- Email: [email protected]
Gynecologic cancer screening in the transgender male population and its current challenges
Maturitas 129 (2019) 40–44
Contents lists available at ScienceDirect
Maturitas journal homepage: www.elsevier.com/locate/maturitas
Gynecologic cancer screening in the transgender male population and its current challenges Jharna M. Patela, Shelley Dolitskya, Gloria A. Bachmana, Alexandre Buckley de Meritensa,b, a b
T
⁎
Department of Obstetrics and Gynecology, Rutgers Robert Wood Johnson Medical School, United States Rutgers Cancer Institute of New Jersey, United States
A R T I C LE I N FO
A B S T R A C T
Keywords: Transgender male Gender nonconforming Gynecologic cancer screening
As the transgender community gains visibility and recognition, healthcare disparities have become more apparent. Reports estimate that 1–1.5 million people belong to this community in the United States. Despite efforts to become more inclusive, access to healthcare is challenging in a system built on a binary model that exacerbates gender dysphoria and on healthcare insurance schemes that do not cover gender affirmation therapy. Another large challenge is the paucity of scientific and medical knowledge when it comes to caring for the transgender community. More research to build knowledge is necessary to provide evidence-based quality care. In an attempt to bring guidance for gynecologic and breast cancer screening for the transgender male population, we conducted a review of the literature published in PubMed. Here, we present a review of the challenges, as well as guidelines for breast, uterus, and cervix screening for the transgender male population.
1. Introduction Recent reports estimate that 1 to 1.5 million people belong to the transgender community in the United States [1]. Unfortunately, national health care databases do not specify gender identification. Instead, the size of the transgender population is extrapolated from smaller state-based and private surveys [2]. As the transgender community gains visibility and recognition, healthcare disparities have become apparent. The transgender community has a disproportionate amount of adverse health care outcomes, and the World Health Organization reports in increased risk for cervical, endometrial, and ovarian cancer [3,4]. In a U.S. national transgender survey, 25% of respondents reported experiencing issues with insurance coverage including care related to gender transition, 23% did not see a physician because of fear of being mistreated and 33% did not see a physician because of cost [5]. Furthermore, several studies have shown significantly less adherence to cancer screening guidelines in the transgender population [6–9].These disparities will not be overcome until we expose the barriers and limitations to care and better understand the needs of this population. The transgender community is diverse and its members are in various stages of transitioning. For those not undergoing gender-affirming intervention or those who have partially transitioned, cancer screening programs are challenging as they may exacerbate body-image
dysphoria. Little is known in the medical literature regarding the interaction between gender-affirming hormonal and surgical therapy and the risk of hormone-dependent and non-hormone dependent malignancies (breast, ovary, uterus) [10,11]. Current guidelines are of low level of evidence and mainly based on expert opinions [11–14]. In this narrative review we examine cancer screening (breast, cervix, uterus) recommendations and its barriers for transgender men. 2. Methods A literature review was conducted searching the PubMed electronic database. We used the following combinations of Medical Subject Heading (MeSH) terms: "Transgender Persons" and "Neoplasms", "Transgender Persons" and "Early Detection of Cancer", "Transgender Persons" and "Breast Neoplasms", "Transgender Persons" and "Uterine Cervical Neoplasms", and "Transgender Persons" and "Uterine Neoplasms." We did not limit our search to a specific timeframe. The combination of terms resulted in 185 results. Out of the 185 articles, 87 duplicates were removed, 57 were removed after reviewing and determining lack of relevance (pertaining to male-to-female transgender patients, not pertaining to cancer), and 6 were unavailable. These articles included case reports, epidemiologic studies, and review articles. Articles referenced in these retrieved articles were examined and included as secondary references if they were noted to be relevant.
⁎
Corresponding author at: Department of Obstetrics and Gynecology, Rutgers Robert Wood Johnson Medical School, United States. E-mail addresses: [email protected] (J.M. Patel), [email protected] (S. Dolitsky), [email protected] (G.A. Bachman), [email protected] (A. Buckley de Meritens). https://doi.org/10.1016/j.maturitas.2019.08.009 Received 8 June 2019; Received in revised form 25 July 2019; Accepted 19 August 2019 0378-5122/ © 2019 Elsevier B.V. All rights reserved.
