- Email: [email protected]
Pap Test Use Is Lower Among Female-to-Male Patients Than Non-Transgender Women
Pap Test Use Is Lower Among Female-to-Male Patients Than Non-Transgender Women Sarah M. Peitzmeier, MSPH, Karishma Khullar, BS, Sari L. Reisner, ScD, MA, Jennifer Potter, MD Background: A paucity of empirical research to date has examined cervical cancer screening in female-to-male (FTM) transgender men who retain their natal reproductive structures compared to non-transgender women. Purpose: To examine patient and provider characteristics associated with being up-to-date on Pap tests, with a focus on gender identity and sexual orientation. Methods: Retrospective chart review of 5,232 patients (4,882 women, 350 FTM transgender men) at an urban community health center. All HIV-negative primary care patients aged 21–64 years (inclusive) with at least one medical visit during the 2012 calendar year and who had a cervix as of December 31, 2012, were included. Data were analyzed in 2013 using a multilevel logistic regression model nesting patients within providers. Results: FTM patients were significantly less likely to be up-to-date on Pap tests (AOR¼0.63, 95% CI¼0.47, 0.85) compared to non-transgender women, after adjusting for individual- and providerlevel factors. Behaviorally bisexual patients, compared to patients who had sex with men exclusively, were more likely to be up-to-date (AOR¼1.73, 95% CI¼1.32, 2.26); patients reporting only sex with women were not significantly more or less likely to be up-to-date (AOR¼1.01, 95% CI¼0.83, 1.23). Conclusions: Transgender patients are not accessing the same level of preventive cervical screening care as non-transgender female patients. There is a need to better understand barriers to care in this population. Contrary to findings in other settings, history of sex with women was not negatively associated with Pap utilization. (Am J Prev Med 2014;47(6):808–812) & 2014 American Journal of Preventive Medicine
Introduction
S
cant research has addressed cervical cancer screening in female-to-male (FTM) transgender men. Transgender men are individuals assigned a female sex at birth who identify as men, transmen, or along a transmasculine spectrum; the majority retain a cervix and should undergo Pap testing. FTM individuals are often marginalized, lack access to health care, and may have unique barriers to receiving gynecologic examinations despite a higher prevalence of certain cervical cancer risk factors, such as smoking and sexual violence.1,2 From the Fenway Institute (Peitzmeier, Reisner), Fenway Health (Khullar, Potter), Harvard School of Public Health (Reisner), Harvard Medical School (Potter), Harvard University; Beth Israel Deaconess Medical Center (Potter), Boston, Massachusetts; Bloomberg School of Public Health (Peitzmeier), Johns Hopkins University, Baltimore, Maryland; and the University of Cincinnati College of Medicine (Khullar), Cincinnati, Ohio Address correspondence to: Jennifer Potter, MD, Fenway Health, 1340 Boylston Street, Boston MA 02215-4302. E-mail: [email protected]. edu. 0749-3797/$36.00 http://dx.doi.org/10.1016/j.amepre.2014.07.031
808 Am J Prev Med 2014;47(6):808–812
Understanding Pap utilization among transgender men is important.3 This study describes the prevalence of Pap test utilization among FTM compared to non-transgender female patients and examines predictors of adherence to Pap testing at Fenway Health (FH), an urban primary healthcare clinic in Boston MA that serves a large lesbian, gay, bisexual, and transgender (LGBT) patient population.4
Methods This study was an observational retrospective chart review. Data were extracted from the electronic medical record (EMR) via electronic query and manual review of patient charts at FH in 2013. All HIV-negative primary care patients aged 21–64 years (inclusive) with a medical visit in 2012 and who had a cervix as of December 31, 2012, were included in the study. HIV-positive patients were excluded, as they follow different screening guidelines. The study was approved by the FH IRB.
Measures Individual-level variables were selected based on literature review to determine factors known to be associated with screening (e.g., sexual behavior), as well as factors hypothesized to be related
& 2014 American Journal of Preventive Medicine
Published by Elsevier Inc.
Peitzmeier et al / Am J Prev Med 2014;47(6):808–812 (e.g., transgender identity), and were extracted from the EMR. Three primary care provider–level variables hypothesized to affect a patient’s likelihood of being up-to-date were assigned to each patient. Variable definitions and procedures used for handling missing data are described in the Appendix (available online).
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variables and the outcome, but each provider was assigned a random intercept term. Random intercept terms are not presented, as the analytic goal was to identify individual- and provider-level risks related to being up-to-date.
