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Attitudes and experiences of health care professionals when caring for transgender men undergoing fertility preservation by egg freezing: a qualitative study

Background: As gender-affirming treatment may have a negative impact on fertility, reproductive health counseling to patients seeking medical or surgical gender-affirming treatment should be provided, including the option to undergo fertility preservation (FP). Experiences of transgender men undergoing FP treatments aimed at oocyte freezing have reported a negative impact of the treatments on gender dysphoria. No previous studies have investigated the experiences of health care professionals’ (HCP) when caring for transgender men undergoing such treatments. Aim: The aim of this study was to investigate HCP’s attitudes and experiences when meeting transgender men undergoing FP through oocyte freezing. Methods: Individual interviews were conducted in 2016 with 13 HCPs working at a Reproductive Medicine clinic in Sweden. Data were analyzed by thematic content analysis. Results: The main theme found, How to maintain professionalism, showed that HCPs experienced important challenges to their professionalism when their preconceived opinions and values about gender and transgender were confronted. Discussion: Our findings demonstrate the need of continuous efforts on assessing learning needs as well as addressing preconceived opinions and values of HCP. By gaining knowledge and self-confidence in the care of transgender individuals undergoing FP, a professional care for transgender people can be achieved and a safe environment can be established for the patients. This in turn may alleviate some of the distress that may arise when transgender men undergo FP.


Introduction
Transgender individuals experience discomfort between their assigned sex at birth and their gender identity (gender dysphoria) and some of them need to undergo treatments, including gender-affirming hormone therapy and surgery, to align their bodies with their gender identity. 1,2 These procedures may have a negative impact on future fertility. 3,4 Guidelines for gender-affirming medical treatment, 1,5 as well as the American Society of Reproductive Medicine 6

and the European Society of Human
Reproduction and Embryology 7 recommend that all transgender individuals seeking medical intervention should be informed about the risk of future infertility associated to their treatments and options for fertility preservation (FP).
For transgender men, that is, individuals assigned female at birth with a male gender identity, the clinically established FP options currently available include freezing of embryos or of mature gametes (mature oocytes), 8 and case series have been reported. 9 Embryo cryopreservation requires Attitudes and experiences of health care professionals when caring for transgender men undergoing fertility preservation by egg freezing: a qualitative study journals.sagepub.com/home/reh Therapeutic Advances in Reproductive Health 14 fertilization of oocytes at the time of extraction using sperm from a partner or a donor. If the transgender man is having an oophorectomy, cryopreservation of ovarian tissue may also be an option. However, this method will require auto transplantation of the tissue in the future, or a further establishment of methods such as in vitro follicle growth of oocytes obtained from the tissue, which are still under development. 10 The option of cryopreservation of mature oocytes, colloquially known as egg freezing, has achieved clinical standards and it does not involve another party other than the patient. In transgender patients, timely FP is preferably performed before the gender-affirming hormone treatment (GAHT) is initiated, to ensure optimal outcome. 1 Fertilizable oocytes are retrieved after conventional controlled ovarian stimulation (COS) and ultrasound-guided transvaginal ovarian follicular aspiration.
In Sweden and other Scandinavian countries, FP has been included in the publicly funded health care system for over 20 years and the services are provided at large programs for FP established at university hospitals. Previous reports of FP in cisgender patients in that setting are available. 9,11 However, FP was not offered to transgender patients in Sweden until 2013, when sterilization as a prerequisite for change of legal gender, was removed by a change in the legislation. 12 The Swedish sterilization prerequisite has been considered an example of difficulties in accessing health care for transgender individuals in favor of social marginalization, stigma, discrimination, and violence. 13 In general healthcare, transgender individuals have reported negative experiences worldwide, [14][15][16][17][18] which had negatively impacted on their general health and quality of life. 15 On the other hand, only a few studies have so far investigated healthcare providers' (HCPs) experiences of caring for transgender individuals. Studies among HCPs working in diverse health care areas show that there is limited knowledge about gender dysphoria and the appropriate care strategies. 19,20 A study among physicians showed that insensitivity toward transgender individuals could be understood mainly in moral terms, where some physicians had personal beliefs about gender identity, sexuality, and sexual health that clashed with their patients' lives. 20 The lack of knowledge and competence in transgender health among HCP could maybe also be explained by lacking of discussion on this topic in most HCP's educational curriculum. 21 Although studies investigating medical and mental health specialist's perception of FP in transgender parents are available, 22 no study has previously assessed healthcare specialists in the field of reproductive medicine.
At the reproductive medicine center at Karolinska University Hospital in Stockholm, a program for transgender people aiming at FP was initiated in 2013, following the change in legislation allowing such treatments. 12 We have previously reported on the experiences of transgender patients undergoing FP procedures aimed at oocyte freezing. 23 That study indicated an increase of gender dysphoria during FP, which was triggered by several factors, such as the discontinuing of testosterone treatment; the pelvic examinations, including transvaginal ultrasound; the hormonal stimulation required to achieve follicle development; and oocyte maturation, but also due to factors related to healthcare provision such as the use of a wrong pronoun or of gendered words for body parts during the consultations. 23 The present study was thus designed to investigate HCP' experiences when caring for transgender men undergoing FP by oocyte freezing and capture the difficulties, aiming to further improve the healthcare that is provided to transgender patients.