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Table 1 Screening guidelines for cisgender Females. Type of Cancer
Recommendations
Breast Cancer
Clinical Exams Clinical Breast Exam
Mammography
Cervical Cancer
Uterine Cancer
Ovarian Cancer
Vulvar Cancer
Population < 21 years of age 21-29 years of age 29-65 years of age
Recommendations for average risk patients [41] May be offered every 1-3 years in context of shared decision making to patients age 25-39 and annually in women > 40 years of age. Recommended yearly in patients who have underwent mastectomies and are no longer receiving mammograms. Start at age 40 or initiate from age 40-49 but no later than age 50. Screening interval annually or biennially. Continue until age 75 and screening after age 75 should be based on shared decision-making process. Recommendations [43] No Screening Cervical cytology alone every 3 years Cervical cytology alone every 3 years OR hrHPV testing alone every 5 years OR Cervical cytology and hrHPV testing every 5 years No screening
Women age > 65 years or have had hysterectomy with removal of cervix with no history of high-grade lesion or cervical cancer Patients who are not at high risk (have germ line mutations such as Lynch Syndrome) should not be routinely screened with transvaginal ultrasound [45]. Patients who are high risk can undergo annual screening with transvaginal ultrasound and endometrial biopsy. Prophylactic hysterectomies can be discussed on a case by case basis [45]. Clinical Exams Recommendations for average risk patients [46] Transvaginal Screening with ultrasounds not recommended at this time due to decreased PPV and increased false positive rates. Ultrasound Cancer Antigen 125 Tumor Marker No current evidence of a single cutoff value that has acceptable PPV or sensitivity to be used for a screening test. There is no current screening examination recommended for the detection of vulvar cancer [44]. Detection is made by clinical inspection with biopsy to confirm the diagnosis [44].
• •
• •
these patients, screening recommendations are made irrespective of the patient’s hormonal therapy history [23]. For patients that have not undergone top surgery, the breast cancer screening recommendations are the same as cisgender women. For women who have undergone gender affirming surgery, recommendations for screening are not well established [23]. Top surgery involves bilateral nipple sparing mastectomies, which commonly leave residual breast tissue, including the nipple areolar complex. In one anatomic study on cadavers, ductal tissue remained in 83% of patients [24]. Prior to the procedure, patients should meet with their doctor to discuss if they fall into the high-risk category. Patients identified as high-risk could consider more complete mastectomies including nipple areolar grafts to further reduce their risk of cancer [15,25]. Even with this surgery however, the risk of cancer drops only 90% and therefore screening is still important [26]. Mammograms do not have much utility in this population, but these patients should be followed with yearly clinical breast exams of the chest wall and axilla, and with ultrasounds of any palpable lesions [23,24,27].
