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Human Fertility an international, multidisciplinary journal dedicated to furthering research and promoting good practice

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Knowledge, attitudes and awareness regarding fertility preservation among oncologists and clinical practitioners in Lebanon Ghina Ghazeeri, Dina Zebian, Anwar H. Nassar, Sally Harajly, Alain Abdallah, Stephanie Hakimian, Bassem Skaiff, Hussein A. Abbas & Johnny Awwad To cite this article: Ghina Ghazeeri, Dina Zebian, Anwar H. Nassar, Sally Harajly, Alain Abdallah, Stephanie Hakimian, Bassem Skaiff, Hussein A. Abbas & Johnny Awwad (2016) Knowledge, attitudes and awareness regarding fertility preservation among oncologists and clinical practitioners in Lebanon, Human Fertility, 19:2, 127-133, DOI: 10.1080/14647273.2016.1193636 To link to this article: http://dx.doi.org/10.1080/14647273.2016.1193636

Published online: 04 Jul 2016.

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Date: 08 August 2016, At: 04:52

HUMAN FERTILITY, 2016 VOL. 19, NO. 2, 127–133 http://dx.doi.org/10.1080/14647273.2016.1193636

ORIGINAL ARTICLE

Knowledge, attitudes and awareness regarding fertility preservation among oncologists and clinical practitioners in Lebanon Ghina Ghazeeria, Dina Zebianb, Anwar H. Nassara, Sally Harajlya, Alain Abdallaha, Stephanie Hakimiana, Bassem Skaiffa, Hussein A. Abbasa and Johnny Awwada

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a Department of Obstetrics and Gynecology, American University of Beirut Medical Center, Beirut, Lebanon; bDepartment of Emergency Medicine, American University of Beirut Medical Center, Beirut, Lebanon

ABSTRACT

ARTICLE HISTORY

Fertility preservation (FP) aims to help individuals overcome the infertility associated with cancer treatments such as chemotherapy and radiation. The objective of this study was to assess the awareness, attitudes and knowledge of oncologists’ and clinical practitioners’ (CPs) about fertility preservation and its options in Lebanon. This was a cross-sectional study with surveys carried out between March 2012 and February 2013 on CPs at the American University of Beirut Medical Centre and Saint Jude’s Children Cancer Centre as well as all registered oncologists in Lebanon. Ninety percent of CPs (n ¼ 88) and 94% of oncologists (n ¼ 53) agreed that fertility preservation should be discussed with patient before their cancer treatment. Our data showed a gender bias in relation to patients being informed of their FP options, as well as conflicting knowledge of FP options available in Lebanon among oncologists. The CPs were more likely to have accurate knowledge of FP options and treatment than oncologists. A proactive approach is required to: (1) increase the awareness and knowledge of FP; (2) improve attitudes towards FP; and (3) encourage its communication between CPs, oncologists and patients in Lebanon. Increased education programs, awareness campaigns and development of dedicated FP centres are needed.

Received 8 February 2015 Accepted 26 August 2015

Introduction Fertility preservation (FP) is a rapidly developing medical field that aims to help women, men and children overcome infertility associated with cancer treatments such as radiation and chemotherapy. Other patients who might benefit from FP techniques are those with medical conditions affecting their fertility such as polycystic ovary syndrome, galactosaemia, family history of early menopause, lupus, Turner’s syndrome, chemical treatment of hepatitis or autoimmune diseases (Oktay, Goswami, & Darzynkiewicz, 2011). Increasing survival rates of cancer patients emphasize the significance of quality of life concerns including preservation of fertility. Time is a major survival factor among cancer patients and it is essential that FP is discussed and undertaken as early as possible and prior to initiation of cancer treatment. Potential current FP options include emergency embryo and oocyte cryopreservation, ovarian tissue freezing and sperm banking (Jensen, Morbeck, & Coddington, 2011). However, it is well established that the success rate of FP and subsequent delivery of live birth infants

Cancer patients; fertility preservation; FP awareness and attitudes; FP knowledge; oncologists

post-survival of cancer treatment is highly dependent on the type and timing of FP, the type of cancer treatment and the physiological state of the patient (Lee et al., 2006). Therefore, the role of the oncologists in raising the patients’ knowledge and awareness about the conditions that may threaten childbearing ability cannot be over emphasized. A proactive approach towards FP is required by the treating oncologist at all phases of treatment as he/she plays a key role in raising patient awareness about FP options. Oncologists have the obligation of sharing with their patients information about the availability of FP as an option to avoid future sterility and protect the reproductive potentials of cancer survivors (Snyder & Pearse, 2011). Despite the availability of guidelines by the American Society of Clinical Oncology (ASCO) published in 2006, and improved FP services worldwide, studies on FP referrals by oncologists have revealed that less than 50% refer cancer patients of child bearing age to a reproductive endocrinologist (Quinn et al., 2009) and less than 25% of oncologists follow the