Context
The tax-funded Swedish health care system provides the basis of an equitable health care system where all residents have the same opportunity to receive good health care. Transgender medicine gender teams with specialists in psychiatry, psychology, endocrinology, plastic surgery, speech and language pathology, dermatology, gynecology, and andrology have been available at the Swedish university hospitals including ours since 1999 for diagnostic evaluation, support, and gender-affirming treatment including hormone treatment, top surgery, gender-affirming genital surgery, voice treatment and hair removal. 24,25 In connection with the 2012 change in the legislation, 12 the Reproductive Medicine unit of Karolinska University Hospital became a part of the extended transgender medicine team of the hospital.
In order to develop a program for the new patient group and aiming at achieving optimal care, a pilot et al.
journals.sagepub.com/home/reh 3 project ( Figure 1) was introduced at our center using the framework suggested by INVOLVE, 26 to involve individuals in research. The aim was to interview and obtain feed-back from the patients during the process of developing a FP program, within the frame of qualitative research. 23 At the clinic, the following preparations were made to fill in the knowledge gaps: (1) Lectures by professionals from the gender team of the hospital aiming to increase knowledge about the transgender patients, the evaluation process and the gender-affirming treatments. (

Study participants and procedure
This study was conducted between January and April 2016, at the time when most HCPs at our center have cared of transgender patients undergoing FP. All HCPs working at the center were contacted by e-mail and invited to the study. Inclusion criteria were having cared for at least one transgender man after the patient group had been introduced at the clinic. Participation was voluntary and could be interrupted at any time. No incentives for study participation were offered. Informed consent was obtained from all participants before the interview.
Semi-structured interview: The semi-structured interviews started with one question: "In what way have you been involved in the care of transgender men undergoing cryopreservation of oocytes or ovarian tissue at the clinic?" The interviews covered the following areas: preparations at the clinic, experiences of meeting the patient group and practical circumstances. When needed, supplementary questions were asked, such as "Can you tell me more?" or "What did you do then?" Field notes were taken with reflections about the interviews, and these were used as a  Participants' characteristics Thirteen HCP including 12 women and 1 man, all cisgender, participated in face-to-face semistructured interviews ( Table 1). The participants were involved in one or more situations of the patient's flow chain of healthcare, from the booking of appointment and outpatient reception (administrative personnel), to the clinical evaluations, physical exams, oocyte pick-up and postoperative care (physicians, midwifes, embryologist). The interviews lasted between 17 and 53 minutes (mean 34.7, SD 10.56). The staff ratio female/ male was 10/1 at time of the study.