Additionally, separate searches were conducted by using PubMed and American College of Obstetrics and Gynecology website to find incidence and prevalence of cancers in the cisgender population. 3. Screening guidelines Table 1 summarizes recommendations on screening. 3.1. Breast cancer screening Breast cancer is the most common cancer in women and the second leading cause of cancer mortality in the United States. The incidence of breast cancer in women is 1 in 8, or 12.4%. The risk of breast cancer in men is 1 in 833, or 0.12%. Risk factors for breast cancer in the general population include: age, personal history of breast cancer, family history, genetics, radiation to chest or face before age 30, white race, obesity, nulliparity, early menarche, late menopause, use of HRT, alcohol, dense breast tissue, lack of exercise, and smoking [13]. For female to male (FtM) transgender patients, the incidence of breast cancer is not well defined [14,15]. The incidence of breast cancer in patients who have not undergone gender affirming breast surgery (“top surgery”) is thought to be similar to cisgender females, however the incidence of breast cancer in patients who are status post mastectomies is unknown [15]. The reports of transgender men with breast cancer are limited to case reports only, and long-term data is very limited [16,17]. Risk factors in this population are similar to the cisgender female population, with the addition of irregular screening. The effect of hormonal therapy on breast cancer risk has not been well established [18]. The role of testosterone supplementation is unknown, though some hypothesize that high circulating androgens may increase the risk of breast cancer. A proposed mechanism for this is the aromatization of testosterone to estrogens in peripheral tissues, leading to an increased estrogen exposure. Another possible mechanism is the activation of androgen receptors that lead to cellular growth and proliferation in mammary tissues [18–21]. Because these theories are based on low level evidence, and no studies have been able to adequately demonstrate an increased risk in
3.2. Cervical cancer Cervical cancer is the fourth most common cancer in women and is a leading cause of morbidity and mortality worldwide. In 2015 the CDC reported 12,845 new cases of cervical cancer and estimated that 4210 women died from this disease [28,29]. Due to the introduction of screening methods, namely the papanicolaou (PAP) smear and Human Papilloma Virus (HPV) testing, the incidence of cervical cancer has decreased in the past 40 years [30] and currently it is estimated that 43% of the U.S. adult cisgender female population undergoes routine pap smear testing [31]. In contrast, the National Transgender Survey found that of the FtM patients who still have a cervix, only 27% had reported that they had undergone routine pap smear testing [31]. Many transgender individuals chose to not undergo routine gynecological examinations due to heightened sense of conflict between gender identity and physical anatomy [31]. This population has a decreased rate of reported high-risk HPV infection (hrHPV) despite high-risk behaviors, a misrepresentation attributable to decreased routine screening. Studies have shown that there is an underreporting of cases 41
Maturitas 129 (2019) 40–44
J.M. Patel, et al.
Table 2 Current screening guidelines for FtM transgender patients. Type of Cancer
Recommendations
Breast Cancer
Clinical Exams Breast Examinations
Cervical Cancer
Uterine Cancer Ovarian Cancer Vulvar Cancer
Recommendations for average risk patients [41] For patients who have not undergone top surgery, breast examinations may be offered every 1-3 years. Examinations should include axilla and chest wall. Mammography Limited utility of mammograms. Population Recommendations [41,42] < 21 years of age No Screening 21-29 years of age Cervical cytology alone every 3 years 29-65 years of age Cervical cytology alone every 3 years OR hrHPV testing alone every 5 years OR Cervical cytology and hrHPV testing every 5 years Patients who have neovaginas Need to undergo routine cervical cancer screening with insurance of appropriate cytology collection. No routine screening recommendations in low or high risk patients. No routine screening recommendations in low or high risk patients No routine screening recommendations in low or high risk patients.
• • •
menopausal women [39]. When a transvaginal ultrasound is required for diagnosis, a transrectal or transabdominal ultrasound should be discussed as a transvaginal probe may cause emotional trauma. As it stands, it is recommended to have open-dialogue with patients regarding recognition of abnormal uterine bleeding in FtM patients who have amenorrhea either secondary to hormone therapy or have undergone hysterectomies. Providing culturally competent care is crucial in making this subset of patients feel comfortable presenting with their gynecological concerns so that early detection and treatment of endometrial cancer can be pursued.
of cervical cancer in this population due to decreased access to healthcare, negative health care experiences, discrimination, and refusal of health services [31,32]. There are several considerations that can help improve rates of screening and routine follow up in the FtM patients and increase comfort during gynecological examinations [33,35]. Recent studies have shown that the use of frontal, patient-collected HPV swabs are less invasive and invoke less emotional trauma when compared to providercollected swabs, especially in patients who have reported medical discrimination in the past [34,37]. Although, patients who reported a positive relationship with their providers preferred provider-collected swabs.34 Other strategies to promote adherence to future screening and colposcopy involve creating a pain-free experience for patients including using culturally sensitive language, interviewing prior to disrobing, and asking the patient to change from the waist down only [37]. Routine cervical cancer screening recommended by the United States Preventive Services Task Force should begin in FTM patients at the age of 21 with hrHPV screening starting at age 30 [31]. As patients begin their transition, it is important to note that prophylactic cervical cancer screening is not required prior to initiation of testosterone therapy even though there is an increased incidence of unsatisfactory results in pap smears in transgender male patients compared to their cisgender counterparts. This is thought to be due to their increased length of time on testosterone hormone therapy, and because of this, careful attention must be paid when collecting the appropriate cytology [39]. More research is needed to discern screening of transgender men prior to gender affirmation surgery. At this time, it is also recommended that MtF patients who have undergone gender affirmation surgery and have neovaginas undergo routine cervical cancer screening. Studies have shown that cytological findings from neovaginas have resembled that of cervical cytology with parabasal cells as well as Döderlein bacilli and are susceptible precancerous lesions and invasive carcinoma [36].
