https://orcid.org/0000-0003-0611-305X
Abstract
We estimated the population-level incidence of human papillomavirus (HPV)–positive oropharyngeal, cervical, and anal cancers by smoking status. We combined HPV DNA genotyping data from the Centers for Disease Control and Prevention’s Cancer Registry Sentinel Surveillance System with data from the Kentucky Cancer Registry and Behavioral Risk Factor Surveillance System across smoking status. During 2004-2005 and 2014-2015 in Kentucky, most cases of oropharyngeal (63.3%), anal (59.7%), and cervical (54.9%) cancer were among individuals who ever smoked. The population-level incidence rate was higher among individuals who ever smoked than among those who never smoked for HPV-positive oropharyngeal (7.8 vs 2.1; adjusted incidence rate ratio = 2.6), cervical (13.7 vs 6.8; adjusted incidence rate ratio = 2.0), and anal (3.9 vs 1.6; adjusted incidence rate ratio = 2.5) cancers. These findings indicate that smoking is associated with increased risk of HPV-positive oropharyngeal, cervical, and anal cancers, and the population-level burden of these cancers is higher among individuals who ever smoked.
Persistent infection with human papillomavirus (HPV) is an established cause of oropharyngeal, cervical, and anal cancers (1). Several case-control and cohort studies have shown that smoking is a recognized cofactor to HPV infection for the risk of cervical cancer (2-4) and could be an important cofactor to HPV infection for oropharyngeal (5) and anal (6) cancers. The population-level burden of HPV-positive cancers by smoking status, however, is less characterized. While case-control and cohort epidemiologic study designs are optimal for quantifying the association of smoking with these cancers, they are not amenable for directly estimating population-level cancer incidence rates (7). By contrast, although central cancer registries provide direct estimates of population-level cancer incidence rates, critical information about HPV infection and smoking status is not consistently available, thus precluding the estimation of the incidence of HPV-positive cancers by smoking status. Quantifying the population-level burden of HPV-positive oropharyngeal, cervical, and anal cancers by smoking status could have implications for prevention, prognosis, and cancer treatment (8,9). For example, individuals with HPV-positive oropharyngeal cancers who smoke have an increased risk of progression and poorer prognosis relative to those who do not smoke (10,11).
In this study, we used a novel approach combining molecular epidemiologic investigations of tumor tissues from the Centers for Disease Control and Prevention (CDC) Cancer Registry Sentinel Surveillance System with health surveys (Kentucky Behavioral Risk Factor Surveillance System [BRFSS]) and central cancer registry data to estimate the population-level incidence of HPV-positive oropharyngeal, cervical, and anal cancers among individuals who ever and never smoked in Kentucky.
The data sources, linkages, and methods used in this study are presented in Supplementary Figure 1 (available online). Briefly, as part of the CDC Cancer Registry Sentinel Surveillance System, oropharyngeal, cervical, and anal cancers diagnosed during 2 calendar periods (2004-2005 and 2014-2015) in Kentucky were randomly sampled and tested for the presence of HPV DNA types. Formalin-fixed, paraffin-embedded tumor tissues were retrieved by the Kentucky Cancer Registry (KCR) and tested for HPV using the Linear Array HPV genotyping test (Roche Diagnostics, Indianapolis, IN), and samples with negative or inadequate results were retested using the INNO-LiPA HPV genotyping assay (Innogenetics, Ghent, Belgium) (12,13). We used these data to determine the unweighted prevalence of any HPV DNA in oropharyngeal, cervical, and anal cancers. Cancer sites were defined according to the International Classification of Diseases for Oncology, 3rd Edition (14) site and histology codes C01.9, C02.4, C02.8, C05.1-05.2, C09.0-09.1, C09.8-09.9, C10.0-10.4, C10.8-10.9, C14.0, C14.2, C14.8 (oropharynx), C53.0-53.9 (cervix), and C21.0-21.8, 20.9 (anus), excluding histology codes 8720-8790 (melanoma), 8800-8991 (sarcoma), 9050-9055 (mesothelioma), 9140 (Kaposi sarcoma), and 9590-9992 (lymphoma, myeloma, and leukemia).
