ABSTRACT
Background:
The temporary delay in fertility treatments due to the coronavirus disease 2019 (COVID-19) pandemic, in combination with the imposed lockdowns, has created psychological distress and anxiety amongst infertile patients.
Aims:
The aim of this study was to evaluate how the pandemic has influenced assisted reproduction technology (ART) patients in Greece, during the second wave of the pandemic. An additional aim was to examine the effects of the pandemic on cross-border patients in particular, compared to national ones.
Settings and Design:
This study was a cross-sectional, questionnaire-based study, distributed to 409 patients of a single in vitro fertilisation (IVF) clinic in Greece, during the period between January until the end of April 2021.
Materials and Methods:
The survey was conducted online via E-mail and was distributed to national and international female patients of a single IVF clinic in Greece, who were undergoing ART treatment during the second wave of the COVID-19 pandemic. Patient participation was anonymous, and participants provided informed consent for collection and publication of data.
Statistical Analysis Used:
The mean values of baseline characteristics, along with answer percentages per questionnaire item, were calculated. Collected data were cross-tabulated, and the Chi-square test was used as a measurement of the differences between national and cross-border patients. A P value lower than 0.05 was considered statistically significant. All analyses were conducted using the SPSS Statistics software.
Results:
From 409 initial candidates, 106 women, with a mean age of 41.2 years, completed the questionnaire (26% response rate). The majority of national patients did not experience any delays in their fertility plans (62%), while cross-border patients experienced over 6 months of delays (54.7%). The main reason for fertility postponement was travel restrictions due to COVID-19 for cross-border patients (62.5%), while national patients cited additional reasons. The majority of patients experienced a degree of stress (65.2%) due to the delays, however were not fearful of COVID-19 infection (54.7%). Most patients were aware of the protective measures taken by IVF clinics (80.2%), and this was a determinant factor (71.7%) for their decision to restart their fertility treatment.
Conclusion:
The COVID-19 pandemic lockdowns had a significant emotional impact on patient receiving or undergoing ART treatment in Greece. This impact was more pronounced on cross-border patients. This highlights the need for continuation of ART care, with the appropriate protective measures, during the pandemic, as well as during similar times of crisis in the future.
KEYWORDS: Assisted reproductive technology, coronavirus disease 2019 pandemic, cross-border reproductive care patients, suspension of fertility treatments
INTRODUCTION
Infertility has been repeatedly shown to exert a severe psychological impact on affected couples, leading to distress, anxiety, depression and feelings of inadequacy or inferiority.[1] Assisted reproduction technology (ART) treatments represent a significant source of stress for couples, impacting most aspects of their life.[2] During national or global crises, medical services other than ART might be prioritised, thus further exacerbating the impact of infertility on couples’ lives.
The most recent example of such a crisis is the coronavirus disease 2019 (COVID-19) pandemic, as well as the impact of lockdowns and closure of fertility clinics that followed. Nationwide lockdowns were implemented since March 2020 to combat the spread of the virus in most countries. Fertility clinics were recommended to cease all activities, both to limit the spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), as well as to reallocate healthcare resources.[3] The present study aimed to assess the impact of the second wave of the pandemic on national as well as international (or cross-border) patients, seeking or already undergoing fertility treatment in Greece. With this study, we aimed to report on the findings and observations from our clinic and compare those to relevant data from the available literature. This could contribute to the formation of a more effective strategy regarding fertility treatment, should another national or international crisis appear.
MATERIALS AND METHODS
This was a cross-sectional, anonymous, online survey conducted by a single, private in vitro fertilisation (IVF) clinic in Greece. No ethics committee approval was requested, as the anonymous and observational nature of our study ensured that no clinical decision-making was based on the design or results of the present study, thus not affecting the participants. However, our methodology was based on and defined by the Helsinki Declaration principles for ethical medical research. The survey was based on 17 multiple-choice questions, which were optional. Four questions concerned the access to fertility treatment, six assessed the psychological impact of COVID-19, four were about their future fertility plans and three questions regarded communication with fertility service. Patient demographic information, namely country of residence and age of the female partner, was collected and its disclosure was mandatory for participation to the survey.