Results Outcome Ascertainment Patients were classified as up-to-date or not on December 31, 2012, based on U.S. Preventive Services Task Force (USPSTF)5 and American Cancer Society/American Society of Colposcopy and Cervical Pathology/American Society for Clinical Pathology (ACS/ ASCCP/ASCP) screening guidelines,6 and ASCCP consensus guidelines for managing abnormal cervical cancer screening tests (operationalization described in Table 1).7
Statistical Analysis A multilevel logistic regression model with patients (Level 1) nested under providers (Level 2) was fit with Pap up-to-date status (up-to-date¼1, not up-to-date¼0) as the outcome and the patientand provider-level independent variables as statistical predictors. This multilevel model accounts for nesting of patients hierarchically within providers (non-independence of observations).8–11 A fixed-slopes relationship was modeled between all independent
Table 1. Study definition of up-to-date on Pap tests
A total of 5,232 patients were included. Overall, 3,815 of patients (72.9%) were up-to-date with Pap testing (Table 2), and 3,590 (73.5%) female patients and 225 (64.3%) FTM patients were up-to-date. FTM patients had a 37% lower odds of being up-to-date compared to non-transgender female patients after adjustment for other variables. Additional factors negatively associated with being up-to-date were never having had sex or unknown sexual history (compared to sex exclusively with men); student status; and a higher missed appointment percentage. Factors positively associated with being up-to-date were sex with men and women (compared with men only); health insurance; higher number of medical appointments at FH; being a patient for a longer time; smoking cigarettes; experiencing sexual violence; and receiving birth control at FH in the last 3 years. No provider-level characteristics were significantly associated with up-todate status.
Participants were considered up-to-date if the most recent Pap in their chart was one of the following: a negative Pap in the last 3 years an ASCUS, HPV negative Pap in the last 3 years for those 30 years or older at the time of the Pap, a negative Pap and negative HPV co-test in the last 5 years as ASCUS Pap with no HPV co-test in the last year an ASCUS with HPV, LSIL, or HSIL Pap followed by a colposcopy, unless the abnormal Pap was taken less than 3 months before the end of the study period. After colposcopy, patients had to return within a year, unless the colposcopy took place less than 1 year before the end of the study period Pap done within 1 year of a LEEP following CIN3 colposcopy, unless the LEEP took place less than 1 year before the end of the study period two inadequate Paps followed by a colposcopy, unless the inadequate Pap took place within 3 months of the end of the study period. Note: These definitions were derived from three sources: the independently developed but generally consistent cervical cancer screening recommendations published by the U.S. Preventive Services Task Force and the American Cancer Society/American Society of Colposcopy and Cervical Pathology (ASCCP)/American Society for Clinical Pathology in 2012, and the 2006 ASCCP consensus guidelines for managing abnormal cervical cancer screening tests. Fenway providers were specifically trained to follow these guidelines during the study period. American College of Obstetrics and Gynecology guidelines were not included, as they were not revised to align with those of the other organizations until 2013. Up-to-date status was ascertained using the above criteria regardless of what screening guidelines individual providers utilized during the study period. Because of evolution of screening guidelines in recent years, providers sometimes recommended more aggressive screening and follow-up than endorsed by the aforementioned professional societies in 2012 or currently. ASCUS, atypical squamous cells of uncertain significance; HPV, human papillomavirus; LSIL, lowgrade squamous intraepithelial lesion; HSIL, high-grade squamous intraepithelial lesion, LEEP, loop electrosurgical excision procedure
