Breast Cancer Screening Referral Patterns and Compliance in Transgender Male Patients

Abstract

Purpose:

Screening guidelines for breast cancer (BC) in transgender male (TM) patients are not well defined. This study describes referral patterns and compliance with referral for BC screening among TM patients receiving care at a tertiary care center.

Methods:

This was a retrospective cohort study of TM patients, 40–74 years of age, presenting for care between 2017 and 2020. The electronic medical record was queried for medical history and cancer screening data. Compliance with referral and screening was defined as occurring within 2 years of when screening would be expected.

Results:

Of the 266 patients identified, 45 met inclusion criteria. One (2.2%) had a history of BC, 0 (0%) had hereditary BC risk, and 11 (24.4%) had a family history of BC. Of the patients, 18 (40%) were referred for BC screening, of whom 13 (72.2%) were compliant with screening. Ten (55.6%) were referred by a primary care provider, 2 (11.1%) were referred by a transgender medicine specialist, and 6 (33.3%) were referred by both. Of the cohort, 27 (60%) had undergone masculinizing mastectomy. Six (22.2%) of these patients were referred for screening, of whom 0 (0%) had pre-screening clinical findings indicating need for screening. Of the 18 (40%) patients who had not undergone masculinizing mastectomy, 12 (66.7%) were referred for BC screening.

Conclusions:

There was heterogeneity in referral patterns for BC screening between TM patients who had undergone masculinizing mastectomy and those who had not. BC screening guidelines should be established for TM patients who have undergone masculinizing mastectomy.

Introduction

It is estimated that ∼1.3 million adults in the United States identify as transgender.¹ Transgender males (TM), or those who were assigned female at birth, but identify as male, have specific health care needs that persist throughout their unique transition journeys.² Some TM patients choose to pursue transition, or “gender-affirming” therapies. These include testosterone hormonal therapy and surgical masculinization procedures such as “top surgery” (subcutaneous mastectomy or chest contouring), “bottom surgery” (phalloplasty, metoidioplasty, hysterectomy, and oophorectomy), or facial masculinization.^3–5 However, several barriers to health care exist, which can limit access to hormonal or surgical therapies, and thus, many TM maintain their natal female organs.^6,7 Recommendations for general health screening and maintenance for TM should be individualized based upon the organs present rather than labeled gender identity. For TM, cancer screening for present gynecologic organs and breast cancer (BC) is especially essential.^6,7

It is estimated that ∼1.3 million adults in the United States identify as transgender.¹ Transgender males (TM), or those who were assigned female at birth, but identify as male, have specific health care needs that persist throughout their unique transition journeys.² Some TM patients choose to pursue transition, or “gender-affirming” therapies. These include testosterone hormonal therapy and surgical masculinization procedures such as “top surgery” (subcutaneous mastectomy or chest contouring), “bottom surgery” (phalloplasty, metoidioplasty, hysterectomy, and oophorectomy), or facial masculinization.^3–5 However, several barriers to health care exist, which can limit access to hormonal or surgical therapies, and thus, many TM maintain their natal female organs.^6,7 Recommendations for general health screening and maintenance for TM should be individualized based upon the organs present rather than labeled gender identity. For TM, cancer screening for present gynecologic organs and breast cancer (BC) is especially essential.^6,7

The risk of BC in TM and how the different types of transition therapies impact this risk are not well characterized. BC screening guidelines for TM differ between various organizations, and little is known about compliance with screening referrals in the TM population. For example, the U.S. Preventive Services Task Force (USPSTF) recommends that TM, like cis-women, have BC screening, between the ages of 50–74, every 2 years regardless of the presence or absence of masculinizing mastectomy.^3,8,9 The American College of Radiology (ACR), on the other hand, has recently published guidelines for BC screening in TM patients stratified by risk based on the presence of masculinizing surgery and medical history.^10,11 Such stratification is especially important in the setting of chest contouring surgery and/or masculinizing mastectomy as residual breast tissue may pose a risk for BC.^12–14

Much of the nuanced discussion regarding BC risk and screening recommendations remains the responsibility of individual providers to determine in partnership with their patients. We currently know very little about what happens in actual practice with regard to BC screening. Therefore, the primary objective of this study is to describe patterns of referral for BC screening as well as compliance with screening recommendations in a TM population seeking care at a tertiary care center.