The questionnaire was translated into three languages (Greek, Italian and Serbian). The survey was designed using the NEX-Forms platform, uploaded to the IVF clinic's website. Patients were asked to participate via E-mail during the period between 18 January and 24 February 2021. Eligibility criteria included couples of the clinic who were undergoing or intended to undergo ART treatment during the second wave of the COVID-19 pandemic. Upon clicking the survey link, information relevant to the study, research policy and the questionnaire was presented to the participants. Data were collected over a 3-month period. In total, 409 couples were invited to participate via E-mail.
No sample size calculation (statistical power analysis) was conducted, as all available patients who fulfilled the established eligibility criteria were invited to participate. The collected data were analysed per question and correlations between the answers given and the patients’ demographic characteristics were sought, in particular country of origin. Given the travel restriction and the multiple risks and complicated procedures regarding cross-border travel during the time period of the study, patients were categorised into two groups, national and cross-border patients, in order to more accurately assess this effect. Data were cross-tabulated and assessed using the Chi-square test, with a significance level below 0.05 (P < 0.05) being considered statistically significant. SPSS Statistics for Macintosh, Version 27.0. Armonk, NY, USA: IBM Corp. Software was used to conduct data collection and to perform all analyses.
RESULTS
From the 409 couples who were invited to participate, 106 completed the survey (response rate of 26%). In particular, 42 out of 169 sent Greek questionnaires were answered (response rate for Greek-speaking participants: 24.9%), 31 out of 101 sent Serbian questionnaires were answered (response rate for Serbian-speaking participants: 30.7%), 22 out of 93 sent English questionnaires were answered (response rate for English-speaking participants: 23.7%) and 11 out of 46 Italian questionnaires were answered (response rate for Italian-speaking participants: 23.9%).
The demographic characteristics of the participants are presented in Table 1. The female mean age was 41.2 years (standard deviation ± 5.2). The majority of participants (62.2%) were in the age group of 36–45 years. Overall, 39.6% of the participants were from Greece, 26.4% from Serbia, 11.3% from the United Kingdom, 10.4% from Italy and the remaining 12.3% were responders from other countries [Table 2].
Table 1.
Demographic characteristics of the survey participants
| Parameter | Result |
|---|---|
| Participants, n | 106 |
| Age (years), mean±SD | 41.22±5.201 |
| Age group, n (%) | |
| 25–35 | 18 (17) |
| 36–45 | 66 (62.2) |
| 46–50 | 22 (20.8) |
| Country of residence, n (%) | |
| Greece | 42 (39.6) |
| Serbia | 28 (26.4) |
| UK | 12 (11.3) |
| Italy | 11 (10.4) |
| Others* | 13 (12.3) |
*Others include Australia (n=1, 0.9%), Chile (n=1, 0.9%), Estonia (n=1, 0.9%), France (n=1, 0.9%), Germany (n=2, 2%), Ireland (n=1, 0.9%), Kosovo (n=1, 0.9%), the Republic of North Macedonia (n=1, 0.9%) and the USA (n=4, 4%). SD=Standard deviation
Table 2.
Results of Chi-square test per question, in relation to country of origin and age group
| Parameters | Q1 | Q2 | Q3 | Q4 | Q5 | Q6 | Q7 | Q8 |
|---|---|---|---|---|---|---|---|---|
| Correlation with Country | ||||||||
| χ2 | 28.674 | 22.319 | 35.387 | 5.028 | 5.821 | 0.260 | 8.322 | 4.879 |
| df | 3 | 4 | 6 | 4 | 2 | 2 | 2 | 2 |
| P | <0.001* | <0.001* | <0.001* | 0.284 | 0.054 | 0.878 | 0.016* | 0.087 |
|
| ||||||||
| Parameters | Q9 | Q10 | Q11 | Q12 | Q13 | Q14 | Q15 | Q16 |
|
| ||||||||
| Correlation with Country | ||||||||
| χ2 | 13.231 | 0.308 | 7.949 | 2.746 | 59.241 | 18.400 | 0.653 | 0.006 |
| df | 3 | 1 | 1 | 1 | 3 | 5 | 1 | 1 |
| P | 0.004* | 0.579 | 0.005* | 0.097 | <0.001* | 0.002* | 0.419 | 0.939 |
*Statistically significant. χ2=Pearson’s Chi-square value, df=Degrees of freedom
A total of 40 couples with infertility (37.7%) had their treatment cancelled for more than 6 months due to the COVID-19 pandemic, 13.3% of participants got their treatment cancelled for 3–6 months and 11.3% for <3 months, while 37.7% did not experience any delay. There was a statistically significant difference between national and cross-border patients, with 62% of the former reporting no postponement, whereas 54.7% of the latter reporting a delay of at least 6 months (P < 0.001) [Figure 1]. The main reason cited for treatment postponement was access restrictions (44.3%) while financial reasons, health conditions and psychological reasons were significantly less frequently cited. A number of patients (13.2%) cited multiple reasons. Once more, there was a statistically significant difference amongst national and cross-border patients, with the latter citing access restrictions, as the main reason significantly more frequently (P < 0.001) than national patients, whose answers were more evenly distributed [Figure 2].