CONTACT Ghina Ghazeeri Abiad [email protected]; Johnny Awwad [email protected] University of Beirut Medical Center, P.O. Box 11-0236, Riad El-Solh/Beirut 1107 2020, Lebanon ß 2016 The British Fertility Society

KEYWORDS

Department of Obstetrics and Gynecology, American

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ASCO guidelines despite willingness to discuss infertility in relation to cancer therapy (Kohler et al., 2011). A pilot qualitative cross-sectional study in the US explored the attitudes and perceptions of nurses in relation to fertility preservation and its discussion with cancer patients. They found that the majority of nurses discussed FP and its techniques with patients. They did so due to their belief that this was part of their role as a nurse and that they had the adequate knowledge, positive attitudes and behaviours towards FP (King et al., 2008). A dedicated fertility preservation unit is a centre that has the facilities and technologies to provide the latest research in preserving fertility as well as provision of fertility counselling to patients. Currently in Lebanon, no dedicated FP centres are available. The only widely available method of FP is sperm cryopreservation. In addition private insurance does not cover FP or other assisted reproductive technologies. Hence, cancer patients cannot benefit from the emerging field of FP and unfortunately their reproductive needs and choices remain unaddressed. To date, no study has assessed the knowledge and awareness of oncologists and clinical practitioners about FP in Lebanon. Therefore the aims of this study are: (i) to assess the knowledge and awareness of FP among clinical practitioners at the American University of Beirut Medical Centre (AUBMC), St Jude’s Children Cancer Centre and all oncologists in Lebanon; and (ii) to gather evidence of oncologists’ perceptions and practice patterns towards FP as well as their willingness to discuss FP with their patients and possible referral to a fertility specialist.

Materials and methods This study involved two groups of participants: clinical practitioners at the American University of Beirut Medical Centre (AUBMC) and St. Jude’s Children Cancer Centre, and all registered oncologists in Lebanon. Recruitment of respondents for each section of the study occurred between March 2012 and February 2013. Ethical approval for the study protocol was obtained from the Institutional Review Board at the American University of Beirut, Lebanon (Reference # OBG.GG.09). Whilst clinical practitioners gave informed written consent to take part in the study, oncologists were recruited anonymously. Oncologists were individually contacted via e-mail using a list of all practicing oncologists in Lebanon obtained from the Lebanese Society of Medical Oncology (LSMO) website. During the survey period, a total of 81 oncologists worked in Lebanon and were

distributed as follows: Beirut (n ¼ 49), Mount Lebanon (n ¼ 17), South Lebanon (n ¼ 7), North (n ¼ 7) and Bekaa (n ¼ 1). Each oncologist was individually contacted via e-mail and asked to participate in the study by completing the online anonymous survey. Three reminder e-mails were sent to each oncologist after which the data were collected by downloading the content from the online survey. In contrast, on a randomly selected day, clinical practitioners (nurses-specialized/general, doctorsspecialized/general and students) employed at the private clinics at AUBMC and at Saint Jude’s Children Cancer Centre were directly invited to partake in the study by five research assistants. After a brief explanation of the study in order to obtain consent, a hard copy of the survey was given to each CP to be completed and returned immediately. The research assistants circulated each floor of each centre and randomly selected CPs and invited them to partake in the study. The private clinics at AUBMC include: internal medicine (obstetrics and gynaecology, multiple sclerosis, dietetics, surgery and ophthalmology) otolaryngology, paediatrics, special children’s clinic, dermatology and psychiatry. Clinical practitioners (CP) and oncologists received different surveys. The first section of both surveys collected the demographic data and included the variables gender, age, nationality, speciality and years of experience. The second part of both surveys differed between CPs and oncologists. Questions relating to attitudes and knowledge towards FP amongst oncologists and CPs were derived from the published literature (Balthazar, Fritz, & Mersereau, 2011; Lee et al., 2006; Rabah, Wahdan, Merdawy, Abourafe, & Arafa, 2010). Section two of the CP’s survey comprised six items relating to knowledge and attitudes towards FP (five-point Likert scale and true-false). Section two of the oncologist’s survey was comprised of 23 items relating to attitudes and knowledge towards FP (fivepoint Likert scale and true-false). The statistical analyses were performed using the Statistical Package for the Social Sciences version 20.0 (SPSS Inc., Chicago, IL). Frequencies, means and standard deviations (SD) were used to describe various demographic characteristics of the study participants. Categorical variables were compared among groups using chi-square tests. Pearson’s correlation was used to compare FP knowledge scores with the various demographic characteristics. Results with p-value 0.05). Overall, 84.8% of oncologists believed that both males and females should be referred to a fertility specialist. However, only 39.6% of oncologists actually regularly did so, with 30.2% sometimes doing so, and 30.2% never doing so (Figure 1).

