Demographic, medical and treatment characteristics associated with couples’ decisions to donate fresh spare embryos for research

M. Choudhary1,4, E. Haimes2, M. Herbert1, M. Stojkovic3 and A.P. Murdoch1

1 Newcastle Fertility Centre at Life, Bioscience Centre, International Centre for Life, Newcastle upon Tyne, NE1 4EP, 2 PEALS, Bioscience Centre, International Centre for Life, Newcastle upon Tyne NE1 4EP and 3 Institute of Human Genetics, University of Newcastle upon Tyne, International Centre for Life, Newcastle upon Tyne NE1 4BZ, UK

4 To whom correspondence should be addressed. Email: meenakshi.choudhary{at}newcastle.ac.uk


    Abstract
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 Abstract
 Introduction
 Materials and methods
 Statistics
 Results
 Discussion
 References
 
BACKGROUND: Isolation of human embryonic stem cell lines has opened a promising and pioneering area of basic and applied medical research. The issues in relation to a couple' decision in donating their supernumerary embryos for research need to be investigated further. METHODS: We carried out a prospective study of 300 couples who underwent IVF/ICSI treatment cycles in our unit. We analysed various factors contributing to their decision to consent to donate spare embryos for stem cell or preimplantation genetic diagnosis research. RESULTS: The majority of couples (54%) consented to donate their surplus embryos for research. Couples of ethnic minority origin were less willing to consent for research compared to Caucasian couples. The number of ovarian follicles at pre-hCG scan and the number of embryos obtained were significantly higher in couples consenting for research. The funding source of treatment did not appear to influence the decision to donate. Couples with previous failed fertilization were less likely to consent to embryo research. CONCLUSIONS: Physical characteristics based on ovarian response during a treatment cycle may positively influence a couple's decision to donate embryos. Further studies are needed to identify those couples who are likely to agree to research so that counselling for research can be directed efficiently.

Key words: consent/decision/embryonic stem cells/embryo research/human


    Introduction
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 Abstract
 Introduction
 Materials and methods
 Statistics
 Results
 Discussion
 References
 
Research on human embryos raises concerns about treating embryos with respect and dignity and about women's health and rights (Cohen, 2000Go). However, the establishment of the first permanent human embryonic stem (ES) cell lines from the inner cell mass of surplus blastocyst-stage embryos has opened a promising and pioneering area of basic and applied medical research (Thomson et al., 1998Go; Reubinoff et al., 2000Go). Due to their prolonged self-renewal and pluripotent properties, human ES cells could potentially be an important source of unlimited provision of different types of tissue for transplantation therapy and also for treatment of hitherto incurable diseases (Eiges and Benvenisty, 2002Go; Gepstein, 2002Go).

However, the isolation of ES cells from pre-implantation embryos has raised controversy especially in relation to the moral status of the embryos. Global debate on the ethical issues related to embryo donation for ES cell research (Wert and Mummery, 2003Go) led to statements from prominent professional advisory bodies accepting embryo research related to the derivation of human ES cell lines [ESHRE Taskforce on Ethics and Law (ESHRE, 2001Go, 2002Go) and the American Society for Reproductive Medicine Ethics Committee (ASRM, 1997Go, 2002Go)]. Debate in the UK Parliament led to a change in the law to enable the use of spare embryos from assisted conception treatment for this research (House of Lords, 2002Go).

With the success of assisted reproductive technologies, a significant proportion of infertile couples are now able to fulfil their wishes of having a child. The recommended practice in the UK is to transfer no more than two embryos during any one cycle of IVF treatment (National Institute for Clinical Excellence, 2004Go) and hence there is a likelihood of more embryos generated than can be transferred to the uterus. Many of these are of poor quality, are unsuitable for cryopreservation and are therefore discarded. Furthermore some cyropreserved embryos are subsequently not required for treatment. Several studies have examined decision making and attitudes regarding the disposition of these supernumerary embryos (Laruelle and Englert, 1995Go; Lornage et al., 1995Go; Darlington and Matson, 1999Go; Van Voorhis et al., 1999Go; Oghoetuoma et al., 2000Go; Klock et al., 2001Go; Hoffman et al., 2003Go). Some studies have investigated the participants' attitudes toward the destiny of their supernumerary embryos (Laruelle and Englert, 1995Go) and towards the donation of frozen embryos for medical research in general (McMahon et al., 2003Go) and there has been no study considering the issues relating to a couple's decision towards donating fresh spare embryos for ES cell research.