4. Conclusions Current recommendations for screening for gynecologic and breast cancer are limited by the lack of scientific data regarding the influence of hormonal and surgical gender affirming therapies. Also, behavioral and environmental risk factors are not well understood since the transgender community has not been well represented in a health system built on a binary model. All recommendations presented in this article are extrapolated from current available data and based on expert opinions. 5. Summary The current guidelines for gynecologic and breast cancer care for FtM patients are summarized in Table 2. These guidelines are challenged by the paucity of transgender specific knowledge regarding risk factors for those cancers. Creating an inclusive healthcare system and providing culturally competent care will allow expanding our medical knowledge to prevent, detect and treat early gynecologic and breast cancer in the FtM community. Future research should focus on identifying the barriers to access health care and understanding the impact of sexual practices and gender affirming therapies (hormonal and surgical) on the risk of cancer. Careful clinical considerations should also be taken to ensure FtM patients feel comfortable with their providers (see Table 3). The
3.3. Uterine cancer In 2015, the CDC reported 54,644 new cases of uterine cancer in the US population [31]. The incidence of endometrial cancer in the transgender population is currently unknown. Currently the American College of Obstetrics and Gynecologists (ACOG) does not recommend routine screening for endometrial cancer and does not endorse routine screening via gynecological examinations for cisgender and transgender patients. Routine hysterectomies for primary prevention of endometrial cancer or screening for cancer prior to initiation of testosterone therapy is not recommended [39]. Studies have found that the risk of endometrial hyperplasia is low in the FtM patient population due to endometrial atrophy associated with testosterone therapy [38–40]. Histological analysis of FtM patients undergoing hysterectomies revealed atrophy similar to that of post-
Table 3 Practice points. rapport with patients and discussing preferred pronouns and gender • Establishing identity and sexual orientation. steps of all examinations prior to performing them, ask permission to • Explain perform exams, and discuss any alternatives if any. patient-collected HPV swab kits as an alternative to HPV testing. • Discussing patient to disrobe in private, and only from waist down for pelvic • Allow examinations and from waist up for breast examinations. a trans-rectal and trans-abdominal approach as an alternative to trans-vaginal • Using ultrasounds as a diagnostic tool.
42
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medical system, though founded on a binary model, is now diversifying to incorporate the unique needs of the transgender patient population. As awareness grows, hospital systems are transforming and physicians and investigators are trying to close the gap of knowledge to provide the highest quality of care the transgender community deserves.
[13] [14] [15]
Contributors
[17]
Jharna M. Patel contributed to the literature search and review, and the writing of the original draft. Shelley Dolitsky contributed to the literature search and review, and the writing of original draft. Gloria A. Bachmann contributed to the review and editing of the draft, and to supervision. Alexandre Buckley de Meritens contributed to the literature search and review, the writing of original draft, review and editing, and to supervision.
[18] [19] [20]
[21]
[23] [24]
Funding
[25]
No funding was received for the preparation of this review.
[26]
Provenance and peer review [27]
This article has undergone peer review.
[28]
CRediT authorship contribution statement
[29]
Jharna M. Patel: Conceptualization, Data curation, Writing - original draft. Shelley Dolitsky: Conceptualization, Data curation, Writing - original draft. Gloria A. Bachman: Writing - review & editing, Supervision. Alexandre Buckley de Meritens: Conceptualization, Data curation, Writing - original draft, Writing review & editing, Supervision.
