RESEARCH AND PRACTICE

Adherence to Mammography Screening Guidelines Among Transgender Persons and Sexual Minority Women Angela Robertson Bazzi, PhD, MPH, Debra S. Whorms, BS, Dana S. King, BA, and Jennifer Potter, MD

We used retrospective (2012– 2013) chart review to examine breast cancer screening among transgender persons and sexual minority women (n = 1263) attending an urban community health center in Massachusetts. Transgender were less likely than cisgender patients and bisexuals were less likely than heterosexuals and lesbians to adhere to mammography screening guidelines (respectively, adjusted odds ratios = 0.53 and 0.56; 95% confidence intervals = 0.31, 0.91 and 0.34, 0.92) after adjustment for sociodemographics. Enhanced cancer prevention outreach is needed among gender and sexual minorities. (Am J Public Health. 2015;105: 2356–2358. doi:10.2105/AJPH.2015. 302851)

Sexual minority women (those who report partnering with women or identify as lesbian or bisexual) may experience elevated breast cancer risk1; however, research suggests they obtain screening mammography less often than other women. 2---5 Little is known about mammography use among transgender persons (those whose gender identity is incongruent with their birthassigned sex). Consensus groups recommend that female-to-male transmen without bilateral mastectomy follow screening guidelines for cisgender women.6---8 Recommendations for male-to-female transwomen are less clear.9 Some experts suggest following similar guidelines for transwomen,7 especially for those

with additional risk factors, such as being older than 50 years, 8 family history, body mass index greater than 35 kilograms per meters squared, or estrogen or progestin use for 5 or more years.6 Understanding mammography utilization among these often-marginalized groups is important in addressing breast cancer disparities. We investigated adherence to mammography screening guidelines at an urban community health center in Massachusetts that serves a large population of gender and sexual minorities.

METHODS For this retrospective study, we extracted and reviewed patient and provider data entered into electronic medical records during registration and health care visits from January 1, 2012, to December 31, 2013. Patients were eligible if they were cisgender women, transwomen taking estrogen for 5 or more years, or preoperative transmen; were aged 40 to 67 years as of January 1, 2012; and attended 1 or more medical appointments at the center. We excluded patients with previous breast cancer or bilateral mastectomy. At patient registration, the center required birth date and health insurance information. Voluntary self-reported measures included sociodemographic information (e.g., age, race/ ethnicity), sexual minority status (e.g., bisexual according to reported sexual orientation and female-gendered sexual partners), and gender identity. We extracted health care utilization and provider characteristics from records (Appendix A, available as a supplement to the online version of this article at http://www. ajph.org). We defined adherence to mammography guidelines according to 2012 Healthcare Effectiveness Data and Information Set criteria as having 1 or more mammograms during the 2-year study period.10 Descriptive statistics (medians, frequencies) compared adherent and nonadherent patients. Multivariable logistic regression with clustered standard errors to account for correlation among patients with the same providers (i.e., nonindependence) identified patient- and provider-level factors independently associated with mammography adherence.11 We assessed interactions,

2356 | Sexual Orientation and Health | Peer Reviewed | Bazzi et al.

confounding,12 and model fit.13 We used Stata version 12 for our analyses (StataCorp LP, College Station, TX).

RESULTS Among 1263 patients (15% sexual minority women, 6% transgender), median age was 51 years (interquartile range = 45---58 years), and 72% (n = 904) adhered to mammography screening guidelines (Appendix A). In our final multivariable logistic regression model (Table 1), transgender were less likely than cisgender patients (adjusted odds ratio [AOR] = 0.53; 95% confidence interval [CI] = 0.31, 0.91) and bisexual women were less likely than heterosexual and lesbian women (AOR = 0.56; 95% CI = 0.34, 0.92) to adhere to mammography recommendations. This model controlled for other covariates: age (AOR = 1.06/year increase; 95% CI = 1.04, 1.08), private insurance status (AOR = 1.80; 95% CI = 1.33, 2.44), health care engagement (AOR = 1.08/appointment kept in the past 3 years; 95% CI = 1.05, 1.10), and gender breakdown of provider’s panels (AOR = 1.01/point increase in the percentage of female patients; 95% CI = 1.00, 1.02; P = .099).

