Abstract
Prostate cancer treatment significantly impacts sexual health and function. Sexual function is a vital aspect of human health and a critical component of cancer survivorship, and it is important to understand the potential impacts of different treatment modalities on sexual health. Existing research has described the effects of treatment on male erectile tissues and function, including as it relates to heterosexual intercourse. There is minimal evidence regarding their impacts on sexual health and function in sexual and gender minority populations. This includes sexual minority men, or gay and bisexual men, and transgender women or trans feminine people in general. Such unique impacts might include altered sexual function in relation to receptive anal intercourse and evolutions in sexual roles. Sexual dysfunctions following prostate cancer treatment affecting quality of life in sexual minority men include anodyspareunia, erectile dysfunction, climacturia, anejaculation, altered pleasurable sensation, and changes in penile length. Clinical trials investigating sexual outcomes after prostate cancer treatment do not collect sexual orientation and gender identity demographic data or outcomes specific to members of these populations perpetuating an uncertainty regarding optimal management. This review comprehensively identifies the toxic effects of prostate cancer treatments on sexual minority men, addresses sexual dysfunction in transgender women, summarizes therapies to assist in sexual function restoration, and highlights the nuances of management in these understudied populations. This review seeks to provide clinicians with an evidence base with which to communicate recommendations and tailor interventions for sexual and gender minority patients with prostate cancer.
Short Summary:
This review discusses the impacts of prostate cancer treatments on sexual health in sexual and gender minorities, summarizes therapies to assist in sexual function restoration, and highlights the nuances of management in these historically oppressed patient populations.
Introduction
Prostate cancer is the most common cancer in the male population with a 5-year overall survival of 98%.1 Due to the relatively high overall survival, treatment paradigms focus on both survival and quality of life (QoL). Prostate cancer can be treated with radical prostatectomy (RP), external beam radiation (EBRT), brachytherapy, androgen deprivation therapy (ADT), or combination therapies depending on risk group.2 Each of these treatments is associated with toxicity profiles which can impact patient QoL.
Sexual function is a vital aspect of human health and maintaining the capacity for pleasurable sexual activity after cancer therapy is a critical component of both QoL and survivorship.3 Sexual dysfunction is one of the most common and debilitating effects of prostate cancer treatment.4 Substantial evidence exists describing the impact of prostate cancer treatment on male penile erectile tissues and its impact on heterosexual intercourse.5,6
However, there are a paucity of data analyzing the impact of treatment on sexual function in sexual and gender minorities (SGM). Sexual and gender minorities include individuals who identify as lesbian, gay, bisexual, transgender, gender diverse, asexual, queer, and intersex as well as those who do not but whose sexual orientation, gender identity, or reproductive development vary from traditional, societal, cultural, or physiological norms.7 It is estimated that approximately 1 in 81 gay and bisexual men, or sexual minority men (SMM), will develop prostate cancer as there is no evidence to support SMM are at greater risk to develop prostate cancer.8 And while the prevalence data is limited for transgender women (TGW), people recorded male sex at birth or who have feminine gender identity; TGW likely have a substantially lower risk of developing prostate cancer compared to the cisgender male population.9
The most common sexual activities among SMM include masturbation, oral intercourse, and anal intercourse,10 while TGW sexual practices continue to be investigated, they also commonly include masturbation, oral intercourse, and anal intercourse.11,12 In receptive anal intercourse, the prostate is the primary organ responsible for sexual pleasure; however, the damage and toxicity to this vital organ, the surrounding tissues, and the supplying neurovasculature is poorly understood.13,14 Increasing the understanding of the impact of prostate cancer treatment in patients who participate in anal intercourse is essential. The American Society of Clinical Oncology (ASCO) has reported that there is insufficient knowledge on the healthcare needs and outcomes for effective interventions among SMM and TGW populations;15 furthermore, practitioners lack the necessary tools to guide treatment discussions, promote patient centered conversations, and enable shared decision making, when appropriate, in this population.16,17 This continues to be perpetuated as both SMM and TGW remain absent from cancer related clinical trials.18
To provide a framework to guide treatment related discussions and future biomedical research with these populations with prostate cancer, this review provides a detailed overview of how sexual dysfunction in SMM and TGW patients differs from heterosexual cisgender male (HET) patients following prostate cancer treatment. To accomplish this, we aim to understand how the prostate functions in anal intercourse as a context to interpret the existing literature on sexual outcomes in SMM following prostate cancer treatment. Additionally, we identify techniques and therapies used to manage treatment-related damage responsible for sexual dysfunction in SMM following prostate cancer treatment. Lastly, given the limited literature on TGW with prostate cancer, we address sexual dysfunction in this patient population. This review seeks to establish a framework for clinicians to counsel SMM and TGW with prostate cancer as well as provide equitable and personalized care to these historically oppressed patient populations.
The prostate and anal intercourse
To understand the effects of prostate cancer treatments on sexual health for SMM, it is important to recognize the role of the prostate in receptive anal intercourse. The prostate provides seminal fluid for male ejaculate (procreative function) and facilitates orgasm (recreative function).19 An orgasm occurs with the release of neurotransmitters resulting in muscular, sensory, and vascular changes experienced locally and globally throughout the body. Although a large component of the orgasm is a neuropsychiatric phenomenon, the neural circuitry of an orgasm is poorly understood. Moreover, orgasms are multifactorial and can be experienced by physical stimulation (including areas outside the genitalia) and psychological stimulation.20 In many people with a prostate gland, an orgasm is accompanied by ejaculation; however, the two events occur through separate neuropsychological pathways, and therefore can occur independently. Additionally, it is possible to have an orgasm or ejaculate without a penile erection or penile structures.21–23
In addition to stimulation of the prostate, it is hypothesized that pleasure from receptive anal intercourse is experienced through pressure and stimulation of the surrounding nerves in the perianal skin and rectal wall. Additionally, the anus is an erogenous zone, thus making anilingus a source of sexual pleasure.24–26 Manipulation of the anus and its surrounding area induces erotic stimulation through the perineal nerves (a branch of the pudendal nerve).24,27 Furthermore, the neural network between the genitalia and the anorectal area suggests that stimulation of one area can cause reaction in the other (e.g., pressure on the perineum might cause an erection in a male).28 Moreover, touching the skin adjacent to the anus can stimulate anal sphincter contraction, which can lead to changes in breathing and physiological behavior.26
Pressure on the prostate, anal sphincter, and rectal wall can also induce penile excitation and orgasm. The anus and rectum contain their own sensory networks and stimulation of the anorectal area can heighten sexual pleasure.24 Studies have suggested that involuntary erections during enemas or digital rectal exams might occur, thus implicating this connection.24 Inserting an object such as a finger or penis into the anus and/or rectum can stimulate the nerves surrounding the prostate, seminal vesicles, anus, and rectal wall, leading to sexual arousal. 24,29 Reports have suggested a greater intensity of orgasm through deep prostatic massage with 12 pelvic muscle contractions compared to 4-8 contractions associated with penile orgasm.22
Supporting the role of the prostate in orgasm are prostate pleasure toys, which place pressure on the prostate and rectal wall in order to induce an erection and intensify orgasm.30 A recent study of 806 participants analyzing differences in sexual behavior found that men in same sex relationships experienced extreme pleasure and frequent orgasms from anal intercourse. Men who have sex with men had a similar satisfaction of orgasm from anal entry (mean: 4.60, 5 is most satisfactory) compared to men who have vaginal intercourse with women (mean: 4.69). Additionally, although the significance is unknown, these orgasms were rated higher than oral-penile orgasms in male-male relationships (mean: 4.18) and male-female relationships (mean: 4.36).31 These studies have helped uncover the complex roles for the prostate, perianal skin and surrounding nerves on creating powerful and pleasurable orgasms during anal intercourse. Thus, a comprehensive understanding by clinicians of the anatomy and pathophysiology of anal intercourse is essential to effectively counsel SMM patients undergoing prostate cancer treatment.
Sexual dysfunction in sexual minorities
Sexual dysfunction after prostate cancer treatment is multifactorial and has significant impacts on QoL and survivorship outcomes. Issues influencing sexual dysfunction and distress include patient age, comorbidities, baseline sexual function and practices, and treatment modality (FIG. 1).
Fig. 1: Comprehensive assessment of sexual and gender minorities for sexual dysfunction.
Assessing sexual dysfunction in a patient is multifactorial. It is imperative to understand a patient’s gender identity, birth recorded sex, sexual orientation; sexual behavior and role (top, bottom, versatile, side), comorbidities that could influence sexual function (e.g. vascular disorders, heart disease, depression), medications and substances that could impair sexual function (e.g. SSRIs), patient’s relationship status and psychosocial support, as well as disease characteristics and treatment selection.
Patient demographics including age and comorbidities can influence sexual dysfunction and are an important consideration. SMM with prostate cancer might be younger compared to the general population, but also might have a higher comorbidity burden. The median age of a prostate cancer patient is 67 years old.32 A cross-sectional survey study of 401 SMM with prostate cancer revealed a mean age of 63.5 years (standard deviation [SD]: 6.6),33 while a cross-sectional survey study of 92 SMM from the US and Canada found that the average age of diagnosis was 57.8.34 Another cross-sectional study from Australia of 119 SMM and 224 HET found a significant difference in age with SMM having a younger average age of 64.25 (SD: 8.18) compared to 71.54 (SD: 8.98) (p < 0.001).35 It is hypothesized that SMM are diagnosed with prostate cancer at a younger age due to older SMM not disclosing their sexual orientations8,36 potentially skewing data as well as higher PSA detection among this population due to prostate stimulation during receptive anal intercourse.37 Moreover, the earlier detection of prostate cancer in SMM might also be explained by the unique health-seeking behavior of this cohort. Due to a potential lack of incomplete healthcare services from a primary care provider, many SMM might have multiple caregivers to address their specific healthcare needs. For example, many SMM separate their sexual health provider from their primary care provider.38 Additionally, sexual health, along with mental health, is a primary health concern for SMM.39 Thus, due to this healthcare fragmentation and increased concern regarding sexual health compared to HET, SMM might be more inclined to seek medical care for sexual dysfunction—which can be from an underlying cause, such as prostate cancer—leading to earlier detection of prostate cancer.
Comorbidities might also differ for SMM. Polter et al. analyzed 383 SMM and compared comorbidity prevalence to published samples of HET prostate cancer survivors. They found a similar prevalence of diabetes for SMM (12%) and HET (13%), and a lower prevalence of obesity for SMM (20%) compared to HET (32%).40 However, both blood vessel disease and mental health disorders were significantly more common among SMM (53% versus 45% and 46.6% versus 15–27%, respectively). This study also found that comorbidities within SMM were associated with worse QoL and sexual function. It has been demonstrated that patients with higher comorbidity scores experience decreased recovery to baseline erectile function following RP (independent of age). 41 Additionally, baseline erectile score is an important prognosticator for erectile function following treatment17.
Maintaining the capacity for pleasurable sexual activity after cancer therapy3 is especially important for SMM survivors who might engage in more frequent and variable sexual activities than HET. In fact, studies show that SMM are more sexually active than HET and have more casual and multiple sexual partnerships.42,43 In a study of SMM prostate cancer survivors, the frequency of sexual practices among this populations included: masturbation (87%), penile oral intercourse performance (55%), penile oral intercourse reception (42%), receptive anal intercourse (37%), insertive anal intercourse (25%), and insertive vaginal intercourse (6%).44 Moreover, compared to HET, SMM were more likely to be single with approximately 46%- 50% of SMM being married and/or living with a partner.33,34 Differences in relationship status are further underlined by Ussher et al., where 50% of SMM were partnered compared to 86% of HET (p < 0.001).35 This study also found that the length of the relationship for partnered SMM patients is significantly shorter, as only 81% of SMM relationships are more than 2 years compared to 93% of HET relationships. Sexual dysfunction following treatment can be distressing to patients without a partner who might be sexually active and seeking relationships.
In addition to age, comorbidities, relationship status, and baseline sexual function/practices, sexual dysfunction is affected by treatment modality,2 as well as anatomical preservation during treatment.45,46 In both surgery and radiotherapy, the extent of anatomical preservation, including nerve and vessel preservation, can be predictive of the extent of erectile dysfunction.45,46 In the general population, RP is associated with short-term worsening of sexual function compared to EBRT alone for the treatment of localized prostate cancer. The prospective CEASAR study compared RP, EBRT, and active surveillance at 3 year follow up, and found that the adjusted mean expanded prostate index composite (EPIC) sexual domain score for men undergoing RP had declined significantly more than for men undergoing EBRT (mean difference −11.9 points, 95% CI [−15.1, −8,7]).17 Follow-up data from the ProtecT trial illustrated that RP had an increased incidence of erectile dysfunction compared to EBRT at 6 years.5 Additionally, on the Prostate Cancer Outcomes Study (PCOS), patients undergoing RP were more likely to have erectile dysfunction compared to EBRT at 2 years and 5 years, though no difference was observed at 16 years.6 Moreover, EBRT might be given with ADT; when compared to EBRT alone, the addition of ADT is associated with worse sexual outcomes, including an increased incidence of erectile dysfunction, ejaculatory issues, decreased libido, and worse sexual recovery.47,48 While different fractionation regimens are commonly employed for EBRT, data have demonstrated that hypofractionated radiotherapy does not increase erectile dysfunction when compared to conventionally fractionated radiotherapy.48,49 Thus, shorter courses of EBRT can be utilized without an increased risk of erectile dysfunction. Additionally, brachytherapy might be associated with better erectile function compared to EBRT.47 Lastly, while limited data exists regarding proton irradiation, one study found that erections firm enough for vaginal penetration decreased from 90% to 72% and 67% at 1 and 5 year follow up, respectively. Comparative studies investigating photon and proton therapy are required to understand the effects of these treatment modalities on sexual dysfunction.50 However, a bias might be present, as younger patients with prostate cancer with fewer comorbidities tend to select surgery compared to EBRT and brachytherapy.51 Nevertheless, it is important to note that not all treatment options are available to all patients as treatment recommendations are a function of cancer characteristics, disease extent, patient comorbidities, and patient age.