Clinical practitioners A total of 88 CPs were approached to participate in the survey and all of them agreed to do so (100% response rate). The majority of CPs were females (78.4%), Lebanese (93.1%), had a mean age of 28.74 ± 7.15 years, were general nurses (61.2%) and had a mean number of 6.56 ± 6.44 years’ experience (Table 3). The majority of CPs (85.5%) had not travelled aboard for study or work.

Attitudes and knowledge of FP among CPs Table 4 shows that 93.2% of CPs agreed that cancer treatment was a major threat to a patient’s fertility. Regarding the timing of sperm cryopreservation, 84.1% of CPs answered correctly (i.e. that it should be carried out before the start of treatment). The majority (70.6%) correctly responded that the success rate of FP is gender dependent. There was an agreement (89.8%) that discussion of FP and its impact on future reproductive health should be done with patients or their parents prior to cancer therapy. Most CPs (95.4%) believed that Lebanon is in need of FP units and 39.1% thought that Lebanon did not have FP units.

Discussion In Lebanon, little is known about health professionals’ attitudes towards FP practices for cancer patients. This study achieved its aims to investigate the

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Table 2. Attitudes, awareness, knowledge and practices towards fertility preservation among oncologists.

Table 2. Continued

Survey question

False 31 (72.1%) Total 43 The success rate of FP is equal in females and males True 18 (35.3%) False 33 (64.7%) Total 51 When should sperm cryopreservation be done? Before treatment 48 (92.3%) Anytime 1 (1.9%) Before or during therapy 2 (3.8%) Not sure 1 (1.9%) Total 52 Practices How often do you discuss cryopreservation with the patient? Routinely 38 (73.1%) Rarely 12 (23.1%) Never 2 (3.8%) Total 52 Do you refer patients to a fertility specialist? Regularly 21 (39.6%) Sometimes 16 (30.2%) Never 16 (30.2%) Total 53 Do you discuss sperm cryopreservation with parents of pre-pubertal patients? Routinely 26 (50.0%) Rarely 14 (26.9%) Never 11 (21.2%) N/A 1 (1.9%) Total 52 How important do you think sperm cryopreservation is? Very important 31 (62.0) Just important 17 (34.0) Not important 2 (4.0) Total 50

N (%)

Attitude/Awareness Cancer treatment is a major threat to patients’ fertility Agree/Strongly agree 47 (88.7%) Disagree 3 (5.7%) Strongly disagree 0 Undecided 3 (5.7%) Total 53 Discussion of FP and its future impact on reproductive health should always be done with patients and/or their parents Agree/Strongly agree 50 (94.4%) Disagree 1 (1.9%) Strongly disagree 0 Undecided 2 (3.8%) Total 53 All pre- and pubertal males should be told about FP prior to cancer treatment Agree/Strongly agree 50 (94.3%) Disagree 1 (1.9%) Strongly disagree 0 Undecided 2 (3.8%) Total 53 All pubertal males should be advised to do sperm banking prior to cancer treatment to preserve their fertility Agree/Strongly agree 45 (84.9%) Disagree 2 (3.8%) Strongly disagree 0 Undecided 6 (11.3%) Total 53 All pre and pubertal males should be referred to a FP unit prior to cancer treatment Agree/Strongly agree 44 (83.1%) Disagree 1 (1.9%) Strongly disagree 0 Undecided 8 (15.1%) Total 53 All pre and pubertal females should be told about FP prior to cancer treatment Agree/Strongly agree 37 (69.8%) Disagree 3 (5.7%) Strongly disagree 0 Undecided 13 (24.5%) Total 53 All pubertal females should be advised to do OTC prior to cancer treatment to preserve their fertility Agree/Strongly agree 35 (67.3%) Disagree 6 (11.5%) Strongly disagree 0 Undecided 11 (21.2%) Total 52 Lebanon is in need for FP units Agree/Strongly agree 39 (75.0%) Disagree 6 (11.5%) Strongly disagree 6 (11.5%) Undecided 1 (1.9%) Total 52 As an oncologist, I continuously do research on FP options, improvements and expenses Yes 17 (34.7%) No 32 (65.3%) Total 49 Are you familiar with ICSI? Yes 29 (55.8%) No 23 (44.2%) Total 52 Do you know where to refer patients for sperm cryopreservation? Yes 37 (69.8%) No 16 (30.2%) Total 53 Do you have a facility for sperm cryopreservation? Yes 34 (66.7%) No 17 (33.3%) Total 51 Knowledge In Lebanon there are no FP units/centres True 12 (27.9%)