Figure 1.

Bar chart of the duration of fertility treatment postponement in national and cross-border patients
Figure 2.

Bar chart of the main reasons for treatment postponement in national and cross-border patients
Regarding patient experience during the COVID-19 pandemic, the desire to have a child remained unaffected for the majority (67%), while 11.3% were extremely adversely affected and 19.8% were mildly adversely affected. Additionally, the majority of survey participants (54.7%) reported no fear of undergoing assisted reproduction treatment during the COVID-19 era, with only 5.7% reporting extreme fear and 35.8% experiencing fear to a lesser degree. Regarding stress due to treatment postponement, 33.2% of female patients were extremely stressed that the delays could potentially decrease their fertility potential, 32% were less stressed, while also 32% answered that the delay did not concern them. This answer distribution is significantly different when country of origin is considered, as the majority of cross-border patients were significantly more prone to stress, while most of the national patients reported no stress whatsoever (P = 0.016). With regard to the potential effects of SARS-CoV-2 infection on the foetus after successful fertility treatment, 31.1% of participants were not concerned, 34% were mildly concerned and 11.3% were extremely concerned.
With regard to COVID-19 vaccination, 21.7% of participants were concerned that the vaccination would lead to additional postponement of their fertility treatment, while 39.6% were concerned about the safety of the vaccine during pregnancy. Some responders (23.6%) mentioned no concerns regarding the vaccination. Safety concerns were more prominent for national patients (P = 0.004), whereas for cross-border patients, the further delays were also important in addition to safety concerns. The vast majority of participants (80.2%) were aware of the protective measures taken by IVF centres during the COVID-19 era, and the majority (71.7%) also stated that a strict COVID-19 policy was a positive determinant of their decision to undergo IVF treatment [Figure 3].
Figure 3.

Pie chart summary of the awareness of protective measures in clinics and the positive effect of protective measures on patient decision-making
Regarding the participants’ future fertility plans, 16% were not considering treatment in the future, 36.9% hoped to travel abroad despite the COVID-19 pandemic in order to undergo fertility treatment, while 29.2% would remain in their home country for treatment. 11.3% of the survey participants were willing to wait until the crisis is over and then restart treatment. The majority of patients (45.3%) were informed through E-mails and phone calls from the IVF centre regarding fertility treatments during COVID-19 pandemic. When the answers were stratified by country, this trend remained consistent, however there was a statistically significant difference (P < 0.002), with cross-border patients being more likely to use the internet to contact the IVF clinic.
All collected answers and questions, stratified by country of origin (national or cross-border), as well as the questions themselves are presented in Supplementary Table 1.
Supplementary Table 1.