Our statistical analyses propensity weighted the HPV tested cases to all KCR cancer cases to allow population-representative inferences. Further, we combined the propensity-weighted KCR cases (numerators) with the BRFSS weighted populations (denominators) to estimate the incidence rates of HPV-positive cancers across demographic characteristics and smoking status. Specifically, data were examined by age, sex, race and ethnicity, stage (classified as localized, regional, distant, and unstaged using the derived SEER Summary Stage 2000 variable), and smoking status. We obtained individual-level demographic, clinical, and smoking status (ever vs never) data on all cancer cases from KCR, which is 1 of the few cancer registries in the United States that collects data on ever and never smoking status. Ever smoking status includes individuals who currently smoke, individuals who smoked in the past, and smokers whose current smoking status is unknown. As HPV genotyping was conducted only on a subset of cases, we estimated the probability of selection from all cancer cases into the HPV testing subset using a logistic regression model with smoking status, age, sex, race and ethnicity, and stage as predictors. Separate models were used for oropharyngeal, cervical, and anal cancers. The inverse of the estimated probability from these logistic models were used as propensity weights for each case, such that the weighted analyses represented all cancer cases in the KCR. The propensity-weighted analyses using cancer cases were used to determine the prevalence of HPV in oropharyngeal, cervical, and anal cancers during 2004-2005 and 2014-2015. These cancer cases across age, sex, race and ethnicity, and smoking status strata also served as the numerators for the estimation of incidence rates for all cancers in the KCR over the 4-year period spanning 2004-2005 and 2014-2015.
We derived Kentucky population denominators across age, sex, race and ethnicity, and smoking status strata for the same 4-year period from the Kentucky BRFSS, a health survey on behavioral risk factors (15). Our analyses accounted for the complex survey design of the BRFSS and used the recommended weights to derive population numbers overall and across strata. We combined the KCR cases with BRFSS data to estimate the crude incidence rates for HPV-positive and HPV-negative oropharyngeal, cervical, and anal cancers (16). Annual incidence rates are presented per 100 000 persons. We estimated adjusted incidence rate ratios to evaluate the association of smoking with the risk of HPV-positive and HPV-negative cancers. Adjusted incidence rate ratios and 95% confidence intervals (CI) were estimated through predictive margins in logistic regression models (17). All analyses were conducted in SAS, version 9.4 (SAS Institute Inc, Cary, NC) and SUDAAN, version 11.0.3 (RTI International, Research Triangle Park, NC).
During 2004-2005 and 2014-2015, there were 1169 oropharyngeal cancers, 860 cervical cancers, and 473 anal cancers in Kentucky (Supplementary Table 1, available online). During the same time periods, an estimated 49.8% of adults (53.6% of male and 46.4% of female individuals) in Kentucky reported ever smoking. The weighted prevalence of any HPV DNA was 70.0% in oropharyngeal, 89.2% in cervical, and 89.9% in anal cancers (Table 1). The burden of HPV-positive cancers was higher among individuals who had ever smoked than among those who had never smoked for oropharyngeal (63.3% vs 16.9%), cervical (54.9% vs 32.1%), and anal (59.7% vs 23.2%) cancers.