December 2014
Discussion The proportion of FTM patients who were up-to-date was 9.2 percentage points lower compared to nontransgender female patients, and being transgender was an independent predictor associated with a 37% lower odds of being up-to-date. Even at a clinic where providers have expertise caring for LGBT populations,4 transgender patients are not achieving screening rates equivalent to non-transgender women. There is a need to better understand barriers to care in this patient population.12–14 In accord with prior studies,15 patients who had never had sex were less likely to be up-to-date compared to patients who exclusively had sex with men, even after adjusting for age. In contrast to studies16,17 suggesting that women who have sex with women are less likely to be upto-date compared to women who have sex with men, no difference
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Table 2. Factors associated with being up-to-date on Pap tests among all patients with a cervix Up-to-date on Paps Risk factor
Yes (n [%] or median [IQR]) (n¼3,815)
No (n [%] or median [IQR]) (n¼1,417)
AORa (95% CI)
PATIENT CHARACTERISTICS FTM transgender Age/10
225 (64.3%) 3.0 (2.6, 3.8)
125 (35.7%) 2.6 (2.3, 3.4)
0.63 (0.47, 0.85)** 1.01 (0.93, 1.10)
Race/ethnicity Non-Hispanic White
2,729 (74.8%)
918 (25.2%)
1.00 (ref)
African American
308 (73.2%)
113 (26.8%)
1.16 (0.88, 1.52)
Hispanic/Latino
212 (68.6%)
97 (31.4%)
0.85 (0.64, 1.15)
Asian
260 (63.4%)
150 (36.6%)
0.84 (0.65, 1.09)
78 (70.3%)
33 (29.7%)
1.05 (0.65,1.69)
131 (63.6%)
75 (36.4%)
0.75 (0.53, 1.07)
97 (75.8%)
31 (24.2%)
1.07 (0.66, 1.73)
105 (64.8%)
57 (35.2%)
0.72 (0.50, 1.03)
1,896 (73.4%)
687 (26.6%)
1.00 (ref)
Overweight (25–30)
895 (75.1%)
296 (24.9%)
1.01 (0.85, 1.20)
Obese Z30
800 (77.2%)
236 (22.8%)
1.05 (0.86, 1.28)
2,389 (73.3%)
868 (26.7%)
1.00 (ref)
Sex with women only
843 (75.9%)
267 (24.1%)
1.01 (0.83, 1.23)
Sex with both
482 (81.8%)
107 (18.2%)
1.73 (1.32, 2.26)***
Never had sex
48 (39.3%)
74 (60.7%)
0.27 (0.18, 0.41)***
Unknown
53 (34.4%)
101 (65.6%)
0.26 (0.18, 0.39)***
86 (78.9%)
23 (21.1%)
1.00 (0.59, 1.69)
Immigrant
381 (65.2%)
203 (34.8%)
0.97 (0.77, 1.22)
Estimated household income/1,000
65.0 (44.7, 73.3)
59.8 (37.5, 77.0)
1.00 (1.00, 1.00)
Multiracial Other Unknown BMI Underweight (o18.5) Normal weight (18.5–25)
Gender of sexual partners Sex with men only
Sex with transgender partners
Insured Number of appointments at Fenway Years at Fenway
3,570 (74.2%) 6 (3, 13) 2.2 (0.9, 3.9)
1,239 (25.8%) 3 (1, 8) 1.2 (0.6, 3.1)
1.48 (1.16, 1.88)** 1.01 (1.00, 1.02)* 1.07 (1.03, 1.11)***
Student
644 (59.2%)
443 (40.8%)
0.49 (0.41, 0.58)***
Ever smoked
884 (80.1%)
220 (19.9%)
1.23 (1.02, 1.48)*
77 (86.5%)
12 (13.5%)
2.44 (1.23, 4.84)*
1,472 (80.7%)
353 (19.3%)
39 (55.7%)
31 (44.3%)
0.66 (0.37, 1.17)
122 (75.3%)
40 (24.7%)
0.79 (0.51, 1.22)
Sexual violence Received recent birth control at Fenway History of homelessness Drug use
1.93 (1.63, 2.27)***
(continued on next page)
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Table 2. Factors associated with being up-to-date on Pap tests among all patients with a cervix (continued) Up-to-date on Paps Risk factor Percent of appointments missed
Yes (n [%] or median [IQR]) (n¼3,815)
No (n [%] or median [IQR]) (n¼1,417)
AORa (95% CI)
0 (0, 0)
0 (0, 0)
0.99 (0.98, 1.00)**
Male provider
372 (52.9%)
331 (47.1%)
0.79 (0.40, 1.54)
Percent of provider’s patient panel that is female
68.5 (62.9, 72.5)
62.9 (41.2, 68.5)
1.01 (1.00, 1.02)
PROVIDER CHARACTERISTICS
Provider years in practice
8 (4, 19)
8 (4, 15)
1.00 (0.98, 1.02)
Note: Boldface indicates statistical significance (*po0.05; **po0.01; ***po0.001). a A multivariable logistic regression model was fit regressing up-to-date on Pap testing (yes/no) on individual-level (Level 1) and provider-level (Level 2) characteristics.