Therefore, this study aims to investigate factors contributing to a couple's decision to donate spare embryos for ES cell research and also the availability of spare embryos for research in general.


    Materials and methods
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 Abstract
 Introduction
 Materials and methods
 Statistics
 Results
 Discussion
 References
 
A total of 300 couples who underwent routine IVF/ICSI procedures at Newcastle Fertility Centre at Life in January–February 2002 (n=60) and March–December 2003 (n=240) were recruited prospectively for this pilot study. During this period, the unit had the approval of the local ethics committee and licenses from the Human Fertilization and Embryology Authority (HFEA) for two research projects involving the isolation and characterization of ES cell lines from human embryos and the effect of blastomere removal for preimplantation genetic diagnosis (PGD) on development of these spare embryos.

Couples had routine IVF/ICSI treatment according to the clinical protocols of the unit. The routine policy was to transfer two fresh cleavage stage embryos. The options offered to the couples for their spare embryos were cryopreservation, donation to research or disposal. The advice given regarding suitability for cryopreservation was that at least four spare embryos should be available at the 4-cell stage on day 2 or 7–8-cell stage on day 3 with <10% fragmentation. If the cryopreservation criteria were not met but the couples desired to have their spare embryos frozen, then these requests for cryopreservation were also considered.

Couples attended for a scan 2 days prior to the oocyte retrieval procedure. At this time, an information leaflet and a separate consent form detailing the nature and purpose of the research study was given to couples together with the HFEA leaflet on embryo donation for research (HFEA, 2000Go). Information given for ES cell research included the potential permanent nature of the cell lines, their long-term storage and their possible injection into animals. The information leaflet on PGD research also included a section permitting the couples to opt for receiving any genetic information obtained during the course of the research that may be relevant to the management of their future treatment. Each couple received an information leaflet for only one research project. The couples undergoing oocyte retrieval on Mondays and Tuesdays were given PGD research information while ES cell research information was given to couples scheduled for oocyte retrieval on Wednesdays and Thursdays. Emphasis was laid on the fact that participation in the research would not affect the management of their treatment cycle. Further information about the study was given verbally if requested.

Couples attended for oocyte retrieval 2 days later and for embryo transfer on day 2 or 3. The signed consent forms were collected either on the day of oocyte retrieval or at embryo transfer. In order to avoid undue pressure to donate embryos, couples were asked by the admitting nurse if they had the forms to return. No direct questioning was carried out to obtain their views or attitudes toward embryo research but the admitting nurse recorded on the forms any information volunteered. The researchers were available to discuss the study further if requested.

Data were obtained on the day of oocyte retrieval from patient records. Demographic and physical characteristics were collected. The demographic information collected included age of partners and ethnic background. Other characteristics collected were cause and duration of infertility, existing children from current or previous union, type of treatment cycle (IVF or ICSI), funding for the treatment (self-funded or funded by NHS), ovarian response and number of oocytes and embryos obtained. Blastocyst development rate was recorded in those who donated to research.


    Statistics
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 Materials and methods
 Statistics
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 Discussion
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Patients were divided into two groups based on their decision to consent. Data were analysed using Statistical Package for the Social Sciences (SPSS version 10) and Microsoft Excel package for Windows XP and presented for each group as mean±SD for donor's age, duration of infertility, number of follicles at pre-hCG scan and oocyte retrieval, number of oocytes and number of embryos obtained. The effects of donor's age and the treatments used (ICSI and IVF) on blastocyst rate were evaluated using ANOVA. The effect of demographic and physical characteristics on giving consent for ES cell research was analysed by either Student's t-test, {chi}2-test or Fisher's exact test as appropriate. P<0.05 was considered statistically significant.


