Wo m e n ’s I m a g i n g • R ev i ew Phillips et al. Breast Imaging in the Transgender Patient

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Women’s Imaging Review

Breast Imaging in the Transgender Patient Jordana Phillips1 Valerie J. Fein-Zachary Tejas S. Mehta Nancy Littlehale Shambhavi Venkataraman Priscilla J. Slanetz

OBJECTIVE. Limited information exists regarding breast health in the transgender population. In this article, we review transgender terminology, barriers faced by transgender patients, current breast care screening recommendations, and normal and abnormal imaging findings in this population. CONCLUSION. Health disparities in the transgender population continue. Educating physicians on the breast health care needs of transgender patients is important for improving their care.

Phillips J, Fein-Zachary VJ, Mehta TS, Littlehale N, Venkataraman S, Slanetz PJ

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imited information exists regarding breast health in the transgender population primarily owing to historical bias throughout the health care system [1]. As a consequence, there are essentially no scientific publications attending to the specific needs of this patient demographic. The Institute of Medicine, in their March 2011 report [1], and Healthy People 2020, a U.S. government–sponsored 10-year agenda for improving the nation’s health, have included the health of transgender people as a major goal. In this article, we clarify the use of transgender terminology, identify barriers faced by transgender patients, review current screening recommendations, and discuss normal breast findings and common breast pathology in this population. Keywords: breast imaging, transgender DOI:10.2214/AJR.13.10810 Received February 22, 2013; accepted after revision August 14, 2013. 1  All authors: Beth Israel Deaconess Medical Center, Harvard Medical School, 330 Brookline Ave, Boston, MA 02215. Address correspondence to J. Phillips ([email protected]).

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Terminology Provider education is crucial to eliminate stigma, improve access, and provide quality care. Of utmost importance is the use of correct terminology, which can be confusing because it is constantly changing. According to the “Standards of care for transsexual, transgender, and gender-nonconforming people, version 7,” “transgender” is an umbrella term “to describe a diverse group of individuals who cross or transcend culturally defined categories of gender” [2]. There is debate, however, as to whom to include within this group: some include transsexuals and cross-dressers; others include

any individual who identifies with a gender aside from male or female, for example, those with no gender identity or those who identify with both male and female. The focus of this review will be on transgender patients who identify with the gender opposite their natal sex, some of whom have altered their bodies with hormones, silicone injections, surgery, or a combination thereof. Some might refer to this subgroup as transsexual; however, given the wide variability in patient presentation and self-identification, we have chosen to use the following terminology: “transgender women,” referring to patients transitioning from male to female; and “transgender man,” referring to those transitioning from female to male. It is important to check with the patient to ensure that you are using the patient’s preferred gender identity and pronouns. Some of the more commonly used terminology in clinical practice is included in Appendix 1. Barriers to Health Care Transgender patients face a number of barriers to quality health care most of which relate to the stigma associated with being transgender [1]. One of the primary barriers relates to social stigma. This refers to the perceived inferior status of the transgender population and may be overtly expressed or implied through subtle behaviors. The National Transgender Discrimination Survey recently collected data from 6,450 self-identified transgender and

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Phillips et al. gender-nonconforming people around the United States and found that 25% of the studied group experienced some form of harassment in the medical setting [3]. The consequence is that many—reportedly up to 70% of transgender patients—hide their gender identity to avoid discrimination [3]. The challenge of identifying these patients must be met to correctly advise them, particularly in matters relating to breast health, while doing so in a way that does not alienate them. A second barrier involves lack of provider knowledge and training [1]. The National Transgender Discrimination Survey reported that 50% of transgender respondents worked with health care providers who lacked knowledge of their health care needs [3]. A third barrier is lack of sufficient health insurance coverage. As a result of the U.S. system of employer-sponsored health insurance and the higher levels of unemployment and poverty among the transgender population as compared with the general population, many transgender people are uninsured. In addition, because of legal discrimination with regard to relationship status, many transgender people are unable to access insurance through their life partners and spouses. Of those who do have insurance, most plans do not cover sex reassignment treatments or routine screening procedures that are not related to their natal sex [1]. A fourth barrier relates to the layout of physician practices. Many women’s imaging practices, which are designed specifically for women, may not have a comfortable space for natal men and transgender men to wait for examinations. In areas where there is a large transgender population, it may be feasible and desirable to reconfigure the layout of a practice to make it more comfortable for transgender men; however, this may not be practical in all cases. In one of our affiliated facilities with a sizeable transgender clientele, the patients change directly in the mammography room. Importantly, to further improve patients’ comfort, ask how they would prefer to be addressed both by name and by pronoun. If possible, this information should be recorded in the medical record alongside the patient’s legal name and natal sex. In addition, patient questionnaires may need to be reevaluated to ensure that they do not assume any particular gender.