The study questionnaire, along with answers stratified based on country of origin and age group
| Questions and answers | Patient origin | Total (answers) n, (%) | |
|---|---|---|---|
|
| |||
| National n, (%) | Cross-border n, (%) | ||
| Q1. Fertility treatment postponement due to COVID-19 outbreak | |||
| <3 months | 8 (19) | 4 (6.2) | 12 (11.3) |
| 3–6 months | 3 (7.1) | 11 (17.2) | 14 (13.3) |
| >6 months | 5 (11.9) | 35 (54.7) | 40 (37.7) |
| No postponement | 26 (62) | 14 (21.9) | 40 (37.7) |
| No response given | 0 | 0 | 0 |
| Q2. If you have postponed your treatment which are the main reasons? | |||
| Access restrictions | 7 (17) | 40 (62.5) | 47 (44.3) |
| Financial reasons | 4 (9.5) | 0 | 4 (3.8) |
| Health condition | 2 (4.7) | 0 | 2 (1.9) |
| Psychological reasons | 0 | 2 (3.1) | 2 (1.9) |
| >2 answers | 3 (7.1) | 11 (17.2) | 14 (13.2) |
| No response given | 26 (61.7) | 11 (17.2) | 37 (34.9) |
| Q3. Which of the following access restrictions have you experienced as a result of the COVID-19 outbreak in your fertility treatment? | |||
| My healthcare provider cancelled my IVF treatment | 5 (12) | 1 (1.6) | 6 (5.7) |
| My healthcare provider suggests to freeze my embryos/sperm | 1 (2.4) | 0 | 1 (0.9) |
| My visits (consultation) changed from in-person to phone or telemedicine/video | 1 (2.4) | 1 (1.6) | 2 (1.9) |
| Nothing changed in my IVF care or birth plan | 16 (38) | 6 (9.4) | 22 (20.7) |
| Limited travelling options | 6 (14.3) | 40 (67.3) | 46 (43.6) |
| I (or my partner) was tested positive for SARS-CoV-2 | 4 (9.5) | 1 (1.6) | 5 (4.7) |
| >2 and/or other answers | 4 (9.5) | 12 (18.8) | 16 (15) |
| No response given | 5 (11.9) | 3 (4.7) | 8 (7.5) |
| Q4. Type of fertility treatment that was postponed | |||
| Fertility consultation | 1 (2.4) | 5 (7.8) | 6 (5.6) |
| IVF | 1 (2.4) | 1 (1.6) | 2 (1.9) |
| Intrauterine insemination | 11 (26.2) | 23 (36) | 34 (32) |
| Frozen embryo transfer | 1 (2.4) | 0 | 1 (0.9) |
| Reproductive surgery | 5 (11.9) | 22 (34.3) | 27 (25.5) |
| No response given | 23 (54.7) | 13 (20.3) | 36 (34.1) |
| Q5. How has the COVID-19 outbreak affected your desire to have a child? | |||
| My desire was extremely adversely affected | 1 (2.4) | 11 (17.2) | 12 (11.3) |
| My desire was mildly adversely affected | 9 (21.4) | 12 (18.8) | 21 (19.8) |
| My desire has not been affected at all | 32 (76.2) | 39 (60.9) | 71 (67) |
| No response given | 0 | 2 (3.1) | 2 (1.9) |
| Q6. Did you experience fear to undergo an assisted reproduction treatment during COVID-19 pandemic crisis? | |||
| Extremely | 2 (4.8) | 4 (6.3) | 6 (5.7) |
| Mildly | 16 (38) | 22 (34.4) | 38 (35.8) |
| Not at all | 22 (52.3) | 36 (56.2) | 58 (54.7) |
| No response given | 2 (4.9) | 2 (3.1) | 4 (3.8) |
| Q7. Did you experience stress of a decrease in fertility potential due to the postponement of your fertility treatment for an undefined period of time? | |||
| Extremely | 9 (21.4) | 26 (40.6) | 35 (33.2) |
| Mildly | 12 (28.6) | 22 (34.4) | 34 (32) |
| Not at all | 20 (47.6) | 14 (21.9) | 34 (32) |
| No response given | 1 (2.4) | 2 (3.1) | 3 (2.8) |
| Q8. In case you had a successful fertility treatment, have you experienced added stress or fear due to potential effects of COVID-19 pandemic in your health and your foetus? | |||
| Extremely | 8 (19) | 4 (6.3) | 12 (11.3) |
| Mildly | 14 (33.3) | 22 (34.4) | 36 (34) |
| Not at all | 10 (23.8) | 23 (35.9) | 33 (31.1) |
| No response given | 10 (23.9) | 15 (23.4) | 25 (23.6) |
| Q9. What are your thoughts and feelings regarding the COVID-19 vaccination? | |||
| I am concerned that my fertility potential will decrease further due to additional postponement of my fertility treatment | 2 (4.8) | 21 (32.8) | 23 (21.7) |
| I am worried about the safety of the COVID-19 vaccine during pregnancy | 22 (40.5) | 20 (31.3) | 42 (39.6) |
| I do not have any concerns regarding the COVID-19 vaccine | 12 (28.6) | 13 (20.3) | 25 (23.6) |