was found in screening rates between these groups in this FTM and female patient sample. The finding that behaviorally bisexual FTM and female patients were more likely to be screened compared to their counterparts who reported sex with men only also differs from other studies, which demonstrated either no difference18 or reduced19 screening rates in this group. Findings may not be directly comparable to studies that did not include transgender men and measured current sexual identity rather than lifetime sexual behavior. The current study was also performed in a clinic with specific focus on providing LGBT-sensitive care, whereas other studies focused on population-based surveys of non-transgender women receiving care in a wide variety of settings that may be less responsive to their needs. Greater adherence to Pap testing was found among longstanding clinic patients and those with a higher number of medical appointments, and lower adherence among students and those prone to missing appointments. Findings are consistent with studies16,20 documenting better adherence with higher continuity of care and patient engagement, and suggest an ongoing need for outreach to patients at risk for loss to follow-up, particularly as the majority of cervical cancers occur in patients who have not been screened in the past 5 years.6 In contrast to other studies,21–24 BMI, provider gender, and race/ethnicity were not associated with Pap adherence in this study, and smoking was positively associated with Pap use. The smoking measure included both current and former smoking, and current smokers may have lower Pap utilization while former smokers may have higher Pap utilization compared to never smokers.25 Future assessment of the relationship of current/recent smoking and sexual violence with Pap utilization among FTMs is important, as studies show a high prevalence of both in transgender communities1,2,13,26 and each has been independently December 2014
associated with reduced screening and increased cervical cytologic abnormalities in non-transgender women.27,28 There were limitations to this cross-sectional study. As a retrospective chart review, reviewing patients’ entire medical record was possible, but directly surveying participants was not. This increased the accuracy of items prone to recall bias (e.g., result and date of last Pap test) while decreasing the accuracy of items assessed or recorded inconsistently (e.g., sexual violence). Although some patients who received Pap tests at outside facilities may not have informed FH, confirmation of Pap testing via EMR review represents a strength, given previous research showing that patients tend to over-report participation in screening.29,30 As a single-site study at a LGBTfocused health center, results may not be generalizable. Despite these limitations, the demonstration of a disparity in Pap use by gender identity is cause for concern. The finding that more than one in three FTM patients at Fenway were not up-to-date and that FTM patients had 37% lower odds of being up-to-date compared to non-transgender women likely represents an underestimate of national screening disparities given the LGBT expertise that exists at FH. Mixed-methods research is needed to identify and understand Pap testing barriers specific to FTM patients and their providers in order to optimize care and design interventions to promote cervical cancer screening. There are no conflicts of interest to declare. This work was funded through the FY 2012 Supplemental Funding for Quality Improvement in Health Centers grant (No. H80CS00303) provided by the Health Resources and Services Administration at the U.S. Department of Health and Human Services. No financial disclosures were reported by the authors of this paper.
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References 1. Conron KJ, Scott G, Stowell GS, Landers SJ. Transgender health in Massachusetts: results from a household probability sample of adults. Am J Public Health 2012;102(1):118–22. 2. Grant JM, Mottet LA, Tanis J, Harrison J, Herman JL, Keisling M. Injustice at every turn: a report of the National Transgender Discrimination Survey. Washington DC: National Center for Transgender Equality and National Gay and Lesbian Task Force, 2011. 3. Dutton L, Koenig K, Fennie K. Gynecologic care of the female-to-male transgender man. J Midwifery Womens Health 2008;53(4):331–7. 4. Mayer K, Mimiaga M, VanDerwarker R, Goldhammer H, Bradford J. Fenway Community Health’s model of integrated, community-based LGBT care, education, and research. In: Meyer I, Northridge M, eds. The health of sexual minorities. New York NY: Springer, 2007. 5. Screening for Cervical Cancer: Clinical Summary of U.S. Preventive Services Task Force Recommendation. AHRQ Publication No. 1105156-EF-3. U.S. Preventive Services Task Force. 2012. www.uspreven tiveservicestaskforce.org/uspstf11/cervcancer/cervcancersum.htm. 6. Saslow D, Solomon D, Lawson HW, et al. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin 2012;62(3):147–72. 7. Wright TCJ, Massad LS, Dunton CJ, Spitzer M, Wilkinson EJ, Solomon D, 2006 ASCCP-Sponsored Consensus Conference. 2006 consensus guidelines for the management of women with abnormal cervical screening tests. J Low Genit Tract Dis 2007;11(4):201–22. 8. Dickinson LM, Basu A. Multilevel modeling and practice-based research. Ann Fam Med 2005;3(suppl 1):S52–S60. 9. Snijders TAB, Bosker RJ. Multilevel analysis: an introduction to basic and advanced multilevel modeling. Thousand Oaks, CA: Sage Publications, 1999. 10. Hox J. Multilevel analysis: techniques and applications. 2nd ed. New York NY: Taylor & Francis, 2010. 11. Raudenbush SW, Bryk AS. Hierarchical linear models: applications and data analysis methods. Newbury Park, CA: Sage Publications, 2002. 12. Reisner SL, Gamarel KE, Dunham E, Hopwood R, Hwahng S. Female-tomale transmasculine adult health: a mixed-methods community-based needs assessment. J Am Psychiatr Nurses Assoc 2013;19(5):293–303. 13. Bradford J, Reisner SL, Honnold JA, Xavier J. Experiences of transgender-related discrimination and implications for health: results from the Virginia Transgender Health Initiative Study. Am J Public Health 2013;103(10):1820–9. 14. Poteat T, German D, Kerrigan D. Managing uncertainty: a grounded theory of stigma in transgender health care encounters. Soc Sci Med 2013;84:22–9. 15. Valanis BG, Bowen DJ, Bassford T, Whitlock E, Charney P, Carter RA. Sexual orientation and health: comparisons in the Womenʼs Health Initiative sample. Arch Fam Med 2000;9(9):843–53. 16. Matthews AK, Brandenburg DL, Johnson TP, Hughes TL. Correlates of underutilization of gynecological cancer screening among lesbian and heterosexual women. Prev Med 2004;38(1):105–13.