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Transgender Women General Health Concerns Feminizing hormonal therapy primarily includes estrogen and androgen-reducing medications such as spironolactone. The use of progestins is controversial. Some believe it is necessary for full breast development, although studies have not proven this; however, others are concerned with its adverse affects, including an increased breast cancer risk as seen in postmenopausal patients in the Women’s Health Initiative study [2, 4, 5]. This is especially concerning because these patients may be exposed to the combined hormonal therapy from adolescence into later life, beyond the age natal women typically go through menopause. Because none of the breast cancer data registries ask or record a patient’s transgender status, we have no knowledge of the incidence of breast cancer in this population. Only case reports of breast cancer in transgender women currently exist [6–8]. A few studies have evaluated the breast cancer risk in patients taking variable hormone regimens and have not shown an increased risk [9–11]; however, these studies are limited in sample size. One study evaluated the feasibility of mammography in transgender women and showed that mammography and ultrasound are easily achievable [12] but did not measure breast cancer risk. Screening Recommendations Given the limited data, current screening guidelines are as follows: for those patients with a prior or current history of hormone use, annual mammography beginning at 50 years old is recommended if the patient has additional risk factors such as estrogen and progestin use for more than 5 years, body mass index (weight in kilograms divided by the square of height in meters) above 35, and a family history of breast cancer. Clinical breast examinations and self-examinations are recommended for educational pur-

poses only [13]. Screening mammography is not currently recommended for transgender women who are not taking hormones, except in patients with other known risk factors, such as Klinefelter syndrome. Breast augmentation has not been shown to increase a patient’s risk for breast cancer in the natal female population and therefore is not considered likely to increase risk in the transgender population [13, 14] (Table 1). Imaging Findings There are expected physiologic changes that occur in the breasts of a transgender woman after taking hormonal therapy that should not be viewed as pathologic, nor do they warrant additional imaging. Breast tissue will increase over time, reaching maturity by 2–3 years with a more pronounced nipple-areola complex [2] (Fig. 1). Transgender women can develop a spectrum of breast tissue density including heterogeneously dense and extremely dense breast tissue (Fig. 2). The breast tissue that develops should not be referred to as gynecomastia. One study has shown that this tissue more closely resembles breast tissue seen in natal women because it contains lobules [15]. These changes may be associated with clear bilateral non­ spontaneous nipple discharge. If the discharge is unilateral, bloody, or spontaneous, further evaluation may be necessary to exclude other pathology. Diagnostic evaluation of nipple discharge should begin with ultrasound if the patient is younger than 30 years old. Breast augmentation with implants is commonly used as part of sex reassignment surgery and will have the typical appearance of breast implants on mammography. Evaluation for implant rupture is similar to that performed in natal woman, incorporating ultrasound, mammography, and possibly MRI. Some transgender women may opt to have large volumes of liquid silicone injected into their breasts for breast augmentation. The practice of silicone injection for cosmetic use is not condoned in the United States

TABLE 1: Screening Recommendations for Transgender Women Group

Recommendation(s)

Transgender women ≥ 50 years old with past or current hormone use

Annual mammography if the patient has additional risk factors such as estrogen and progestin use for > 5 years, body mass index (weight in kilograms divided by the square of height in meters) > 35, and family history; clinical breast examination recommended only for educational benefit, not for formal cancer screening

Transgender women with no hormone use Routine screening is not indicated unless the patient has other known risk factors, e.g., Klinefelter syndrome