Materials and Methods

Study design

This was a retrospective cohort study of all TM patients who presented for care at the LGBTQ+ center at the Cleveland Clinic Foundation (CCF), a tertiary care referral center, between January 1, 2017, and December 31, 2020. Consent was not required for this exempt protocol that was approved by CCF's Institutional Review Board.

Inclusion and exclusion criteria

Patients were identified by the International Statistical Classification of Diseases and Related Health Problems 10th revision (ICD-10) codes for transsexualism, gender dysphoria, other gender identity disorder, and gender identify disorder (unspecified). The electronic medical record (EMR) was queried for inclusion criteria. Patients between the ages of 40 and 74, who were assigned female at birth and identify as male, were included. These criteria included patients eligible for BC screening per both the USPSTF and the American College of Obstetricians and Gynecologists (ACOG) guidelines for cisgender women.^9,15 Patients were excluded if they were determined to be either cisgender females (patients who were assigned female at birth and also identify as female) or transgender females (patients who were assigned male at birth, but identify as female).

Data collection

All data were collected and stored in a secure REDCap database.¹⁶ Patient characteristics, including age, race, medical insurance type, body mass index (BMI), and smoking history, were recorded. History of masculinization therapy, including gender-affirming hormone therapy and surgical therapy, was recorded. This included masculinizing mastectomy, hysterectomy, salpingectomy/oophorectomy, vaginectomy, phalloplasty, fascial masculinization therapy, and body masculinization therapy.

Up-to-date referral for BC screening was defined as having a referral placed in the EMR for a mammogram or breast ultrasound within the last 2 years. The specialty of the provider placing the referral was noted. Compliance with BC screening was defined as having completed either a mammogram or breast ultrasound within the last 2 years. For those patients who had a mammogram, the Breast Imaging-Reporting and Data System (BI-RADS) score was recorded. Compliance with colon and cervical cancer screening guidelines per the USPSTF was also noted for those patients who met eligibility criteria.

Statistical analysis

This was a descriptive study. Categorical variables were presented as n (%) and continuous variables were presented as mean±standard deviation (SD). We used JMP v15.0 (SAS Institute, Inc., Cary, NC) as our statistical package to perform these analyses. No comparison was made.

Results

Of the 266 patients identified and screened, 45 patients met our inclusion criteria. A large majority of patients excluded (n=211, 95.5%) were male-to-female transgender patients. The remainder of excluded patients was identified by one of the four utilized ICD-10 diagnoses, but their identities did not align with TM. Table 1 demonstrates patient characteristics. The mean age of the cohort was 50.7 (SD 8.1) years and BMI was 30.5 (SD 6.5) kg/m². The majority of patients were of Caucasian race (n=33, 73.3%), and insurance types were equally distributed between private (n=22, 48.9%) and government (n=22, 48.9%) insurance. Twenty-seven patients (60%) had a history of smoking. One patient (2.2%) had a past medical history of BC, and 11 patients (24.4%) had a family history of BC. No (n=0) patient (0%) in our cohort underwent genetic testing for hereditary risk for BC.

Table 1.

Demographics and Medical History of Transgender Male Patients Eligible for Breast Cancer Screening (n=45)

Characteristic	N (%) or mean (SD)
Age	50.7 (8.1)
Race
Caucasian	33 (73.3)
African American	5 (11.1)
Hispanic or Latino	1 (2.2)
Other	6 (13.3)
Insurance type
Private	22 (48.9)
Medicaid/Medicare	22 (48.9)
Other	1 (2.2)
BMI (kg/m2)	30.5 (6.5)
History of smoking	27 (60)
Personal history of breast cancer	1 (2.2)
Family history of breast cancer	11 (24.4)
Tested for hereditary breast cancer risk	0 (0)
Use of gender-affirming hormone therapy	43 (95.6)
History of masculinization surgery	36 (80)
Type of masculinization surgery
Mastectomy	27 (60)
Hysterectomy	27 (60)
Salpingectomy and/or oophorectomy	16 (35.6)
Vaginectomy	2 (4.4)
Phalloplasty	9 (20.0)
Facial masculinization	0 (0)
Body masculinization	0 (0)

BMI, body mass index; SD, standard deviation.

With regard to masculinization therapy, 43 patients (95.6%) had a history of gender-affirming hormone therapy use, and 36 patients (80%) had undergone some form of masculinization surgery. More specifically, 27 patients (60%) had a masculinizing mastectomy, 27 patients (60%) had a hysterectomy, 16 patients (35.6%) had a salpingectomy and/or oophorectomy, 2 patients (4.4%) had a vaginectomy, and 9 patients (20.0%) had a phalloplasty.