The effects of prostate cancer treatments on QoL within the SMM community are multifactorial. Restore-2, one of the largest studies investigating the toxic effects of prostate cancer treatment on SMM observed that when compared to the general population, SMM had significantly worse urinary, sexual, bowel, and hormonal functional outcomes.33 Within the SMM cohort of 401 patients, the type of treatment significantly affected sexual and hormonal outcomes, while age and race/ethnicity did not. More specifically, there was no difference in sexual outcomes between RP (mean=38.2, SD: 21.7) and radiation only (mean=45.0, SD: 22.5); however, combination with hormonal treatment was statistically worse 25.9 (18.8) measured by the Expanded Prostate Index Composite (EPIC)-Domain Scores.33 In a study by the same group, there was no significant difference between surgery and radiation alone on sexual function QoL by multivariate analysis; however, combination therapies had significantly worse outcomes when controlled for race, age, relationship status, and sexual orientation.44
The toxic effects of treatment
The toxic effects following prostate cancer treatment experienced by SMM include: anejaculation (94%), erectile dysfunction (90%), change in orgasm (87%), decreased sexual confidence (78%), penile changes (66%), anodyspareunia (65%), and climacturia (49%). 52
Anodyspareunia
Anodyspareunia refers to pain during or after receptive anal intercourse. Anatomical and physiological factors that can make receptive anal intercourse painful include lack of natural lubrication, the anorectal angle, and the tightness of the anal sphincter.53,54 Painful receptive anal intercourse was first acknowledged as a sexual dysfunction by Rosser et al. in 1997, who cited parallels between painful vaginal intercourse or dyspareunia and painful anal intercourse or anodyspareunia.55 Inadequate lubrication, lack of foreplay, and psychological factors such as anxiety and internalized homophobia were identified as increasing the risk of anodyspareunia.56,57 The lifetime prevalence of anodyspareunia in the general SMM community is 61%, which is notably higher than the lifetime prevalence of difficulty getting an erection (40%) and difficulty ejaculating (39%) in SMM.55 Damon et al. observed that 14% of 404 SMM in the general population could not have intercourse at all due to anodyspareunia.57 A larger study of 1,752 SMM found that 59% of 1,190 SMM engaging in receptive anal intercourse experienced some degree of pain in the last 4 weeks.56 Still, while painful receptive intercourse and anodyspareunia are exceedingly prevalent in the SMM population, only 6% of SMM with prostate cancer reported that their providers even discuss anal intercourse let alone mention anodyspareunia as a toxic effect of prostate cancer treatment.58
In Restore-1, 35% of SMM with prostate cancer described receptive anal intercourse as poor to fair and 27% reported dissatisfaction with quality of receptive anal intercourse after treatment. A single painful anal intercourse event was reported by 57% of participants and anodyspareunia was reported by 34% of participants, markedly higher than the general population.44 In a secondary analysis of Restore-1, the authors sought to understand anodyspareunia further.58 In this study, the prevalence of anodyspareunia was 23% in SMM, again notably higher than in the general population; additionally, patient demographics did not correlate with anodyspareunia.57 Worse mental health function (measured by SF-12 Mental) correlated with a higher likelihood of experiencing anodyspareunia (Odds Ratio [OR]: 0.95; 95% CI: 0.91–0.99). While not statistically significant, worse bowel symptomatology trended toward a higher likelihood of experiencing anodyspareunia (OR: 0.97; 95% CI: 0.94–1.00). Following surgery, 24% of SMM experienced anodyspareunia, while following radiation (EBRT/brachytherapy), 1 of 4 (25%) SMM experienced anodyspareunia. Surprisingly, following combination therapy (e.g., EBRT+ADT) 0 of 7 (0%) SMM experienced anodyspareunia. Thus, ADT might offer a protective effect on bowel symptoms and anodyspareunia. In a retrospective study of 2,752 prostate cancer patients, ADT was shown to have a protective effect against proctitis and rectal bleeding when combined with brachytherapy.59 The authors hypothesize that this is likely due to ADTs reduction of prostate size and resultant reduction in radiation target volume. As ADT is known to decrease libido and affect erectile function negatively, it is of relevance that ADT might help protect against anodyspareunia. Further studies are required to elucidate how various treatment modalities and combinations influence the incidence of anodyspareunia in prostate cancer survivors (Table 1).
Table 1.
Treatment-related sexual dysfunction in sexual minority men
Sexual Dysfunction | Importance | Treatment Consideration | Rehabilitation and restoration |
---|---|---|---|
Anodyspareunia | In the general SMM, lifetime prevalence of AD is 61%55 and point prevalence is 14%.57 In SMM prostate cancer survivors, the point prevalence of AD ranges from 23%-34%.57,58 | RP: removes prostate (24%).58 EBRT: damages prostate, surrounding structures; causes bowel toxicity (25%).58 BT: damages prostate, surrounding structures; causes bowel toxicity (25%).58 ADT: might be protective against AD and bowel toxicity when combined with radiation.58,59 |
Anal dilator,140 Dildos, Butt plugs,140 Prostate massage vibrator,150,151 Lubricant,30,152 Alkyl nitrites (‘poppers’) 130 |
Climacturia | Oral intercourse is more common in SMM compared to HET.79 This toxicity can be embarrassing when engaging in insertive oral intercourse. | More studies are needed to understand treatment differences. | Pelvic floor exercises,134 Penile constriction ring (‘cock’ ring),135 Surgical management (mini-jupette) 137,138 |
Anejaculation | Ejaculate can be important to some SMM and be symbolic of sexual pleasure. 71–74 | RP: 100%.66 EBRT: 11-91%.67 BT: 11-91%.67 ADT: might worsen ejaculatory dysfunction. 68 |
Research is needed to circumvent anejaculation following prostate cancer treatment. |
Erectile Dysfunction | An erection must be 33% more rigid for anal intercourse compared to vaginal intercourse.63,64 | RP: worse at 6 years,5 no difference at 16 years compared to EBRT.6 EBRT: worse with ADT.47,48 |
PDE-5 inhibitors, 125,126 VEDs, 128,129 Penile constriction ring (‘cock’ ring) |
Penile Changes | The size and shape of the penis is important to participants of insertive anal and oral intercourse. Penis size is emphasized in gay culture.99 | RP: penile shortening ranges from 0.5 to 5 cm. 95,96 EBRT: when combined with ADT, there might be penile shortening.98 |
PDE-5 inhibitors, 133 VEDs129,132 |
Orgasm changes | Orgasm function and type at baseline might differ between the SMM and HET.92 | RP: anorgasmia (37%),82 dysorgasmia (12%-18%).83
84 EBRT: anorgasmia (29%)86 and dysorgamia (15%).88 BT: anorgasmia (49%)86 and dysorgasmia (26% to 40%).89 90 ADT: Might weaken orgasm sensation.91 |
Tamsulosin82 Cabergoline139 |
AD, anodyspareunia; SMM, sexual minority men; HET, cisgender heterosexual men; RP, radical prostatectomy; EBRT, external beam radiation therapy, BT, brachytherapy; ADT, androgen deprivation therapy; PDE-5, phosphodiesterase-5; VED, Vacuum erectile device
Erectile Dysfunction
Erectile dysfunction is a common, well-established toxic effect of prostate cancer treatment (Table 1). In a study of SMM following prostate cancer treatment, 85% reported that their erections were not firm enough for intercourse.44 However, in a study by Ussher et al., the authors found that erectile function was significantly better for SMM (EPIC EF: 21.2) compared to heterosexual men (16.5) following treatment.35 In subsequent analyses by Ussher et al., they identified that 72% of SMM reported erectile dysfunction approximately 5.9 years following diagnosis.60 In a study by Hart et al., 89 SMM patients noted better erectile function (38.7, SD: 2.6) versus 225 heterosexual patients (29.5, SD: 1.5) using the EPIC instrument to assess sexual function.34 Additionally, using EPIC sexual function, SMM from Restore 1 (40.5, SD: 23.6) noted significantly better erectile scores compared to SMM in Restore-2 (35.5, SD: 21.2) and the HET validation sample (29.5, SD: 23.8).33 Wassersug et al. found that there were similar rates of erectile dysfunction (p = 0.83) and ability to orgasm with penetration (p = 0.91) between SMM and HET. 61 Conversely, a pilot study analyzing bicalutamide (ADT monotherapy) for prostate cancer treatment in SMM (12 patients) and heterosexual men (17 patients), found that SMM scored lower (28.7) than heterosexual men (56.1) on the international index of erectile function score.62
While erectile function is important to all patients, it might be of particular clinical significance among the SMM community, as studies have estimated that an erection must be 33% more rigid for anal intercourse compared to vaginal intercourse.63,64 Furthermore, there might be increased distress regarding erectile dysfunction in the SMM community as a survey study in the general community found that patients who engage in more sexual activity reported more distress from erectile dysfunction.65
Anejaculation
Anejaculation is an expected sequalae following RP,66 as it is due to the removal of the prostate and seminal vesicles (Table 1). Reported rates of anejaculation vary widely, ranging from 11-91%.67 In a prospective study of 225 men receiving EBRT and 112 receiving brachytherapy, 72% of patients lost the ability to ejaculate normally. The proportion of patients experiencing anejaculation at 1, 3, and 5 years was 16%, 69%, and 89%, respectively.68 The etiology of ejaculatory dysfunction following radiation therapy might be due to atrophy, fibrosis, scarring of ejaculatory ducts, and urethral strictures leading to obstruction. The addition of ADT to a radiation regimen will likely worsen ejaculatory dysfunction. 68
In a study of 1,273 healthy men in the general population without prostate cancer, 46% reported reduced ejaculatory volume and 66% were bothered by this condition.69 However, in a study conducted by Wassersug et al., ejaculatory dysfunction following prostate cancer treatment caused more distress for SMM than heterosexual men.61 A database review of 308 SMM and 306 heterosexual men illustrated that while treatment effectiveness was most important to both SMM and heterosexual men (69.1% SMM versus 70.4% HSM, p = 0.54), ejaculatory function was significantly more important for SMM (53.7%) compared to heterosexual men (26.4%, p < 0.0001). In this study, there was no difference in importance of preservation of penile length or erectile function between SMM and heterosexual men, further underlining the importance of ejaculation to SMM.70 Ussher et al. also identified that ejaculatory concern was significantly greater for SMM compared to HET (2.62 versus 1.85, p < 0.0001).35 Ejaculation is considered important in some SMM relationships and intercourse, as the visual representation of ejaculate can be symbolic to show that sexual pleasure was achieved.71,72 In fact, it is noted that following RP, SMM associate the inability to visualize ejaculate with worse sexual outcomes.73,74
Climacturia
Climacturia or orgasm-associated urinary incontinence occurs when there is expulsion of urine during orgasm (Table 1). O’Neil et al. published a retrospective study of 412 patients who underwent EBRT or RP. They found climacturia to be present in 5.2% and 28.3% of post EBRT and RP patients, respectively. 75 Approximately 47% of all prostate cancer survivors find climacturia bothersome.76 Climacturia tends to improve over time. The mechanism and development of climacturia are unknown and might be due to damage to the internal sphincter combined with relaxation of the external sphincter during orgasm, leading to urination.77 There has not been an association between incontinence and climacturia.66 Additionally, loss of urethral length during surgery might be a cause of climacturia, as decrease in penile length was found to be an independent predictor of climacturia.78
Climacturia causes distress to the SMM community, possibly because both insertive and receptive oral intercourse are more common in this population compared to heterosexual men.79 Approximately 52% of SMM following prostate cancer treatment reported involuntary urination during intercourse or at orgasm.44 In a study of 124 SMM, 65% noted change in urinary patterns and 40% noted that activities were limited due to urinary issues.60 In a qualitative study of 16 SMM, urinary incontinence and climacturia were particularly anxiety provoking as the majority of the patients participated in oral sex and mutual masturbation.80 Further studies are needed to understand how treatment modality affects climacturia in this patient population and how climacturia might differ between SMM and HET.
Orgasm changes
Changes in orgasm function include anorgasmia, altered or decreased orgasm sensation, and dysorgasmia (orgasm-associated pain, Table 1). Treatment for prostate cancer has been associated with all of these changes.81 After RP, patients might experience anorgasmia (37%),82 decreased orgasm (37%),82 or dysorgasmia (12%-18%).83 84 Nerve sparing techniques and younger age might be associated with better orgasm-related outcomes.85 Following radiation, patients might also experience anorgasmia (EBRT: 29.1%, brachytherapy: 49.3% [decreased orgasm/anorgasmia])86 decreased orgasm (29.6% EBRT, 23.7% EBRT + brachytherapy),87 or dysorgasmia (EBRT: 15%,88 brachytherapy: 26%-40%).89 90 Additionally, when combining radiation with hormonal therapy, orgasm function might be further diminished.91
Orgasm changes following prostate cancer treatment might not differ significantly between SMM and HET. A study of 460 HET and 96 SMM showed there was no difference in orgasm satisfaction after prostate cancer treatment between the two groups.61 In another study, SMM had better orgasms (4.24; SD: 3.31) compared to HET (2.33; SD: 2.53; p < 0.001) following prostate cancer treatment.35 Conversely, in the general population, SMM might have more difficulty experiencing orgasm pleasure: orgasm ability was the same among gay (52.2; 95% confidence interval [CI]: 50.8-53.7, n = 293) bisexual (50.6; 95% CI: 48.2-53.1, n = 121), and heterosexual (52.0; 95% CI: 51.4-52.6, n = 1382) men, but orgasm pleasure was lower for gay (48.9; 95% CI: 47.6-50.2) and bisexual (46.7; 95% CI: 44.0-49.5) men compared to heterosexual men (51.1; 95% CI: 50.5-51.7).92 Thus, while changes in orgasm after prostate cancer treatment might not differ between SMM and HET, it is important to recognize that orgasm function at baseline might differ between the cohorts.
Decreased libido
Loss of libido following prostate cancer and its treatment is very common and can be worsened by hormone therapy93 (Table 1). In a study by Ussher et al., SMM had significantly better sexual interest (7.82; SD: 3.12) and sexual frequency (4.40; SD: 1.97) compared to HET (interest: 5.43; SD: 3.22; frequency: 2.63; SD: 2.22) following prostate cancer treatment.35 Another study by Ussher et al. analyzing 124 SMM prostate cancer survivors found that 58% of men report “absent,” “poor,” or “okay” libido and 65% of these patients state that low libido was problematic.60 In an exploratory qualitative study of three gay couples managing sexual dysfunction after RP, patients noted a decrease in libido after RP and one patient stated that he felt “castrated.” However, within this exploratory study, two of the three patients also attributed symptoms to confounding variables, such as medical comorbidities and advancing age.94
Change in penis size and shape
Prostate cancer treatment can affect the length and girth of the penis (Table 1). In the general population, following RP, studies show penile shortening ranges from 0.5 cm to 5 cm.95,96 This might be due to hypoxia in the penile tissue and resultant muscle loss and fibrosis.97 Although substantially less evidence exists describing radiation affecting the size and shape of the penis, one study found that EBRT combined with ADT can shorten the penis.98
Among men who have sex with men, penis size might be more emphasized due to the focus on body image in gay culture and the “double presence” of the penis in sexual minority relationships and encounters.99 Additionally, the size and shape of the penis might be particularly important to those who participate in the insertive role in anal intercourse.100 Regardless, even if there are treatment effects on penile shape from prostate cancer therapies, SMM might not experience any difference in self-esteem and self-image compared to HET following RP101 or other treatments. However, these data should be interpreted with caution as a major limitation of this study was a small sample size (SMM, n=16 and HET, n=131). Still, it is possible that penile size and shape is not the only thing important to self-esteem and image for SMM, underscoring that overall sexual satisfaction in SMM is multifactorial.