17. Kerker BD, Mostashari F, Thorpe L. Health care access and utilization among women who have sex with women: sexual behavior and identity. J Urban Health 2006;83(5):970–9. 18. Agenor M, Krieger N, Austin SB, Haneuse S, Gottlieb BR. Sexual orientation disparities in Papanicolau test use among US women: the role of sexual and reproductive health services. Am J Public Health 2014;104(2):368–73. 19. Charlton BM, Corliss HL, Missmer SA, et al. Reproductive health screening disparities and sexual orientation in a cohort study of U.S. adolescent and young adult females. J Adolesc Health 2011;49(5):505–10. 20. Ackerson K, Gretebeck K. Factors influencing cancer screening practices of underserved women. J Am Acad Nurse Pract 2007;19(11): 591–601. 21. Maruthur NM, Bolen SD, Brancati FL, Clark JM. The association of obesity and cervical cancer screening: a systematic review and metaanalysis. Obesity (Silver Spring) 2009;17(2):375–81. 22. Lurie N, Slater J, McGovern P, Ekstrum J, Quam L, Margolis K. Preventive care for women. Does the sex of the physician matter? N Engl J Med 1993;329(7):478–82. 23. Olesen SC, Butterworth P, Jacomb P, Tait RJ. Personal factors influence use of cervical cancer screening services: epidemiological survey and linked administrative data address the limitations of previous research. BMC Health Serv Res 2012;12:34. 24. Agenor M, Krieger N, Austin SB, Haneuse S, Gottlieb BR. At the intersection of sexual orientation, race/ethnicity, and cervical cancer screening: Assessing Pap test use disparities by sex of sexual partners among black, Latina, and white U.S. women. Soc Sci Med 2014;116(1): 110–8. 25. Rakowski W, Clark MA, Ehrich B. Smoking and cancer screening for women ages 42 -75: associations in the 1990 -1994 National Health Interview Surveys. Prev Med 1999;29(6):487–95. 26. Bockting WO, Miner MH, Swinburne Romine RE, Hamilton A, Coleman E. Stigma, mental health, and resilience in an online sample of the US transgender population. Am J Public Health 2013;103(5):943–51. 27. Roura E, Castellsague X, Pawlita M, et al. Smoking as a major risk factor for cervical cancer and pre-cancer: results from the EPIC cohort. Int J Cancer 2014;135(2):453–66. 28. Sadler AG, Mengeling MA, Syrop CH, Torner JC, Booth BM. Lifetime sexual assault and cervical cytologic abnormalities among military women. J Womens Health (Larchmt) 2011;20(11):1693–701. 29. Howard M, Agarwal G, Lytwyn A. Accuracy of self-reports of Pap and mammography screening compared to medical record: a metaanalysis. Cancer Causes Control 2009;20(1):1–13. 30. Rauscher GH, Johnson TP, Cho YI, Walk JA. Accuracy of self-reported cancer-screening histories: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2008;17(4):748–57.
Appendix Supplementary data Supplementary data associated with this article can be found at http://dx.doi.org/10.1016/j.amepre.2014.07.031.