| I am planning to do the COVID-19 vaccine and wait until it is safe to start my fertility treatment | 3 (7.1) | 7 (10.9) | 10 (9.4) |
| No response given | 3 (7.1) | 3 (4.7) | 6 (5.7) |
| Q10. Are you trying to achieve pregnancy by natural conception during COVID-19 pandemic? | |||
| Yes | 18 (42.9) | 30 (46.9) | 48 (45.3) |
| No | 24 (52.3) | 32 (50) | 56 (52.8) |
| No response given | 0 | 2 (3.1) | 2 (1.9) |
| Q11. Are you aware of the protective measures taken by IVF centre to guarantee your safety during COVID-19? | |||
| Yes | 40 (95.2) | 45 (70.3) | 85 (80.2) |
| No | 2 (4.8) | 16 (25) | 18 (17) |
| No response given | 0 | 3 (4.7) | 3 (2.8) |
| Q12. Did the implementation of a strict COVID-19 policy by your IVF centre affect positively your decision to undergo treatment? | |||
| Yes | 36 (85.6) | 40 (60.9) | 76 (62.2) |
| No | 5 (12) | 14 (21.9) | 29 (27.4) |
| No response given | 1 (2.4) | 10 (17.2) | 11 (10.4) |
| Q13. What are your future fertility plans? | |||
| I will perform fertility treatment in my home country to avoid travelling restrictions | 27 (64.3) | 4 (6.3) | 31 (29.2) |
| I will travel abroad seeking for fertility treatment in the following months despite the COVID-19 pandemic | 1 (2.4) | 38 (59.3) | 39 (36.9) |
| I will wait until COVID-19 crisis is over | 1 (2.4) | 11 (17.2) | 12 (11.3) |
| I am not currently thinking about future fertility plans | 10 (23.8) | 7 (10.9) | 17 (16) |
| No response given | 3 (7.1) | 4 (6.3) | 7 (6.6) |
| Q14. What sources of information regarding COVID-19 and infertility treatment do you use during the COVID-19 pandemic? | |||
| Internet | 9 (21.4) | 24 (37.5) | 33 (31.1) |
| TV | 0 | 9 (14) | 9 (8.5) |
| Webinars | 1 (2.4) | 5 (7.8) | 6 (5.7) |
| Social media | 0 | 2 (3.1) | 2 (1.9) |
| E-mails and phone calls from your IVF centre | 26 (61.9) | 22 (34.4) | 48 (45.3) |
| Others | 4 (9.5) | 1 (1.6) | 5 (4.7) |
| No response given | 2 (4.8) | 1 (1.6) | 3 (2.8) |
| Q15. Have you communicated with your IVF centre to talk about the reasons (access, physiological, medical and financial) of your treatment postponement due to COVID-19 outbreak? | |||
| Yes, our communication helped to find solutions | 24 (57.2) | 42 (65.7) | 66 (62.3) |
| No, I don’t find useful | 8 (19) | 9 (14) | 17 (16) |
| No response given | 10 (23.8) | 13 (20.3) | 23 (21.7) |
| Q16. Would you like to receive more information from the IVF centre about COVID-19 and its implications on IVF treatment/pregnancy? | |||
| Yes, I would like to receive professional guidance instead of other sources | 29 (69) | 45 (70.3) | 74 (69.8) |
| No, I don’t think it is necessary | 12 (28.6) | 18 (28.1) | 30 (28.3) |
| No response given | 1 (2.4) | 1 (1.6) | 2 (1.9) |
| Total (categories) | 42 (39.6) | 64 (60.4) | 106 (100) |
IVF=In vitro fertilisation, COVID-19=Coronavirus disease 2019, SARS-CoV-2=Severe acute respiratory syndrome coronavirus 2
DISCUSSION
The results of this study validate our initial hypothesis with regard to the significance of the impact that the COVID-19 pandemic had on IVF patients, cross-border ones in particular. We showed that cross-border patients were significantly more prone to prolonged delays in their fertility care plan, with the most significant underlying cause being travel restrictions. On the contrary, the majority of national patients experienced no delays and those that did, cited various other reasons apart from travel restrictions. The effect of added stress due to COVID-19-related delays was significantly more pronounced in cross-border patients compared to national ones, highlighting the significance of fertility care, especially when the patients are travelling abroad to receive it, while the majority of patients regardless of nationality were not fearful of COVID-19 infection itself as much as the delays. These observations make apparent the significance of ART treatment for patients and that maybe they should be considered a part of essential healthcare services due to their time-sensitive nature and emotional impact on patients.