Change in sexual role
In patients with prostate cancer and survivors who participate in anal related intercourse, the damage and toxic effects to the prostate, rectal wall, perianal skin and the surrounding neurovasculature necessary for sexual pleasure can lead to a change in sexual role.13 Within the general SMM community, 8%-29% of SMM are the insertive partner (“tops”), 13-50% are the receptive partner (“bottoms”), and 29-58% are both (“versatile” or “vers”),102,103 Change in role can have many negative implications on intercourse and mental health as sexual role can be part of one’s identity in the SMM community.104
In a study by Ussher et al. examining change or loss in sexual role before and after surgery or radiation, the authors found that patients identifying as the insertive partner (“tops”) decreased from 31% to 12%, the receptive partner (“bottoms”) increased from 19% to 24%, the versatile partners (“vers”) decreased from 20% to 8%, and engaging in no anal intercourse increased from 31% to 56%.60 Additionally, patient interviews have identified that change in sexual role challenged relationship dynamics due to partner incompatibility.60 This sentiment was echoed by Hart et al. who noted from qualitative interviews that changes in sexual function and position were distressing to partners of SMM prostate cancer survivors. Similarly, from this study, Hart noted that of the insertive patients who were “tops” before treatment, only 40% continued to be strict “tops”.34 In Restore-1, Rosser et al. also noted that while approximately 92% of SMM had a strong sense of sexual role pretreatment, only 45% had any sense of sexual role posttreatment.44 More specifically, the authors noted that patient sexual role identification included: 42% “tops/vers-tops”, 37% “bottoms/vers-bottoms”, and 18% “vers” pretreatment compared to 8% “tops/vers-tops”, 65% “bottoms/vers-bottoms” and 5% “vers” posttreatment. Moreover, an overall decrease in total percentage suggests treatment affects sexual role and sexual activity (FIG 2).
Figure 2: Patient centered conversations based on sexual role.
At consultation inquire about the sexual role of a patient. A patient’s sexual role can influence treatment recommendations, guide conversations, and, when applicable, impact shared decision making. While discussing all treatment-related sexual dysfunctions is important, particular toxic effects of interest include—top: erectile dysfunction, penile changes, anejaculation, dysorgasmia as it relates to the penis, libido; versatile: anodyspareunia, erectile dysfunction, penile changes, anejaculation, dysorgasmia as it relates to the penis and prostate, libido; bottom: anodyspareunia, anejaculation, dysorgasmia as it relates to prostate sensation, libido; and side: climacturia, erectile dysfunction, penile changes, anejaculation, libido. Additionally at consultation and again at follow up, physicians should explain the implications of changing sexual role, the contraindication of combining alkyl nitrites (‘poppers’) with PDE-5 inhibitors, and the time course of abstinence from engaging in receptive anal intercourse with sexual and gender minorities.
Changes in role might be dependent on treatment modality. In a study of 15 SMM who underwent different prostate cancer therapies, patients were asked about role before and after treatment. Within the surgery group, 3 of 4 “tops” and 3 of 3 “bottoms” had to change their sexual role identity. Within the radiation group (EBRT +/− ADT and brachytherapy), all patients maintained their sexual role identity before and after treatment (5 “tops” continued to be “tops” and 2 “bottoms” continued to be “bottoms”). These results similarly suggest that prostate cancer treatments might affect sexual roles, however, such a small sample size warrants further study and evaluation.105
Anal penetration requires preparation for the receptive partner which can be burdensome for some SMM and a barrier to participate. An internet-based survey of 24,787 SMM aged 18–87 years old in the United States showed that the most common behavior among SMM was kissing a partner on the mouth (74.5%), oral sex (72.7%), and partnered masturbation (68.4%). In this cohort, anal intercourse occurred among less than half of participants (37.2%) and was most common among younger SMM aged 18–24 (42.7%),10 which is younger than the median age of SMM with prostate cancer. This suggests that there might be SMM who do not engage in anal intercourse (insertive or receptive) and engage in other sexual activities such as oral intercourse. This sexual role has recently been colloquially termed “side.”
Psychological Distress
The impact of a cancer diagnosis can lead to significant psychological distress, including anxiety, depression and potentially decreased sexual desire. Prostate cancer patients are not an exception, and are known to suffer from mental health conditions including depression and anxiety.106 Associated psychological treatments might also contribute to sexual dysfunction. Antidepressants such as selective serotonin reuptake inhibitors (SSRI) and tricyclic antidepressants (e.g. clomipramine), antipsychotics,107 benzodiazepines108 have a risk of sexual dysfunction and might cause decreased libido, ejaculatory issues, and erectile dysfunction109,110 (FIG. 1).
Compared to the general population, SMM are known to have more mental health conditions, including anxiety, depression, and substance use disorder.111 Consistently, SMM prostate cancer survivors have worse mental health compared to HET. In one study of SMM prostate cancer survivors, SMM patients scored significantly worse (mean: 46, SD: 0.8) compared to HET (mean: 58, SD:−0.7; p < 0.0001) using the short form-12 QoL survey.44 This is further underlined by both Rosser33 et al. and Ussher35 et al. who found that SMM scored significantly worse on Functional Assessment of Cancer Therapy Prostate (FACT-P) subscales and overall FACT-P compared to normative samples. Additionally, these studies found that SMM scored significantly higher on the psychological distress QoL scales including higher on the depression, anxiety, and overall psychological distress scale. Mental disorders and associated treatments might develop and contribute to sexual dysfunction in SMM prostate cancer survivors. It is essential to review medications and monitor the development of these conditions from treatment in this vulnerable population.
Mitigating sexual toxicity
Patient centered communication
It is essential for practitioners to inquire about sexual orientation and practices with their patients13 (FIG. 3). Frameworks to help physicians ask about sexual orientation and sexual health include consensus reports from the National Academy of Science Engineering and Medicine (NASEM) and the British Association of Sexual Health and HIV (BASHH). The report from NASEM offers principles (inclusiveness, precision, autonomy, parsimony, and privacy) for collecting sexual orientation and gender identity data and proposes specific questions to ask.112 Key principles from BASHH guidelines include confidentiality, communication, sexual health, documentation, and specific circumstances.113 These resources exist and might be useful to help physicians overcome anxiety when discussing sexuality and sexual health with SMM.
Figure 3: Patient centered consultation guidance for patients with prostate cancer.
To guide patient centered conversations about prostate cancer treatment selection, physicians should inquire about gender identity, sexual orientation, sexual practices, sexual role, gender affirming hormone therapy, gender affirming surgery (specifically genital reconstruction surgery). Answers to these questions will guide patient centered treatment conversations that align with sexual role, sexual orientation, and gender identity and allow for informed treatment selection.
However, these guidelines are not specific to cancer patients and more research is needed to assist oncological physicians in discussing sexual orientation and sexual practices. In one study, only two thirds of SMM report being out to their healthcare prostate cancer provider.44 In a survey from the American Urological Society, 112 adult urologists (89 males, 23 females) reported that they were significantly more comfortable discussing sexual health with heterosexual patients (80%) compared to SMM (64%). Additionally, 63% of respondents do not ask patients about sexual orientation and 26% assume the patient to be heterosexual.114 A survey study of ASCO members revealed that less than half of providers ask about sexual orientation, and that 17% of respondents thought it was not important to collect sexual orientation data.115 This study cited healthcare provider discomfort, institutional culture, and lack of training, resources, and time as barriers to sexual orientation collection. Similarly, a systematic review revealed that healthcare professionals might fail to discuss sexual health related issues with patients due to time constraints, lack of education, concern for offending the patient, and personal discomfort.116
Nevertheless, on the masculine self-esteem scale, SMM patients who disclosed their sexual orientation had a significantly higher self-esteem (77, SD: 18) compared to those who did not (62, SD: 20). This openness likely improves the physician-patient relationships, which can promote better sexual and disease outcomes.117 Lack of sexual orientation and preference discussion might be related to reported reduced satisfaction with prostate cancer care among SMM patients. This was demonstrated by Ussher et al. who reported that SMM have a significantly lower satisfaction level with treatment than HET.35
When considering prostate cancer treatments and the associated toxic effects, it is important to not only ask about sexuality and sexual practices, but also sexual role (FIG. 1 and FIG 3). Knowing the sexual role of a patient might influence treatment recommendations, guide conversations, and impact shared decision making in this population as the side effects differ and interests of men might be different (FIG. 2).118 For example, from a qualitative interview, a prostate cancer survivor who identified as a “bottom” noted that treatment-related erectile dysfunction was not distressing due to the lack of importance his erection has on his sexual life and identity.94 Thus, a “bottom” or “vers” might be interested in learning about anodyspareunia, dysorgasmia and prostate sensation after prostate cancer treatment, a “top” or “vers” might be interested in learning how specific therapies affect erection firmness and penile shape/length, and a “side” might be interested in learning about climacturia and anejaculation.13 By appropriately guiding conversations, patients will be able to make an informed decision, which could help decrease the rate of sexual identity change in this patient population. Thus, it is extremely important to consider the entire patient when discussing treatment options treatment related sexual dysfunction, especially in SMM (FIG. 2).
Sexual rehabilitation and devices
Sexual devices and medications can help patients restore their capacity to experience arousal and orgasm by altering physiology and increasing sensation, and sexual rehabilitation, restoration and assistance is important to SMM with prostate cancer. A qualitative study conducted by Ussher et al. identified that significantly more SMM prostate cancer survivors are likely to try an assistive sexual aid compared to heterosexual prostate cancer survivors.119 These aids include oral medications, penile injections/implants, vacuum pumps, and vibrators. Furthermore, while both SMM and HET were dissatisfied with sexual aids, SMM were more likely to seek information and support about sexual rehabilitation from the internet, therapists, and support groups.119 This further illustrates SMM openness to utilizing sexual assistive devices and the need for providers to discuss sexual rehabilitation with this population.
Information regarding sexual assistive devices should be provided to prostate cancer patients at consultation to help guide treatment option discussion and future sexual rehabilitation.120 SMM prostate cancer survivors report that limited information is provided on sexual restoration at consultation. This lack of education about sexual rehabilitation might delay treatment and lead to worse sexual outcomes.121–123
Erectile Dysfunction Rehabilitation
Sexual restoration after prostate cancer treatment has been primarily focused on improving erectile function. Common treatments for erectile dysfunction following prostate cancer treatment include phosphodiesterase-5 (PDE-5) inhibitors (e.g., tadalafil, sildenafil), penile injection therapy, penile implants, and vacuum erectile devices (VED).121,124 In the general population, approximately half of prostate cancer survivors utilize a rehabilitation method for penile erection restoration. Although penile rigidity increases, approximately 73% of general patients discontinue these rehabilitation methods.119,121 Compared to heterosexual patients, SMM are more likely to use oral medications (66% versus 38%, p < 0.001), penile injections (26% versus 13%, p < 0.001), vacuum pumps (27% versus 11%, p < 0.001), and penile constriction rings (36% versus 16%, p < 0.001)119 (Table 1).
In the general population, sildenafil has been found to help with erectile dysfunction. Initiating sildenafil before radiation and continuing it during radiation demonstrated improved erectile function.125 Additionally, in a randomized controlled cross-over study, 36% of men responded to sildenafil but not to placebo.126 Similarly, starting sildenafil after RP helps improve erectile dysfunction and starting sildenafil sooner shows better rehabilitation.127 In addition to PDE-5 inhibitors, VEDs might help with erectile dysfunction following radiation therapy and RP. This is especially important in patients who might have a contraindication to PDE-5 inhibitors due to a concomitant medication or comorbidity. 128,129
Of important note to clinicians is the recreational use of alkyl nitrites (“poppers”) in the SMM community. “Poppers” are inhalants used to circumvent anodyspareunia through the the upregulation of cyclic guanosine monophosphate (cGMP). This promotes relaxation of musculature, including the internal sphincter, which can assist with accommodation of a partner’s penis. One study found that approximately 46% of 1,745 general SMM used alkyl nitrites in the last 6 months, primarily to facilitate penetration.130 It is essential to inquire about and counsel patients on the use of “poppers” when prescribing a PDE-5 inhibitor (e.g., sildenafil, tadalafil), as the combination of these drugs can cause hemodynamic instability, hypotension and syncope131 (FIG. 2).
Penile stretching
In addition to assistance with erectile dysfunction, VEDs and PDE-5 inhibitors might have a role in the restoration of penile length, girth, and shape following prostate cancer treatment (Table 1). There have been trials investigating the use of VEDs for penile changes following RP. In a cohort of 28 patients following RP, VED use was found to preserve penile length when used starting one month following surgery.132 Additionally, the use of VEDs was associated with smaller decreases in penile size compared to no treatment.129 While there is not as strong of an association between penile shortening and changes with radiation treatment, there are ongoing studies to understand VEDs to prevent penile shrinkage during radiation.128 Moreover, PDE-5 inhibitors might also help with changes in penile length. In a randomized study investigating the effect of tadalafil 5 mg daily, tadalafil 20 mg as needed, or placebo following RP for prostate cancer found that 5 mg tadalafil helped preserve penile length compared to placebo.133
Climacturia Rehabilitation
Climacturia rehabilitation includes pelvic floor exercises, blood flow restriction, and surgical intervention (Table 1). Additionally, emptying one’s bladder before intercourse and using condoms might help manage climacturia.76 In a randomized controlled trial, patients who underwent RP had significantly less climacturia events after the use of pelvic floor exercises compared to those who underwent RP and did not participate in pelvic floor exercises (p = 0.004).134 In addition to pelvic floor exercises, blood flow restriction might help decrease climacturia. Penile constriction (‘cock’) rings work similarly to VEDs and prevent blood flow out of the penile vasculature and can be a helpful intervention for patients with mild erectile difficulties, can increase pleasure during orgasm,30 and can help reduce symptoms of climacturia.135
Constriction bands have been investigated for treatment in the general population for patients with climacturia after RP. In a study of 14 men who underwent RP, a reduction of the frequency of climacturia at 6 months was found following the addition of a ‘cock’ ring. In fact, 48% of patients experienced no climacturia with a cock ring at 6 months.135 It is important to note that cock rings should not be left on for more than 20 minutes.30 Surgical management is another intervention to help alleviate climacturia. In a cohort of patients following RP, those who received an artificial urinary sphincter or sling placement had improvement in sexual urinary symptoms and QoL.136 More recently a mini-jupette, a sling placed and sutured over the urthera, has been utilized to help climacturia.137 In a cohort of 38 patients with erectile dysfunction, a mini-juppete was placed and among 30 patients previously with climacturia, 92.8% noticed improvement in symptoms.138
Treatment of orgasm changes
Few studies have identified possible treatments for issues with orgasm (Table 1). In the general population, tamsulosin might help with dysorgasmia following RP and in one study, dysorgasmia pain improved in 77% of patients after tamsulosin initiation.82 In a retrospective study of 131 men in the general population with orgasm disorders, cabergoline helped improve dysorgasmia. A subset of men in this population had prior RP and responded positively to the treatment.139 However, more studies are required to understand how to restore orgasms in SMM after prostate cancer treatment, especially in patients participating as the receptive partner in receptive anal intercourse.
Receptive anal intercourse rehabilitation
There is an unmet need to understand how other sexual assistive devices such as vibrators, dildos, lubricants, and other products might help SMM prostate cancer survivors’ sexual dysfunction, especially anodyspareunia (Table 1). Ussher et al. observed that SMM are more likely to use vibrators and dildos compared to heterosexual men (36% versus 16%, p < 0.001).119 Moreover, from the Restore-1 study, Rosser et al. identified that, while erectile enhancing drugs, pelvic floor exercises, penile injections, and vacuum pumps were the most commonly discussed treatment options with SMM; surgical implants, referral to a sexual counselor, and the use of dildos, butt plugs, or anal dilators received higher satisfaction ratings among SMM prostate cancer survivors. This highlights the critical need to investigate ways to restore receptive anal intercourse functioning.140
Treatment for other cancers, such as cervical cancer, have demonstrated that sexual devices, including dilators and vibrators can assist in sexual rehabilitation in patients with reduced sensation or arousal following treatment. In a pilot study of 15 females with cervical cancer, a clitoral therapy device significantly improved sexual desire, arousal, orgasm, sexual satisfaction and decreased associated pain. The female sexual function index score increased from 17 to 29.4 after three months of treatment (maximum score of 36; p < 0.001). Gynecological examinations revealed an improvement in vaginal elasticity and mucosal color, a decrease in bleeding and ulceration, as well as an increase in moisture.141 Additionally, vaginal dilators are commonly used after pelvic cancer therapy to prevent stenosis and stretch the vagina.142
Like vaginal dilators, anal dilators might be useful for SMM prostate cancer survivors receiving radiation. Acutely, radiation can cause irritation, pain, and friability due to inflammation.143 These changes are mediated by the inflammatory response, thus fibromuscular tissue and adhesions might develop and lead to anal stenosis.144 To help shape the anal canal and prevent anal stenosis, it might be useful to use anal dilators after radiation treatment.145–147 Through the use of dilators, patients can prevent scar tissue from forming and help break down existing scar tissue145–147 which will in turn help the anus and rectum to become more elastic.148,149 Studies are needed to investigate the feasibility and outcome of anal dilators to help mitigate anodyspareunia in SMM prostate cancer survivors.