Table 2 demonstrates screening data for our cohort. Thirty-five (83.3%) were seen by a family medicine or internal medicine physician within the last 2 years. Twenty-eight patients (73.7%) had seen a transgender medicine specialist in the last 2 years. Of the 22 patients eligible for colon cancer screening, 8 patients (36.3%) were up to date on their colonoscopy. Of the 18 patients who did not have a hysterectomy, 10 patients (55.6%) were up to date with cervical cancer screening guidelines.

Table 2.

Cancer Screening Parameters for Eligible Transgender Male Patients

Characteristic	n	n (%)
Follow-up in the past 2 years	45
Primary care provider		35 (83.3)
Transgender medicine specialist		28 (73.7)
Up to date with referral for breast cancer screening	45	18 (40.0)
Referring provider for screening	18
PCP		10 (55.6)
Transgender medicine specialist		2 (11.1)
Both		6 (33.3)
Type of referral	18
Mammogram		16 (88.9)
Mammogram and ultrasound		2 (11.1)
Up to date with cancer screening
Breast cancer	18	13 (72.2)
Colon cancer	22	8 (36.3)
Cervical cancer	18	10 (55.6)

PCP, primary care physician.

With regard to BC screening, 18 patients (40.0%) in our cohort had an up-to-date BC screening referral in the EMR, of which 16 (88.9%) were for a mammogram and 2 (11.1%) were for both a mammogram and ultrasound. Of the 18 patients referred for BC screening, 13 patients (72.2%) were compliant with screening recommendations. Eleven BI-RADS scores were recorded, of which 1 (9.1%) was abnormal (BI-RADS=3) and 2 (18.2%) indicated a need for further evaluation (BI-RADS=0). The majority of patients were referred for BC screening by their primary care physician (n=10, 55.6%), whereas 2 patients (11.1%) were referred by a transgender medicine specialist and 6 patients (33.3%) were referred by both.

We further analyzed referral patterns in our cohort based upon risk for BC after masculinizing mastectomy. Of the 18 patients who did not have a masculinizing mastectomy, 12 (66.7%) were referred for BC screening. Six of the 27 (22.2%) patients who had a masculinizing mastectomy were referred for BC screening. None (n=0, 0%) of these six patients had clinical findings indicating need for further BC evaluation. Table 3 compares the patients with and without masculinizing mastectomy, who were referred for BC screening. Two of 6 (33%) patients with masculinizing mastectomy in comparison to 10 of 12 (83.3%) without masculinizing mastectomy were in compliance with BC screening guidelines.

Table 3.

Patients Referred for Breast Cancer Screening, Comparing Patients With and Without Masculinizing Mastectomy

Characteristic	n	Masculinizing mastectomy, n (%)	n	No masculinizing mastectomy, n (%)
Follow-up in the past 2 years	6		12
Primary care provider		5 (83.3)		12 (100)
Transgender medicine specialist		5 (83.3)		9 (75.0)
Referring provider for screening	6		12
Referred by PCP		3 (50.0)		7 (58.3)
Referred by transgender medicine specialist		2 (33.3)		0 (0)
Both		1 (16.7)		5 (41.7)
Type of referral	6		12
Mammogram		5 (83.3)		11 (91.7)
Mammogram and ultrasound		1 (16.7)		1 (8.3)
Up to date with cancer screening
Breast cancer	6	2 (33.3)	12	10 (83.3)
Colon cancer	2	1 (50.0)	7	4 (57.1)
Cervical cancer	3	3 (100)	7	4 (57.1)

Referral patterns with respect to further risk factors, such as family history of BC and absence of oophorectomy, were analyzed. Of the 11 patients with a family history of BC, 5 (45.5%) were referred for BC screening. Nine of 14 (64.3%) patients who did not have a masculinizing mastectomy or oophorectomy had an up-to-date referral for BC screening. Of the two patients with a family history of BC, who also did not have a masculinizing mastectomy or oophorectomy, 1 (50%) had an up-to-date referral for BC screening.