    Results
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 Abstract
 Introduction
 Materials and methods
 Statistics
 Results
 Discussion
 References
 
Of 300 couples undergoing treatment during this period, 287 couples were given the research Information Leaflets and Consent Forms. Forms were not given to 13 couples for the following reasons: language problem requiring interpreter (n=1), low (three only) follicle numbers (n=6), felt to be inappropriate clinically (n=3) and clinical omission to give out forms (n=3). Of the 287 couples, 171 couples were given an ES cell research information leaflet and consent form while 116 couples received a PGD information leaflet and consent form. Of the 287 couples given forms, 156 (54.3%) consented for research while 131 (46%) did not give consent. Of the 171 couples given ES cell research information, 57% consented for research while 51% of 116 couples consented for PGD research. Although separate analysis was carried out for PGD and ES cell research groups, the data are presented collectively for convenience since no significant difference was observed between these two groups. Most (94%) of the couples who consented for embryo research did so on the day of oocyte retrieval procedure, indicating a decision made regardless of the fertilization outcome. The remaining couples (6%) made the decision on the day of embryo transfer.

Of the 156 couples consenting to research, 21 couples (14%) had no spare embryos. A summary of the outcome of embryos is given in Table I. Of the 30 couples (10% of total couples) who had embryos frozen, 19 (63%) had consented to research on oocyte retrieval day while 11 (37%) did not consent. After cryopreservation, if the couples who had consented for research still had any suboptimal spare embryos left, then they were used for research.


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Table I. Outcome of preimplantation embryos obtained during treatment cycle

 
The average age of women undergoing treatment was 32.8±4.1 (range 20–43) years, and for men was 36.6±5.3 (range 26–58) years. There was no difference in the age distribution of the couples consenting for research and those not consenting; 270 (94%) couples were Caucasian and 17 (6%) were of ethnic minority origin. Of the 270 Caucasian couples who were given forms, 151 (56%) consented whereas only five couples consented out of 17 in the ethnic minority group who were given forms. This difference was found to be statistically significant (P<0.05).

Of all couples, 103 couples (36%) had a male factor problem leading to infertility, 75 (26%) had a tubal problem, six (2%) ovulatory dysfunction, 11 (4%) combined male and female infertility and 92 (32%) had an unexplained cause for their infertility. The average duration of infertility was 4.2±2.3 years (range 1–14). No association was identified between the duration of infertility and the giving of consent for research. Of 30 couples that had existing children from the current union, 14 had had spontaneous conceptions and 16 couples had previous successful IVF treatment. Of these, 50% consented for research with no difference observed based on the nature of previous conceptions (spontaneous or IVF). Forty-four couples had children from previous unions as shown in Table II. Sixty per cent of couples (n=12) where male partner had children from previous union and had a previous vasectomy did not consent for research (not statistically significant). When both partners or only the female partner had children from previous unions (total n=12), 75% of them consented for research. Table III shows the various demographic and physical characteristics and its effect on giving consent for embryo research. Couples with higher numbers of follicles at pre-hCG scan were more likely to donate their embryos (P<0.05). Five couples with previous failed fertilization were given research forms and interestingly none of them consented for research. There was no evidence to suggest that the funding source of treatment influenced the decision about donation.


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Table II. Couples with children from previous union

 

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Table III. Effect of demographic and physical factors on consenting for embryo research

 
None of the couples who gave consent for research asked any further questions relating to ES cell research. The reasons for not consenting for research volunteered by six couples were: only one partner willing (n=2); do not like the idea of injecting into animals for stem cell research (n=1); very strong religious beliefs (n=2); no limit or control over storage and duration of use of stem cells (n=1).

Of 671 donated embryos, 464 embryos were donated to ES cell research and 207 embryos were donated to PGD research. Of a total of 464 donated to ES cell research, 230 embryos were assessed for blastocyst development rate; 91 (40%) developed to morulae and blastocysts on day 5 (Figure 1). Of these, 78 (34%) progressed to expanded or hatched blastocysts on day 6 (Figure 1) and were used for ES cell derivation. Blastocyst development rate was adversely influenced by the treatment type but not by female age. ICSI embryos had a lower blastocyst formation rate than IVF embryos (P=0.05).



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Figure 1. Total in vitro developmental rates of donated embryos on day 5 (morulae and blastocysts) and day 6 (blastocysts, expanded and hatched blastocysts). Day 6 embryos were used for further in vitro culture and derivation of embryonic stem cells.