Moreover, prostate massage vibrators might be a useful recommendation for sexual dysfunction restoration in SMM prostate cancer survivors. Prostate massage vibrators can assist men by achieving orgasm through stimulation of the prostate gland. Even if the prostate is removed or damaged, the surrounding sensory nerves might be stimulated and enhanced by a prostate massage vibrator. In the general population, prostate massage vibrators can alleviate overall prostate pain, as two studies with a total of 115 participants found a statistically significant decrease in prostatic pain score with prostate massage vibrators compared to no intervention.150,151 This might be a useful intervention for SMM prostate cancer survivors; however, more studies are required to confirm their benefit. These interventions to help restore and preserve receptive anal intercourse function might help SMM prostate cancer survivors preserve sexual role identity in receptive anal intercourse.
Maintaining Sexual Health
Questionnaires to monitor toxicity
In addition to discussing treatment options and outcomes at consultation, it is important to follow up with patients after treatment to monitor the toxic effects of treatment. Within the SMM community, it is important to follow up on aspects relevant to anal intercourse in addition to erectile function. Currently, many practices monitor the toxic effects of prostate cancer treatment using standardized questionnaires. These questionnaires include the Male Sexual Health Questionnaire (MSHQ),153 Expanded Prostate Cancer Index Composite (EPIC),154 International Index of Erectile Function (IIEF),155 and Sexual Health Inventory for Men (SHIM), an abbreviated version of IIEF (IIEF-5).156 These questionnaires focus on erectile function necessary for vaginal intercourse and omit information related to anal intercourse, neglecting the needs of many SMM patients.157 Additionally, questionnaires were developed in cohorts with uniform sexual orientation and gender representation limiting the validity and usefulness within a sexually diverse patient population.157 The IIEF was modified to IIEF-MSM for HIV-positive SMM which contains information relevant to insertive and receptive anal intercourse, but still focuses on erectile function.158 Additionally, the score was developed for the HIV population and has not been validated among prostate cancer survivors who might suffer from different sexual toxicities than people living with HIV.
New questionnaires are being developed with more inclusive questions to address the needs of SMM. In a group of 53 SMM following prostate cancer treatment, 64% reported a belief that the prostate is a source of sexual pleasure (p < 0.0001) and 53% felt that it is important to measure sexual satisfaction after receptive anal intercourse (p < 0.01).159 Lee et al.157 also created a questionnaire consisting of 13 domains including libido, ejaculation, erection, orgasm, receptive/insertive anal intercourse, masturbation, oral sex, urinary incontinence or climacturia, and other general sexual questions encompassing a wider range of sexual practices. This questionnaire covers the broader SMM sexual experience; however further analysis is necessary for validation.157 Polter et al.160 also sought to develop and evaluate a more inclusive QoL questionnaire for SMM called the Sexual Minorities and Prostate Cancer Scale (SMACS) using patients from the Restore-2 study.33,161,162 The questionnaire contains three sections: behavior/desire, problems, and role in sex as well as 5 validated subscales: sexual satisfaction, sexual confidence, frequency of issues, urinary incontinence in sex, and problematic receptive anal intercourse. The scale is reliable and can be used in conjunction with other existing scales. These questionnaires must be implemented into daily clinical practice and research.
Receptive anal intercourse resumption after treatment
For men who engage in receptive anal intercourse (“bottoms”), it is important to counsel on the safe resumption of receptive anal intercourse following treatment. The UK has developed guidance based on a panel of 15 clinical oncologists and 11 urologists utilizing a modified Delphi technique to understand the timing for when patients can resume receptive anal intercourse.163 Still no clear consensus was reached for many of the interventions, and further research is required to define the time interval necessary before intercourse can safely be resumed.
Ninety one percent of panel members agreed that patients should refrain from receptive intercourse after surgery. Abstaining from intercourse after RP will allow the vesicourethral anastomosis to heal and reduce the risk of leakage and urinary incontinence. Additionally, RP might weaken the rectal wall, leaving it susceptible to trauma from receptive anal intercourse, which could prolong recovery or cause perforation. The recommended time to avoid receptive anal intercourse after RP is 2 weeks. Seventy three percent of panel members agreed that patients should abstain from intercourse after EBRT. This time will allow the inflammation from radiation to subside. Without allowing sufficient time to heal, trauma to this area could exacerbate inflammation and radiation induced proctitis. Patients should refrain from anal intercourse for 6 weeks following EBRT.
All the panelists recommended abstinence from receptive anal intercourse after brachytherapy (high and low dose rate). Following high dose rate brachytherapy, patients should abstain for 2 months and following low dose rate, patients should abstain from anal intercourse for 1-2 months.163 The panel members cite the need to allow prostate and rectal inflammation to subside and to decrease potential exposure to the patient’s partner as important reasons to abstain. Similarly, a study investigating wait times for receptive anal intercourse and sustained cuddling (or “spooning”) after low dose brachytherapy treatment concluded that patients treated with I125 should avoid “spooning” for 2 months and those treated with Pd103 do not need to avoid “spooning” following treatment. The authors additionally state that patients should avoid receptive anal intercourse following I125 seed placement for 6 months and following Pd103seed placement for 2 months.164 The results from this study differ from the UK panel consensus demonstrating further research is needed. Additionally, given that Pd103 is usually given in combination with EBRT, a patient should be counseled on avoiding anal intercourse for 2 months after the last day of treatment with brachytherapy or EBRT (FIG. 2).
Sexual practices following treatment
During consultation and again following treatment, patients should be counseled on common sexual practices to be avoided after treatment. For example, in any male receiving low dose rate brachytherapy, a condom should be used to avoid ejecting a radioactive seed into a partner. However, there should be specific recommendations for men who participate in receptive anal intercourse. Anal intercourse and vaginal intercourse are associated with different sets of risks. Anal mucosa is less compliant and accommodating than vaginal mucosa, resulting in a higher risk of STI and HIV contraction during anal intercourse due to mucosal tear and damage.165–167 Within the SMM community, condom use is already sparse. In fact, within a cohort of prostate cancer SMM survivors, approximately 22% of participants reported unprotected insertive anal intercourse.44 It is imperative as a provider to counsel patients on condom use following prostate cancer treatment to decrease the risk of HIV/STI acquisition (FIG. 2).
In both the Restore-144 and Restore-2162 studies, evidence showed that patients became infected with HIV or other STIs after treatment. In Restore-2162, approximately 11.4% of patients became infected with an STI following prostate cancer treatment. These infections include syphilis (4.3%) gonorrhea (2.8%), chlamydia (2.5%), and HIV (1%, n = 4).162 Similarly, in Restore-1,44 3 (1.8%) of the 171 at risk patients became infected with HIV following prostate cancer treatment. Risk factors for HIV/STI acquisition post treatment can include changes in sexual role (top to bottom can increase risk of STI/HIV),44,104 varied relationships, and less condom use.168 Thus, providers must discuss safe sex practices including HIV/STI risk, the importance of condoms, and HIV pre-exposure prophylaxis (PrEP). (FIG. 2)
Providers might also want to discuss the appropriate lubricant to help with anal intercourse following prostate cancer treatment. Lubricant can help with anal intercourse accommodation and can help intensify and prolong sexual intercourse.152 For receptive anal intercourse, silicone-based lubricants have the advantage of persisting on the mucous membranes and after treatment silicone lubricant can adhere to scar tissue. 30,152
In addition to lubricant, counseling SMM on safe anal intercourse preparation following prostate cancer treatment is also recommended. Given the presence of fecal matter in the rectum, many patients will cleanse the rectal vault with douches (or enemas) before engaging in receptive anal intercourse.169 In fact, in a large survey study of 5,000 SMM, approximately 88% of patients who have receptive anal intercourse practice anal douching.170 Men might use regular water, soapy water, salt-water, or commercial products such as saline solution, sodium phosphates, mineral oils/glycerins and laxatives.170
Douching can damage the rectal lining and cause bleeding, which in turn leads to increased risk of infection from HIV/STIs.171,172 Additionally, it can alter the rectal microbiome,130 which is essential for maintaining the rectal epithelium and host immunity,173 as well as preventing surgical and procedural complications.174 Furthermore, the microbiome has been implicated in acute radiation proctitis. Synbiotics, or mixtures of probiotics (helpful gut bacteria) and prebiotics (non-digestible compounds for probiotic growth assistance), have been shown to help reduce the risk of acute proctitis.175 Future research is needed to understand how to safely cleanse before anal intercourse as well as the role of the microbiome in mediating toxicity. While research is ongoing,176 it is important to counsel patients on the risks of vigorous anal douching following prostate cancer treatment and to consider alternatives, including high-fiber diets with external gentle shower rinsing before intercourse.
Gender Minorities with Prostate Cancer
While research is emerging regarding SMM with prostate cancer, little information exists regarding gender minority patients with prostate cancer, including transgender women and trans feminine people in general (TGW, people who are recorded male at birth with feminine gender identity). Issues surrounding gender minorities can be subsumed within discussions of sexual identity and this population’s specific needs might become neglected. In the forthcoming section we highlight issues specific to gender minorities.
Gender minorities are a diverse cohort
Contributing to the nuance of this population is that gender minorities are a heterogenous cohort with a range of anatomy and hormonal milieu with a diverse sexual script. Physicians might care for TGW who are just beginning their use of gender affirming hormone therapy (GAHT) or for TGW who have been using GAHT for extended periods of time. Additionally, physicians might care for TGW who have undergone, plan to undergo, do not plan to undergo, or are undecided about receiving gender affirming surgery (GAS). These various factors contribute to the individualized profile and resultant necessary personalized treatment discussion for TGW with prostate cancer. It is extremely important to be sensitive and aware of the range of TGW experiences and presentations when managing TGW with prostate cancer, as 48% of transgender patients avoid or delay care due to medical insensitivity.177
Epidemiology and presentation of prostate cancer in gender minorities
With a lifetime prevalence of 12.1%, prostate cancer is the most common non-dermatologic malignancy in cisgender males, including SMM;1 however, the prevalence and incidence of prostate cancer in TGW is likely significantly lower.178,179 One of the largest studies to date of a cohort study of 2,281 TGW in the Netherlands, concluded that women receiving androgen deprivation therapy and estrogens were at substantially lower risk for prostate cancer than the general male population.9 The low incidence and prevalence of prostate cancer in TGW is multifactorial. Contributory factors might include barriers to care for TGW180, the use of estrogen-supplementing GAHT, which might be protective against prostate cancer181, and a younger overall mortality for TGW.182,183
Despite a lower relative incidence and prevalence, studies suggest that prostate cancer might have a more aggressive presentation in TGW. A non-systematic review of the literature identified 10 case reports of TGW with prostate cancer and found that 6 patients presented with metastatic disease, 3 with local or locally advanced disease, and 1 with unknown disease.184 In TGW, the development of prostate cancer has been debated as the estrogen-testosterone balance plays a role in prostate cancer development. In transgender patients, estrogen is given to suppress testosterone. This combination has been shown to increase the risk of prostate cancer in rats, as the incidence of prostate cancer increased from 35-40% in rats treated with testosterone alone to 90-100% in rats treated with combination testosterone and estrogen.185,186 Furthermore, TGW who begin their transition at older ages might have increased risk for prostate cancer than those who transitioned at a younger age and have presumably had prolonged exposure to estrogen therapy.
Prostate cancer in TGW might develop in the setting of medical or surgical castration from GAHT or feminizing GAS; therefore, prostate cancer in TGW is likely castration-resistant.184 Castration resistance portends worse outcomes in patients with prostate cancer with a median overall survival ranging from 9 to 36 months depending on the extent of metastatic disease.187–190 Thus, if TGW are at risk for prostate cancer and potentially develop more aggressive castration resistant disease, it is important to consider that the treatment course might be more aggressive,191–193 leading to more severe sexual health-related side effects.
Sexual health and dysfunction in gender minorities
Little information exists regarding management of sexual dysfunction in TGW with prostate cancer. At baseline, there are important factors to consider when managing sexual dysfunction in TGW. A systematic review evaluating sexual dysfunction in transgender people in general identified that feminizing GAHT might decrease libido in the short term, while feminizing genital reconstruction surgery can increase libido and arousal.194 Still, decreased libido might not be a concern for TGW and in one study with 45% of patients experiencing decreased libido, 20% reported it as a dysfunction and 25% reported it without causing distress.195 Additionally, patients who have undergone GAS might experience dyspareunia (pain during vaginal intercourse). The standard procedure is penile inversion vaginoplasty in which the neovagina does not self-lubricate196 In cases where there is insufficient penoscrotal tissue or when penile inversion failed, bowel segment vaginoplasty can be utilized which can result in different lubrication and dyspareunia outcomes.197 Still, after GAHT and GAS, TGW have more sexual encounters, suggesting that these procedures increase confidence, comfort198,199 and potentially even happiness.194,200 Lastly, understanding the diversity of sexuality among trans feminine individuals is important. A physician might make the well-intentioned assumption that a TGW would have a similar sexual script to other women and that a TGW would not want to involve their penis as part of their sexual pleasure; however, this is not always the case as TGW might wish to use their penis in a range of sexual activities including being insertive partners.201,202
Thus, when considering sexual dysfunction in TGW with prostate cancer, one must approach sexual toxicities differently than when considering sexual dysfunction in SMM with prostate cancer. For example, TGW might experience dyspareunia through intercourse with the neovagina. 169 Additionally, within this population, questions and questionnaires must be customized as TGW might experience orgasm and sexual arousal from the neoclitoris rather than (or in addition to) the prostate.169,203
Discussing treatment-related sexual dysfunction with gender minorities
TGW must be counseled on sexual dysfunction and treatment options for prostate cancer at consultation and follow up (FIG. 3). Managing sexual dysfunction in transgender patients with prostate cancer depends on whether the patient has already undergone, or might later undergo GAS.184 For TGW who have not undergone GAS, discussion must include the patient’s desire to have GAS surgery in the future. If a TGW wishes to pursue GAS following prostate cancer treatment, further discussions are necessary before definitive cancer management. Analogous to breast reconstruction management following breast cancer management, there must be a multidisciplinary discussion among the surgical oncologist, radiation oncologist, and reconstructive surgeon.204 A more nuanced and detailed conversation should then ensue regarding sexual practices and relevant toxicities. Careful consideration should be given to safety and effectiveness of the cancer treatment as well as feasibility and cosmesis of future GAS. This conversation will enable fully informed treatment decisions. For example, while a labiaplasty might be feasible after RP, EBRT, or brachytherapy, a vaginoplasty after treatment might have higher risks including fistula formation, urethral meatus stenosis, and incontinence.184 For TGW who have already undergone GAS, prostate cancer treatment might be complex as RP might lead to fistula formation and EBRT and brachytherapy might lead to neovaginal stenosis requiring rehabilitation with dilators.142 As such, treating surgeons and radiation oncologists must be aware of anatomical changes.205 In addition, as many patients might be surgically or chemically castrate, management might follow castrate-resistant prostate cancer guidelines.191–193 While decisions in this population might focus on disease eradication, as treatments for castration resistant prostate cancer advance,206 conversations surrounding sexual health might move to the forefront. Further research is necessary to understand how treatment should be modified and ideally personalized for TGW with prostate cancer.