The rapid spread of the COVID-19 pandemic around the globe, combined with the inadequacy of most healthcare systems to hospitalise all patients in need, led to the suspension of all non-urgent medical services in early 2020.[2,4] This included fertility treatments at the start of the pandemic and at different times during the 2 years since, both for reallocation of resources and to protect fertility patients from the effects of SARS-CoV-2 on gamete quality and function.[5] Both the pandemic and associated protective measures had a significant psychological impact on fertility patients worldwide, as shown by multiple studies, with opinions on several aspects of the situation being recorded.
A consistent finding in most studies was that the majority of patients, up to 90% in some cases, disagreed with clinic closure and wished to continue treatment regardless of the pandemic.[6,7,8,9,10] The same held true in our study, with the majority of patients (54.7%) not fearing the effects of the pandemic and wishing to continue regardless. This consistent trend indicates that ageing and reduction of fertility potential, is a more important factor for IVF patients, thus leading to many advocating for the continuation of clinic operation and prioritisation of cases in similar times of crisis.[11] However, patient safety is paramount as well, and in this regard, proper patient education of the risks and the necessity of protective measures was shown to significantly affect patient opinion in comparison to the control group.[10] Proper information was valued by our patients as well, since the majority (69.5%) wished to be provided with information and education by the clinic, highlighting the guiding role that IVF clinics should play for their patients in such times of crisis.
Significant changes were noted in the emotional outlook and behaviour of the general population during the pandemic,[12,13] with changes noticed in fertility patients as well. Based on observations from the available studies, there was a consistent trend of negative feelings prevalence in IVF patients due to clinic closure; feelings of stress and depression in particular,[2,9,10,14,15,16,17,18,19] with a couple of studies reporting even more severe effects, such as sleep disturbances.[7,20] These observations highlighted the role of mental health support and provision of mental health services to patients.[8] A similar trend was present on our patients as well, with the majority (65.1%) experiencing stress to some degree due to clinic closure, while also finding contact with the clinic useful, thus indicating the supportive role that the clinic could play in challenging times in the future. The data from the available literature is summarised in Table 3.
Table 3.
Summary of the main characteristics of the available studies in the literature
| Study | Country | Participants | Response rate (%) | Mean age (years) | Disagreement with closure (%) | Wish to continue regardless/no fear (%) | Negative feelings (stress, etc.) (%) | Main stressor | Need for measures (social support, etc.) |
|---|---|---|---|---|---|---|---|---|---|
| Ben-Kimhy et al.[2] | Israel | 168 | 57 | 37 | 50 | 72 | N/R | N/A | Yes |
| Boivin et al.[14] | UK | 446 | 48 | 33.4 | N/A | N/A | N/A | Clinic closure | N/A |
| Cirillo et al.[15] | Italy | 140 | 44.5 | 39.4 | N/A | N/A | >50 | Fertility plan | N/A |
| Gordon and Balsom[20] | Canada | 92 | N/A | 34.2 | N/A | N/A | 86 | Clinic closure | Yes |
| Gupta et al.[6] | India | 170 | N/A | 30.23 | N/A | 100 | 90 | Clinic closure | Yes (mainly prioritisation) |
| Marom Haham et al.[9] | Canada | 181 | 40 | 37.7 | 43 | 82 | 66 | Clinic closure | Yes |
| Kaur et al.[7] | India | 86 | 86 | Majority: 25–35 | 52 | 49 | >70 | Clinic closure | Yes |
| Lawson et al.[10] | USA (control group) | 787 | 42.6 | 37.2 | <50 (greater agreement in intervention group) | >50 (both groups, no difference) | >70 (both groups, no difference) | N/A | Yes |
| Seifer et al.[8] | USA | 214 | 29.2 | 35.5 | N/A | 40.2 | N/A | Mental health | Yes |
| Tippett[16] | UK | 124 | 96 | Majority: 26–39 | N/A | N/A | N/A | N/A | Yes |
| Tokgoz et al.[17] | Turkey | 101 | 55.6 | 33.3 | >50 | N/A | 71.3 | Effects on pregnancy | Yes |
| Vaughan et al.[18] | USA | 2202 | 34 | 35.4 | >90 | N/A | N/A | Infertility | N/A |
| Esposito et al.[19] | Italy | 627 | 41.9 | Majority: 31–39 | N/A | N/A | 64 | Effects on pregnancy | Yes |
| Current study | Greece | 106 | 26 | 41.22 | N/A | 54.7 | 65.1 | Clinic closure | Yes (mainly information- education) |
N/A=Not assessed
The present study has several strengths. In particular, this survey is amongst the few studies that assessed cross-border patients and their differences compared to national patients during the pandemic, highlighting a need for particular attention and care to this group, especially since cross-border fertility care is on the rise.[21] Additionally, our study assessed patient experience during the second wave of the pandemic, thus providing insight to the way opinions formed and shifted 1 year after the initial shock and with more information available. Finally, our study was able to assess the views of fertility patients regarding COVID-19 vaccination, a useful insight into a vulnerable group with multiple other contributing factors.