 
The one oocyte donor in this study who was given research information consented for research, but her recipient declined to give consent and was included in the non-consent group.


    Discussion
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 Abstract
 Introduction
 Materials and methods
 Statistics
 Results
 Discussion
 References
 
This study gives an insight into the possible contributing factors in a couple's decision to donate their supernumerary embryos for embryo research. It shows that the number of follicles and embryos and previous failed fertilization has a significant influence on a couple's decision to donate the spare embryos for research. Ethnic origin may also influence a couple's decision to consent for embryo research.

Several studies have examined the possibility of donating cryopreserved embryos for research (Van Voorhis et al., 1999Go; Oghoetuoma et al., 2000Go; Klock et al., 2001Go), but, to our knowledge, very limited research has been done on donation of fresh spare embryos for research (Bjuresten and Hovatta, 2003Go). In our study, 54% of couples consented for research, which was higher than (10–21%) in most of the other reported studies (Van Voorhis et al., 1999Go; Oghoetuoma et al., 2000Go; Klock et al., 2001Go). In a recent study carried out in Sweden, 92% of couples preferred donating their supernumerary embryos for stem cell research. This may be related to awareness of the importance of human ES cells and the altruistic nature of Swedish couples (Bjuresten and Hovatta, 2003Go).

It has been mentioned in a previous study that the aims of medical research are often not explained adequately to the public, and medical experiments have always been fertile ground for mythology, both of which might contribute to lower participation in research (Laruelle and Englert, 1995Go). In an attempt to overcome these problems, our research information leaflet detailed the type of research as well as possible future implications of the isolated cell lines. According to the HFEA Act of 1990, Section 3 (1), all human embryo research in the UK must be licensed by the HFEA. We gave all couples a copy of the HFEA information sheet about research to ensure that they were fully aware of the legal status of the research. Giving the research information 2 days prior to oocyte retrieval allowed time to ensure that both partners had thoroughly considered the proposed research study and its implications before consenting for research. Willingness to consent for research was not influenced by the type of research project, as shown by the percentage of couples consenting for ES cell and PGD research projects.

Commitment to the practice of religion has been shown to influence the decision on donating embryos for research (McMahon et al., 2003Go). As we did not ask the couples about their religious affiliation and retrieved the demographic and social data through the notes only, it is not possible to comment on the influence of commitment to religion and the decision to donate embryos for research. Although some studies comment on religious commitment and embryo research, there are no studies specifically on the influence of ethnic origin on couples' decision to donate surplus embryos for research. In our study, 94% of couples were Caucasian, 6% of ethnic minority origin. These demographic data are consistent with the general profile of our IVF unit. It was noted that among the 17 couples belonging to an ethnic minority background, five couples who did consent for research were second generation (born and raised in England). This finding may suggest a more receptive attitude towards embryo research, but needs to be treated cautiously due to low numbers. This warrants a need to further explore the issue relating to ethnic origin and its influence on couples' decision making for embryo donation to research.

Earlier research has indicated that the existence of a child conceived through IVF influences a couple's perception of embryos (McMahon et al., 2000Go). Also, couples who consider the embryo to be a child are less likely to authorize experimentation (Laruelle and Englert, 1995Go). In our study, couples with existing children conceived by IVF from the current union had no specific predilection towards donating or not donating spare embryos for research. It was interesting to note that if both partners or only the female partner had children from previous unions, they were more open to donating their surplus embryos for research (75%) as compared to 40% of couples consenting if a male partner had existing children from previous unions and female partner had none, especially if the cause of the infertility was due to previous vasectomy and/or failed reversal. Direct interviews with couples would throw more light in identifying the issues relating to this and also whether women felt more strongly regarding embryo research than men.