Human papillomavirus DNA prevalence among invasive oropharyngeal, cervical, and anal cancers,a Kentucky, 2004-2005 and 2014-2015
| Human papillomavirus prevalence | |||||||||
|---|---|---|---|---|---|---|---|---|---|
| Oropharyngeal cancer | Cervical cancer | Anal cancer | |||||||
| Unweighted | Weighted | Unweighted | Weighted | Unweighted | Weighted | ||||
| No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | |
| Total | 132 (67.7) | 806 | 70.0 (62.8 to 77.2) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 68 (89.5) | 427 | 89.9 (82.9 to 96.9) |
| Age, y | |||||||||
| <50 | 50 (80.7) | 189 | 78.5 (64.7 to 92.4) | 137 (97.9) | 481 | 97.6 (94.9 to 100.0) | 29 (96.7) | 131 | 94.5 (83.4 to 100.0) |
| ≥50 | 82 (61.7) | 617 | 67.7 (59.3 to 76.1) | 92 (82.1) | 282 | 77.7 (65.8 to 89.5) | 39 (84.8) | 296 | 88.0 (79.0 to 97.1) |
| Sex | |||||||||
| Male | 109 (71.2) | 670 | 74.3 (66.7 to 81.9) | — | — | — | 26 (86.7) | 137 | 84.9 (70.4 to 99.5) |
| Female | 23 (54.8) | 136 | 54.4 (36.3 to 72.5) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 42 (91.3) | 291 | 92.5 (84.8 to 100.0) |
| Race and ethnicity | |||||||||
| Whiteb | 119 (73.0) | 774 | 72.2 (64.6 to 79.7) | 193 (91.0) | 693 | 89.0 (82.7 to 95.3) | 60 (89.6) | 407 | 90.1 (82.9 to 97.4) |
| Otherc | 13 (40.6) | 32 | 40.4 (21.9 to 59.0) | 36 (90.0) | 70 | 91.0 (82.0 to 99.9) | 8 (88.9) | 21 | 85.7 (53.9 to 100.0) |
| Smoking status | |||||||||
| Never | 22 (73.3) | 136 | 72.9 (55.0 to 90.7) | 88 (92.6) | 245 | 92.5 (87.0 to 98.1) | 16 (80.0) | 99 | 79.5 (59.5 to 99.4) |
| Ever | 94 (66.2) | 510 | 69.8 (61.4 to 78.1) | 117 (89.3) | 419 | 86.5 (77.2 to 95.9) | 43 (93.5) | 255 | 93.1 (85.2 to 100.0) |
| Unknown | 16 (69.6) | 160 | 68.3 (47.0 to 89.6) | 24 (92.3) | 98 | 92.9 (82.6 to 100.0) | 9 (90.0) | 73 | 95.5 (84.5 to 100.0) |
| Human papillomavirus prevalence | |||||||||
|---|---|---|---|---|---|---|---|---|---|
| Oropharyngeal cancer | Cervical cancer | Anal cancer | |||||||
| Unweighted | Weighted | Unweighted | Weighted | Unweighted | Weighted | ||||
| No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | |
| Total | 132 (67.7) | 806 | 70.0 (62.8 to 77.2) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 68 (89.5) | 427 | 89.9 (82.9 to 96.9) |
| Age, y | |||||||||
| <50 | 50 (80.7) | 189 | 78.5 (64.7 to 92.4) | 137 (97.9) | 481 | 97.6 (94.9 to 100.0) | 29 (96.7) | 131 | 94.5 (83.4 to 100.0) |
| ≥50 | 82 (61.7) | 617 | 67.7 (59.3 to 76.1) | 92 (82.1) | 282 | 77.7 (65.8 to 89.5) | 39 (84.8) | 296 | 88.0 (79.0 to 97.1) |
| Sex | |||||||||
| Male | 109 (71.2) | 670 | 74.3 (66.7 to 81.9) | — | — | — | 26 (86.7) | 137 | 84.9 (70.4 to 99.5) |
| Female | 23 (54.8) | 136 | 54.4 (36.3 to 72.5) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 42 (91.3) | 291 | 92.5 (84.8 to 100.0) |
| Race and ethnicity | |||||||||
| Whiteb | 119 (73.0) | 774 | 72.2 (64.6 to 79.7) | 193 (91.0) | 693 | 89.0 (82.7 to 95.3) | 60 (89.6) | 407 | 90.1 (82.9 to 97.4) |
| Otherc | 13 (40.6) | 32 | 40.4 (21.9 to 59.0) | 36 (90.0) | 70 | 91.0 (82.0 to 99.9) | 8 (88.9) | 21 | 85.7 (53.9 to 100.0) |
| Smoking status | |||||||||
| Never | 22 (73.3) | 136 | 72.9 (55.0 to 90.7) | 88 (92.6) | 245 | 92.5 (87.0 to 98.1) | 16 (80.0) | 99 | 79.5 (59.5 to 99.4) |
| Ever | 94 (66.2) | 510 | 69.8 (61.4 to 78.1) | 117 (89.3) | 419 | 86.5 (77.2 to 95.9) | 43 (93.5) | 255 | 93.1 (85.2 to 100.0) |
| Unknown | 16 (69.6) | 160 | 68.3 (47.0 to 89.6) | 24 (92.3) | 98 | 92.9 (82.6 to 100.0) | 9 (90.0) | 73 | 95.5 (84.5 to 100.0) |
Cancer sites were defined by the International Classification of Diseases for Oncology, 3rd Edition, site codes C01.9, C02.4, C02.8, C05.1-05.2, C09.0-09.1, C09.8-09.9, C10.0-10.4, C10.8-10.9, C14.0, C14.2, C14.8 (oropharynx), C53.0-53.9 (cervix), and C21.0-21.8, 20.9 (anus), excluding histology codes 8720-8790 (melanoma), 8800-8991 (sarcoma), 9050-9055 (mesothelioma), 9140 (Kaposi sarcoma), and 9590-9992 (lymphoma, myeloma, and leukemia). CI = confidence interval.