www.ajpmonline.org
Introduction
S
cant research has addressed cervical cancer screening in female-to-male (FTM) transgender men. Transgender men are individuals assigned a female sex at birth who identify as men, transmen, or along a transmasculine spectrum; the majority retain a cervix and should undergo Pap testing. FTM individuals are often marginalized, lack access to health care, and may have unique barriers to receiving gynecologic examinations despite a higher prevalence of certain cervical cancer risk factors, such as smoking and sexual violence.1,2 From the Fenway Institute (Peitzmeier, Reisner), Fenway Health (Khullar, Potter), Harvard School of Public Health (Reisner), Harvard Medical School (Potter), Harvard University; Beth Israel Deaconess Medical Center (Potter), Boston, Massachusetts; Bloomberg School of Public Health (Peitzmeier), Johns Hopkins University, Baltimore, Maryland; and the University of Cincinnati College of Medicine (Khullar), Cincinnati, Ohio Address correspondence to: Jennifer Potter, MD, Fenway Health, 1340 Boylston Street, Boston MA 02215-4302. E-mail: [email protected]. edu. 0749-3797/$36.00 http://dx.doi.org/10.1016/j.amepre.2014.07.031
808 Am J Prev Med 2014;47(6):808–812
Understanding Pap utilization among transgender men is important.3 This study describes the prevalence of Pap test utilization among FTM compared to non-transgender female patients and examines predictors of adherence to Pap testing at Fenway Health (FH), an urban primary healthcare clinic in Boston MA that serves a large lesbian, gay, bisexual, and transgender (LGBT) patient population.4
Methods This study was an observational retrospective chart review. Data were extracted from the electronic medical record (EMR) via electronic query and manual review of patient charts at FH in 2013. All HIV-negative primary care patients aged 21–64 years (inclusive) with a medical visit in 2012 and who had a cervix as of December 31, 2012, were included in the study. HIV-positive patients were excluded, as they follow different screening guidelines. The study was approved by the FH IRB.
Measures Individual-level variables were selected based on literature review to determine factors known to be associated with screening (e.g., sexual behavior), as well as factors hypothesized to be related
& 2014 American Journal of Preventive Medicine
Published by Elsevier Inc.
Peitzmeier et al / Am J Prev Med 2014;47(6):808–812 (e.g., transgender identity), and were extracted from the EMR. Three primary care provider–level variables hypothesized to affect a patient’s likelihood of being up-to-date were assigned to each patient. Variable definitions and procedures used for handling missing data are described in the Appendix (available online).
809
variables and the outcome, but each provider was assigned a random intercept term. Random intercept terms are not presented, as the analytic goal was to identify individual- and provider-level risks related to being up-to-date.
Results Outcome Ascertainment Patients were classified as up-to-date or not on December 31, 2012, based on U.S. Preventive Services Task Force (USPSTF)5 and American Cancer Society/American Society of Colposcopy and Cervical Pathology/American Society for Clinical Pathology (ACS/ ASCCP/ASCP) screening guidelines,6 and ASCCP consensus guidelines for managing abnormal cervical cancer screening tests (operationalization described in Table 1).7
Statistical Analysis A multilevel logistic regression model with patients (Level 1) nested under providers (Level 2) was fit with Pap up-to-date status (up-to-date¼1, not up-to-date¼0) as the outcome and the patientand provider-level independent variables as statistical predictors. This multilevel model accounts for nesting of patients hierarchically within providers (non-independence of observations).8–11 A fixed-slopes relationship was modeled between all independent
Table 1. Study definition of up-to-date on Pap tests
A total of 5,232 patients were included. Overall, 3,815 of patients (72.9%) were up-to-date with Pap testing (Table 2), and 3,590 (73.5%) female patients and 225 (64.3%) FTM patients were up-to-date. FTM patients had a 37% lower odds of being up-to-date compared to non-transgender female patients after adjustment for other variables. Additional factors negatively associated with being up-to-date were never having had sex or unknown sexual history (compared to sex exclusively with men); student status; and a higher missed appointment percentage. Factors positively associated with being up-to-date were sex with men and women (compared with men only); health insurance; higher number of medical appointments at FH; being a patient for a longer time; smoking cigarettes; experiencing sexual violence; and receiving birth control at FH in the last 3 years. No provider-level characteristics were significantly associated with up-todate status.