Conclusion:
There is a paucity of data regarding the impact of prostate cancer therapies on sexual health outcomes in SMM and TGW. Existing studies illustrate that there are differences in the sexual health outcomes of SMM and HET. Treatment-related sexual dysfunctions following prostate cancer treatment experienced by sexual minority men include anodyspareunia, erectile dysfunction, climacturia, anejaculation, altered pleasurable sensation, and changes in penile shape. At consultation patients should be asked about sexual orientation, gender identity, and sexual role. Patients should be counseled on treatment related toxicities tailored to sexual role (top, bottom, versatile, side). Additionally, physicians should ask gender minority patients about hormones and surgical assignment surgery. Understanding the holistic patient will allow for informed patient conversations at consultation and shared decision making, when appropriate, for prostate cancer treatment selection.
While we acknowledge the role of the prostate, rectal wall, perianal skin and the surrounding neurovasculature in receptive anal intercourse, more research is needed to understand the mechanism of damage to surrounding anatomical structures from prostate cancer treatment and resultant sexual dysfunction. Knowing the mechanism of treatment related damage to the prostate and surrounding structures can allow researchers to develop novel ways to alleviate treatment related damage to the prostate and surrounding tissues as well as potentially restore prostate sensation. These advancements would help further correct the inequities in scientific and biomedical research.
Sexual health QoL questionnaires for prostate cancer patients are beginning to incorporate domains and questions relevant to SMM patients, especially related to receptive anal intercourse. Information from more inclusive questionnaires will empower clinicians with evidence when discussing anatomy, physiology and pathophysiology of organ function related to sexual pleasure in SMM and TGW with prostate cancer. Additionally, these data could empower the sexual and gender minority community to advocate for more equitable care and further research. Further information from validated questionnaires on sexual dysfunction and research on how prostate cancer treatment affects sexual role in SMM survivors would also enable scientific advancements in technologies to prevent and mitigate these toxicities.
Prostate cancer providers should commit to understanding the management of sexual health and dysfunction in sexual and gender minorities following prostate cancer treatment. Urologists, radiation oncologists, medical oncologists, and clinical oncologists must move beyond a narrow definition of sexual activity and sexual pleasure focused on heterosexual intercourse and reproductive ability in prostate cancer patients. Providers should incorporate the functional and physiologic anatomic basis for sexual pleasure in all prostate cancer patients, regardless of sexual or gender identity.
Key Points:
Anal intercourse can induce orgasm through pressure on the rectal wall and stimulation of nerves surrounding the prostate and seminal vesicles as well as within the rectum and anus.
Sexual dysfunctions following prostate cancer treatment experienced by sexual minority men include anodyspareunia, erectile dysfunction, climacturia, anejaculation, altered pleasurable sensation, and changes in penile length.
Sexual minority patients with prostate cancer should be counseled on different treatment related toxicities depending on sexual role (top, bottom, versatile, side).
Anal dilators (to assist with receptive anal intercourse), vacuum pumps (to induce stronger erections for insertive intercourse), and penile constriction rings (to manage climacturia) should be discussed with sexual minority men.
Gender minorities with prostate cancer are a heterogenous cohort with a range of anatomy and hormonal milieu requiring a nuanced and detailed conversation when discussing treatment and relevant toxicities.
Prostate cancer consultations with sexual minority men should include counseling on receptive anal intercourse resumption, condom use, HIV pre-exposure prophylaxis, and anal douching.
Acknowledgements:
Research reported in this publication was supported by the Office of The Director, National Institutes of Health under Award Number DP5OD031876. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health
Competing Interests:
MDG would like to report research funding from Bristol Myers Squibb, Novartis, Dendreon, Astra Zeneca, Merck, Genentech and is a paid advisory board consultant for Bristol Myers Squibb, Merck, Genentech, AstraZeneca, Pfizer, EMD Serono, SeaGen, Janssen, Numab, Dragonfly, GlaxoSmithKline, Basilea, UroGen, Rappta Therapeutics, Alligator, Silverback, Fujifilm, Curis. The other authors declare no competing interests.
Glossary of terms:
- Sexual and gender minority
individuals who identify as lesbian, gay, bisexual, transgender, gender diverse, asexual, queer, and intersex as well as those who do not but whose sexual orientation, gender identity, or reproductive development varies from traditional, societal, cultural, or physiological norms
- Sexual identity
refers to a person’s identity more broadly in sexual intercourse and relationships
- Sexual role
the role a person identifies with during sexual intercourse (e.g. top, bottom, versatile, side)
- Top
The insertive partner in anal intercourse; although this term has been generalized in sexual minority culture to include the insertive partner in oral intercourse
- Bottom
The receptive partner in anal intercourse; although this term has been generalized in sexual minority culture to include the receptive partner in oral intercourse
- Vers
Or verse, short for versatile, a person who engages in both the receptive and insertive role in intercourse
- Side
A SMM who does not engage in anal intercourse or identify with “top,” “bottom,” or “vers”
- Poppers
alkyl nitrites, inhalants used to relax anal musculature used for receptive anal intercourse
- Anodyspareunia
Pain during receptive anal intercourse
- Neovagina
A reconstructed or created vagina
- Neoclitoris
A reconstructed or created clitoris
Footnotes
Author contributions:
DRD researched data and wrote initial manuscript draft. All made a substantial contribution to the discussion of content as well as revised it critically for intellectual content. All authors approve the version to be published
References:
- 1.Siegel RL, Miller KD, Fuchs HE & Jemal A Cancer Statistics, 2021. CA: A Cancer Journal for Clinicians 71, 7–33, doi: 10.3322/caac.21654 (2021). [DOI] [PubMed] [Google Scholar]
- 2.Carroll PH & Mohler JL NCCN Guidelines Updates: Prostate Cancer and Prostate Cancer Early Detection. J Natl Compr Canc Netw 16, 620–623, doi: 10.6004/jnccn.2018.0036 (2018). [DOI] [PubMed] [Google Scholar]
- 3.Marshall DC et al. Female erectile tissues and sexual dysfunction after pelvic radiotherapy: A scoping review. CA Cancer J Clin, doi: 10.3322/caac.21726 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Hyun JS Prostate cancer and sexual function. World J Mens Health 30, 99–107, doi: 10.5534/wjmh.2012.30.2.99 (2012). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Donovan JL et al. Patient-Reported Outcomes after Monitoring, Surgery, or Radiotherapy for Prostate Cancer. New England Journal of Medicine 375, 1425–1437, doi: 10.1056/NEJMoa1606221 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Resnick MJ et al. Long-term functional outcomes after treatment for localized prostate cancer. N Engl J Med 368, 436–445, doi: 10.1056/NEJMoa1209978 (2013). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Health N. I. o.. Sexual and Gender Minority Populations in NIH-Supported Research, <https://grants.nih.gov/grants/guide/notice-files/NOT-OD-19-139.html> (2019).
- 8.Alexis O & Worsley AJ The Experiences of Gay and Bisexual Men Post-Prostate Cancer Treatment: A Meta-Synthesis of Qualitative Studies. Am J Mens Health 12, 2076–2088, doi: 10.1177/1557988318793785 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.de Nie I et al. Prostate Cancer Incidence under Androgen Deprivation: Nationwide Cohort Study in Trans Women Receiving Hormone Treatment. J Clin Endocrinol Metab 105, e3293–3299, doi: 10.1210/clinem/dgaa412 (2020). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Rosenberger JG et al. Sexual behaviors and situational characteristics of most recent male-partnered sexual event among gay and bisexually identified men in the United States. J Sex Med 8, 3040–3050, doi: 10.1111/j.1743-6109.2011.02438.x (2011). [DOI] [PubMed] [Google Scholar]
- 11.Gil-Llario MD, Gil-Juliá B, Giménez-García C, Bergero-Miguel T & Ballester-Arnal R Sexual behavior and sexual health of transgender women and men before treatment: Similarities and differences. Int J Transgend Health 22, 304–315, doi: 10.1080/26895269.2020.1838386 (2021). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Nematollahi A, Gharibzadeh S, Damghanian M, Gholamzadeh S & Farnam F Sexual behaviors and vulnerability to sexually transmitted infections among transgender women in Iran. BMC Women’s Health 22, 170, doi: 10.1186/s12905-022-01753-7 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Dickstein DR & Marshall DC Top, bottom or vers? Creating a more equitable health system for sexual and gender minority patients with prostate cancer. Nat Rev Urol, doi: 10.1038/s41585-022-00600-6 (2022). [DOI] [PubMed] [Google Scholar]
- 14.Goldstone SE The Ups and Downs of Gay Sex After Prostate Cancer Treatment. Journal of Gay & Lesbian Psychotherapy 9, 43–55, doi: 10.1300/J236v09n01_04 (2005). [DOI] [Google Scholar]
- 15.Griggs J et al. American Society of Clinical Oncology Position Statement: Strategies for Reducing Cancer Health Disparities Among Sexual and Gender Minority Populations. Journal of Clinical Oncology 35, 2203–2208, doi: 10.1200/jco.2016.72.0441 (2017). [DOI] [PubMed] [Google Scholar]
- 16.Chen RC et al. Association Between Choice of Radical Prostatectomy, External Beam Radiotherapy, Brachytherapy, or Active Surveillance and Patient-Reported Quality of Life Among Men With Localized Prostate Cancer. Jama 317, 1141–1150, doi: 10.1001/jama.2017.1652 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Barocas DA et al. Association Between Radiation Therapy, Surgery, or Observation for Localized Prostate Cancer and Patient-Reported Outcomes After 3 Years. Jama 317, 1126–1140, doi: 10.1001/jama.2017.1704 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Ludmir EB et al. Reporting and exclusion of sexual and gender minorities in cancer clinical trials. Int J Cancer 146, 2360–2361, doi: 10.1002/ijc.32700 (2020). [DOI] [PubMed] [Google Scholar]
- 19.Levin RJ Prostate-induced orgasms: A concise review illustrated with a highly relevant case study. Clinical Anatomy 31, 81–85, doi: 10.1002/ca.23006 (2018). [DOI] [PubMed] [Google Scholar]
- 20.Mah K & Binik YM Are orgasms in the mind or the body? Psychosocial versus physiological correlates of orgasmic pleasure and satisfaction. J Sex Marital Ther 31, 187–200, doi: 10.1080/00926230590513401 (2005). [DOI] [PubMed] [Google Scholar]
- 21.Krassioukov A & Elliott S Neural Control and Physiology of Sexual Function: Effect of Spinal Cord Injury. Top Spinal Cord Inj Rehabil 23, 1–10, doi: 10.1310/sci2301-1 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Emhardt E, Siegel J & Hoffman L Anatomic variation and orgasm: Could variations in anatomy explain differences in orgasmic success? Clin Anat 29, 665–672, doi: 10.1002/ca.22703 (2016). [DOI] [PubMed] [Google Scholar]
- 23.Levin RJ in Forensic Medicine: Clinical and Pathological Aspects (eds Payne-James Jason, Busuttil Anthony, & Smock William) Ch. 26, (London, United Kingodm, 2003). [Google Scholar]
- 24.Agnew J Some anatomical and physiological aspects of anal sexual practices. J Homosex 12, 75–96, doi: 10.1300/j082v12n01_04 (1985). [DOI] [PubMed] [Google Scholar]
- 25.Goligher JC, Duhle HL & Nixon HH Surgery of The Anus, Rectum and Colon. 4th edn, (Bailliere Tindale, 1981). [Google Scholar]
- 26.Kinsey AC, Pomery WB & Martin CE Sexual behavior in the human male. (W.B. Saunders Co., 1948). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Cunningham DJRGJ Cunningham’s Textbook of anatomy. (Oxford University Press, 1972). [Google Scholar]
- 28.Bennett CJ, Seager SW & McGuire EJ Electroejaculation for recovery of semen after retroperitoneal lymph node dissection: case report. J Urol 137, 513–515, doi: 10.1016/s0022-5347(17)44094-8 (1987). [DOI] [PubMed] [Google Scholar]
- 29.Gorsch RV Proctologic anatomy. (Williams &Wilkins, 1955). [Google Scholar]
- 30.Dewitte M & Reisman Y Clinical use and implications of sexual devices and sexually explicit media. Nature Reviews Urology 18, 359–377, doi: 10.1038/s41585-021-00456-2 (2021). [DOI] [PubMed] [Google Scholar]
- 31.Blair KL, Cappell J & Pukall CF Not All Orgasms Were Created Equal: Differences in Frequency and Satisfaction of Orgasm Experiences by Sexual Activity in Same-Sex Versus Mixed-Sex Relationships. J Sex Res 55, 719–733, doi: 10.1080/00224499.2017.1303437 (2018). [DOI] [PubMed] [Google Scholar]
- 32.National Cancer Institute. Surveillance, E., and End Results Program. Cancer stat facts: prostate cancer. (2022). <https://seer.cancer.gov/statfacts/html/prost.html>. [Google Scholar]
- 33.Rosser BRS et al. Health Disparities of Sexual Minority Patients Following Prostate Cancer Treatment: Results From the Restore-2 Study. Front Oncol 12, 812117, doi: 10.3389/fonc.2022.812117 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Hart TL et al. Changes in sexual roles and quality of life for gay men after prostate cancer: challenges for sexual health providers. J Sex Med 11, 2308–2317, doi: 10.1111/jsm.12598 (2014). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Ussher JM et al. Health-Related Quality of Life, Psychological Distress, and Sexual Changes Following Prostate Cancer: A Comparison of Gay and Bisexual Men with Heterosexual Men. J Sex Med 13, 425–434, doi: 10.1016/j.jsxm.2015.12.026 (2016). [DOI] [PubMed] [Google Scholar]