Non-Hispanic.
“Other” includes non-Hispanic Black or African American, Asian or Native Hawaiian and Pacific Islander, American Indian or Alaska Native, and Hispanic individuals.
Human papillomavirus DNA prevalence among invasive oropharyngeal, cervical, and anal cancers,a Kentucky, 2004-2005 and 2014-2015
| Human papillomavirus prevalence | |||||||||
|---|---|---|---|---|---|---|---|---|---|
| Oropharyngeal cancer | Cervical cancer | Anal cancer | |||||||
| Unweighted | Weighted | Unweighted | Weighted | Unweighted | Weighted | ||||
| No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | |
| Total | 132 (67.7) | 806 | 70.0 (62.8 to 77.2) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 68 (89.5) | 427 | 89.9 (82.9 to 96.9) |
| Age, y | |||||||||
| <50 | 50 (80.7) | 189 | 78.5 (64.7 to 92.4) | 137 (97.9) | 481 | 97.6 (94.9 to 100.0) | 29 (96.7) | 131 | 94.5 (83.4 to 100.0) |
| ≥50 | 82 (61.7) | 617 | 67.7 (59.3 to 76.1) | 92 (82.1) | 282 | 77.7 (65.8 to 89.5) | 39 (84.8) | 296 | 88.0 (79.0 to 97.1) |
| Sex | |||||||||
| Male | 109 (71.2) | 670 | 74.3 (66.7 to 81.9) | — | — | — | 26 (86.7) | 137 | 84.9 (70.4 to 99.5) |
| Female | 23 (54.8) | 136 | 54.4 (36.3 to 72.5) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 42 (91.3) | 291 | 92.5 (84.8 to 100.0) |
| Race and ethnicity | |||||||||
| Whiteb | 119 (73.0) | 774 | 72.2 (64.6 to 79.7) | 193 (91.0) | 693 | 89.0 (82.7 to 95.3) | 60 (89.6) | 407 | 90.1 (82.9 to 97.4) |
| Otherc | 13 (40.6) | 32 | 40.4 (21.9 to 59.0) | 36 (90.0) | 70 | 91.0 (82.0 to 99.9) | 8 (88.9) | 21 | 85.7 (53.9 to 100.0) |
| Smoking status | |||||||||
| Never | 22 (73.3) | 136 | 72.9 (55.0 to 90.7) | 88 (92.6) | 245 | 92.5 (87.0 to 98.1) | 16 (80.0) | 99 | 79.5 (59.5 to 99.4) |
| Ever | 94 (66.2) | 510 | 69.8 (61.4 to 78.1) | 117 (89.3) | 419 | 86.5 (77.2 to 95.9) | 43 (93.5) | 255 | 93.1 (85.2 to 100.0) |
| Unknown | 16 (69.6) | 160 | 68.3 (47.0 to 89.6) | 24 (92.3) | 98 | 92.9 (82.6 to 100.0) | 9 (90.0) | 73 | 95.5 (84.5 to 100.0) |
| Human papillomavirus prevalence | |||||||||
|---|---|---|---|---|---|---|---|---|---|
| Oropharyngeal cancer | Cervical cancer | Anal cancer | |||||||
| Unweighted | Weighted | Unweighted | Weighted | Unweighted | Weighted | ||||
| No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | No. (%) | No. | % (95% CI) | |
| Total | 132 (67.7) | 806 | 70.0 (62.8 to 77.2) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 68 (89.5) | 427 | 89.9 (82.9 to 96.9) |
| Age, y | |||||||||
| <50 | 50 (80.7) | 189 | 78.5 (64.7 to 92.4) | 137 (97.9) | 481 | 97.6 (94.9 to 100.0) | 29 (96.7) | 131 | 94.5 (83.4 to 100.0) |