DISCUSSION Most patients (72%) adhered to mammography screening guidelines. After adjustment for specific patient and provider characteristics, transgender patients were less likely than cisgender patients and bisexual women were less likely than heterosexual and lesbian women to adhere to guidelines. Although small sample sizes prevented separate subgroup analyses for transwomen and transmen, our finding that transgender patients had reduced odds of mammography adherence is of particular concern for transmen without bilateral mastectomy who remain at risk for breast cancer.14 Some experts recommend mammography for all transwomen 7 or for those older than 50 years, 8 especially with extended duration of hormone use.6 However, a recent study of 2307 transwomen patients taking estrogen for more than 5 years found breast cancer incidence equivalent

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TABLE 1—Characteristics Associated With Adherence to Mammography Screening Guidelines Among Patients Attending an Urban Community Health Center: Massachusetts, 2012–2013

screening utilization by gender and sexual minority patients. Collection of gender identity and sexual orientation information, which has been shown to be feasible and acceptable,18 should be done routinely to allow more nuanced subgroup comparisons and better understand cancer disparities. j

Adherent Patients (n = 904, 71.6%)

Unadjusted OR (95% CI)a

AOR (95% CI)

Median age, y (IQR)

52 (47–59)

1.07 (1.05, 1.09)

1.06 (1.04, 1.08)

Insurance type,b % Public

59.4

0.52 (0.35, 0.76)

1.00 (Ref)

About the Authors

73.8

1.00 (Ref)

1.80 (1.33, 2.44)

8 (5–13)

1.07 (1.03, 1.11)

1.08 (1.05, 1.10)

69 (61–72)

1.01 (1.00, 1.02)

1.01 (1.00, 1.02)

Angela Robertson Bazzi is with the Department of Community Health Sciences, Boston University School of Public Health, Boston, MA. Debra S. Whorms, Dana S. King, and Jennifer Potter are with Fenway Health, Boston. Jennifer Potter is also with the Harvard Medical School, Boston. Correspondence should be sent to Jennifer Potter, MD, Fenway Health, 1340 Boylston St, Boston, MA 02215 (e-mail: [email protected]). Reprints can be ordered at http://www.ajph.org by clicking the “Reprints” link. This article was accepted July 26, 2015.

Characteristic

Private Appointments kept, past 3 y, median (IQR) Provider’s patients who were female, % (IQR) Gender identity, no. (%) Cisgender female

1.00 (Ref)

1.00 (Ref)

Transwomen

863 (72.7) 28 (54.9)

0.46 (0.24, 0.85)

0.53c (0.31, 0.91)

Transmen Sexual orientation

13 (50.0)

0.37 (0.13, 1.12)

NA

Heterosexual/straight

244 (74.5)

1.00 (Ref)

Lesbian/gay/homosexual

124 (79.0)

1.28 (0.91, 1.80)

21 (61.8)

0.55 (0.27, 1.12)

Other/don’t know

32 (62.7)

0.57 (0.38, 0.86)

Missing/unknowne

483 (70.0)

0.78 (0.51, 1.21)

d

Bisexual

1.00 (Ref) 0.56 (0.34, 0.92) 0.68 (0.30, 1.20)

Note. AOR = adjusted odds ratio; CI = confidence interval; IQR = interquartile range; NA = not applicable; OR = odds ratio. The sample size was n = 1263. a From unadjusted (bivariable) logistic regression models with clustered standard errors for patients with the same providers. b Private insurance was the reference in the unadjusted analysis and public insurance was the reference in the adjusted analysis. c Transwomen and men were combined into 1 category for the adjusted model. d Bisexual (self-identified bisexual orientation or reported having both male and female sexual partners) vs heterosexual/ straight or lesbian/gay/homosexual for the adjusted model. e Missing/unknown vs heterosexual/straight or lesbian/gay/homosexual for the adjusted model.

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to rates among natal males. Large prospective studies are needed to inform screening recommendations and identify mammography barriers among transgender individuals. We also found that bisexual women were less likely to adhere to mammography guidelines. We combined sexual identity and behavior data to identify sexual minority women as completely as possible in light of recent research highlighting how important health disparities can be missed when reported identity or behaviors alone are relied on.16,17 Because elevated breast cancer incidence among sexual minority women1 has not been fully explained by differences in insurance coverage, 2,3 additional investigation is needed to elucidate why mammography services are underutilized in this population.