[30]
[31]
[32]
Declaration of Competing Interest [33]
The authors declare that they have no conflict of interest.
[34]
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Contents lists available at ScienceDirect
Maturitas journal homepage: www.elsevier.com/locate/maturitas
Gynecologic cancer screening in the transgender male population and its current challenges Jharna M. Patela, Shelley Dolitskya, Gloria A. Bachmana, Alexandre Buckley de Meritensa,b, a b
T
⁎
Department of Obstetrics and Gynecology, Rutgers Robert Wood Johnson Medical School, United States Rutgers Cancer Institute of New Jersey, United States
A R T I C LE I N FO
A B S T R A C T
Keywords: Transgender male Gender nonconforming Gynecologic cancer screening
As the transgender community gains visibility and recognition, healthcare disparities have become more apparent. Reports estimate that 1–1.5 million people belong to this community in the United States. Despite efforts to become more inclusive, access to healthcare is challenging in a system built on a binary model that exacerbates gender dysphoria and on healthcare insurance schemes that do not cover gender affirmation therapy. Another large challenge is the paucity of scientific and medical knowledge when it comes to caring for the transgender community. More research to build knowledge is necessary to provide evidence-based quality care. In an attempt to bring guidance for gynecologic and breast cancer screening for the transgender male population, we conducted a review of the literature published in PubMed. Here, we present a review of the challenges, as well as guidelines for breast, uterus, and cervix screening for the transgender male population.
1. Introduction Recent reports estimate that 1 to 1.5 million people belong to the transgender community in the United States [1]. Unfortunately, national health care databases do not specify gender identification. Instead, the size of the transgender population is extrapolated from smaller state-based and private surveys [2]. As the transgender community gains visibility and recognition, healthcare disparities have become apparent. The transgender community has a disproportionate amount of adverse health care outcomes, and the World Health Organization reports in increased risk for cervical, endometrial, and ovarian cancer [3,4]. In a U.S. national transgender survey, 25% of respondents reported experiencing issues with insurance coverage including care related to gender transition, 23% did not see a physician because of fear of being mistreated and 33% did not see a physician because of cost [5]. Furthermore, several studies have shown significantly less adherence to cancer screening guidelines in the transgender population [6–9].These disparities will not be overcome until we expose the barriers and limitations to care and better understand the needs of this population. The transgender community is diverse and its members are in various stages of transitioning. For those not undergoing gender-affirming intervention or those who have partially transitioned, cancer screening programs are challenging as they may exacerbate body-image
dysphoria. Little is known in the medical literature regarding the interaction between gender-affirming hormonal and surgical therapy and the risk of hormone-dependent and non-hormone dependent malignancies (breast, ovary, uterus) [10,11]. Current guidelines are of low level of evidence and mainly based on expert opinions [11–14]. In this narrative review we examine cancer screening (breast, cervix, uterus) recommendations and its barriers for transgender men. 2. Methods A literature review was conducted searching the PubMed electronic database. We used the following combinations of Medical Subject Heading (MeSH) terms: "Transgender Persons" and "Neoplasms", "Transgender Persons" and "Early Detection of Cancer", "Transgender Persons" and "Breast Neoplasms", "Transgender Persons" and "Uterine Cervical Neoplasms", and "Transgender Persons" and "Uterine Neoplasms." We did not limit our search to a specific timeframe. The combination of terms resulted in 185 results. Out of the 185 articles, 87 duplicates were removed, 57 were removed after reviewing and determining lack of relevance (pertaining to male-to-female transgender patients, not pertaining to cancer), and 6 were unavailable. These articles included case reports, epidemiologic studies, and review articles. Articles referenced in these retrieved articles were examined and included as secondary references if they were noted to be relevant.
⁎
Corresponding author at: Department of Obstetrics and Gynecology, Rutgers Robert Wood Johnson Medical School, United States. E-mail addresses: [email protected] (J.M. Patel), [email protected] (S. Dolitsky), [email protected] (G.A. Bachman), [email protected] (A. Buckley de Meritens). https://doi.org/10.1016/j.maturitas.2019.08.009 Received 8 June 2019; Received in revised form 25 July 2019; Accepted 19 August 2019 0378-5122/ © 2019 Elsevier B.V. All rights reserved.