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Breast Imaging in the Transgender Patient and often either takes place illegally or is performed in a foreign country. The mammographic findings vary and may reveal rounded well-defined high-density masses or more-poorly-defined masses some of which may have a calcified rim [16] (Fig. 3). On ultrasound, direct silicone injections often present as echogenic areas with a well-defined superficial border but posterior acoustic shadowing and loss of posterior detail. Sometimes they may appear as hypoechoic or even anechoic masses (Fig. 4). On MRI, these areas will appear dark on T1-weighted fat-suppressed sequences, bright on T2weighted water-suppressed sequences, and bright on dedicated silicone sequences [17]. The dangers of this type of augmentation include disfigurement with hard lumpy breasts as well as complications such as infection, pulmonary embolism, and death [18–20]. It is important to recognize that as breast tissue begins to develop, there may be lobule formation similar to that occurring in natal women. Therefore, entities typically not seen in natal men, such as cysts (Fig. 5) and fibroadenoma, can develop [21, 22]. To our knowledge, there are no published studies discussing the appearance of fibroadenoma in this population, but we have seen two cases at our institution of fibroadenoma in transgender women, which, as one might expect, have a similar imaging appearance to fibroadenoma seen in natal women’s breasts (Fig. 6). Breast cancer, although rare, can occur in transgender women. The appearance may vary as it does in natal women; however, there should be a heightened level of concern for a new palpable mass, especially if the patient has been on hormonal therapy for more than 5 years (Fig. 7). Invasive ductal carcinoma or invasive lobular carcinoma may be seen. Transgender Men General Health Concerns Transgender men who have not had sex reassignment surgery, regardless of whether they take hormonal supplementation, have a similar lifetime risk for breast cancer as natal women of approximately 12.4% [23]. Once a transgender man undergoes bilateral subcutaneous mastectomies with male chest contouring including nipple repositioning as part of sex reassignment surgery, his breast cancer risk dramatically decreases by nearly 90%, as has been shown in natal women with moderate and high risk of breast cancer who had undergone mastectomy [24, 25], although this is still higher than a natal man’s risk [13]. The

TABLE 2: Screening Recommendations for Transgender Men Group

Recommendation(s)

Transgender men who underwent reduction mammoplasty or no chest surgery

Breast examinations and screening mammography are recommended as for natal women

Transgender men after bilateral mastectomy

Yearly chest wall and axillary examinations

Preoperative transgender men

Mammography only if patient meets usual natal female requirements

transgender community more commonly refers to this procedure to as “top surgery.” Although there are a few case reports, studies have not shown an increased risk of breast cancer in transgender men receiving longterm testosterone therapy [1, 26–28]. Screening Recommendations Screening recommendations are made irrespective of the patient’s hormonal supplementation with testosterone. For those who have retained their natal anatomy, annual screening mammography is still recommended beginning at 40 years old for the average-risk patient as for natal women. Screening is similarly recommended if the patient undergoes breast reduction because residual breast tissue remains. However, for those transgender men who have undergone bilateral mastectomies, screening mammography is not indicated [13]. Clinical chest examinations and breast care education are advised because there remains a small possibility that breast cancer may develop in residual breast tissue. Should the patient pursue top surgery, presurgical mammogram is indicated only if the patient meets the usual natal female requirements (Table 2). Imaging Findings The primary imaging findings in transgender men relate to postmastectomy complications, including hematoma and seroma (Fig. 8) and abscess formation (Fig. 9). Imaging-guided drainage may be performed if clinically indicated. Breast cancer in transgender men who have not undergone surgery has the same imaging presentation as in natal women. Breast cancer may occur in residual breast tissue of those patients who underwent bilateral mastectomies and will most commonly be discovered clinically as a palpable mass. Ultrasound and ultrasound-guided biopsy are the preferred diagnostic imaging tests to confirm the diagnosis. Conclusion A number of barriers exist to high-quality breast health care for the transgender pop-

ulation, most of which relate to the stigma associated with being a transgender person. As a result, many individuals may not present to the health care system, and those who do may hide their natal sex, making it more difficult for breast imagers to appropriately treat them. It is important for breast imagers to become more knowledgeable and sensitive to the specific needs of the transgender community so that they may provide better and more individualized care for their patients. This added knowledge will also enable the transgender community to access better health care and to better educate themselves about their own health care needs. References 1. Committee on Lesbian, Gay, Bisexual, and Transgender Health Issues and Research Gaps and Opportunities, Board on the Health of Select Populations, Institute of Medicine. The Health of Lesbian, Gay, Bisexual, and Transgender People: Building a Foundation for Better Understanding. Washington, DC: National Academies Press, 2011 2. Coleman E, Bockting W, Botzer M, et al. Standards of care for the health of transsexual, transgender, and gender-nonconforming people, version 7. Int J Transgenderism 2012; 13:165–232 3. 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: The National Gay and Lesbian Task Force and the National Center for Transgender Equality, 2011 4. Mueller A, Gooren L. Hormone-related tumors in transsexuals receiving treatment with cross-sex hormones. Eur J Endocrinol 2008; 159:197–202 5. Rossouw JE, Anderson GL, Prentice RL, et al.; Writing Group for the Women’s Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial. JAMA 2002; 288:321–333 6. Pritchard TJ, Pankowsky DA, Crowe JP. Breast cancer in a male-to-female transsexual. A case report. JAMA 1988; 259:2278–2280 7. Dhand A, Dhaliwal G. Examining patient conceptions: a case of metastatic breast cancer in an Af-

