSN261201800009I). The New Jersey State Cancer Registry was also supported by the state of New Jersey, the Maryland Cancer Registry was supported by the state of Maryland and the Maryland Cigarette Restitution Fund, the Louisiana Tumor Registry was also supported by the state of Louisiana (0587200015), and the New York State Cancer Registry was also supported by the state of New York.
The following HIV registries were supported by the HIV Incidence and Case Surveillance Branch of the CDC, National HIV Surveillance Systems: Colorado (NU62PS003960), Connecticut (5U62PS001005-05), Florida (NU62PS924532), Louisiana (NU62PS924522-02-00), Michigan (U62PS004011-02), New Jersey (U62PS004001-2), New York (NU62PS924546-02-00; PS18-1802: Integrated HIV Surveillance and Prevention Programs for Health Departments, National Center for HIV, Viral Hepatitis, STD, and TB Prevention).
Disclaimer. The views expressed here are those of the authors and should not be interpreted to reflect the views or official policies of the National Cancer Institute, CDC, Department of Health and Human Services, and HIV/AIDS or cancer registries, or their contractors, nor does the mention of trade names, commercial practices, or organizations imply endorsement by the US government.
Financial support. This work was funded by the Intramural Research Program of the National Cancer Institute. The research was supported, in part, by the Intramural Research Program of the National Cancer Institute.
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