Maturitas 129 (2019) 40–44
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Table 1 Screening guidelines for cisgender Females. Type of Cancer
Recommendations
Breast Cancer
Clinical Exams Clinical Breast Exam
Mammography
Cervical Cancer
Uterine Cancer
Ovarian Cancer
Vulvar Cancer
Population < 21 years of age 21-29 years of age 29-65 years of age
Recommendations for average risk patients [41] May be offered every 1-3 years in context of shared decision making to patients age 25-39 and annually in women > 40 years of age. Recommended yearly in patients who have underwent mastectomies and are no longer receiving mammograms. Start at age 40 or initiate from age 40-49 but no later than age 50. Screening interval annually or biennially. Continue until age 75 and screening after age 75 should be based on shared decision-making process. Recommendations [43] No Screening Cervical cytology alone every 3 years Cervical cytology alone every 3 years OR hrHPV testing alone every 5 years OR Cervical cytology and hrHPV testing every 5 years No screening
Women age > 65 years or have had hysterectomy with removal of cervix with no history of high-grade lesion or cervical cancer Patients who are not at high risk (have germ line mutations such as Lynch Syndrome) should not be routinely screened with transvaginal ultrasound [45]. Patients who are high risk can undergo annual screening with transvaginal ultrasound and endometrial biopsy. Prophylactic hysterectomies can be discussed on a case by case basis [45]. Clinical Exams Recommendations for average risk patients [46] Transvaginal Screening with ultrasounds not recommended at this time due to decreased PPV and increased false positive rates. Ultrasound Cancer Antigen 125 Tumor Marker No current evidence of a single cutoff value that has acceptable PPV or sensitivity to be used for a screening test. There is no current screening examination recommended for the detection of vulvar cancer [44]. Detection is made by clinical inspection with biopsy to confirm the diagnosis [44].
• •
• •
these patients, screening recommendations are made irrespective of the patient’s hormonal therapy history [23]. For patients that have not undergone top surgery, the breast cancer screening recommendations are the same as cisgender women. For women who have undergone gender affirming surgery, recommendations for screening are not well established [23]. Top surgery involves bilateral nipple sparing mastectomies, which commonly leave residual breast tissue, including the nipple areolar complex. In one anatomic study on cadavers, ductal tissue remained in 83% of patients [24]. Prior to the procedure, patients should meet with their doctor to discuss if they fall into the high-risk category. Patients identified as high-risk could consider more complete mastectomies including nipple areolar grafts to further reduce their risk of cancer [15,25]. Even with this surgery however, the risk of cancer drops only 90% and therefore screening is still important [26]. Mammograms do not have much utility in this population, but these patients should be followed with yearly clinical breast exams of the chest wall and axilla, and with ultrasounds of any palpable lesions [23,24,27].