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Phillips et al. rican American male to female transgender patient. J Gen Intern Med 2010; 25:158–161 8. Ganly I, Taylor EW. Breast cancer in a trans-sexual man receiving hormone replacement therapy. Br J Surg 1995; 82:341 9. van Kesteren PJ, Asscheman H, Megens JA, Gooren LJ. Mortality and morbidity in transsexual subjects treated with cross-sex hormones. Clin Endocrinol (Oxf) 1997; 47:337–342 10. Asscheman H, Giltay EJ, Megens JA, de Ronde WP, van Trotsenburg MA, Gooren LJ. A longterm follow-up study of mortality in transsexuals receiving treatment with cross-sex hormones. Eur J Endocrinol 2011; 164:635–642 11. Wierckx K, Mueller S, Weyers S, et al. Long-term evaluation of cross-sex hormone treatment in transsexual persons. J Sex Med 2012; 9:2641–2651 12. Weyers S, Villeirs G, Vanherreweghe E. Mammography and breast sonography in transsexual women. Eur J Radiol 2010; 74:508–513 13. Makadon HJ, Mayer KH, Potter J. Fenway guide to lesbian, gay, bisexual and transgender health, 1st ed. Philadelphia, PA: American College of Physicians, 2007:3–22, 35–36, 331–392 14. Deapen D, Hamilton A, Bernstein L, Brody GS. Breast cancer stage at diagnosis and survival among patients with prior breast implants. Plast Reconstr Surg 2000; 105:535–540 15. Kanhai RC, Hage JJ, van Diest PJ, Bloemena E, Mulder JW. Short-term and long-term histologic

effects of castration and estrogen treatment on breast tissue of 14 male-to-female transsexuals in comparison with two chemically castrated men. Am J Surg Pathol 2000; 24:74–80 16. Yang N, Muradali D. The augmented breast: a pictorial review of the abnormal and unusual. AJR 2011; 196:249; [web]W451–W460 17. Caskey CI, Berg WA, Hamper UM. Imaging spectrum of extracapsular silicone: correlation of US, MR imaging, mammographic, and histopathologic findings. RadioGraphics 1999; 19(spec no):S39–S51 18. Schoeller T, Gschnitzer C, Wechselfberger G, Otto A, Hussl H, Piza-Katzer H. Chronic recurrent, locally destructive siliconomas after breast augmentation by liquid silicone oil [in German]. Chirurg 2000; 71:1370–1373 19. Parsons RW, Thering HR. Management of the silicone-injected breast. Plast Reconstr Surg 1977; 60:534–538 20. Restrepo CS, Artunduaga M, Carrillo JA, et al. Silicone pulmonary embolism: report of 10 cases and review of the literature. J Comput Assist Tomogr 2009; 33:233–237 21. Kanhai RC, Hage JJ, Bloemana E, van Diest PJ, Karim RB. Mammary fibroadenoma in a male-to-female transsexual. Histopathology 1999; 35:183–185 22. Lemmo G, Garcea N, Corsello S. Breast fibroadenoma in a male-to-female transsexual patient after hormonal treatment. Eur J Surg Suppl 2003; (588):69–71