- 36.Latkin C et al. Social network predictors of disclosure of MSM behavior and HIV-positive serostatus among African American MSM in Baltimore, Maryland. AIDS Behav 16, 535–542, doi: 10.1007/s10461-011-0014-z (2012). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Santillo VM & Lowe FC Prostate Cancer and the Gay Male. Journal of Gay & Lesbian Psychotherapy 9, 9–27, doi: 10.1300/J236v09n01_02 (2005). [DOI] [Google Scholar]
- 38.Griffin M, Krause KD, Kapadia F & Halkitis PN A Qualitative Investigation of Healthcare Engagement Among Young Adult Gay Men in New York City: A P18 Cohort Substudy. LGBT Health 5, 368–374, doi: 10.1089/lgbt.2017.0015 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Tadele G & Amde WK Health needs, health care seeking behaviour, and utilization of health services among lesbians, gays and bisexuals in Addis Ababa, Ethiopia. Int J Equity Health 18, 86, doi: 10.1186/s12939-019-0991-5 (2019). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Polter EJ et al. Health-related quality of life by human immunodeficiency virus status in a cross-sectional survey of gay and bisexual prostate cancer survivors. Psychooncology 28, 2351–2357, doi: 10.1002/pon.5228 (2019). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Briganti A et al. Predicting erectile function recovery after bilateral nerve sparing radical prostatectomy: a proposal of a novel preoperative risk stratification. J Sex Med 7, 2521–2531, doi: 10.1111/j.1743-6109.2010.01845.x (2010). [DOI] [PubMed] [Google Scholar]
- 42.Solomon SE, Rothblum ED & Balsam KF Money, housework, sex, and conflict : Same-sex couples in civil unions, those not in civil unions, and heterosexual married siblings. Sex roles 52, 561–575, doi: 10.1007/s11199-005-3725-7 (2005). [DOI] [Google Scholar]
- 43.Gotta G et al. Heterosexual, Lesbian, and Gay Male Relationships: A Comparison of Couples in 1975 and 2000. Family Process 50, 353–376, doi: 10.1111/j.1545-5300.2011.01365.x (2011). [DOI] [PubMed] [Google Scholar]
- 44.Rosser BRS et al. The Sexual Functioning of Gay and Bisexual Men Following Prostate Cancer Treatment: Results from the Restore Study. Arch Sex Behav 49, 1589–1600, doi: 10.1007/s10508-018-1360-y (2020). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Lee JY, Spratt DE, Liss AL & McLaughlin PW Vessel-sparing radiation and functional anatomy-based preservation for erectile function after prostate radiotherapy. Lancet Oncol 17, e198–208, doi: 10.1016/s1470-2045(16)00063-2 (2016). [DOI] [PubMed] [Google Scholar]
- 46.Kumar A et al. Nerve-sparing robot-assisted radical prostatectomy: Current perspectives. Asian J Urol 8, 2–13, doi: 10.1016/j.ajur.2020.05.012 (2021). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Sanda MG et al. Quality of life and satisfaction with outcome among prostate-cancer survivors. N Engl J Med 358, 1250–1261, doi: 10.1056/NEJMoa074311 (2008). [DOI] [PubMed] [Google Scholar]
- 48.Dearnaley D et al. Conventional versus hypofractionated high-dose intensity-modulated radiotherapy for prostate cancer: 5-year outcomes of the randomised, non-inferiority, phase 3 CHHiP trial. The Lancet Oncology 17, 1047–1060, doi: 10.1016/S1470-2045(16)30102-4 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Fransson P et al. Ultra-hypofractionated versus conventionally fractionated radiotherapy for prostate cancer (HYPO-RT-PC): patient-reported quality-of-life outcomes of a randomised, controlled, non-inferiority, phase 3 trial. Lancet Oncol 22, 235–245, doi: 10.1016/s1470-2045(20)30581-7 (2021). [DOI] [PubMed] [Google Scholar]
- 50.Ho CK et al. Long-term outcomes following proton therapy for prostate cancer in young men with a focus on sexual health. Acta Oncol 57, 582–588, doi: 10.1080/0284186x.2018.1427886 (2018). [DOI] [PubMed] [Google Scholar]
- 51.Gore JL, Kwan L, Lee SP, Reiter RE & Litwin MS Survivorship Beyond Convalescence: 48-Month Quality-of-Life Outcomes After Treatment for Localized Prostate Cancer. JNCI: Journal of the National Cancer Institute 101, 888–892, doi: 10.1093/jnci/djp114 (2009). [DOI] [PubMed] [Google Scholar]
- 52.Rosser BRS et al. What Gay and Bisexual Men Treated for Prostate Cancer Want in a Sexual Rehabilitation Program: Results of the Restore Needs Assessment. Urol Pract 5, 192–197, doi: 10.1016/j.urpr.2017.05.001 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Grabski B & Kasparek K Sexual Anal Pain in Gay and Bisexual Men: In Search of Explanatory Factors. The Journal of Sexual Medicine 17, 716–730, doi: 10.1016/j.jsxm.2020.01.020 (2020). [DOI] [PubMed] [Google Scholar]
- 54.Cheng PJ Sexual Dysfunction in Men Who Have Sex With Men. Sex Med Rev 10, 130–141, doi: 10.1016/j.sxmr.2021.01.002 (2022). [DOI] [PubMed] [Google Scholar]
- 55.Rosser BR, Metz ME, Bockting WO & Buroker T Sexual difficulties, concerns, and satisfaction in homosexual men: an empirical study with implications for HIV prevention. J Sex Marital Ther 23, 61–73, doi: 10.1080/00926239708404418 (1997). [DOI] [PubMed] [Google Scholar]
- 56.Vansintejan J, Vandevoorde J & Devroey D The GAy MEn Sex StudieS: Anodyspareunia Among Belgian Gay Men. Sex Med 1, 87–94, doi: 10.1002/sm2.6 (2013). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Damon W & Rosser BR Anodyspareunia in men who have sex with men: prevalence, predictors, consequences and the development of DSM diagnostic criteria. J Sex Marital Ther 31, 129–141, doi: 10.1080/00926230590477989 (2005). [DOI] [PubMed] [Google Scholar]
- 58.Wheldon CW et al. Pain and Loss of Pleasure in Receptive Anal Sex for Gay and Bisexual Men following Prostate Cancer Treatment: Results from the Restore-1 Study. J Sex Res, 1–8, doi: 10.1080/00224499.2021.1939846 (2021). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Price JG, Stone NN & Stock RG Predictive factors and management of rectal bleeding side effects following prostate cancer brachytherapy. Int J Radiat Oncol Biol Phys 86, 842–847, doi: 10.1016/j.ijrobp.2013.04.033 (2013). [DOI] [PubMed] [Google Scholar]
- 60.Ussher JM et al. Threat of Sexual Disqualification: The Consequences of Erectile Dysfunction and Other Sexual Changes for Gay and Bisexual Men With Prostate Cancer. Arch Sex Behav 46, 2043–2057, doi: 10.1007/s10508-016-0728-0 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Wassersug RJ, Lyons A, Duncan D, Dowsett GW & Pitts M Diagnostic and outcome differences between heterosexual and nonheterosexual men treated for prostate cancer. Urology 82, 565–571, doi: 10.1016/j.urology.2013.04.022 (2013). [DOI] [PubMed] [Google Scholar]
- 62.Motofei IG, Rowland DL, Popa F, Kreienkamp D & Paunica S Preliminary study with bicalutamide in heterosexual and homosexual patients with prostate cancer: a possible implication of androgens in male homosexual arousal. BJU Int 108, 110–115, doi: 10.1111/j.1464-410X.2010.09764.x (2011). [DOI] [PubMed] [Google Scholar]
- 63.Gebert S Are penile prostheses a viable option to recommend for gay men? International Journal of Urological Nursing 8, 111–113, doi: 10.1111/ijun.12048 (2014). [DOI] [Google Scholar]
- 64.Bancroft J, Carnes L, Janssen E, Goodrich D & Long JS Erectile and ejaculatory problems in gay and heterosexual men. Arch Sex Behav 34, 285–297, doi: 10.1007/s10508-005-3117-7 (2005). [DOI] [PubMed] [Google Scholar]
- 65.Sommers BD et al. Predictors of patient preferences and treatment choices for localized prostate cancer. Cancer 113, 2058–2067, doi: 10.1002/cncr.23807 (2008). [DOI] [PubMed] [Google Scholar]
- 66.Green TP, Saavedra-Belaunde J & Wang R Ejaculatory and Orgasmic Dysfunction Following Prostate Cancer Therapy: Clinical Management. Med Sci (Basel) 7, doi: 10.3390/medsci7120109 (2019). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 67.Ramirez-Fort MK et al. Prostatic irradiation-induced sexual dysfunction: a review and multidisciplinary guide to management in the radical radiotherapy era (Part I defining the organ at risk for sexual toxicities). Reports of practical oncology and radiotherapy : journal of Greatpoland Cancer Center in Poznan and Polish Society of Radiation Oncology 25, 367–375, doi: 10.1016/j.rpor.2020.03.007 (2020). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68.Sullivan JF, Stember DS, Deveci S, Akin-Olugbade Y & Mulhall JP Ejaculation profiles of men following radiation therapy for prostate cancer. J Sex Med 10, 1410–1416, doi: 10.1111/jsm.12101 (2013). [DOI] [PubMed] [Google Scholar]
- 69.Walz J et al. Ejaculatory disorders may affect screening for prostate cancer. J Urol 178, 232–237; discussion 237-238, doi: 10.1016/j.juro.2007.03.037 (2007). [DOI] [PubMed] [Google Scholar]
- 70.Amarasekera C et al. MP40-01: The impact of sexual orientation on treatment decision-making and perceptions of sexual side-effects from prostate cancer. Journal of Urology 201, e586–e586, doi: 10.1097/01.JU.0000556093.77159.95 (2019). [DOI] [Google Scholar]
- 71.Prestage G, Hurley M & Brown G “Cum Play” among Gay Men. Archives of Sexual Behavior 42, 1347–1356, doi: 10.1007/s10508-013-0074-4 (2013). [DOI] [PubMed] [Google Scholar]
- 72.Danemalm Jägervall C, Brüggemann J & Johnson E Gay men’s experiences of sexual changes after prostate cancer treatment-a qualitative study in Sweden. Scand J Urol 53, 40–44, doi: 10.1080/21681805.2018.1563627 (2019). [DOI] [PubMed] [Google Scholar]
- 73.Harris J Living with Prostate Cancer: One Gay Man’s Experience. Journal of Gay & Lesbian Psychotherapy 9, 109–117, doi: 10.1300/J236v09n01_09 (2005). [DOI] [Google Scholar]
- 74.Mitteldorf D Psychotherapy with Gay Prostate Cancer Patients. Journal of Gay & Lesbian Psychotherapy 9, 57–67, doi: 10.1300/J236v09n01_05 (2005). [DOI] [Google Scholar]
- 75.O’Neil BB et al. Climacturia after definitive treatment of prostate cancer. J Urol 191, 159–163, doi: 10.1016/j.juro.2013.06.122 (2014). [DOI] [PubMed] [Google Scholar]
- 76.Lee J, Hersey K, Lee CT & Fleshner N Climacturia following radical prostatectomy: prevalence and risk factors. J Urol 176, 2562–2565; discussion 2565, doi: 10.1016/j.juro.2006.07.158 (2006). [DOI] [PubMed] [Google Scholar]
- 77.Koeman M, van Driel MF, Schultz WC & Mensink HJ Orgasm after radical prostatectomy. Br J Urol 77, 861–864, doi: 10.1046/j.1464-410x.1996.01416.x (1996). [DOI] [PubMed] [Google Scholar]
- 78.Choi JM, Nelson CJ, Stasi J & Mulhall JP Orgasm associated incontinence (climacturia) following radical pelvic surgery: rates of occurrence and predictors. J Urol 177, 2223–2226, doi: 10.1016/j.juro.2007.01.150 (2007). [DOI] [PubMed] [Google Scholar]
- 79.Frederick D, Gillespie BJ, Lever J, Berardi V & Garcia JR Sexual Practices and Satisfaction among Gay and Heterosexual Men in Romantic Relationships: A Comparison Using Coarsened Exact Matching in a U.S. National Sample. The Journal of Sex Research 58, 545–559, doi: 10.1080/00224499.2020.1861424 (2021). [DOI] [PubMed] [Google Scholar]
- 80.Lee TK et al. Impact of Prostate Cancer Treatment on the Sexual Quality of Life for Men-Who-Have-Sex-with-Men. J Sex Med 12, 2378–2386, doi: 10.1111/jsm.13030 (2015). [DOI] [PubMed] [Google Scholar]
- 81.Nolsøe AB, Jensen CFS, Østergren PB & Fode M Neglected side effects to curative prostate cancer treatments. International Journal of Impotence Research 33, 428–438, doi: 10.1038/s41443-020-00386-4 (2021). [DOI] [PubMed] [Google Scholar]
- 82.Barnas JL et al. The prevalence and nature of orgasmic dysfunction after radical prostatectomy. BJU Int 94, 603–605, doi: 10.1111/j.1464-410X.2004.05009.x (2004). [DOI] [PubMed] [Google Scholar]
- 83.Matsushita K, Tal R & Mulhall JP The evolution of orgasmic pain (dysorgasmia) following radical prostatectomy. J Sex Med 9, 1454–1458, doi: 10.1111/j.1743-6109.2012.02699.x (2012). [DOI] [PubMed] [Google Scholar]
- 84.Mogorovich A et al. Radical prostatectomy, sparing of the seminal vesicles, and painful orgasm. J Sex Med 10, 1417–1423, doi: 10.1111/jsm.12086 (2013). [DOI] [PubMed] [Google Scholar]
- 85.Hollenbeck BK, Dunn RL, Wei JT, Montie JE & Sanda MG Determinants of long-term sexual health outcome after radical prostatectomy measured by a validated instrument. J Urol 169, 1453–1457, doi: 10.1097/01.ju.0000056737.40872.56 (2003). [DOI] [PubMed] [Google Scholar]
- 86.Gay HA et al. External Beam Radiation Therapy or Brachytherapy With or Without Short-course Neoadjuvant Androgen Deprivation Therapy: Results of a Multicenter, Prospective Study of Quality of Life. Int J Radiat Oncol Biol Phys 98, 304–317, doi: 10.1016/j.ijrobp.2017.02.019 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 87.Olsson CE et al. Patient-reported sexual toxicity after radiation therapy in long-term prostate cancer survivors. Br J Cancer 113, 802–808, doi: 10.1038/bjc.2015.275 (2015). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 88.Frey A et al. Prevalence and Predicting Factors for Commonly Neglected Sexual Side Effects to External-Beam Radiation Therapy for Prostate Cancer. J Sex Med 14, 558–565, doi: 10.1016/j.jsxm.2017.01.015 (2017). [DOI] [PubMed] [Google Scholar]
- 89.Merrick GS, Wallner K, Butler WM, Lief JH & Sutlief S Short-term sexual function after prostate brachytherapy. Int J Cancer 96, 313–319, doi: 10.1002/ijc.1028 (2001). [DOI] [PubMed] [Google Scholar]
- 90.Finney G et al. Cross-sectional analysis of sexual function after prostate brachytherapy. Urology 66, 377–381, doi: 10.1016/j.urology.2005.03.045 (2005). [DOI] [PubMed] [Google Scholar]
- 91.Helgason AR, Fredrikson M, Adolfsson J & Steineck G Decreased sexual capacity after external radiation therapy for prostate cancer impairs quality of life. Int J Radiat Oncol Biol Phys 32, 33–39, doi: 10.1016/0360-3016(95)00542-7 (1995). [DOI] [PubMed] [Google Scholar]