The number of previous unsuccessful attempts at IVF/ICSI did not influence a couple's decision to consent for research but previous failed fertilization dissuaded them from consenting. The number of follicles and oocytes and its influence on consenting for ES cell research has not been studied earlier. We noted that the higher the number of follicles, the greater the likelihood of couples donating the spare embryos for research, which may be a good predictor of intention to donate for research. This may be explained by the possibility of these couples regarding a good ovarian response as a successful cycle and their being more assured of obtaining embryos for their own treatment. Although the majority of couples consented on the oocyte retrieval day prior to the procedure when they were not aware of the number of oocytes that would be retrieved, the decision to donate embryos for research was based on the information obtained at pre-hCG scan regarding the number of growing follicles. The higher the number of follicles at pre-hCG scan, the more likely it was for couples to consent for research. Six per cent of all couples consented for research after the embryo transfer when they were more positive toward the success of their treatment cycles and had suboptimal spare embryos not suitable for their treatment. The number of embryos obtained was statistically higher in the group consenting for research. These two parameters may suggest that when a couple is more optimistic about their successful ovarian response and possible treatment outcome, they are more willing to donate their surplus embryos for research.

Previous studies have suggested that a high percentage of couples are choosing to freeze embryos (Laruelle and Englert, 1995Go). Current rates of embryo freezing in the UK are unknown although extrapolation from HFEA data (HFEA Annual Report, 2002Go) suggests that the ratio of cycles started to frozen embryo transfers is ~5:1, indicating that only a minority of couples have frozen–thawed embryos transferred. In our unit, NHS funding for freezing of spare embryos is not available to most couples, which may have influenced their decision. The number of couples opting for cryopreservation (10% of couples) in this study was lower than our current rate (12%). Since the research was ongoing during the year, we do not feel that the study influenced the freezing decision.

A recent survey of nearly 400 000 cryopreserved embryos in all assisted reproduction practices in USA, and their availability for research, noted that only 2.8% of these embryos were available for research (Hoffman et al., 2003Go). A similar study carried out in Canada also revealed that only 2% of cryopreserved embryos are donated to research, of a total of 15 615 embryos in store (Baylis et al., 2003Go). Comparative data of availability of all cryopreserved embryos for research in the UK is not available, although a study carried out in the UK reported 21% of couples donating their cryopreserved embryos of >5 years duration to research (Oghoetuoma et al., 2000Go). During our study period, some couples offered their unwanted cryopreserved embryos for research; although this will be a future resource, details of these patients are not included in this study.

For isolation of an ES cell line from the inner cell mass, it is essential that these suboptimal surplus embryos develop to blastocyst stage. The recent survey of all cryopreserved embryos in the USA mentions that cryopreserved embryos are less likely to produce viable blastocysts than non-frozen embryos (Hoffman et al., 2003Go). Of the total 671 spare embryos donated to research, 464 (69%) were donated and used for isolation of ES cell lines. Of these 464 embryos, 230 embryos were further assessed up to blastocyst stage; 34% developed to the blastocyst stage and were then used for isolation of inner cell mass to derive cell lines. It has been noted (Bjuresten and Hovatta, 2003Go) that the donated embryos are of sub-optimal quality and only a small percentage (10%) develops to the blastocyst stage in culture. Of the 78 blastocysts obtained on day 6, 50 (64%) were expanded and seven (9%) were hatched. We studied different culture conditions prior to establishing the optimal culture conditions, which resulted in 34% blastocyst rate of the embryos donated to research. In our study, IVF treatment resulted in a higher blastocyst rate compared to ICSI treatment, which reflects the effect on the embryo quality due to an invasive procedure such as ICSI (Griffiths et al., 2000Go). These data may help us to predict those couples who would be more suitable to be approached for ES cell research.

In conclusion, increasing general awareness among the public about human embryo research and ES cell lines, similar to the extensive media coverage in Sweden, may improve the availability of embryos for ES cell research. Physical characteristics based on ovarian response during a treatment cycle may positively influence a couple's decision to donate embryos and it may be more worthwhile to concentrate on IVF embryos for stem cell isolation rather than ICSI embryos. With ongoing debates on stem cell research and the launch of the UK Stem Cell Bank, it has become more crucial to identify suitable participants for donating embryos, which will represent a potential source of the ES cells for advancing medical knowledge and also for therapeutic use.


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 Abstract
 Introduction
 Materials and methods
 Statistics
 Results
 Discussion
 References
 
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Submitted on July 31, 2003; resubmitted on May 17, 2004; accepted on June 9, 2004.





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