| ≥50 | 82 (61.7) | 617 | 67.7 (59.3 to 76.1) | 92 (82.1) | 282 | 77.7 (65.8 to 89.5) | 39 (84.8) | 296 | 88.0 (79.0 to 97.1) |
| Sex | |||||||||
| Male | 109 (71.2) | 670 | 74.3 (66.7 to 81.9) | — | — | — | 26 (86.7) | 137 | 84.9 (70.4 to 99.5) |
| Female | 23 (54.8) | 136 | 54.4 (36.3 to 72.5) | 229 (90.9) | 763 | 89.2 (83.4 to 94.9) | 42 (91.3) | 291 | 92.5 (84.8 to 100.0) |
| Race and ethnicity | |||||||||
| Whiteb | 119 (73.0) | 774 | 72.2 (64.6 to 79.7) | 193 (91.0) | 693 | 89.0 (82.7 to 95.3) | 60 (89.6) | 407 | 90.1 (82.9 to 97.4) |
| Otherc | 13 (40.6) | 32 | 40.4 (21.9 to 59.0) | 36 (90.0) | 70 | 91.0 (82.0 to 99.9) | 8 (88.9) | 21 | 85.7 (53.9 to 100.0) |
| Smoking status | |||||||||
| Never | 22 (73.3) | 136 | 72.9 (55.0 to 90.7) | 88 (92.6) | 245 | 92.5 (87.0 to 98.1) | 16 (80.0) | 99 | 79.5 (59.5 to 99.4) |
| Ever | 94 (66.2) | 510 | 69.8 (61.4 to 78.1) | 117 (89.3) | 419 | 86.5 (77.2 to 95.9) | 43 (93.5) | 255 | 93.1 (85.2 to 100.0) |
| Unknown | 16 (69.6) | 160 | 68.3 (47.0 to 89.6) | 24 (92.3) | 98 | 92.9 (82.6 to 100.0) | 9 (90.0) | 73 | 95.5 (84.5 to 100.0) |
Cancer sites were defined by the International Classification of Diseases for Oncology, 3rd Edition, site codes C01.9, C02.4, C02.8, C05.1-05.2, C09.0-09.1, C09.8-09.9, C10.0-10.4, C10.8-10.9, C14.0, C14.2, C14.8 (oropharynx), C53.0-53.9 (cervix), and C21.0-21.8, 20.9 (anus), excluding histology codes 8720-8790 (melanoma), 8800-8991 (sarcoma), 9050-9055 (mesothelioma), 9140 (Kaposi sarcoma), and 9590-9992 (lymphoma, myeloma, and leukemia). CI = confidence interval.
Non-Hispanic.
“Other” includes non-Hispanic Black or African American, Asian or Native Hawaiian and Pacific Islander, American Indian or Alaska Native, and Hispanic individuals.
Population-level incidence of HPV-positive cancers was higher among individuals who had ever smoked than among those who had never smoked for oropharyngeal (adjusted incidence rate ratio = 2.6, 95% CI = 1.6 to 4.4; incidence rate = 7.8 vs 2.1 per 100 000 persons), cervical (adjusted incidence rate ratio = 2.0, 95% CI = 1.5 to 2.7; incidence rate = 13.7 vs 6.8 per 100 000 persons), and anal (adjusted incidence rate ratio = 2.5, 95% CI = 1.4 to 4.5; incidence rate = 3.9 vs 1.6 per 100 000 persons) cancers (Figure 1). Similarly, population-level incidence for HPV-negative cancers was significantly higher among individuals who had ever smoked than among those who had never smoked for oropharyngeal (adjusted incidence rate ratio = 3.0, 95% CI = 1.6 to 5.3) and cervical (adjusted incidence rate ratio = 3.7, 95% CI = 1.7 to 8.0) cancers.