Although our data were self-reported, incomplete, and cross-sectional, we were able to control for statistically significant patientand provider-level characteristics, which also yielded important findings. We found that older, privately insured patients and those who kept more appointments were more likely to adhere to mammography guidelines, suggesting a need for outreach to patients with lower financial stability or health care engagement. In addition, we identified a trend that having providers with higher percentages of female patients was associated with a small, although not statistically significant (P = .099), increase in the likelihood of mammography adherence, which may relate to provider---patient communication and suggests a need for continuing education on current screening guidelines. Our study represents a first attempt at understanding suboptimal mammography

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Contributors A. Robertson Bazzi contributed to the idea for this study and conducted the analysis. D. S. Whorms and D. S. King contributed to data collection and management. J. Potter originated the idea for this study. All authors wrote and edited the article.

Human Participant Protection The institutional review board of Fenway Health approved study protocols.

References 1. Meads C, Moore D. Breast cancer in lesbians and bisexual women: systematic review of incidence, prevalence and risk studies. BMC Public Health. 2013;13: 1127. 2. Buchmueller T, Carpenter CS. Disparities in health insurance coverage, access, and outcomes for individuals in same-sex versus different-sex relationships, 2000---2007. Am J Public Health. 2010;100 (3):489---495. 3. Cochran SD, Mays VM, Bowen D, et al. Cancerrelated risk indicators and preventive screening behaviors among lesbians and bisexual women. Am J Public Health. 2001;91(4):591---597. 4. Austin SB, Pazaris MJ, Nichols LP, Bowen D, Wei EK, Spiegelman D. An examination of sexual orientation group patterns in mammographic and colorectal screening in a cohort of U.S. women. Cancer Causes Control. 2013;24(3):539---547. 5. 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---979. 6. Center of Excellence for Transgender Health. Primary Care Protocol for Transgender Patient Care. San Francisco, CA: Department of Family and Community Medicine, University of California; 2011. 7. Hembree WC, Cohen-Kettenis P, Delemarre-van de Waal HA, et al. Endocrine treatment of transsexual persons: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2009;94(9):3132---3154.

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8. Guidelines and Protocols for Comprehensive Primary Care for Trans Clients. Toronto, Ontario, Canada: Sherbourne Health Centre; 2009. 9. Coleman EC, Bockting W, Botzer M, et al. Standards of care for the health of transsexual, transgender, and gender-nonconforming people, version 7. Int J Transgend. 2012;13(4):165---232. 10. National Committee for Quality Assurance. Healthcare effectiveness data and information set (HEDIS). 2012. Available at: http://www.ncqa.org. Accessed August 3, 2015. 11. Rabe-Hesketh S, Skrondal A. Multilevel and Longitudinal Modeling Using STATA. 2nd ed. College Station, TX: Stata Press; 2008. 12. Greenland S. Modeling and variable selection in epidemiologic analysis. Am J Public Health. 1989;79 (3):340---349. 13. Akaike H. A new look at the statistical model identification. IEEE Trans Automat Contr. 1974;19 (6):716---723. 14. Phillips J, Fein-Zachary VJ, Mehta TS, Littlehale N, Venkataraman S, Slanetz PJ. Breast imaging in the transgender patient. AJR Am J Roentgenol. 2014;202(5): 1149---1156. 15. Gooren LJ, van Trotsenburg MA, Giltay EJ, van Diest PJ. Breast cancer development in transsexual subjects receiving cross-sex hormone treatment. J Sex Med. 2013;10(12):3129---3134. 16. Matthews DD, Blosnich JR, Farmer GW, Adams BJ. Operational definitions of sexual orientation and estimates of adolescent health risk behaviors. LGBT Health. 2014;1(1):42---49. 17. Midanik LT, Drabble L, Trocki K, Sell RL. Sexual orientation and alcohol use: identity versus behavior measures. J LGBT Health Res. 2007;3(1):25---35. 18. Cahill S, Singal R, Grasso C, et al. Do ask, do tell: high levels of acceptability by patients of routine collection of sexual orientation and gender identity data in four diverse American community health centers. PLoS One. 2014;9(9):e107104.

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American Journal of Public Health | November 2015, Vol 105, No. 11

Adherence to Mammography Screening Guidelines Among Transgender Persons and Sexual Minority Women.

We used retrospective (2012-2013) chart review to examine breast cancer screening among transgender persons and sexual minority women (n = 1263) atten...
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