key: cord-0696891-rvfydvkb authors: Haham, Lilach Marom; Youngster, Michal; Shani, Adi Kuperman; Yee, Samantha; Ben-Kimhy, Reut; Medina-Artom, Tamar R.; Hourvitz, Ariel; Kedem, Alon; Librach, Clifford title: Suspension of fertility treatment during the COVID-19 pandemic: Views, emotional reactions and psychological distress among female fertility patients date: 2021-01-19 journal: Reprod Biomed Online DOI: 10.1016/j.rbmo.2021.01.007 sha: 1169f5e7fe4065202f102d49118765a5102cd2d4 doc_id: 696891 cord_uid: rvfydvkb RESEARCH QUESTION: : What are the patients' views and emotional reactions towards fertility treatment suspension during the COVID-19 pandemic as well as the factors affecting their psychological distress? DESIGN: : A cross-sectional study conducted in an academic fertility center. Online questionnaires were distributed between April 18(th) to April 23(rd) 2020 to patients whose treatment cycle had been postponed or discontinued. The outcome measures included (a) Agreement with the reproductive society guidelines to postpone treatments (b) Willingness to resume treatments, given the choice (c) Patients’ emotional reactions (d) Psychological distress level, measured by the Mental Health Inventory validated scale. A multivariate linear regression was conducted to identify factors associated with psychological distress. RESULTS: : Due to the small number of male respondents, only female patients were included in the analysis (N=181). 43% expressed disagreement with the guidelines and 82% were willing to resume treatments, given the choice. Sadness and anxiety were the most common emotional reactions expressed towards the guidelines. In the multivariate analysis, COVID-19 related anxiety and disagreement with treatment suspension were found to be significantly associated with patients' psychological distress. Patients' background characteristics did not contribute significantly to their distress. CONCLUSIONS: : Fertility treatment suspension during the initial phase of the COVID-19 pandemic was associated with patients' negative emotional reactions. Anxiety related to COVID-19 and disagreement with treatment suspension were found to be significantly associated with psychological distress among female fertility patients, regardless of their background characteristics. Our findings suggest the need to monitor patients' mental health and provide psychological support should a shutdown of fertility care re-occur. Since it was first recognized in Hubei Province, China, in December 2019, the novel Coronavirus Infectious Disease has spread rapidly throughout the world, leading the WHO, on March 2020, to declare a pandemic (WHO, 2020) . Facing a rapidly evolving emergency, most countries implemented outbreak control measures, including travel restrictions and border closure, social distancing, closure of educational and employment facilities, and wide scale quarantines (Anderson et al., 2020) . The outbreak impacted all medical fields resulting in formulation of new clinical guidelines for each, based on public health directives. This included suspension of all non-urgent care, averting further strains on the medical system, while enabling reallocation of healthcare resources to COVID-19 care (CDC, 2020) . Based on the aforementioned public health considerations put forth by the WHO and the lack of data regarding the impact of maternal infection in the first and second trimesters on pregnancy and neonatal outcomes Li et al., 2020; Yu et al., 2020; Dong et al., 2020) (ESHRE, 2020; CFAS, 2020; Cochrane, 2020) . It is well known that large-scale human disasters, such as: global pandemic diseases, natural disasters, war conflicts, social crises, etc., can lead to massive stress related disorders in the population affected (Ćosić et al., 2020; Lee et al., 2007) . Similar effects on the general population's mental health were demonstrated during the current outbreak. In a survey conducted in China during the early phase of the COVID-19 outbreak more than half of the respondents rated the psychological impact on them as moderate-to-severe and about one-third reported moderate-to-severe anxiety . However, studies evaluating the psychological effects of the COVID-19 pandemic on the infertile population are scarce. Infertility impacts the psychological, relational, and emotive aspects of the lives of most fertility patients, and is often described as their most stressful life event (Klonoff-Cohen et al., 2001; Slade et al., 2007) . Fertility treatments place physical, economical and emotional burdens on couples, hence serving as a major stress factor (El Kissi et al., 2013; Cwikel et al., 2004) . Several adaptive coping strategies including problem-focused coping, emotional processing and expression and positive reappraisal (Musa et al., 2014; Berghuis and Stanton, 2002; Stanton, 1991; Lancastle et al. 2008; Ockhuijsen et al., 2014) , as well as social support (Martins et al., 2011; Peterson et al., 2006) were found to help mitigate psychosocial distress and serve as potential protective mechanisms. The outbreak, as well as the response, imposed unprecedented negative social and psychological effects on the general population including fear of infection and its consequences, frustration, anger, anxiety and depression, social isolation due to large scale quarantines and financial uncertainty (Brooks et al., 2020; Rodríguez-Rey et al., 2020) . The unique circumstances of the COVID-19 pandemic, together with the unexpected suspension of fertility treatments, could aggravate the psychological and emotional distress of the fertility patients hence it was important to assess the mental health of this