Discussion

In this retrospective cohort study, the referral rate for BC screening in TM patients was low with only 40% of patients having documentation of BC screening referral in the last 2 years. Those patients who were referred demonstrated a high rate of compliance with screening guidelines. There was significant heterogeneity, however, in referral patterns with regard to patients who had undergone masculinizing mastectomy versus those who had not. These results demonstrate an unmet need to better define the risk of BC in TM patients and standardize the screening guidelines for BC with regard to history of masculinizing mastectomy.

The lifetime risk of BC is 12% in cis-females and 0.1% in cis-males, but BC risk in the TM population is not well described.^17,18 Only few isolated studies have reported cases of BC in TM since 2003.^3,17–19 The degree to which masculinizing therapies impact BC risk in the TM population is unknown. In our cohort, nearly all (95.6%) the patients had exposure to gender-affirming hormone therapy, and over half (60%) had a history of masculinizing mastectomy. Gender-affirming hormone therapy is hypothesized to have a protective role for BC in TM.^5,20–23 A nationwide retrospective cohort study in the Netherlands found a decreased risk of BC in TM, who used gender-affirming hormone therapy in comparison to cis-females.¹⁷ However, the role of gender-affirming hormone therapy on the development and progression of androgen receptor-positive BC is a potential consideration.¹⁸

Mastectomy is protective against BC in all populations with at least 90% risk reduction reported in studies of cis-females undergoing risk-reducing mastectomy.^24,25 Major organizations, such as the USPSTF and ACOG, have not established specific guidelines for BC screening in TM, especially those with masculinizing mastectomy.^9,26–28

Recently published ACR Appropriateness Criteria on Transgender Breast Cancer Screening indicates that TM patients with masculinizing reduction mammoplasty or no chest surgery should follow BC screening guidelines for cis-females. The recommendations also state that TM patients with masculinizing mastectomy do not require BC screening in the form of imaging, but there is no clear guideline for what type of screening these patients should have.¹⁰ Residual breast glandular tissue is not only found after chest contouring surgery but also after all types of mastectomy, and isolated incidents of BC after masculinizing mastectomy in TM have been reported, demonstrating that the oncologic risk in this population is not zero.^{12–14,18,29–33}

One approach for BC screening in TM with masculinizing mastectomy is through breast examinations, referring those patients with pre-screening clinical findings for further imaging such as ultrasound. For cis-females, ACOG recommends clinical breast examinations every 1–3 years in patients 25–39 years of age and annually in patients 40 years of age and older.¹⁵ However, there are conflicting reports on their efficacy in decreasing mortality from BC. Further, breast examinations may result in increased false positive findings, leading major organizations such as the National Comprehensive Cancer Network, American Cancer Society, and USPSTF to provide differing guidance.^9,15,34

There is also insufficient evidence to demonstrate the efficacy of breast examinations in TM with masculinizing mastectomy.^27,28 In our cohort, 22.2% of patients with masculinizing mastectomy were referred for BC screening in the form of a mammogram and/or ultrasound, but none (0%) of these patients was referred due to clinical findings. There is a need to clarify recommendations for BC screening in TM with masculinizing mastectomy and to examine the efficacy of clinical breast examinations and imaging in this population.

As mentioned above, one in five patients in this study were referred for BC screening in the setting of previous masculinizing mastectomy. There are likely several reasons for this over-referral of patients. The World Professional Association for Transgender Health EMR Working Group highlights the need for accurate documentation of preferred names, pronouns, sex/gender designation, and organ inventory for transgender patients to properly refer patients for screening.³⁵ However, some of these referrals were made through reflex systems built in the EMR based upon sex assigned at birth, not gender identity and organ inventory, due to inaccurate documentation.

In addition, this referral pattern may be attributed to provider's lack of knowledge, which has been reported as a barrier to health care access for many patients who identify as lesbian, gay, bisexual, transgender, queer and questioning (LGBTQ+).^36–38 For example, a survey in 2015 of 352 obstetricians and gynecologists found that only 29% of providers reported comfort with caring for female-to-male transgender patients.³⁶ Similarly, a recent survey of breast radiologists indicated that a majority of providers had minimal confidence and training in caring for LGBTQ+ populations, and 65% did not provide screening recommendations for TM patients.³⁹ In our cohort, of those patients referred for screening, only 33.3% of patients with mastectomies versus 83.3% of patients without mastectomies were in compliance with their referrals. This may indicate that TM patients are well informed about their BC screening needs, despite the health care barriers that they face.

