Screening for cervical cancer in transgender men

Introduction

Transgender men are at risk for cervical cancer. Cervical cancer is the third most common cancer globally [1]; more than 99% of which are caused by infection with one of several high risk oncogenic strains of the human papilloma virus (hr-HPV).[2] Pelvic exams to obtain pap smears may be challenging for transgender patients. Inadequate screening for cervical cancer is linked to the barriers transgender individuals face in accessing culturally sensitive health care.[3] Transgender men are less likely to be current on cervical cancer screening than non-transgender women.[4] Individuals who have never or have rarely been screened for cervical cancer are at the highest risk for progression of chronic hr-HPV infection to malignancy, morbidity and mortality.[5]

Transgender men who have sex with non-transgender men (trans MSM) report inconsistent condom use during receptive oral, vaginal and anal sex with non-transgender male sexual partners, and are at increased risk for hr-HPV infection and undetected disease progression.[6,7] HPV vaccination between the ages of 9 to 26 has the potential to significantly reduce rates of cervical, oral and anal cancer.[8-10] Adolescent non-transgender males are receptive to HPV vaccination, and 74% of non-transgender men who self-identify as gay or bisexual are willing to get vaccinated for HPV if recommended by their health care provider.[11,12]

Screening recommendations

Cervical cancer screening should never be a requirement for testosterone therapy. Cervical cancer screening for transgender men, including interval of screening and age to begin and end screening follows recommendations for non-transgender women as endorsed by the American Cancer Society, American Society of Colposcopy and Cervical Pathology (ASCCP), American Society of Clinical Pathologists, U.S. Preventive Services Task Force (USPSTF) and the World Health Organization (Grading: X C S).[13-15] As with non-transgender women, transgender men under the age of 21 should not have pap smears regardless of their age of sexual debut.[13] Pap smears on transgender men have a ten-fold higher incidence of an unsatisfactory result compared to non-transgender women, which is positively correlated with length of time on testosterone.[16] If erythema of vaginal and/or cervical tissue is noted, evaluation for usual causes of inflammation is warranted prior to reaching a diagnosis of exclusion of testosterone-mediated atrophic cervicovaginitis. Inflammation may obscure cervical cytological evaluation and result in an unsatisfactory result. In addition, the requisition should indicate any testosterone use as well as the presence of amenorrhea, to allow the pathologist can accurately interpret cell morphology.

Improving patient experiences

Strategies to promote a more supportive and sensitive setting include using culturally sensitive language, interviewing the patient prior to disrobing, and asking the patient to change from the waist down only. A painful pap smear experience is correlated with non-adherence to future screening and colposcopy.[17] Several anecdotal techniques may reduce pain associated with speculum exams. A pediatric speculum may allow visualization of the cervix and can reduce discomfort with the exam; however it is important to avoid using a speculum so short that it requires excessive external pressure to visualize the cervix. Moving the buttocks past the end of the exam table and encouraging pelvic relaxation may also increase comfort and improve visualization of the cervix. If the examiner notes tension or anxiety, taking time to go through a verbal relaxation exercise can be helpful. Warm water may be used to lubricate a narrow speculum prior to insertion to minimize a patient's discomfort and dysphoria without compromising pap results. Water-based lubricant can reduce discomfort; using a minimal amount of lubricant on the outer portion of a speculum may reduce patient discomfort while minimally increasing the risk of an unsatisfactory sample.[18,19] Excessive lubricant should be avoided; studies have conflicting results on the effect of excessive lubricant on pap results. Some clinicians find inserting a speculum less uncomfortable for patients by first placing a finger or two in the vagina and performing posterior pressure while asking the patient to flex and relax their pelvic floor muscles. A digital (not bimanual) exam may also help identify the location of the cervix and minimize manipulation during the speculum exam. A formal bimanual exam on an otherwise asymptomatic patient may not add clinical value and may add to the patient's discomfort.[20] Other approaches to reduce discomfort might include allowing the patient to insert the speculum themselves or watch the procedure using a mirror, administration of oral benzodiazepines prior to the exam, or the use of vaginal estrogens for 1 week prior to the exam.

Preliminary research on self-collected vaginal samples for HPV compared to clinician obtained samples shows promise, this approach may also be more acceptable to transgender men.[21,22] Future initial HPV screening for transgender men may also utilize non-vaginal sourced specimens; studies supporting concordance of HPV in the urine with HPV in the cervix represent a potential method for a non-vaginal triage algorithm.