(continued)

Survey question

N (%)

OTC ¼ Ovarian tissue cryopreservation; ICSI ¼ Intra-cytoplasmic sperm injection.

knowledge, attitudes and awareness of FP among clinical practitioners and oncologists. At AUBMC, although the majority of oncologists routinely discuss cryopreservation with their patients, there is little practice to refer patients to seek FP prior to cancer treatment. It is possible that the lack of welldeveloped FP centres in Lebanon impedes oncologists from referring their patients despite the fact that the majority of oncologists claim to discuss the matter with the patients. Similarly, Quinn et al. (2009) showed that only 47% of oncologists in the USA routinely referred their cancer patients to reproductive endocrinologists prior to cancer treatment and in Saudi Arabia less than 20% of males were referred for sperm banking (Rabah et al., 2010). In the UK, only one third of oncologists reported that they did not usually refer their patients to a specialist fertility service despite the patient expressing their concern about the impact of cancer treatment on their fertility (Adams, Hill, & Watson, 2013). Furthermore, UK oncologists viewed FP to be mainly a women’s issue, yet felt that they were more knowledgeable about sperm cryopreservation (Adams et al., 2013).

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Figure 1. Comparison of the percentage of oncologists (N ¼ 53) who believe that males and females should be referred to a fertility specialist prior to cancer treatment with the percentage of frequency of referrals.

Gender bias may exist among oncologists when discussing FP options because cryopreservation discussions occurred predominantly with male cancer patients. The gender bias is likely due to the practicality and high positive fertility outcomes associated with sperm cryopreservation when compared with ovarian tissue cryopreservation (Quinn et al., 2008). Such an attitude was also found by Quinn et al. (2008) whereby the less-advanced FP techniques for females led oncologists to believe that discussing such an issue with patients is to be avoided. In addition, Kohler et al. (2011) found significantly fewer women were referred to fertility specialists compared with males prior to their cancer treatment. Yet in this study the results indicated that oncologists believed that the difference in success rates between the sexes was not the key factor when making their referrals. The likelihood of referrals may depend on the gender of the oncologist and their attitudes towards FP (Quinn et al., 2008, 2009; Rabah et al., 2010; Schover, Brey, Lichtin, Lipshultz, & Jeha, 2002), however, this could not be elucidated from our data. It is more likely that oncologists remain naive about the various FP options (Adams et al., 2013) and their relative success rates among the sexes and thus cannot correctly communicate FP options to their patients. Lebanese oncologists are less informed about options, success and cost of FP, and were not familiar with intra-cytoplasmic sperm injection (ICSI), a keyassisted fertility option for couples seeking fertility in the Arab world (Rabah et al., 2010). Knowledge about FP resources is a major barrier to discussion of FP

options with cancer patients (Goodwin, Oosterhuis, Kiernan, Hudson, & Dahl, 2007; Quinn et al., 2007). In spite of the fact that more than 90% of the oncologists had at least six years of experience and 43.1% had more than 16 years of experience, they still lacked FP knowledge. This is contrary to the existing evidence that suggests an inverse relationship between physician knowledge regarding FP and time elapsed since graduation from medical school (Quinn et al., 2007). Thus, it is important to establish postgraduate education programs that educate oncologists in Lebanon about FP. Moreover, FP programs should be affordable for all sectors of Lebanese society: with the current healthcare system and insurance plans in Lebanon, it is most likely that FP programs would be accessible to only those who can afford it. A large proportion of CPs in this study were nurses whose attitude towards FP was generally positive with adequate knowledge of FP options. Confusion existed among CPs about whether FP centres were available in Lebanon. Similarly, King et al., (2008) found that although oncology nursing staff had the right attitude towards FP discussion with cancer patients, the major barrier to discussions was lack of knowledge of FP options. Lebanon unfortunately does not have dedicated FP centres, nor are there centres that counsel patients on their fertility options prior to cancer treatment, it is left solely to the discretion of the oncologist to mention this issue. The major strength of this study is the fact that it is the first study of its kind in Lebanon. It serves as a platform for further investigation in Lebanon into the

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Table 3. General characteristics of clinical practitioners.