23. Howlader N, Noone AM, Krapcho M, et al., eds. SEER Cancer Statistics Review, 1975–2009 (Vintage 2009 Populations). Bethesda, MD: National Cancer Institute, 2012 24. Hartmann LC, Schaid DJ, Woods JE, et al. Efficacy of bilateral prophylactic mastectomy in women with a family history of breast cancer. N Engl J Med 1999; 340:77–84 25. Rebbeck TR, Friebel T, Lynch HT, et al. Bilateral prophylactic mastectomy reduces breast cancer risk in BRCA1 and BRCA2 mutation carriers: the PROSE study group. J Clin Oncol 2004; 22:1055–1062 26. Jacobeit JW, Gooren LJ, Schulte HM. Safety aspects of 36 months of administration of long-acting intramuscular testosterone undecanoate for treatment of female-to-male transgender individuals. Eur J Endocrinol 2009; 161:795–798 27. Gooren LJ, Giltay EJ, Bunck MC. Long-term treatment of transsexuals with cross-sex hormones: extensive personal experience. J Clin Endocrinol Metab 2008; 93:19–25 28. Shao T, Grossbard ML, Klein P. Breast Cancer in female-to-male transsexuals: two cases with a review of physiology and management. Clin Breast Cancer 2011; 11:417–419 29. Glossary of gender and transgender terms. Fenway Health website. www.fenwayhealth.org/site/ DocServer/Handout/7-C/Glossary/of/Gender/ and/TransgenderTerms. Published January 2010; Accessed February 10, 2014

APPENDIX 1: Glossary of Transgender Terminology Sex: Designation of a person as male or female at birth, i.e., natal male or natal female, on the basis of anatomic and biologic markers, genitalia, or chromosomes [29]. Gender identity: Identification as man, woman, or something else that may or may not coincide with a person’s natal sex [29]. Gender expression: External manifestation of a person’s gender identity, which may or may not conform to societal norms of masculine and feminine [29]. Gender nonconformity: Differing of a person’s gender identity from the cultural norms prescribed for people of that particular sex [2]. Transgender: Umbrella term describing a diverse group of people who cross culturally defined categories of gender [2]. Gender dysphoria: Distress caused by discrepancy between a person’s gender identity and natal sex [2]. Transsexual: A person whose gender identity and natal sex differ. Transsexuals may medically alter their sex to live life as their identified gender by using hormonal therapy and possibly sex reassignment surgery [2]. Male-to-female (MTF) transsexual: A natal male whose gender identity is female and presents socially as a woman sometimes after medical intervention [13]. Female-to-male (FTM) transsexual: A natal female whose gender identity is male and presents socially as a man sometimes after medical intervention [13].

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Breast Imaging in the Transgender Patient

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Fig. 1—25-year-old transgender woman treated with estradiol 0.5 mg daily and spironolactone 150 mg daily for 1 year. A, Baseline mammogram shows unilateral nipple discharge. B, Follow-up mammogram 6 months later shows increasing retroareolar breast tissue (arrows).

A

A

B

B

Fig. 2—Spectrum of breast tissue density on mammography. A, 43-year-old transgender woman treated with hormonal therapy for 10 years. Mammogram shows heterogeneously dense breast parenchyma. B, 41-year-old transgender woman who received intramuscular injection of estradiol 20 mg once every 2 weeks for 20 years. Mammogram shows dense breast parenchyma.

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Fig. 3—45-year-old transgender woman treated with silicone injections. Mammogram shows resultant innumerable bilateral silicone granulomas.

Fig. 4—41-year-old transgender woman with silicone granulomas. A and B, On ultrasound, some granulomas are hyperechoic superficially with marked posterior shadowing (A), whereas others are hypoechoic masses with variable posterior acoustic enhancement (B).

A

B

Fig. 5—Ultrasound image of 28-year-old transgender woman on hormonal therapy for 1 year reveals fibrocystic changes.

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Breast Imaging in the Transgender Patient

A

B Fig. 6—39-year-old transgender woman on hormonal therapy for 3 years. A, Circumscribed hypoechoic mass with no internal vascularity is shown on ultrasound. B and C, This finding correlates with circumscribed enhancing lesion (arrow, B and C) on MRI that has nonenhancing internal septations (B) and is T2 bright (C), consistent with fibroadenoma.

C

A

B

Fig. 7—50-year-old transgender woman treated remotely with hormonal therapy for 5 years. A, Palpable mass was seen in upper outer left breast on craniocaudal and mediolateral oblique mammographic views. B, This finding correlates with complex cystic mass on ultrasound. Biopsy revealed invasive ductal carcinoma.

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Phillips et al.

Fig. 8—Ultrasound image of 21-year-old transgender man with history of bilateral mastectomy shows postoperative seroma.

Fig. 9—Ultrasound image of 48-year-old transgender man after bilateral breast reduction shows abscess in residual breast tissue.

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Breast imaging in the transgender patient.

Limited information exists regarding breast health in the transgender population. In this article, we review transgender terminology, barriers faced b...
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