- 92.Flynn KE, Lin L & Weinfurt KP Sexual function and satisfaction among heterosexual and sexual minority U.S. adults: A cross-sectional survey. PLoS One 12, e0174981, doi: 10.1371/journal.pone.0174981 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 93.Helgason AR et al. Waning sexual function--the most important disease-specific distress for patients with prostate cancer. Br J Cancer 73, 1417–1421, doi: 10.1038/bjc.1996.268 (1996). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 94.Hartman ME et al. Exploring gay couples’ experience with sexual dysfunction after radical prostatectomy: a qualitative study. J Sex Marital Ther 40, 233–253, doi: 10.1080/0092623x.2012.726697 (2014). [DOI] [PubMed] [Google Scholar]
- 95.Munding MD, Wessells HB & Dalkin BL Pilot study of changes in stretched penile length 3 months after radical retropubic prostatectomy. Urology 58, 567–569, doi: 10.1016/s0090-4295(01)01270-5 (2001). [DOI] [PubMed] [Google Scholar]
- 96.Savoie M, Kim SS & Soloway MS A Prospective Study Measuring Penile Length in Men Treated With Radical Prostatectomy for Prostate Cancer. The Journal of Urology 169, 1462–1464, doi: 10.1097/01.ju.0000053720.93303.33 (2003). [DOI] [PubMed] [Google Scholar]
- 97.Gontero P et al. New Insights Into the Pathogenesis of Penile Shortening After Radical Prostatectomy and the Role of Postoperative Sexual Function. The Journal of Urology 178, 602–607, doi: 10.1016/j.juro.2007.03.119 (2007). [DOI] [PubMed] [Google Scholar]
- 98.Haliloglu A, Baltaci S & Yaman O Penile length changes in men treated with androgen suppression plus radiation therapy for local or locally advanced prostate cancer. J Urol 177, 128–130, doi: 10.1016/j.juro.2006.08.113 (2007). [DOI] [PubMed] [Google Scholar]
- 99.Drummond M & Filiault S The long and short of it: Gay men’s perceptions of penis size. Gay and Lesbian Issues and Psychology Review 3 (2007). [Google Scholar]
- 100.Brennan J Size Matters: Penis Size and Sexual Position in Gay Porn Profiles. J Homosex 65, 912–933, doi: 10.1080/00918369.2017.1364568 (2018). [DOI] [PubMed] [Google Scholar]
- 101.Thomas C, Wootten AC, Robinson P, Law PCF & McKenzie DP The impact of sexual orientation on body image, self-esteem, urinary and sexual functions in the experience of prostate cancer. Eur J Cancer Care (Engl) 27, e12827, doi: 10.1111/ecc.12827 (2018). [DOI] [PubMed] [Google Scholar]
- 102.Galea JT et al. Rectal Douching Prevalence and Practices Among Peruvian Men Who have Sex with Men and Transwomen: Implications for Rectal Microbicides. AIDS Behav 20, 2555–2564, doi: 10.1007/s10461-015-1221-9 (2016). [DOI] [PubMed] [Google Scholar]
- 103.Noor SW & Rosser BR Enema use among men who have sex with men: a behavioral epidemiologic study with implications for HIV/STI prevention. Arch Sex Behav 43, 755–769, doi: 10.1007/s10508-013-0203-0 (2014). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 104.Dangerfield DT 2nd, Smith LR, Williams J, Unger J & Bluthenthal R Sexual Positioning Among Men Who Have Sex With Men: A Narrative Review. Arch Sex Behav 46, 869–884, doi: 10.1007/s10508-016-0738-y (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 105.Lee TK, Breau RH & Eapen L Pilot study on quality of life and sexual function in men-who-have-sex-with-men treated for prostate cancer. J Sex Med 10, 2094–2100, doi: 10.1111/jsm.12208 (2013). [DOI] [PubMed] [Google Scholar]
- 106.Guo Z et al. Incidence and risk factors of suicide after a prostate cancer diagnosis: a meta-analysis of observational studies. Prostate Cancer and Prostatic Diseases 21, 499–508, doi: 10.1038/s41391-018-0073-6 (2018). [DOI] [PubMed] [Google Scholar]
- 107.Schmidt HM et al. Management of sexual dysfunction due to antipsychotic drug therapy. Cochrane Database Syst Rev 11, Cd003546, doi: 10.1002/14651858.CD003546.pub3 (2012). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 108.Hosseinzadeh Zoroufchi B, Doustmohammadi H, Mokhtari T & Abdollahpour A Benzodiazepines related sexual dysfunctions: A critical review on pharmacology and mechanism of action. Rev Int Androl 19, 62–68, doi: 10.1016/j.androl.2019.08.003 (2021). [DOI] [PubMed] [Google Scholar]
- 109.Jing E & Straw-Wilson K Sexual dysfunction in selective serotonin reuptake inhibitors (SSRIs) and potential solutions: A narrative literature review. Ment Health Clin 6, 191–196, doi: 10.9740/mhc.2016.07.191 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 110.Rothmore J Antidepressant-induced sexual dysfunction. Medical Journal of Australia 212, 329–334, doi: 10.5694/mja2.50522 (2020). [DOI] [PubMed] [Google Scholar]
- 111.Cochran S & Mays V Prevalence of Primary Mental Health Morbidity and Suicide Symptoms among Gay and Bisexual Men. Unequal Opportunity: Health Disparities Affecting Gay and Bisexual Men in the United States, doi: 10.1093/acprof:oso/9780195301533.003.0004 (2009). [DOI] [Google Scholar]
- 112.National Academies of Sciences, E. et al. in The National Academies Collection: Reports funded by National Institutes of Health (eds Becker T, Chin M, & Bates N) (National Academies Press (US), 2022). [Google Scholar]
- 113.Brook G et al. 2019 UK National Guideline for consultations requiring sexual history taking : Clinical Effectiveness Group British Association for Sexual Health and HIV. Int J STD AIDS 31, 920–938, doi: 10.1177/0956462420941708 (2020). [DOI] [PubMed] [Google Scholar]
- 114.Amarasekera C et al. Urologists’ Knowledge, Attitudes and Practice Behaviors regarding Sexual Minority Patients. Journal of Urology 201, e201–e201, doi: 10.1097/01.JU.0000555329.66277.a2 (2019). [DOI] [Google Scholar]
- 115.Kamen CS et al. Sexual Orientation and Gender Identity Data Collection in Oncology Practice: Findings of an ASCO Survey. JCO Oncol Pract 18, e1297–e1305, doi: 10.1200/op.22.00084 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 116.Dyer K & das Nair R Why don’t healthcare professionals talk about sex? A systematic review of recent qualitative studies conducted in the United kingdom. J Sex Med 10, 2658–2670, doi: 10.1111/j.1743-6109.2012.02856.x (2013). [DOI] [PubMed] [Google Scholar]
- 117.Allensworth-Davies D et al. The Health Effects of Masculine Self-Esteem Following Treatment for Localized Prostate Cancer Among Gay Men. LGBT Health 3, 49–56, doi: 10.1089/lgbt.2015.0090 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 118.Blank TO Gay Men and Prostate Cancer: Invisible Diversity. Journal of Clinical Oncology 23, 2593–2596, doi: 10.1200/JCO.2005.00.968 (2005). [DOI] [PubMed] [Google Scholar]
- 119.Ussher JM, Perz J, Rose D, Kellett A & Dowsett G Sexual Rehabilitation After Prostate Cancer Through Assistive Aids: A Comparison of Gay/Bisexual and Heterosexual Men. J Sex Res 56, 854–869, doi: 10.1080/00224499.2018.1476444 (2019). [DOI] [PubMed] [Google Scholar]
- 120.Beck AM, Robinson JW & Carlson LE Sexual intimacy in heterosexual couples after prostate cancer treatment: What we know and what we still need to learn. Urol Oncol 27, 137–143, doi: 10.1016/j.urolonc.2007.11.032 (2009). [DOI] [PubMed] [Google Scholar]
- 121.Walker LM, Wassersug RJ & Robinson JW Psychosocial perspectives on sexual recovery after prostate cancer treatment. Nat Rev Urol 12, 167–176, doi: 10.1038/nrurol.2015.29 (2015). [DOI] [PubMed] [Google Scholar]
- 122.Chung E & Gillman M Prostate cancer survivorship: a review of erectile dysfunction and penile rehabilitation after prostate cancer therapy. Med J Aust 200, 582–585, doi: 10.5694/mja13.11028 (2014). [DOI] [PubMed] [Google Scholar]
- 123.Mulhall JP, Parker M, Waters BW & Flanigan R The timing of penile rehabilitation after bilateral nerve-sparing radical prostatectomy affects the recovery of erectile function. BJU Int 105, 37–41, doi: 10.1111/j.1464-410X.2009.08775.x (2010). [DOI] [PubMed] [Google Scholar]
- 124.Wassersug R & Wibowo E Non-pharmacological and non-surgical strategies to promote sexual recovery for men with erectile dysfunction. Transl Androl Urol 6, S776–s794, doi: 10.21037/tau.2017.04.09 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 125.Zelefsky MJ et al. Prophylactic sildenafil citrate improves select aspects of sexual function in men treated with radiotherapy for prostate cancer. J Urol 192, 868–874, doi: 10.1016/j.juro.2014.02.097 (2014). [DOI] [PubMed] [Google Scholar]
- 126.Watkins Bruner D et al. Randomized, double-blinded, placebo-controlled crossover trial of treating erectile dysfunction with sildenafil after radiotherapy and short-term androgen deprivation therapy: results of RTOG 0215. J Sex Med 8, 1228–1238, doi: 10.1111/j.1743-6109.2010.02164.x (2011). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 127.Jo JK et al. Effect of Starting Penile Rehabilitation with Sildenafil Immediately after Robot-Assisted Laparoscopic Radical Prostatectomy on Erectile Function Recovery: A Prospective Randomized Trial. J Urol 199, 1600–1606, doi: 10.1016/j.juro.2017.12.060 (2018). [DOI] [PubMed] [Google Scholar]
- 128.Pahlajani G, Raina R, Jones S, Ali M & Zippe C Vacuum Erection Devices Revisited: Its Emerging Role in the Treatment of Erectile Dysfunction and Early Penile Rehabilitation Following Prostate Cancer Therapy. The Journal of Sexual Medicine 9, 1182–1189, doi: 10.1111/j.1743-6109.2010.01881.x (2012). [DOI] [PubMed] [Google Scholar]
- 129.Raina R et al. Early use of vacuum constriction device following radical prostatectomy facilitates early sexual activity and potentially earlier return of erectile function. Int J Impot Res 18, 77–81, doi: 10.1038/sj.ijir.3901380 (2006). [DOI] [PubMed] [Google Scholar]
- 130.Vaccher SJ et al. Prevalence, frequency, and motivations for alkyl nitrite use among gay, bisexual and other men who have sex with men in Australia. International Journal of Drug Policy 76, 102659, doi: 10.1016/j.drugpo.2019.102659 (2020). [DOI] [PubMed] [Google Scholar]
- 131.Schwartz BG & Kloner RA Drug Interactions With Phosphodiesterase-5 Inhibitors Used for the Treatment of Erectile Dysfunction or Pulmonary Hypertension. Circulation 122, 88–95, doi: 10.1161/CIRCULATIONAHA.110.944603 (2010). [DOI] [PubMed] [Google Scholar]
- 132.Köhler TS et al. A pilot study on the early use of the vacuum erection device after radical retropubic prostatectomy. BJU Int 100, 858–862, doi: 10.1111/j.1464-410X.2007.07161.x (2007). [DOI] [PubMed] [Google Scholar]
- 133.Montorsi F et al. Effects of tadalafil treatment on erectile function recovery following bilateral nerve-sparing radical prostatectomy: a randomised placebo-controlled study (REACTT). Eur Urol 65, 587–596, doi: 10.1016/j.eururo.2013.09.051 (2014). [DOI] [PubMed] [Google Scholar]
- 134.Geraerts I et al. Pelvic floor muscle training for erectile dysfunction and climacturia 1 year after nerve sparing radical prostatectomy: a randomized controlled trial. Int J Impot Res 28, 9–13, doi: 10.1038/ijir.2015.24 (2016). [DOI] [PubMed] [Google Scholar]
- 135.Mehta A, Deveci S & Mulhall JP Efficacy of a penile variable tension loop for improving climacturia after radical prostatectomy. BJU Int 111, 500–504, doi: 10.1111/j.1464-410X.2012.11269.x (2013). [DOI] [PubMed] [Google Scholar]
- 136.Jain R, Mitchell S, Laze J & Lepor H The effect of surgical intervention for stress urinary incontinence (UI) on post-prostatectomy UI during sexual activity. BJU Int 109, 1208–1212, doi: 10.1111/j.1464-410X.2011.10506.x (2012). [DOI] [PubMed] [Google Scholar]
- 137.Andrianne R & van Renterghem K VS-01-007 In patients with climacturia and/or mild stress incontinence after radical prostatectomy, scheduled for penile implant, a mini sling called “the mini-jupette” can be incorporated in the procedure. The Journal of Sexual Medicine 14, e137, doi: 10.1016/j.jsxm.2017.03.011 (2017). [DOI] [Google Scholar]
- 138.Yafi FA et al. Andrianne Mini-Jupette Graft at the Time of Inflatable Penile Prosthesis Placement for the Management of Post-Prostatectomy Climacturia and Minimal Urinary Incontinence. J Sex Med 15, 789–796, doi: 10.1016/j.jsxm.2018.01.015 (2018). [DOI] [PubMed] [Google Scholar]
- 139.Hollander AB et al. Cabergoline in the Treatment of Male Orgasmic Disorder-A Retrospective Pilot Analysis. Sex Med 4, e28–33, doi: 10.1016/j.esxm.2015.09.001 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 140.Rosser BRS et al. What Gay and Bisexual Men Treated for Prostate Cancer Are Offered and Attempt as Sexual Rehabilitation for Prostate Cancer: Results from the Restore Study. Urol Pract 5, 187–191, doi: 10.1016/j.urpr.2017.04.002 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 141.Schroder M et al. Clitoral therapy device for treatment of sexual dysfunction in irradiated cervical cancer patients. Int J Radiat Oncol Biol Phys 61, 1078–1086, doi: 10.1016/j.ijrobp.2004.07.728 (2005). [DOI] [PubMed] [Google Scholar]
- 142.Law E et al. Prospective study of vaginal dilator use adherence and efficacy following radiotherapy. Radiother Oncol 116, 149–155, doi: 10.1016/j.radonc.2015.06.018 (2015). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 143.Dalsania RM, Shah KP, Stotsky-Himelfarb E, Hoffe S & Willingham FF Management of Long-Term Toxicity From Pelvic Radiation Therapy. American Society of Clinical Oncology Educational Book, 147–157, doi: 10.1200/EDBK_323525 (2021). [DOI] [PubMed] [Google Scholar]
- 144.Hall EJ Radiobiology for the radiologist. (Hagerstown, Md.: Medical Dept., Harper & Row, [1973] ©1973, 1973). [Google Scholar]
- 145.Bakker RM et al. Sexual rehabilitation after pelvic radiotherapy and vaginal dilator use: consensus using the Delphi method. Int J Gynecol Cancer 24, 1499–1506, doi: 10.1097/igc.0000000000000253 (2014). [DOI] [PubMed] [Google Scholar]
- 146.Summerfield J & Leong A Management of radiation therapy-induced vaginal adhesions and stenosis: A New Zealand survey of current practice. J Med Radiat Sci 67, 128–133, doi: 10.1002/jmrs.386 (2020). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 147.Lee Y Patients’ perception and adherence to vaginal dilator therapy: a systematic review and synthesis employing symbolic interactionism. Patient Prefer Adherence 12, 551–560, doi: 10.2147/ppa.S163273 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 148.Bianco F et al. Short stump and high anastomosis pull-through (SHiP) procedure for delayed coloanal anastomosis with no protective stoma for low rectal cancer. Updates in Surgery 73, 495–502, doi: 10.1007/s13304-021-01022-6 (2021). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 149.Greca F, Nevah E, Hares M & Keighley MR Value of an anal dilator after anal stretch for haemorrhoids. J R Soc Med 74, 368–370 (1981). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 150.Shen SL, He DL & Luo Y [Clinical trials of combined therapy of an oral Chinese medicine with massage for chronic nonbacterial prostatitis]. Zhonghua Nan Ke Xue 12, 851–853 (2006). [PubMed] [Google Scholar]