susceptible population. Data regarding the effect of treatment suspension on the fertility population during the current pandemic are limited. A survey conducted in New York demonstrated that most of the respondents were very upset by the cancellation of fertility treatments (Turcoy et al. 2020) . Another study from the UK found that patients appraised fertility clinic closure as having potential for a more negative than positive impact on their lives and to be very uncontrollable and stressful (Boivin et al., 2020) . The objectives of the current study based in Canada were to (a) investigate patients' views and emotional reactions towards the reproductive society (CFAS) guidelines, (b) assess the variables associated with patients' views (c) evaluate the factors contributing to fertility patients' psychological distress in this challenging situation. This questionnaire-based, mixed methods study was conducted at CReATe Fertility Centre, a large fertility center in Toronto, Canada. A cross-sectional and descriptive design was chosen due to the lack of empirical data on the experience of fertility treatment suspension during previous outbreaks, and in order to assess patients' views, emotional reaction as well as their psychological distress at this limited period of time during the current pandemic. The study protocol was approved by the VERITAS Research Ethics Board (IRB#16553) prior to data collection. All patients, either the female or the male partner and single women, ages 18 to 54, with a valid email address whose fertility treatment cycle had been postponed or discontinued following the COVID-19 CFAS guidelines (CFAS, 2020) were included in the study. Gestational carriers as well as oocyte donors were excluded. The questionnaire, designed and distributed via the google-forms platform, was sent by email to the study population. Patients received an email message with a written explanation regarding the study and a request that the questionnaire should be filled by only one partner. Consent to participate was obtained before the survey was initiated. The survey was distributed to a total of 464 patients between April 18 th and April 23 rd , 2020. Data were collected anonymously until May 7 th , 2020, before the reopening of our clinic. A total of 187 surveys were collected, of these, 6 were completed by patients who were in a same-sex male relationship. Due to the small number of males who completed the survey, only female patients were included in the final analysis (n=181). The questionnaire was constructed and reviewed by a team of reproductive physicians, The fourth part of the questionnaire assessed participants' views and emotional reactions to the guidelines to suspend treatments. First, patients were asked whether they believed the decision to suspend all fertility treatments was justified, and second, whether they would resume treatment, if given the choice. They were also asked to specify the main reason, in their opinion, for treatment suspension and, in case they did not wish to resume treatment, the main reason for this decision. Next, patients were asked to mark the main feelings they had in response to the CFAS guidelines. The choices included: anger, helplessness, anxiety, sadness, confusion, and relief. The last part included well-being and distress evaluation using the MHI-5 (Stewart et al.,1988) , and comprised of 5 items relating to the participant's well-being (e.g., "I felt relaxed and stress-free") and distress (e.g., "I felt sad and upset") during the past week. Responses were rated on a 6-point scale ranged from 1 ("never") to 6 ("all the time"). In this section, Cronbach's alpha was 0.78. The total score was calculated by averaging the responses to all 5 items, with a higher score reflecting greater psychological distress. Comments were imported to Excel spreadsheets for thematic analysis (Chapman et al., 2015; Vaismoradi et al., 2013) . Investigator triangulation was achieved by organizing the data, identifying recurrent themes, and labeling the contents using codes through an iterative process. The codes were then reviewed by L.M.H and A.K.S from the research team to inform the development of commonalities, emergent categories, underlying sub-themes, and interrelated patterns using constant comparative methods (Strauss and Corbin, 1998) . Differences were resolved through revision and discussion until consensus was reached. The data were then presented in a thematic map of a visual presentation of themes, sub-themes and categories to capture participants' main reasons relating to their views regarding the guidelines and resuming fertility treatment, given the choice. Analyses were conducted using Statistical Package for Social Sciences version 26. Chi Square/Fisher's exact, t-tests and ANOVA with post-hoc tests were used, as appropriate, to compare the differences between the study variables. Appropriate correlations were used to evaluate associations between the study independent variables. As this is a new area of study, lacking previous empirical data, a univariate analysis between all the study variables and the dependent variable MHI-5 was performed to look for variables that showed significant association with the outcome measure. Significant variables were then entered in a forward multivariate linear regression model predicting psychological distress. This was done to preserve power while identifying the most parsimonious model and the variables associated with psychological distress. Finally, a forward entry linear regression was used for subgroup analysis according to the attitude to the guidelines (agreement vs. disagreement). P value of <0.05 was considered statistically significant. One hundred and eighty-one women completed the survey for a response rate of 40%. Mean age of the participants was 37.7 years (SD= 4.6, range 29-54). Participants' characteristics are presented in Table 1 . The majority of participants (70%) had no children. 