Participants were considered up-to-date if the most recent Pap in their chart was one of the following: a negative Pap in the last 3 years an ASCUS, HPV negative Pap in the last 3 years for those 30 years or older at the time of the Pap, a negative Pap and negative HPV co-test in the last 5 years as ASCUS Pap with no HPV co-test in the last year an ASCUS with HPV, LSIL, or HSIL Pap followed by a colposcopy, unless the abnormal Pap was taken less than 3 months before the end of the study period. After colposcopy, patients had to return within a year, unless the colposcopy took place less than 1 year before the end of the study period Pap done within 1 year of a LEEP following CIN3 colposcopy, unless the LEEP took place less than 1 year before the end of the study period two inadequate Paps followed by a colposcopy, unless the inadequate Pap took place within 3 months of the end of the study period. Note: These definitions were derived from three sources: the independently developed but generally consistent cervical cancer screening recommendations published by the U.S. Preventive Services Task Force and the American Cancer Society/American Society of Colposcopy and Cervical Pathology (ASCCP)/American Society for Clinical Pathology in 2012, and the 2006 ASCCP consensus guidelines for managing abnormal cervical cancer screening tests. Fenway providers were specifically trained to follow these guidelines during the study period. American College of Obstetrics and Gynecology guidelines were not included, as they were not revised to align with those of the other organizations until 2013. Up-to-date status was ascertained using the above criteria regardless of what screening guidelines individual providers utilized during the study period. Because of evolution of screening guidelines in recent years, providers sometimes recommended more aggressive screening and follow-up than endorsed by the aforementioned professional societies in 2012 or currently. ASCUS, atypical squamous cells of uncertain significance; HPV, human papillomavirus; LSIL, lowgrade squamous intraepithelial lesion; HSIL, high-grade squamous intraepithelial lesion, LEEP, loop electrosurgical excision procedure
December 2014
Discussion The proportion of FTM patients who were up-to-date was 9.2 percentage points lower compared to nontransgender female patients, and being transgender was an independent predictor associated with a 37% lower odds of being up-to-date. Even at a clinic where providers have expertise caring for LGBT populations,4 transgender patients are not achieving screening rates equivalent to non-transgender women. There is a need to better understand barriers to care in this patient population.12–14 In accord with prior studies,15 patients who had never had sex were less likely to be up-to-date compared to patients who exclusively had sex with men, even after adjusting for age. In contrast to studies16,17 suggesting that women who have sex with women are less likely to be upto-date compared to women who have sex with men, no difference
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Table 2. Factors associated with being up-to-date on Pap tests among all patients with a cervix Up-to-date on Paps Risk factor
Yes (n [%] or median [IQR]) (n¼3,815)
No (n [%] or median [IQR]) (n¼1,417)
AORa (95% CI)
PATIENT CHARACTERISTICS FTM transgender Age/10
225 (64.3%) 3.0 (2.6, 3.8)
125 (35.7%) 2.6 (2.3, 3.4)
0.63 (0.47, 0.85)** 1.01 (0.93, 1.10)
Race/ethnicity Non-Hispanic White
2,729 (74.8%)
918 (25.2%)
1.00 (ref)
African American
308 (73.2%)
113 (26.8%)
1.16 (0.88, 1.52)
Hispanic/Latino
212 (68.6%)
97 (31.4%)
0.85 (0.64, 1.15)
Asian
260 (63.4%)
150 (36.6%)
0.84 (0.65, 1.09)
78 (70.3%)
33 (29.7%)
1.05 (0.65,1.69)
131 (63.6%)
75 (36.4%)
0.75 (0.53, 1.07)
97 (75.8%)
31 (24.2%)
1.07 (0.66, 1.73)
105 (64.8%)
57 (35.2%)
0.72 (0.50, 1.03)
1,896 (73.4%)
687 (26.6%)
1.00 (ref)
Overweight (25–30)
895 (75.1%)
296 (24.9%)
1.01 (0.85, 1.20)
Obese Z30
800 (77.2%)
236 (22.8%)
1.05 (0.86, 1.28)
2,389 (73.3%)
868 (26.7%)
1.00 (ref)
Sex with women only
843 (75.9%)
267 (24.1%)
1.01 (0.83, 1.23)
Sex with both
482 (81.8%)
107 (18.2%)
1.73 (1.32, 2.26)***
Never had sex
48 (39.3%)
74 (60.7%)
0.27 (0.18, 0.41)***
Unknown
53 (34.4%)
101 (65.6%)
0.26 (0.18, 0.39)***
86 (78.9%)
23 (21.1%)
1.00 (0.59, 1.69)
Immigrant
381 (65.2%)
203 (34.8%)
0.97 (0.77, 1.22)
Estimated household income/1,000
65.0 (44.7, 73.3)
59.8 (37.5, 77.0)
1.00 (1.00, 1.00)
Multiracial Other Unknown BMI Underweight (o18.5) Normal weight (18.5–25)
Gender of sexual partners Sex with men only
Sex with transgender partners
Insured Number of appointments at Fenway Years at Fenway
3,570 (74.2%) 6 (3, 13) 2.2 (0.9, 3.9)
1,239 (25.8%) 3 (1, 8) 1.2 (0.6, 3.1)
1.48 (1.16, 1.88)** 1.01 (1.00, 1.02)* 1.07 (1.03, 1.11)***
Student
644 (59.2%)
443 (40.8%)
0.49 (0.41, 0.58)***
Ever smoked
884 (80.1%)
220 (19.9%)
1.23 (1.02, 1.48)*
77 (86.5%)
12 (13.5%)
2.44 (1.23, 4.84)*
1,472 (80.7%)
353 (19.3%)
39 (55.7%)
31 (44.3%)
0.66 (0.37, 1.17)
122 (75.3%)
40 (24.7%)