However, our study was not without certain limitations. The most notable one was the low response rate and small sample size. However, this limitation was unavoidable, since our survey's target group was limited to the patients of a single IVF clinic in Greece, during a specific time period; while similar response rates were recorded in other studies as well.[8] Additionally, not all responders answered every question, therefore not all of their opinions and experiences were included in the final data, carrying a risk of misrepresentation of certain opinions. Finally, as is with every cross-sectional study, we cannot completely eliminate the possibility of survey error, response bias and the fact that participants’ perceptions might have changed since then, limitations intrinsic in every questionnaire survey.
Fertility tourism is steadily on the rise in Greece. This fact renders understanding cross-border patient perspectives, views and needs vital for the provision of proper IVF services. For this reason, there are plans to further follow up on the observations and conclusions made in the present study in the future; with the aim to better understand patient needs and explore ways to effectively support patients, improve provided services and simplify the process of cross-border fertility care.
CONCLUSION
IVF clinic shutdown during the COVID-19 pandemic significantly affected fertility patients. We showed, in concordance with other studies, that the majority of patients were actually more fearful of delays than of COVID-19 infection and that the clinic shutdown was a significant source of stress and feelings of depression. These findings are indicative of the importance of IVF clinics for couples facing infertility and that they maybe should be considered amongst essential healthcare services and continue operation during future times of crisis as well. Preparation of patient protection protocols, provision of patient mental health support and continuous vigilance should be a priority for ART institutions. This will facilitate improved management and support of fertility patients in future times of crisis, similar to the COVID-19 pandemic, should they occur.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
Data availability and sharing statement
All primary data are available for disclosure by the corresponding author upon reasonable request.
Acknowledgements
The authors kindly thank the staff of the private IVF clinic “EmbryoClinic” who supported the translation of the questionnaire into three languages (Greek, Italian and Serbian) as well as the data collection process and e-mail communication.
REFERENCES
- 1.Seibel MM, Taymor ML. Emotional aspects of infertility. Fertil Steril. 1982;37:137–45. doi: 10.1016/s0015-0282(16)46029-2. [DOI] [PubMed] [Google Scholar]
- 2.Ben-Kimhy R, Youngster M, Medina-Artom TR, Avraham S, Gat I, Marom Haham L, et al. Fertility patients under COVID-19: Attitudes, perceptions and psychological reactions. Hum Reprod. 2020;35:2774–83. doi: 10.1093/humrep/deaa248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.COVID-19 and Assisted Reproduction 2020-2022. [Last accessed on 2023 Jan 16]. Available from: https://www.eshre.eu/Guidelines-and-Legal/ Position-statements/COVID19 .