76% of respondents were planning to start IVF, while the rest were planning to start IUI or OI treatments. 93% of participants had a partner, about half had a postgraduate education, and 60% reported an above average household income level (≥ 110,000 CAD). A large proportion of the study population (81%) was currently working, about half foresaw an income loss in the upcoming period. However, most of them (78%) reported that a foreseeable income loss would not affect their plan to resume treatments. With regard to participants' attitude towards the CFAS guidelines, 43% expressed disagreement and the majority (82%) were willing to resume treatments, if they were given the choice. Participants' characteristics and COVID-19 related variables according to their agreement or disagreement with the CFAS guidelines and willingness or unwillingness to resume treatments are also presented in Table 1 . Income and infertility diagnosis differed significantly according to agreement with the guidelines: A significantly higher proportion of women in the higher income group disagreed with the guidelines compared to the lower income group (56/110, 50% vs. 14/51, 27%, χ2 = 7.8, p<0.01); as well as women with female factor infertility compared to other infertility diagnosis (35/66, 53% vs. 43/115, 37%, χ2 =4.2, p<0.05). In addition, a significantly greater proportion of women at the age of 35-40 were willing to resume treatments compared to women in the other age groups (χ2 =6.7, p<0.05). The majority of participants expressed feelings of sadness (66%), followed by anxiety (60%) and helplessness (60%) in response to the CFAS guidelines. Nevertheless, only 1 in 10 participants expressed confusion regarding the guidelines. As shown in Table 1 , participants who agreed with the guidelines had a higher COVID-19 anxiety score (2.95 vs. 2.45, t(179)= -3.90, p<0.01) as well as those who were unwilling to resume treatments (3.30 vs 2.61, t(179)= 4.12, p<0.01). In addition, a higher level of COVID-19 social support was found in women who agreed with the guidelines (3.52 vs 3.21, t(179)= -2.63, p<0.01), and in those who didn't wish to resume treatments (3.65 vs. 3.32, t(179) = 2.12, p<0.05). The key themes extracted from the respondents' free-text comments in favor of and against treatment postponement and willingness to resume treatments, despite foreseeable income loss, are listed in Table 2 Prior to performing a regression model, a univariable analysis was performed which showed a significant association between disagreement with the guidelines (t=2.99, p<0.01), lower COVID-19 social support (r=0.16, p=0.03), and higher psychological distress. Forward regression model was then applied in two steps, as presented in Table 3 . Step 1 was insignificant, with none of the background variables contributing significantly to the psychological distress. Step 2 showed significant associations between the main variables: disagreement with the guidelines, greater COVID-19 anxiety, and a higher distress (p<0.01). Due to significant differences in the COVID-19 anxiety score, in agreement with the guidelines shown previously, a point-biserial correlation analysis was performed, which showed a significant correlation between disagreement with the guidelines and COVID-19 anxiety (r= 0.28, p<0.001). Next, a split regression analysis of COVID-19 anxiety by agreement with the guidelines was performed demonstrating a significant association between COVID-19 anxiety and distress only in the agreement group, (p<0.01). More than six months since its onset, the COVID-19 pandemic continues to impact the world with an increasing number of cases and over 1,000,000 deaths worldwide. Resurgence of cases in those countries that loosened their restrictions early (reopening businesses, workplaces etc.) has even created the need to re-impose mitigation measures. At the beginning of the pandemic, many fertility scientific societies worldwide recommended suspension of all non-urgent fertility treatments for an indefinite period of time, leaving the infertility population with a great uncertainty. The objective of the current study was to capture patients' attitudes and emotional reactions to this shut down, as well as to evaluate variables contributing to their psychological distress during this unprecedent situation. Our findings suggest that almost half (43%) of the participants disagreed with the guidelines and a majority would have liked to resume treatment, despite the increasing rates of infection and limited data regarding the effects of COVID-19 infection during pregnancy. Previous recent studies demonstrated similar results regarding patients' views toward treatment suspension. A survey conducted in New York at the beginning of the pandemic found that 86% of patients preferred to have the option to start treatments in consultation with their physician, and 58% chose to resume, given the option (Turcoy et al., 2020) . In another study, evaluating the impact of the COVID-19 pandemic on fertility patients, only 6% of the participants declared that fertility treatments, including IVF, should be postponed (Vaughan et al., 2020) . Interestingly, in our study, participants' statements in favor of treatments' postponement were similar to the reasons stated in the guidelines including prevention of infection, saving health care resources for COVID-19 