Additionally, separate searches were conducted by using PubMed and American College of Obstetrics and Gynecology website to find incidence and prevalence of cancers in the cisgender population. 3. Screening guidelines Table 1 summarizes recommendations on screening. 3.1. Breast cancer screening Breast cancer is the most common cancer in women and the second leading cause of cancer mortality in the United States. The incidence of breast cancer in women is 1 in 8, or 12.4%. The risk of breast cancer in men is 1 in 833, or 0.12%. Risk factors for breast cancer in the general population include: age, personal history of breast cancer, family history, genetics, radiation to chest or face before age 30, white race, obesity, nulliparity, early menarche, late menopause, use of HRT, alcohol, dense breast tissue, lack of exercise, and smoking [13]. For female to male (FtM) transgender patients, the incidence of breast cancer is not well defined [14,15]. The incidence of breast cancer in patients who have not undergone gender affirming breast surgery (“top surgery”) is thought to be similar to cisgender females, however the incidence of breast cancer in patients who are status post mastectomies is unknown [15]. The reports of transgender men with breast cancer are limited to case reports only, and long-term data is very limited [16,17]. Risk factors in this population are similar to the cisgender female population, with the addition of irregular screening. The effect of hormonal therapy on breast cancer risk has not been well established [18]. The role of testosterone supplementation is unknown, though some hypothesize that high circulating androgens may increase the risk of breast cancer. A proposed mechanism for this is the aromatization of testosterone to estrogens in peripheral tissues, leading to an increased estrogen exposure. Another possible mechanism is the activation of androgen receptors that lead to cellular growth and proliferation in mammary tissues [18–21]. Because these theories are based on low level evidence, and no studies have been able to adequately demonstrate an increased risk in
3.2. Cervical cancer Cervical cancer is the fourth most common cancer in women and is a leading cause of morbidity and mortality worldwide. In 2015 the CDC reported 12,845 new cases of cervical cancer and estimated that 4210 women died from this disease [28,29]. Due to the introduction of screening methods, namely the papanicolaou (PAP) smear and Human Papilloma Virus (HPV) testing, the incidence of cervical cancer has decreased in the past 40 years [30] and currently it is estimated that 43% of the U.S. adult cisgender female population undergoes routine pap smear testing [31]. In contrast, the National Transgender Survey found that of the FtM patients who still have a cervix, only 27% had reported that they had undergone routine pap smear testing [31]. Many transgender individuals chose to not undergo routine gynecological examinations due to heightened sense of conflict between gender identity and physical anatomy [31]. This population has a decreased rate of reported high-risk HPV infection (hrHPV) despite high-risk behaviors, a misrepresentation attributable to decreased routine screening. Studies have shown that there is an underreporting of cases 41
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Table 2 Current screening guidelines for FtM transgender patients. Type of Cancer
Recommendations
Breast Cancer
Clinical Exams Breast Examinations
Cervical Cancer
Uterine Cancer Ovarian Cancer Vulvar Cancer
Recommendations for average risk patients [41] For patients who have not undergone top surgery, breast examinations may be offered every 1-3 years. Examinations should include axilla and chest wall. Mammography Limited utility of mammograms. Population Recommendations [41,42] < 21 years of age No Screening 21-29 years of age Cervical cytology alone every 3 years 29-65 years of age Cervical cytology alone every 3 years OR hrHPV testing alone every 5 years OR Cervical cytology and hrHPV testing every 5 years Patients who have neovaginas Need to undergo routine cervical cancer screening with insurance of appropriate cytology collection. No routine screening recommendations in low or high risk patients. No routine screening recommendations in low or high risk patients No routine screening recommendations in low or high risk patients.
• • •
menopausal women [39]. When a transvaginal ultrasound is required for diagnosis, a transrectal or transabdominal ultrasound should be discussed as a transvaginal probe may cause emotional trauma. As it stands, it is recommended to have open-dialogue with patients regarding recognition of abnormal uterine bleeding in FtM patients who have amenorrhea either secondary to hormone therapy or have undergone hysterectomies. Providing culturally competent care is crucial in making this subset of patients feel comfortable presenting with their gynecological concerns so that early detection and treatment of endometrial cancer can be pursued.
of cervical cancer in this population due to decreased access to healthcare, negative health care experiences, discrimination, and refusal of health services [31,32]. There are several considerations that can help improve rates of screening and routine follow up in the FtM patients and increase comfort during gynecological examinations [33,35]. Recent studies have shown that the use of frontal, patient-collected HPV swabs are less invasive and invoke less emotional trauma when compared to providercollected swabs, especially in patients who have reported medical discrimination in the past [34,37]. Although, patients who reported a positive relationship with their providers preferred provider-collected swabs.34 Other strategies to promote adherence to future screening and colposcopy involve creating a pain-free experience for patients including using culturally sensitive language, interviewing prior to disrobing, and asking the patient to change from the waist down only [37]. Routine cervical cancer screening recommended by the United States Preventive Services Task Force should begin in FTM patients at the age of 21 with hrHPV screening starting at age 30 [31]. As patients begin their transition, it is important to note that prophylactic cervical cancer screening is not required prior to initiation of testosterone therapy even though there is an increased incidence of unsatisfactory results in pap smears in transgender male patients compared to their cisgender counterparts. This is thought to be due to their increased length of time on testosterone hormone therapy, and because of this, careful attention must be paid when collecting the appropriate cytology [39]. More research is needed to discern screening of transgender men prior to gender affirmation surgery. At this time, it is also recommended that MtF patients who have undergone gender affirmation surgery and have neovaginas undergo routine cervical cancer screening. Studies have shown that cytological findings from neovaginas have resembled that of cervical cytology with parabasal cells as well as Döderlein bacilli and are susceptible precancerous lesions and invasive carcinoma [36].