References

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011 Apr;61(2):69-90.
2. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999 Sep;189(1):12-9.
3. Rachlin K, Green J, Lombardi E. Utilization of health care among female-to-male transgender individuals in the United States. J Homosex. 2008;54(3):243-58.
4. Peitzmeier SM, Khullar K, Reisner SL, Potter J. Pap test use is lower among female-to-male patients than non-transgender women. Am J Prev Med. 2014 Dec;47(6):808-12.
5. Sung HY, Kearney KA, Miller M, Kinney W, Sawaya GF, Hiatt RA. Papanicolaou smear history and diagnosis of invasive cervical carcinoma among members of a large prepaid health plan. Cancer. 2000 May 15;88(10):2283-9.
6. Sevelius J. "There's no pamphlet for the kind of sex I have": HIV-related risk factors and protective behaviors among transgender men who have sex with nontransgender men. J Assoc Nurses AIDS Care JANAC. 2009 Oct;20(5):398-410.
7. Herbst JH, Jacobs ED, Finlayson TJ, McKleroy VS, Neumann MS, Crepaz N, et al. Estimating HIV prevalence and risk behaviors of transgender persons in the United States: a systematic review. AIDS Behav. 2008 Jan;12(1):1-17.
8. Moscicki A-B. Impact of HPV infection in adolescent populations. J Adolesc Health Off Publ Soc Adolesc Med. 2005 Dec;37(6 Suppl):S3-9.
9. Gillison ML, Chaturvedi AK, Lowy DR. HPV prophylactic vaccines and the potential prevention of noncervical cancers in both men and women. Cancer. 2008 Nov 15;113(10 Suppl):3036-46.
10. Centers for Disease Control and Prevention (CDC). FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep. 2010 May 28;59(20):626-9.
11. Reiter PL, McRee A-L, Kadis JA, Brewer NT. HPV vaccine and adolescent males. Vaccine. 2011 Aug 5;29(34):5595-602.
12. Reiter PL, Brewer NT, McRee A-L, Gilbert P, Smith JS. Acceptability of HPV vaccine among a national sample of gay and bisexual men. Sex Transm Dis. 2010 Mar;37(3):197-203.
13. Saslow D, Solomon D, Lawson HW, Killackey M, Kulasingam SL, Cain J, et al. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin. 2012 May;62(3):147-72.
14. Moyer VA, U.S. Preventive Services Task Force. Screening for cervical cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2012 Jun 19;156(12):880-91, W312.
15. World Health Organization. Cervical Cancer Screening in Developing Countries: Report of a WHO Consultation. World Health Organization; 2002. 90 p.
16. Peitzmeier SM, Reisner SL, Harigopal P, Potter J. Female-to-male patients have high prevalence of unsatisfactory Paps compared to non-transgender females: implications for cervical cancer screening. J Gen Intern Med. 2014 May;29(5):778-84.
17. Brooks SE, Gordon NJ, Keller SJ, Thomas SK, Chen TT, Moses G. Association of knowledge, anxiety, and fear with adherence to follow up for colposcopy. J Low Genit Tract Dis. 2002 Jan;6(1):17-22.
18. Hathaway JK, Pathak PK, Maney R. Is liquid-based pap testing affected by water-based lubricant? Obstet Gynecol. 2006 Jan;107(1):66-70.
19. Holton T, Smith D, Terry M, Madgwick A, Levine T. The effect of lubricant contamination on ThinPrep (Cytyc) cervical cytology liquid-based preparations. Cytopathol Off J Br Soc Clin Cytol. 2008 Aug;19(4):236-43.
20. Bates CK, Carroll N, Potter J. The challenging pelvic examination. J Gen Intern Med. 2011 Jun;26(6):651-7.
21. Jacobson DL, Womack SD, Peralta L, Zenilman JM, Feroli K, Maehr J, et al. Concordance of human papillomavirus in the cervix and urine among inner city adolescents. Pediatr Infect Dis J. 2000 Aug;19(8):722-8.
22. Sellors JW, Lorincz AT, Mahony JB, Mielzynska I, Lytwyn A, Roth P, et al. Comparison of self-collected vaginal, vulvar and urine samples with physician-collected cervical samples for human papillomavirus testing to detect high-grade squamous intraepithelial lesions. Can Med Assoc J. 2000;163(5):513-8.