care, and possible risks of infection during pregnancy. Participants' statements against postponement and in favor of resuming treatments demonstrated concern regarding future strain on fertility clinics, agerelated time sensitivity of treatments, in addition to asserting that IVF is an essential medical service; and thus, a safe way to keep performing fertility treatments needs to be found. Higher household income as well as female factor infertility were found to be Moreover, financial concerns are important factors affecting the decision not to pursue treatment after the initial diagnosis (Eisenberg et al., 2010) . The pandemic contributed to financial instability due to increased rates of unemployment (ILO. March 18, 2020.," n.d.). Hence, patients with lower income tended to agree with the guidelines compared to patients with higher income, possibly due to concerns regarding the ability to pay for the treatments as well as their future financial security. Age was the only background characteristic associated with the desire to resume treatments, with higher rate of women at the age of 35 to 40 willing to resume. Data regarding the variables associated with the will to resume treatment during the COVID-19 pandemic are limited. A recent study ,conducted in Israel, demonstrated that shorter duration of treatment was the only variable found to be significantly associated with the wish to resume treatments during the current pandemic (Ben-Kimhy et al., 2020). However, the sociocultural difference between the Israeli and our study population might limit the generalizability of the results. Increased women's age and perceived poor prognosis were previously shown to be associated with unwillingness to pursue fertility treatment (Eisenberg et al., 2010; Malcolm and Cumming, 2004) . Moreover, both the marked decline in fecundability demonstrated at female's age of 35-40 years (Rothman et al., 2013) and the reduced success rates of MAR treatments after the age of 35 (Committee opinion of American Society for Reproductive Medicine, 2014) might explain our observation that women at the age of 35-40 years feel more pressure to resume treatment due to time sensitivity while older women are less keen to resume treatment due to poor prognosis. However, due to the lack of previous experience of treatment suspension during outbreaks, further studies are needed to establish this observation. Higher COVID-19 related anxiety was associated with unwillingness to resume treatments. Previous studies demonstrated a range of psychological impacts and emotional reactions of people during outbreaks such as fear of infection, falling sick or dying (Hall et al., 2008; Rubin et al., 2010) . A large recent study, from the early phase of the COVID-19 pandemic, showed that most respondents were concerned about family members contracting COVID-19 with higher concern associated with higher anxiety and stress scores . According to our study, although fertility patients made the decision, prior to the pandemic, to undergo fertility treatments, anxiety related to the pandemic had a negative effect on their decision to continue pursuing parenthood. Assessment of the parameters that contributed to participants' distress in our study showed that none of their background characteristics contributed significantly to their psychological distress. Infertility diagnosis and fertility treatments themselves are associated with increased psychological stress, anxiety and depression (Sbaragli et al., 2008; Matsubayashi et al., 2001) . Moreover, stress levels have been shown to be similar to those of patients with life threatening medical illnesses, such as cancer and heart disease (Domar et al., 1993) . Increased age, longer duration of infertility, previous fertility treatments and female factor infertility have been shown to be associated with higher stress levels in infertile women in previous studies (Domar et al., 1992; Ogawa et al., 2011; Patel et al., 2016; Zaidouni et al., 2018) Furthermore, the majority of participants expressed negative feelings in response to the CFAS guidelines. Of note, only 1 in 10 of the respondents felt confused, suggesting that most of the respondents understood the guidelines and confusion didn't play a major part in their emotional reaction. A previous study by Boivin et al. showed similar emotional reaction to clinics closure with more negative than positive emotions reported by the survey participants (Boivin et al., 2020) . Disagreement with the guidelines and higher COVID-19 related anxiety were significantly associated with higher distress. Further regression analysis, split by agreement with the guidelines, showed that COVID-19 related anxiety was associated with increased psychological distress, but only among women who agreed with the guidelines. Therefore, negative attitudes toward the guidelines, independent of the anxiety caused by the pandemic, were associated with higher distress. Social support has a significant effect on the health and social functioning of each individual (Landman-Peeters et al., 2005; Verhaak et al., 2005) . It serves as a protective factor against stress, reducing anxiety and depression levels, in both the infertile and fertile population (Landman-Peeters et al., 2005; Erdem et al., 2014) . In our study, women's perceived social support affected their views toward the guidelines. A higher COVID-19 social support score was associated with greater acceptance of the guidelines and unwillingness to resume treatment. Despite this, COVID-19 social support was not significantly associated with distress in the multivariate analysis. A strength of the present study is