- 4.Madjunkov M, Dviri M, Librach C. A comprehensive review of the impact of COVID-19 on human reproductive biology, assisted reproduction care and pregnancy: A Canadian perspective. J Ovarian Res. 2020;13:140. doi: 10.1186/s13048-020-00737-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Anifandis G, Messini CI, Daponte A, Messinis IE. COVID-19 and fertility: A virtual reality. Reprod Biomed Online. 2020;41:157–9. doi: 10.1016/j.rbmo.2020.05.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Gupta M, Jaiswal P, Bansiwal R, Sethi A, Vanamail P, Kachhawa G, et al. Anxieties and apprehensions among women waiting for fertility treatments during the COVID-19 pandemic. Int J Gynaecol Obstet. 2021;152:441–3. doi: 10.1002/ijgo.13468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Kaur H, Pranesh GT, Rao KA. Emotional impact of delay in fertility treatment due to COVID-19 pandemic. J Hum Reprod Sci. 2020;13:317–22. doi: 10.4103/jhrs.JHRS_144_20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Seifer DB, Petok WD, Agrawal A, Glenn TL, Bayer AH, Witt BR, et al. Psychological experience and coping strategies of patients in the Northeast US delaying care for infertility during the COVID-19 pandemic. Reprod Biol Endocrinol. 2021;19:28. doi: 10.1186/s12958-021-00721-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Marom Haham L, Youngster M, Kuperman Shani A, Yee S, Ben-Kimhy R, Medina-Artom TR, et al. Suspension of fertility treatment during the COVID-19 pandemic: Views, emotional reactions and psychological distress among women undergoing fertility treatment. Reprod Biomed Online. 2021;42:849–58. doi: 10.1016/j.rbmo.2021.01.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Lawson AK, McQueen DB, Swanson AC, Confino R, Feinberg EC, Pavone ME. Psychological distress and postponed fertility care during the COVID-19 pandemic. J Assist Reprod Genet. 2021;38:333–41. doi: 10.1007/s10815-020-02023-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Alviggi C, Esteves SC, Orvieto R, Conforti A, La Marca A, Fischer R, et al. COVID-19 and assisted reproductive technology services: Repercussions for patients and proposal for individualized clinical management. Reprod Biol Endocrinol. 2020;18:45. doi: 10.1186/s12958-020-00605-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Ugbolue UC, Duclos M, Urzeala C, Berthon M, Kulik K, Bota A, et al. An assessment of the novel COVISTRESS Questionnaire: COVID-19 impact on physical activity, sedentary action and psychological emotion. J Clin Med. 2020;9:3352. doi: 10.3390/jcm9103352. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Akkaya-Kalayci T, Kothgassner OD, Wenzel T, Goreis A, Chen A, Ceri V, et al. The impact of the COVID-19 pandemic on mental health and psychological well-being of young people living in Austria and Turkey: A multicenter study. Int J Environ Res Public Health. 2020;17:9111. doi: 10.3390/ijerph17239111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Boivin J, Harrison C, Mathur R, Burns G, Pericleous-Smith A, Gameiro S. Patient experiences of fertility clinic closure during the COVID-19 pandemic: Appraisals, coping and emotions. Hum Reprod. 2020;35:2556–66. doi: 10.1093/humrep/deaa218. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Cirillo M, Rizzello F, Badolato L, De Angelis D, Evangelisti P, Coccia ME, et al. The effects of COVID-19 lockdown on lifestyle and emotional state in women undergoing assisted reproductive technology: Results of an Italian survey. J Gynecol Obstet Hum Reprod. 2021;50:102079. doi: 10.1016/j.jogoh.2021.102079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Tippett A. Life on pause: An analysis of UK fertility patients’ coping mechanisms after the cancellation of fertility treatment due to COVID-19. J Health Psychol. 2022;27:1583–600. doi: 10.1177/1359105321999711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Tokgoz VY, Kaya Y, Tekin AB. The level of anxiety in infertile women whose ART cycles are postponed due to the COVID-19 outbreak. J Psychosom Obstet Gynaecol. 2022;43:114–21. doi: 10.1080/0167482X.2020.1806819. [DOI] [PubMed] [Google Scholar]
- 18.Vaughan DA, Shah JS, Penzias AS, Domar AD, Toth TL. Infertility remains a top stressor despite the COVID-19 pandemic. Reprod Biomed Online. 2020;41:425–7. doi: 10.1016/j.rbmo.2020.05.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Esposito V, Rania E, Lico D, Pedri S, Fiorenza A, Strati MF, et al. Influence of COVID-19 pandemic on the psychological status of infertile couples. Eur J Obstet Gynecol Reprod Biol. 2020;253:148–53. doi: 10.1016/j.ejogrb.2020.08.025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Gordon JL, Balsom AA. The psychological impact of fertility treatment suspensions during the COVID-19 pandemic. PLoS One. 2020;15:e0239253. doi: 10.1371/journal.pone.0239253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Salama M, Isachenko V, Isachenko E, Rahimi G, Mallmann P, Westphal LM, et al. Cross border reproductive care (CBRC): A growing global phenomenon with multidimensional implications (a systematic and critical review) J Assist Reprod Genet. 2018;35:1277–88. doi: 10.1007/s10815-018-1181-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
All primary data are available for disclosure by the corresponding author upon reasonable request.