Although there are few adverse effects from mammograms themselves, BC screening carries a low risk of recall for additional imaging or recommendation for biopsy that results in benign findings.¹¹ In our cohort, 9.1% of patients had abnormal findings on mammogram, and 18.2% of patients required further evaluation per the reported BI-RADS scores. The psychological harm caused from overscreening in this population is hard to quantify. Patients of the LGBTQ+ population face challenges such as refusal of care, harassment, mistreatment, and stigma from health care providers.^40–42 Recognition as a transgender patient is an independent predictor of experiencing discrimination in the workplace.⁴³ Importantly, BC screening is in conflict with TM gender identity, potentially enhancing psychological harm.⁴⁴ Such factors may contribute to low overall compliance with cancer screening in this cohort.

Previous data indicate that cervical and colorectal cancer screening rates are lower in transgender patients in comparison to cis-patients. In the United States, compliance with colorectal cancer screening is greater than 50%, and nearly 80% of patients are compliant with cervical cancer screening.⁴⁵ In our cohort, only 8 of 22 patients (36.3%) eligible for colorectal cancer screening and 10 of 18 patients (55.6%) eligible for cervical cancer screening were in compliance with USPSTF screening guidelines. A large majority of our cohort had follow-up with a primary care provider (83.3%) or transgender health specialist (73.7%) during the study period, indicating that these low rates of screening compliance are unlikely to be explained by lack of follow-up.

The intersectionality of race and gender may also contribute to disparities in cancer screening. Although rates of colon, cervical, and BC screening are relatively similar between different races in the total U.S. population, the discrimination encountered by transgender patients is not captured in this data.^45,46 In our cohort, similar compliance with colorectal cancer screening was noted for eligible Caucasian (n=6, 35.3%) and non-Caucasian (n=2, 40.0%) patients. Unexpectedly, fewer Caucasian patients in comparison to non-Caucasian patients were in compliance with cervical (n=6, 42.9% vs. n=4, 100%) and breast (n=6, 54.5% vs. n=7, 100%) cancer screening recommendations. These findings are limited by our sample size, and future studies should explore race along with additional factors such as lack of physician awareness, stigma, and mistreatment in the health care setting to increase rates of all cancer screening in this population.^36,47

Limitations

The retrospective design of our study has inherent limitations with regard to data collection through the EMR. Further, we present data from a tertiary care hospital with a specialized LGBTQ+ center. Our results may not be generalizable to rural or nonacademic practices. Our study is also limited by a small sample size. No comparison was made to identify potential factors that contribute to BC referral patterns and screening compliance, including the impact of racial disparities in the TM population. However, our study is the first we know that explores referral patterns for BC screening in a TM population. We highlight the heterogenous referral patterns within our practice between TM patients with different levels of BC risk dependent on history of masculinizing mastectomy.

Conclusions

Our study provides an additional perspective in a small, but growing body of literature regarding BC screening guidelines for TM patients. Overall, the referral rates for BC screening in our cohort were lower than expected, and there was heterogeneity in referral rates between TM patients with and without masculinizing mastectomy. Referral for BC screening in patients without masculinizing mastectomy was higher than that for patients with masculinizing mastectomy. Although most major organizations are in agreement about screening guidelines for TM without masculinizing mastectomy, there are no current BC screening guidelines for TM with masculinizing mastectomy. BC screening guidelines must be standardized for TM patients with masculinizing mastectomy, especially elaborating on the utility of clinical breast examination to inform further decision making for TM patients.

Abbreviations Used

ACOG

American College of Obstetricians and Gynecologists

ACR

American College of Radiology

BC

breast cancer

BI-RADS

Breast Imaging-Reporting and Data System

BMI

body mass index

CCF

Cleveland Clinic Foundation

EMR

electronic medical record

ICD-10

International Statistical Classification of Diseases and Related Health Problems 10th revision

PCP

primary care physician

SD

standard deviation

TM

transgender male

USPSTF

U.S. Preventive Services Task Force

Authors' Contributions

S.T.: investigation, writing—original draft, and visualization. C.A.F.: conceptualization, methodology, formal analysis, writing—review and editing, and supervision.

Author Disclosure Statement

The authors declare no conflicts of interest.

Funding Information

The authors report no financial or material support.

Cite this article as: Tewari S, Ferrando CA (2024) Breast cancer screening referral patterns and compliance in transgender male patients, Transgender Health 9:2, 136–142, DOI: 10.1089/trgh.2022.0069.