that all participants were affected by treatment suspension due to the guidelines, which contributes to the reliability of our results. In addition, the use of a validated scale to assess the patients' psychological distress increases the confidence in our findings and the external validity of our results. However, several limitations also need to be considered. First, our study includes patients from a single large fertility center located in a large urban area, in one country, which might limit the generalizability of our results. Second, due to clinic closure and avoidance of non-urgent visits, the questionnaires were distributed only via an on-line platform, which might have dissuaded those with limited computer skills from participating. Third, the questions were written in English, hence only applying to English speakers, which may not reflect the actual demographics of our population. Moreover, about one quarter of the study population engaged in a healthrelated occupation. This population might be keener to participate contributing to the limitation of the generalizability of our findings. Fourth, male population, either same sex couples or heterosexual partners, was not represented in this study, due to the small number of male participants. Previous studies showed different emotional reactions and stress between men and women (Slade et al., 2007; El Kissi et al., 2013) , hence it is important in future research to evaluate the effects on a predominantly male population. Finally, we do not have information regarding the characteristics of the non-responders due to the anonymity of response, which might contribute to a selection bias. However, the respondents' mean age did not differ significantly from that of the overall study population and the anonymity of response is a strength as it could reduce some types of response bias (eg. social desirability, fear of response etc.). Notwithstanding the above limitations, our study provides invaluable information regarding the female fertility population facing an unprecedented event of fertility clinic closures during the COVID-19 outbreak. The abrupt cessation of fertility treatments for an indefinite period of time increased the emotional burden and affected the psychological distress of this vulnerable population, independent of the anxiety related to the pandemic itself. Moreover, postponement of treatment is one the most frequently selected reasons for discontinuing treatment among patients (Gameiro et al., 2012) , thus increasing the risk for abandoning the dream of parenthood. These observations emphasize the importance of reaching out to the infertile population, offering psychological support such as professional online counseling and support groups. Employing extensive communication strategies, such as delivering updates via phone, email or social media regarding preparations for clinic reopening and personal discussions of treatment plans to be initiated at clinic reopening, can help reduce the patients' sense of uncertainty (Boivin et al., 2020) . Inquiring regarding one's coping resources (eg. keeping busy, engaging in physical activity, social support) and encouraging the use of coping strategies such as distraction and positive reappraisal, previously shown to be useful in managing uncontrollable stressful experiences, could promote better tolerance of the unpredictable situation as well as improve the patients' well-being (Ockhuijsen et al., 2014; Boivin et al., 2020) . Early interventions, as described above, might help mitigate foreseeable negative impacts on patients' mental health in future outbreaks of COVID-19 or other calamities. Future longitudinal studies, evaluating the well-being of fertility patients, both female and male, over time, conducted during routine and complex times will enable further understanding of patients' experiences, evaluation of the variables affecting their mental health and assessment of causal relationships, all of which will help us provide a tailored care for our patients. Fertility treatment suspension during the initial phase of the COVID-19 pandemic was associated with female patients' negative emotional reactions. COVID-19 related anxiety and negative attitudes towards treatment suspension were found to be significantly associated with psychological distress among female fertility patients regardless of their background characteristics. Recent experience of significant flares in the incidence of COVID-19 infection raises the concern that restrictive recommendations may need to be re-enacted in specific regions. Our findings suggest the need to closely monitor patients' mental health and provide psychological support should a shutdown of fertility care re-occur in the future. Anxiety related to COVID-19 and disagreement with fertility treatment suspension during the initial phase of the COVID-19 pandemic were found to be significantly associated with psychological distress among female fertility patients. Further studies are needed to evaluate the long-term psychological effects of the pandemic on the infertile population. Lilach Marom Haham MD completed her residency in Obstetrics and Gynecology at 2017 and is currently a clinical and research fellow in Reproductive Endocrinology and Infertility at CReATe Fertility Centre, Canada. Her research interests are preimplantation genetic testing and ART outcomes in the decreased ovarian reserve population. Access to and use of infertility services in the United States: Framing the challenges How will country-based mitigation measures influence the course of the COVID-19 epidemic? 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