Data analysis
All interviews were performed by the first author (G.A.) and conducted face-to-face. The interviewer had no professional connection with the HCPs at the fertility clinic. Interviews were digitally recorded and thereafter transcribed verbatim and analyzed by thematic content analysis. 29 An inductive approach was used, where the analysis is data driven rather than driven by theory or a framework. This is especially recommended where little or nothing is known about the studied phenomenon. 29 Each participant's interview was read carefully to get a sense of the person's story. By using open coding-words, phrases or sentences were identified and summarized using notes. Notes describing the same content were then brought together into categories with subheadings reflecting their content. These were then hierarchically sorted into main-categories, sub-categories and themes. Overlapping and similar categories were grouped together, in order to reduce the number of categories. By using constant comparison, transcripts were read again and compared with the categories and sub-categories in order to ensure that all data related to the study aim were reflected in the results. Analysis, including the identified meaning units, the categorization and abstraction were performed during research group discussions. The study participants did not review or participate in the discussions regarding categorization. The results are illustrated by quotations from the participants. The interviewer's questions, clarifications and excisions (three dots) are marked with squared brackets. The software program NVivo version 11 (QSR International) was used to facilitate data management during the analysis.

Results
The analysis resulted in identification of one main theme consisting of three sub-themes with underlying main-and sub-categories ( Table 2). The main theme, How to maintain professionalism, is about how the HCPs, through The learning experience, Encounters with the patients and Modifying of procedures, learned the needs of the new patient group, developed their professional skills and also identified how their professionalism was challenged as they were obliged to confront their preconceived opinions and cis-normative assumptions. Through a combination of new knowledge, experiences of meeting the transgender men and the adjustments of the FP procedures, HCPs found ways of providing care for transgender men undergoing cryopreservation of oocytes in a professional manner. However, having a small project group was not uniquely positive, where some of the HCPs outside of the group felt excluded and that they had limited knowledge of what was going on. This sometimes created a problem as it was not always feasible to assign a specifically designated gynecologist or midwife to a patient coming for a visit, as the patient group grew quickly and more professionals became involved in their care.
Identifying learning needs. Over time, the HCPs identified learning needs that only became evident when they had met and cared for the transgender men. They felt that they had limited knowledge about the group's situation when it came to mental health, such as problems with self-harm and suicidal behavior:

Encounters with the patients
This sub-theme, which consists of two main-categories and sex sub-categories (Table 2), is about the meetings between HCPs and the transgender men. The encounters led to reactions toward the patient group, both of positive and negative nature. While being aware of shortcomings regarding their professionalism, HCPs hoped that the transgender men could be understanding, as these shortcomings were dependent on the HCPs relative inexperience with the situation.
Reactions toward the group. The understanding of the patients' situation gained by the accommodation of new knowledge, were often followed by feelings of empathy when meeting the patient group. The HCPs theoretical knowledge about transgender individuals' situation in society and about gender dysphoria in general gave them an understanding of why some transgender men reacted as they did, when, for example, a wrong pronoun was used or when they underwent examination by transvaginal ultrasound.
I understand that it feels awkward to come here and do this, you know. Because clearly it's really tough to get here and to awaken something they don't want to acknowledge. (HCP P11) The HCPs also described how the work with the transgender men had forced them to see what cis-normative and binary assumption they harbored, and mostly the HCPs described this as something being positive and refreshing. It had led to a reformulation of earlier knowledge and preconceptions: It was an eye-opener in the beginning . . . that on some forms it was written "woman" and on other forms "man." I think it was quite good, to be awakened. "Why is this so?" (HCP P11) However, others expressed ambivalence toward the group. They found the new patient group as alien as the transgender men's gender expressions were difficult to understand and made them feel uncomfortable. They understood that the transgender men had special needs but found it hard to handle the demands that were set as they sometimes found them unnecessary and needless, such as demanding gender-neutral toilets or paper forms: The perceived strangeness of the new patient group combined with the limited knowledge about needs and expectations also gave rise to a fear of doing wrong, and they described how negative encounters had reinforced these fears, which in turn led to them trying to avoid the patient group. The HCPs also sought understanding for sometimes using the wrong name or pronoun. They explained that it was especially hard to say the right thing when they did not experience the patient's gender expression as masculine. However, even if the patient had what they read as a more masculine gender expression, it was easy to slip and to use the pronoun she when the transgender men were in situations that the HCP perceived as feminine, such as when the transgender men were lying in the examination chair in lithotomy position or during transvaginal ultrasounds:

Modifying procedures
This sub-theme, consisting of two main-categories and four sub-categories (Table 2) is about the HCPs modification of the existing procedures in connection with cryopreservation of oocytes to also fit the new patient group consisting of transgender men.
Adjusting examinations. In the clinical work with transgender patients, some of the HCPs stated that they did not change any routines when it came to the examinations. They described that they were always careful and responsive to all patients and did not feel that the transgender men had different needs. Others, however, described how they perceived the transgender men being tense and more worried than other patients. The HCP knew that some transgender men had never undergone pelvic examinations before, and some had never had receptive/penetrating sex. Also, the knowledge about possible gender dysphoria motivated them to act differently when caring for the transgender men. Some discussed the examination beforehand in order to obtain information about the patients' preferences, for example if they wanted the HCP to show on the monitor during the transvaginal ultrasound or not: I thought it was easier to learn from patients. Actually, saying to them "I don't really know what you want me to say, but let's figure it out together." That one is honest towards the patient. (HCP P11) However, most HCPs described a silent responsiveness as they worked toward being extra sensitive to the patient's reactions and signals during the examinations. They covered the transgender man's genital area in order to guard their integrity, slowed down the examination if the patient became tense, and prepared each movement by telling the man about it: Rethinking communication. A challenging part that was described in the encounter with the transgender men was the communication. The encounters made the HCPs aware of the gendered language and symbols that were used at the clinic, and they were forced to change already settled way in how to communicate about the procedures following FP. Some transgender men felt uncomfortable with gendered words and the HCPs tried to find new ways to communicate about the procedures, for example, by trying to find alternative words, such as gametes or bleeding instead of eggs and menstruation. However, as many of the words are not replaceable some of the HCPs described a restraining behavior in the way that they sometimes held back in their communication, as they were afraid of using the wrong words or the wrong pronoun: An alternative way to handle the issue was to listen to the patient and hear what words the patients used. If the patients' them-self used gendered words such as egg they also used the words, otherwise they used gender-neutral words such as gametes. Importantly, the clinic also adapted the electronic medical records system to enable identification of transgender patients. Also, paper forms given to patients caused problems in the beginning, as the clinic only had had cisgender patients previously and the forms were color coded-blue for cryopreservation of sperm and pink for cryopreservation oocytes. As the transgender men were scheduled to cryopreserve oocytes, they were given pink papers developed for this purpose. Before the clinic changed the color to green, some of the transgender men protested as they felt that the clinic wanted to assign them as females, as pink often symbolize femininity in many cultures: They must experience this a much tougher than our usual patients, and they have probably been very nervous about coming here. And then we comes and hand out pink paper [. . .] One might think 'Why, the color of the paper doesn't matter!' But they really do [feel that that it matters]. (HCP P3) Another administrative problem that arose regarding communication was data systems connected to the FP procedures. The transgender men who came to the clinic to undergo FP were at different points in their transitions and sometimes they had already undergone change of legal sex. The Swedish personal identity numbers are binary and indicate a male or female sex in one of its digits. This raised problems when the cryopreserved oocytes should be registered-the electronic medical record system did not allow a male personal identity number to be tied with the registration of cryopreserved oocytes: In the beginning we had problems with how to freeze eggs with a male personal identification number as only female numbers functioned in the system. Now we have changed it so that you can leave eggs with any personal identification number [. . .] It works, maybe not completely without hitches as the system is not perfect yet, but we constantly get suggestions for improvements.