4. Conclusions Current recommendations for screening for gynecologic and breast cancer are limited by the lack of scientific data regarding the influence of hormonal and surgical gender affirming therapies. Also, behavioral and environmental risk factors are not well understood since the transgender community has not been well represented in a health system built on a binary model. All recommendations presented in this article are extrapolated from current available data and based on expert opinions. 5. Summary The current guidelines for gynecologic and breast cancer care for FtM patients are summarized in Table 2. These guidelines are challenged by the paucity of transgender specific knowledge regarding risk factors for those cancers. Creating an inclusive healthcare system and providing culturally competent care will allow expanding our medical knowledge to prevent, detect and treat early gynecologic and breast cancer in the FtM community. Future research should focus on identifying the barriers to access health care and understanding the impact of sexual practices and gender affirming therapies (hormonal and surgical) on the risk of cancer. Careful clinical considerations should also be taken to ensure FtM patients feel comfortable with their providers (see Table 3). The
3.3. Uterine cancer In 2015, the CDC reported 54,644 new cases of uterine cancer in the US population [31]. The incidence of endometrial cancer in the transgender population is currently unknown. Currently the American College of Obstetrics and Gynecologists (ACOG) does not recommend routine screening for endometrial cancer and does not endorse routine screening via gynecological examinations for cisgender and transgender patients. Routine hysterectomies for primary prevention of endometrial cancer or screening for cancer prior to initiation of testosterone therapy is not recommended [39]. Studies have found that the risk of endometrial hyperplasia is low in the FtM patient population due to endometrial atrophy associated with testosterone therapy [38–40]. Histological analysis of FtM patients undergoing hysterectomies revealed atrophy similar to that of post-
Table 3 Practice points. rapport with patients and discussing preferred pronouns and gender • Establishing identity and sexual orientation. steps of all examinations prior to performing them, ask permission to • Explain perform exams, and discuss any alternatives if any. patient-collected HPV swab kits as an alternative to HPV testing. • Discussing patient to disrobe in private, and only from waist down for pelvic • Allow examinations and from waist up for breast examinations. a trans-rectal and trans-abdominal approach as an alternative to trans-vaginal • Using ultrasounds as a diagnostic tool.
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medical system, though founded on a binary model, is now diversifying to incorporate the unique needs of the transgender patient population. As awareness grows, hospital systems are transforming and physicians and investigators are trying to close the gap of knowledge to provide the highest quality of care the transgender community deserves.
[13] [14] [15]
Contributors
[17]
Jharna M. Patel contributed to the literature search and review, and the writing of the original draft. Shelley Dolitsky contributed to the literature search and review, and the writing of original draft. Gloria A. Bachmann contributed to the review and editing of the draft, and to supervision. Alexandre Buckley de Meritens contributed to the literature search and review, the writing of original draft, review and editing, and to supervision.
[18] [19] [20]
[21]
[23] [24]
Funding
[25]
No funding was received for the preparation of this review.
[26]
Provenance and peer review [27]
This article has undergone peer review.
[28]
CRediT authorship contribution statement
[29]
Jharna M. Patel: Conceptualization, Data curation, Writing - original draft. Shelley Dolitsky: Conceptualization, Data curation, Writing - original draft. Gloria A. Bachman: Writing - review & editing, Supervision. Alexandre Buckley de Meritens: Conceptualization, Data curation, Writing - original draft, Writing review & editing, Supervision.
[30]
[31]
[32]
Declaration of Competing Interest [33]
The authors declare that they have no conflict of interest.
[34]
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