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Characteristics Gender Male Female Total Nationality Lebanese Palestinian Total Age (years) Mean (± SD) 20–25 26–35 36–45 46 Total Qualificationsa Student Doctor specialized Doctor general Nurse specialized Nurse general Total Speciality Not specified Oncology Haematology and Oncology Paediatric Haematology and Oncology Paediatrics/OBGYN Family Medicine/Radiology Total Years of experience Mean (± SD) 5 6–15 16–25 26 Total Worked/Studied abroad No Yes Total Region where the Respondent Worked/Studied Abroad Europe Eastern Mediterranean Americas Total

Mean ± (SD) or N (%)

Table 4. Attitudes and knowledge towards fertility preservation among clinical practitioners. Survey question

19 (21.6%) 69 (78.4%) 88 81 (93.1%) 6 (6.9%) 87 28.74 (± 7.15) 38 (44.2%) 35 (40.7%) 9 (10.5%) 4 (4.7%) 86 16 7 2 8 52

(18.8%) (8.2%) (2.4%) (9.4%) (61.2%) 85

69 5 1 3 4 3

(81.2%) (5.9%) (1.2%) (3.5%) (4.7%) (3.5%) 85

6.56 (± 6.44) 50 (61.0%) 23 (28.0%) 7 (8.5%) 2 (2.4%) 82 71 (85.5%) 12 (14.5%) 83 b

3 (25.0%) 3 (25.0%) 6 (50.0%) 12

a

In qualifications: nurses include nurse aids, nurses in obstetrics, nurses in oncology and registered nurses; medical doctors include obstetricians, gynaecologists, oncologists, radiologists and paediatricians; and medical students include third and fourth year students. b Region to which country has been classified was based on the WHO classification. In this study, Europe specifically refers to Czech Republic, Slovenia & Spain, Eastern Mediterranean refers to Jordan, Kuwait and UAE and the Americas refers to the United States of America.

barriers associated with communication of FP options to patients, lack of knowledge among physicians and awareness of FP options available. The limitations of this study were many and included that the practice behaviour of oncologists and CPs, and system barriers to FP were not examined in significant depth. Moreover, the questions although important in identifying lack of knowledge and basic attitudes towards FP, did not provide much scope for an in depth analysis of the problem. In today’s society both genders equally value their reproductive potential post-cancer treatment and

N (%)

Attitude Cancer treatment is a major threat to patients’ fertility Agree/Strongly agree 82 (93.2%) Disagree 1 (1.1%) Strongly disagree 3 (3.4%) Undecided 2 (2.3%) Total 88 Discussion of FP and its future impact on reproductive health should always be done with patients and/or their parents Agree/Strongly agree 79 (89.8%) Disagree 6 (6.8%) Strongly disagree 3 (3.4%) Undecided 0 Total 88 Lebanon is in need for FP units Agree/Strongly agree 84 (95.4%) Disagree 1 (1.1%) Strongly disagree 1 (1.1%) Undecided 2 (2.3%) Total 88 Knowledge In Lebanon there are no FP units/centres True 34 (39.1%) False 53 (60.9%) Total 87 The success rate of FP is equal in females and males True 25 (29.4%) False 60 (70.6%) Total 85 When should sperm cryopreservation be done? Before treatment 74 (84.1%) Anytime 1 (1.1%) Before or during therapy 4 (4.5%) Not sure 9 (10.2%) Total 88

survival (Gardino, Rodriguez, & Campo-Engelstein, 2011). Thus, it should be encouraged that oncologists aim to avoid gender stigmatization and adhere to the ASCO guidelines on FP, whereby all patients of childbearing age should be informed about FP (Adams et al. 2013). In conclusion, to our knowledge this is the first study that investigates the attitudes, knowledge and awareness of FP among, oncologists and CPs in Lebanon. The AUBMC captures 15.3% of the cancer patients in Lebanon, and with the current fertility rate in Lebanon of 1.76 per childbearing woman (Jabbour, Giacaman, Khawaja, & Nuwayhid, 2012), which is below the replacement rate, more is needed to be done to ensure that oncologists and CPs are communicating and discussing FP with their patients and among themselves. This includes education, training, increasing awareness of risks of cancer treatments and current FP options, and the development of dedicated FP centres.

Disclosure statement The authors report no conflict of interest. The authors alone are responsible for the content and writing of the paper.

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