Discussion
The present study clearly demonstrates that HCPs experienced challenges in their professionalism when meeting the new patient group of transgender men undergoing oocyte freezing. These challenges stemmed not only from the uncertainty about how to communicate and perform the FP procedures, but also from clashes between preconceived opinions and values, and the transgender men's gender expressions and needs. Prior preparations were considered essential by the HCPs, but they also recognized the importance of continued learning. Striving to maintain professionalism, the HCPs worked actively to gain knowledge and experience, as well as to attempt a better understanding of this new patient group. Similarly, a recent grounded theory study among both HCPs and transgender individuals showed that some of the HCPs struggled with the concept of gender dysphoria. 19 However, it was described that interpersonal stigma functioned as a way to reinforce medical power and authority in the face of provider uncertainty. 19 In addition, that study reported that those HCP's who felt empathy for transgender patients were more likely to express resistance to stigmatization. 19 Professionalism in health care is defined as the habitual and judicious use of communication, knowledge, technical skills, clinical reasoning, emotions, values, and reflection in daily practice for the benefit of the individual and the community being served. 30 When analyzing the material of our study, we came to understand that the study participants felt that their knowledge, communication skills, emotions, and values were not sufficient and they described different ways how to overcome the sense of insufficiency of their own capacity and skills.
In the present study, one challenge toward optimal care was to attain good communication, which also has been described by transgender individuals as an important part of professionalism. 16 In the present study, the HCPs described how they struggled with using the right pronoun when communicating with transgender men, especially when the appearance and/or voice of the patient was incongruent with the gender identity-which is often the case in the beginning of the physical gender transition. Transgender individuals have an understanding of this, 16 but it has mostly been experienced as an indicator of their gender identity not being recognized or accepted. 16,19,23 When meeting the transgender patient group, the preferred route to overcome this problem is always being aware of the communication issue and working actively to avoid mistakes-and when a mistake occurs to acknowledge it and apologize without making any evasive comments. Importantly, it is recommended to document the right pronoun in the patients chart, 31,32 and this strategy was also highlighted by the HCPs in the present study. Other problematic aspects of communication beside pronoun use were the use of gendered words such as vagina, uterus, or eggs that made patients feel uncomfortable, as previously reported. 23 The HCPs found different ways to deal with the issue, such as asking the transgender men or by using the words used by the patients themselves. This strategy also opts for a true patient-centered care where the patients define themselves and their problems. 33 Notably, a third response of HCPs to managing the situation was to hold back on communication. However, with this strategy there is a risk that the transgender men might receive less information than other patients, which in turn may compromise patient safety.
Even if communication issues resulted in problems, most HCPs described how the experience had inspired them and stimulated their interest, developing new ways of thinking and acting out of their comfort zone. In the results we did not find any norm critic reflexion from the study participants. However, we found quotes such as regular patient in comparison to the transgender male patients, reflecting an underlying cisgender normativity and maybe also exoticism. Thus, this may indicate that more knowledge is needed but also new ways of thinking. This is supported by previous work, in which an intervention study of interactive theater workshops, aiming at providing a better understanding of sexual and gender minority patients, 34 encouraged HCPs to rethink previously held assumptions about LGBTQ people and their needs regarding reproductive care.
Our aim with this qualitative study was to explore the HCPs experience of providing care for transgender men receiving FP in a university clinic in Sweden, and our results cannot therefore be generalized. Nevertheless, we think that our results could be of value to other reproductive care clinics within different financial care systems, as the medical procedures in connection with FP are similar.
We followed the consolidated criteria recommendations for reporting qualitative research, 35 and the criteria for trustworthiness described by Lincoln and Guba. 36 The co-workers had meetings to discuss the analysis and presentation of data and the research group had different professional and discipline backgrounds, such as nursing, psychiatry, and reproductive care, being an important asset in the analytical process. 36 The research group members had also different knowledge and experience of transgender medicine and transgender patients. Inclusion of HCPs throughout the patients' whole healthcare chain allowed us to capture experiences of caring for transgender men undergoing FP from different Therapeutic Advances in Reproductive Health 14 standpoints. The diverse background with different values and beliefs of the research group was also an asset regarding the analysis. The study participants were not part of the analysis and were not presented to the results. As such, we cannot rule out that this could have added additional information. No one in the research group has a transgender background with that the thematic analysis might have been different.
Not all HCPs working at the clinic participated in the study, however, those who declined participation had not met transgender men at all, or only occasionally. It cannot be entirely dismissed that a larger sample could have captured additional experiences, however, the study was completed when saturation was reached.

Conclusion
In summary, findings presented herein clearly indicate that HCPs meeting transgender men undergoing FP were obliged to confront preconceived opinions and cis-normative assumptions.
In addition, a need to acquire new knowledge was recognized and accepted in order to maintain professionalism. The data demonstrate the difficulties that may arise when introducing a new patient group in an already established clinical routine workflow and how continued professional development is required to assess learning needs of HCPs. Importantly, addressing issues related to negative experiences in patient encounters as well as having open dialogue about the impact of personal values should be encouraged.