- 151.Ateya A et al. Evaluation of prostatic massage in treatment of chronic prostatitis. Urology 67, 674–678, doi: 10.1016/j.urology.2005.10.021 (2006). [DOI] [PubMed] [Google Scholar]
- 152.Dodge B et al. Frequency, reasons for, and perceptions of lubricant use among a nationally representative sample of self-identified gay and bisexual men in the United States. J Sex Med 11, 2396–2405, doi: 10.1111/jsm.12640 (2014). [DOI] [PubMed] [Google Scholar]
- 153.Rosen RC et al. Male Sexual Health Questionnaire (MSHQ): scale development and psychometric validation. Urology 64, 777–782, doi: 10.1016/j.urology.2004.04.056 (2004). [DOI] [PubMed] [Google Scholar]
- 154.Wei JT, Dunn RL, Litwin MS, Sandler HM & Sanda MG Development and validation of the expanded prostate cancer index composite (EPIC) for comprehensive assessment of health-related quality of life in men with prostate cancer. Urology 56, 899–905, doi: 10.1016/s0090-4295(00)00858-x (2000). [DOI] [PubMed] [Google Scholar]
- 155.Rosen RC et al. The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction. Urology 49, 822–830, doi: 10.1016/s0090-4295(97)00238-0 (1997). [DOI] [PubMed] [Google Scholar]
- 156.Rosen RC, Cappelleri JC, Smith MD, Lipsky J & Peña BM Development and evaluation of an abridged, 5-item version of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res 11, 319–326, doi: 10.1038/sj.ijir.3900472 (1999). [DOI] [PubMed] [Google Scholar]
- 157.Lee TK et al. Development of a Sexual Quality of Life Questionnaire for Men-Who-Have-Sex-With-Men With Prostate Cancer. Sex Med 10, 100480, doi: 10.1016/j.esxm.2021.100480 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 158.Coyne K et al. The International Index of Erectile Function: development of an adapted tool for use in HIV-positive men who have sex with men. J Sex Med 7, 769–774, doi: 10.1111/j.1743-6109.2009.01579.x (2010). [DOI] [PubMed] [Google Scholar]
- 159.Amarasekera C et al. A Pilot Study Assessing Aspects of Sexual Function Predicted to Be Important After Treatment for Prostate Cancer in Gay Men: An Underserved Domain Highlighted. LGBT Health 7, 271–276, doi: 10.1089/lgbt.2018.0245 (2020). [DOI] [PubMed] [Google Scholar]
- 160.Polter EJ et al. Creation and Psychometric Validation of the Sexual Minorities and Prostate Cancer Scale (SMACS) in Sexual Minority Patients-The Restore-2 Study. J Sex Med 19, 529–540, doi: 10.1016/j.jsxm.2021.12.012 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 161.Simon Rosser BR et al. Recruiting an underserved, difficult to reach population into a cancer trial: Strategies from the Restore-2 Rehabilitation Trial for gay and bisexual prostate cancer patients. Clin Trials, 17407745221077678, doi: 10.1177/17407745221077678 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 162.Wheldon CW et al. Prevalence and Risk Factors for Sexually Transmitted Infections in Gay and Bisexual Prostate Cancer Survivors: Results From the Restore-2 Study. Front Oncol 12, 832508, doi: 10.3389/fonc.2022.832508 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 163.Ralph S Developing UK Guidance on How Long Men Should Abstain from Receiving Anal Sex before, During and after Interventions for Prostate Cancer. Clinical Oncology 33, 807–810, doi: 10.1016/j.clon.2021.07.010 (2021). [DOI] [PubMed] [Google Scholar]
- 164.Nasser NJ, Cohen GN, Dauer LT & Zelefsky MJ Radiation safety of receptive anal intercourse with prostate cancer patients treated with low-dose-rate brachytherapy. Brachytherapy 15, 420–425, doi: 10.1016/j.brachy.2016.03.012 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 165.Kelley CF et al. The rectal mucosa and condomless receptive anal intercourse in HIV-negative MSM: implications for HIV transmission and prevention. Mucosal Immunol 10, 996–1007, doi: 10.1038/mi.2016.97 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 166.Haase AT Targeting early infection to prevent HIV-1 mucosal transmission. Nature 464, 217–223, doi: 10.1038/nature08757 (2010). [DOI] [PubMed] [Google Scholar]
- 167.Hladik F & McElrath MJ Setting the stage: host invasion by HIV. Nat Rev Immunol 8, 447–457, doi: 10.1038/nri2302 (2008). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 168.Rosser BR et al. The Effects of Radical Prostatectomy on Gay and Bisexual Men’s Mental Health, Sexual Identity and Relationships: Qualitative Results from the Restore Study. Sex Relation Ther 31, 446–461, doi: 10.1080/14681994.2016.1228871 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 169.Carballo-Diéguez A, Lentz C, Giguere R, Fuchs EJ & Hendrix CW Rectal Douching Associated with Receptive Anal Intercourse: A Literature Review. AIDS Behav 22, 1288–1294, doi: 10.1007/s10461-017-1959-3 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 170.Javanbakht M, Stahlman S, Pickett J, LeBlanc M-A & Gorbach PM Prevalence and types of rectal douches used for anal intercourse: results from an international survey. BMC Infectious Diseases 14, 95, doi: 10.1186/1471-2334-14-95 (2014). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 171.Lu T et al. Association between rectal douching and HIV acquisition: the mediating role of condom use and rectal bleeding in a national online sample of Chinese men who have sex with men. Sexually Transmitted Infections 97, 69, doi: 10.1136/sextrans-2019-054415 (2021). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 172.Hassan A et al. Effect of rectal douching/enema on rectal gonorrhoea and chlamydia among a cohort of men who have sex with men on HIV pre-exposure prophylaxis. Sex Transm Infect 94, 508–514, doi: 10.1136/sextrans-2017-053484 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 173.Elizaldi SR et al. Rectal Microbiome Composition Correlates with Humoral Immunity to HIV-1 in Vaccinated Rhesus Macaques. mSphere 4, doi: 10.1128/mSphere.00824-19 (2019). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 174.Shogan BD et al. Alterations of the Rectal Microbiome Are Associated with the Development of Postoperative Ileus in Patients Undergoing Colorectal Surgery. J Gastrointest Surg 24, 1663–1672, doi: 10.1007/s11605-020-04593-8 (2020). [DOI] [PubMed] [Google Scholar]
- 175.Nascimento M et al. Efficacy of Synbiotics to Reduce Symptoms and Rectal Inflammatory Response in Acute Radiation Proctitis: A Randomized, Double-Blind, Placebo-Controlled Pilot Trial. Nutr Cancer 72, 602–609, doi: 10.1080/01635581.2019.1647254 (2020). [DOI] [PubMed] [Google Scholar]
- 176.Galea JT et al. Rectal douching and implications for rectal microbicides among populations vulnerable to HIV in South America: a qualitative study. Sex Transm Infect 90, 33–35, doi: 10.1136/sextrans-2013-051154 (2014). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 177.Hein L Caring for Transgender patients. Nursing Made Incredibly Easy 12, 28–36, doi: 10.1097/01.NME.0000454745.49841.76 (2014). [DOI] [Google Scholar]
- 178.Silverberg MJ et al. Cohort study of cancer risk among insured transgender people. Ann Epidemiol 27, 499–501, doi: 10.1016/j.annepidem.2017.07.007 (2017). [DOI] [PubMed] [Google Scholar]
- 179.Gooren L & Morgentaler A Prostate cancer incidence in orchidectomised male-to-female transsexual persons treated with oestrogens. Andrologia 46, 1156–1160, doi: 10.1111/and.12208 (2014). [DOI] [PubMed] [Google Scholar]
- 180.Safer JD et al. Barriers to healthcare for transgender individuals. Curr Opin Endocrinol Diabetes Obes 23, 168–171, doi: 10.1097/med.0000000000000227 (2016). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 181.Wilson JD & Roehrborn C Long-Term Consequences of Castration in Men: Lessons from the Skoptzy and the Eunuchs of the Chinese and Ottoman Courts. The Journal of Clinical Endocrinology & Metabolism 84, 4324–4331, doi: 10.1210/jcem.84.12.6206 (1999). [DOI] [PubMed] [Google Scholar]
- 182.Hughes LD et al. Differences in All-Cause Mortality Among Transgender and Non-Transgender People Enrolled in Private Insurance. Demography 59, 1023–1043, doi: 10.1215/00703370-9942002 (2022). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 183.Gaglani S, Purohit RS, Tewari AK, Kyprianou N & Lundon DJ Embryologic and hormonal contributors to prostate cancer in transgender women. Am J Clin Exp Urol 10, 63–72 (2022). [PMC free article] [PubMed] [Google Scholar]
- 184.Bertoncelli Tanaka M et al. Prostate cancer in transgender women: what does a urologist need to know? BJU Int 129, 113–122, doi: 10.1111/bju.15521 (2022). [DOI] [PubMed] [Google Scholar]
- 185.Bosland MC, Ford H & Horton L Induction at high incidence of ductal prostate adenocarcinomas in NBL/Cr and Sprague-Dawley Hsd:SD rats treated with a combination of testosterone and estradiol-17 beta or diethylstilbestrol. Carcinogenesis 16, 1311–1317, doi: 10.1093/carcin/16.6.1311 (1995). [DOI] [PubMed] [Google Scholar]
- 186.Bosland MC A perspective on the role of estrogen in hormone-induced prostate carcinogenesis. Cancer Lett 334, 28–33, doi: 10.1016/j.canlet.2012.08.027 (2013). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 187.ČAPOUN O et al. Prognosis of Castration-resistant Prostate Cancer Patients – Use of the AdnaTest® System for Detection of Circulating Tumor Cells. Anticancer Research 36, 2019–2026 (2016). [PubMed] [Google Scholar]
- 188.Heidenreich A et al. EAU guidelines on prostate cancer. Part II: Treatment of advanced, relapsing, and castration-resistant prostate cancer. Eur Urol 65, 467–479, doi: 10.1016/j.eururo.2013.11.002 (2014). [DOI] [PubMed] [Google Scholar]
- 189.Aly M et al. Survival in patients diagnosed with castration-resistant prostate cancer: a population-based observational study in Sweden. Scand J Urol 54, 115–121, doi: 10.1080/21681805.2020.1739139 (2020). [DOI] [PubMed] [Google Scholar]
- 190.Moreira DM et al. Predicting Time From Metastasis to Overall Survival in Castration-Resistant Prostate Cancer: Results From SEARCH. Clin Genitourin Cancer 15, 60–66.e62, doi: 10.1016/j.clgc.2016.08.018 (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 191.Saad F & Hotte SJ Guidelines for the management of castrate-resistant prostate cancer. Can Urol Assoc J 4, 380–384, doi: 10.5489/cuaj.10167 (2010). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 192.Alcaraz Asensio A et al. Non-metastatic castration-resistant prostate cancer: management recommendations. Actas Urol Esp (Engl Ed) 46, 193–213, doi: 10.1016/j.acuroe.2021.11.001 (2022). [DOI] [PubMed] [Google Scholar]
- 193.Sayegh N, Swami U & Agarwal N Recent Advances in the Management of Metastatic Prostate Cancer. JCO Oncol Pract 18, 45–55, doi: 10.1200/op.21.00206 (2022). [DOI] [PubMed] [Google Scholar]
- 194.Mattawanon N, Charoenkwan K & Tangpricha V Sexual Dysfunction in Transgender People: A Systematic Review. Urol Clin North Am 48, 437–460, doi: 10.1016/j.ucl.2021.06.004 (2021). [DOI] [PubMed] [Google Scholar]
- 195.Kerckhof ME et al. Prevalence of Sexual Dysfunctions in Transgender Persons: Results from the ENIGI Follow-Up Study. The Journal of Sexual Medicine 16, 2018–2029, doi: 10.1016/j.jsxm.2019.09.003 (2019). [DOI] [PubMed] [Google Scholar]
- 196.Buncamper ME et al. Surgical Outcome after Penile Inversion Vaginoplasty: A Retrospective Study of 475 Transgender Women. Plast Reconstr Surg 138, 999–1007, doi: 10.1097/prs.0000000000002684 (2016). [DOI] [PubMed] [Google Scholar]
- 197.Bouman MB et al. Patient-Reported Esthetic and Functional Outcomes of Primary Total Laparoscopic Intestinal Vaginoplasty in Transgender Women With Penoscrotal Hypoplasia. J Sex Med 13, 1438–1444, doi: 10.1016/j.jsxm.2016.06.009 (2016). [DOI] [PubMed] [Google Scholar]
- 198.LeBreton M et al. Genital Sensory Detection Thresholds and Patient Satisfaction With Vaginoplasty in Male-to-Female Transgender Women. J Sex Med 14, 274–281, doi: 10.1016/j.jsxm.2016.12.005 (2017). [DOI] [PubMed] [Google Scholar]
- 199.Zavlin D, Wassersug RJ, Chegireddy V, Schaff J & Papadopulos NA Age-Related Differences for Male-to-Female Transgender Patients Undergoing Gender-Affirming Surgery. Sex Med 7, 86–93, doi: 10.1016/j.esxm.2018.11.005 (2019). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 200.Lawrence AA Factors associated with satisfaction or regret following male-to-female sex reassignment surgery. Arch Sex Behav 32, 299–315, doi: 10.1023/a:1024086814364 (2003). [DOI] [PubMed] [Google Scholar]
- 201.Satcher MF et al. Partner-Level Factors Associated with Insertive and Receptive Condomless Anal Intercourse Among Transgender Women in Lima, Peru. AIDS Behav 21, 2439–2451, doi: 10.1007/s10461-016-1503-x (2017). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 202.Nemoto T, Bödeker B, Iwamoto M & Sakata M Practices of receptive and insertive anal sex among transgender women in relation to partner types, sociocultural factors, and background variables. AIDS Care 26, 434–440, doi: 10.1080/09540121.2013.841832 (2014). [DOI] [PubMed] [Google Scholar]
- 203.Hess J et al. Sexuality after Male-to-Female Gender Affirmation Surgery. Biomed Res Int 2018 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 204.Yun JH, Diaz R & Orman AG Breast Reconstruction and Radiation Therapy. Cancer Control 25, 1073274818795489, doi: 10.1177/1073274818795489 (2018). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 205.Ingham MD, Lee RJ, MacDermed D & Olumi AF Prostate cancer in transgender women. Urol Oncol 36, 518–525, doi: 10.1016/j.urolonc.2018.09.011 (2018). [DOI] [PubMed] [Google Scholar]
- 206.Ritch CR & Cookson MS Advances in the management of castration resistant prostate cancer. BMJ 355, i4405, doi: 10.1136/bmj.i4405 (2016). [DOI] [PubMed] [Google Scholar]