0.79 (0.51, 1.22)
Sexual violence Received recent birth control at Fenway History of homelessness Drug use
1.93 (1.63, 2.27)***
(continued on next page)
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Table 2. Factors associated with being up-to-date on Pap tests among all patients with a cervix (continued) Up-to-date on Paps Risk factor Percent of appointments missed
Yes (n [%] or median [IQR]) (n¼3,815)
No (n [%] or median [IQR]) (n¼1,417)
AORa (95% CI)
0 (0, 0)
0 (0, 0)
0.99 (0.98, 1.00)**
Male provider
372 (52.9%)
331 (47.1%)
0.79 (0.40, 1.54)
Percent of provider’s patient panel that is female
68.5 (62.9, 72.5)
62.9 (41.2, 68.5)
1.01 (1.00, 1.02)
PROVIDER CHARACTERISTICS
Provider years in practice
8 (4, 19)
8 (4, 15)
1.00 (0.98, 1.02)
Note: Boldface indicates statistical significance (*po0.05; **po0.01; ***po0.001). a A multivariable logistic regression model was fit regressing up-to-date on Pap testing (yes/no) on individual-level (Level 1) and provider-level (Level 2) characteristics.
was found in screening rates between these groups in this FTM and female patient sample. The finding that behaviorally bisexual FTM and female patients were more likely to be screened compared to their counterparts who reported sex with men only also differs from other studies, which demonstrated either no difference18 or reduced19 screening rates in this group. Findings may not be directly comparable to studies that did not include transgender men and measured current sexual identity rather than lifetime sexual behavior. The current study was also performed in a clinic with specific focus on providing LGBT-sensitive care, whereas other studies focused on population-based surveys of non-transgender women receiving care in a wide variety of settings that may be less responsive to their needs. Greater adherence to Pap testing was found among longstanding clinic patients and those with a higher number of medical appointments, and lower adherence among students and those prone to missing appointments. Findings are consistent with studies16,20 documenting better adherence with higher continuity of care and patient engagement, and suggest an ongoing need for outreach to patients at risk for loss to follow-up, particularly as the majority of cervical cancers occur in patients who have not been screened in the past 5 years.6 In contrast to other studies,21–24 BMI, provider gender, and race/ethnicity were not associated with Pap adherence in this study, and smoking was positively associated with Pap use. The smoking measure included both current and former smoking, and current smokers may have lower Pap utilization while former smokers may have higher Pap utilization compared to never smokers.25 Future assessment of the relationship of current/recent smoking and sexual violence with Pap utilization among FTMs is important, as studies show a high prevalence of both in transgender communities1,2,13,26 and each has been independently December 2014
associated with reduced screening and increased cervical cytologic abnormalities in non-transgender women.27,28 There were limitations to this cross-sectional study. As a retrospective chart review, reviewing patients’ entire medical record was possible, but directly surveying participants was not. This increased the accuracy of items prone to recall bias (e.g., result and date of last Pap test) while decreasing the accuracy of items assessed or recorded inconsistently (e.g., sexual violence). Although some patients who received Pap tests at outside facilities may not have informed FH, confirmation of Pap testing via EMR review represents a strength, given previous research showing that patients tend to over-report participation in screening.29,30 As a single-site study at a LGBTfocused health center, results may not be generalizable. Despite these limitations, the demonstration of a disparity in Pap use by gender identity is cause for concern. The finding that more than one in three FTM patients at Fenway were not up-to-date and that FTM patients had 37% lower odds of being up-to-date compared to non-transgender women likely represents an underestimate of national screening disparities given the LGBT expertise that exists at FH. Mixed-methods research is needed to identify and understand Pap testing barriers specific to FTM patients and their providers in order to optimize care and design interventions to promote cervical cancer screening. There are no conflicts of interest to declare. This work was funded through the FY 2012 Supplemental Funding for Quality Improvement in Health Centers grant (No. H80CS00303) provided by the Health Resources and Services Administration at the U.S. Department of Health and Human Services. No financial disclosures were reported by the authors of this paper.
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Appendix Supplementary data Supplementary data associated with this article can be found at http://dx.doi.org/10.1016/j.amepre.2014.07.031.
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