Incidence rate and adjusted incidence rate ratio of HPV-positive invasive oropharyngeal, cervical, and anal cancers,a by smoking status, in Kentucky, 2004-2005 and 2014-2015. CI = confidence interval; HPV = human papillomavirus.
a Cancer sites were defined by the International Classification of Diseases for Oncology, 3rd Edition, site codes C01.9, C02.4, C02.8, C05.1-05.2, C09.0-09.1, C09.8-09.9, C10.0-10.4, C10.8-10.9, C14.0, C14.2, C14.8 (oropharynx), C53.0-53.9 (cervix), and C21.0-21.8, 20.9 (anus), excluding histology codes 8720-8790 (melanoma), 8800-8991 (sarcoma), 9050-9055 (mesothelioma), 9140 (Kaposi sarcoma), and 9590-9992 (lymphoma, myeloma, and leukemia). Oropharyngeal and anal cancer models were adjusted for age, sex, and race and ethnicity. Cervical cancer model was adjusted for age and race and ethnicity.
Using an innovative approach to combine molecular epidemiology with population surveillance data, we provide novel estimates for the burden of HPV-positive oropharyngeal, cervical, and anal cancers by smoking status to show that the burden (number of cases) and population-level incidence of these cancers is significantly higher among individuals who had ever smoked than had never smoked.
Consistent with previous reports from observational studies (7,18,19), our findings indicate an association between smoking and HPV-positive cancers. The higher incidence among individuals who had ever smoked could reflect, in part, a higher prevalence of HPV infection (20,21). Previous studies have reported that smoking is associated with an increased likelihood of HPV infection (22,23) and may modify its acquisition (24) or persistence (20).
The incidence of oropharyngeal (25) and anal (26) cancer continues to increase in Kentucky, but the incidence of cervical cancer has stabilized in recent years (27). Broader implementation of prevention strategies, such as HPV vaccination and tobacco control, may reduce the incidence of these cancers. These prevention strategies are important, especially because screening and early detection are currently not feasible for oropharyngeal cancer and guidelines for groups at higher risk are still being developed for anal cancer (28). Our findings also have implications for treatment; smoking is a prognostic predictor of oropharyngeal cancer, with higher mortality reported among individuals who have smoked (29).
Our findings should be interpreted with consideration of 3 key limitations. First, we did not have data on potential confounders and effect modifiers on the association of smoking with the risk of HPV-positive cancers. For example, data on sexual history and behaviors, which can influence the link between smoking and HPV infection (22,30), were not available. Second, studies have reported a stronger association and dose-dependent relation between current smoking status and HPV infection (22,30), but our data on smoking status was restricted to ever and never use. Nevertheless, we note that the smoking status data in our study were previously validated using claims-linked cancer registry data (31). Future studies may benefit from data on distinct and disaggregated smoking status and HPV testing (beyond oropharyngeal cancers) in cancer registries or linked with registry data. Third, some stratified estimates have wide confidence intervals due to a small number of cases.
These findings highlight a high population-level incidence of HPV-positive oropharyngeal, cervical, and anal cancers among individuals who smoke and support that smoking increases the risk of these HPV-positive cancers. Widespread implementation of proven tobacco control interventions and increased HPV vaccination coverage could reduce the burden of these HPV-associated cancers.
Data availability
Investigators can access cancer incidence data with smoking information for Kentucky after submitting a data request to the KCR. The BRFSS data are publicly available. Data from the CDC Cancer Registry Sentinel Surveillance System are restricted and not publicly available.
Author contributions
Sameer Vali Gopalani, PhD, MPH (Formal analysis; Methodology; Software; Writing—original draft), Mona Saraiya, MD, MPH (Conceptualization; Methodology; Supervision; Writing—review & editing), Bin Huang, DrPH, MS (Data curation; Methodology; Writing—review & editing), Thomas C. Tucker, PhD, MPH (Conceptualization; Methodology; Writing—review & editing), Jacqueline M. Mix, PhD, MPH (Methodology; Writing—review & editing), Anil K. Chaturvedi, PhD, MPH (Conceptualization; Formal analysis; Methodology; Supervision; Writing—review & editing).
Funding
Not applicable.
Conflicts of interest
The authors have no potential conflicts of interest to disclose.
Acknowledgements
This project was supported in part by an appointment (S.V.G. and J.M.M.) to the Research Participation Program at the CDC administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the US Department of Energy and the CDC.
The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the CDC and the National Institutes of Health.
The authors are grateful for the efforts of cancer registry coordinators as well as BRFSS coordinators and survey participants.
Results in this manuscript were presented in part as a poster presentation at the International Papillomavirus Conference in April 2023.
