Hum. Reprod. Advance Access originally published online on November 28, 2006
Human Reproduction 2007 22(2):323-336; doi:10.1093/humrep/del402
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ESHRE PGD Consortium data collection VI: cycles from January to December 2003 with pregnancy follow-up to October 2004
1 Centre for Medical Genetics 2 Centre for Reproductive Medicine, University Hospital and Medical School of the Dutch-speaking Brussels Free University (Vrije Universiteit Brussel, VUB), Brussels, Belgium 3 Genetics and IVF Institute, Fairfax, VA, USA 4 Service de la Biologie de la Reproduction, SIHCUS-CMCO, Schiltigheim, France 5 Center for Reproductive Medicine, Academic Medical Center, Fertility Laboratory, Amsterdam, The Netherlands 6 Department of Cytogenetics and Center for Preimplantation Genetic Diagnosis, Guy’s and St. Thomas’ NHS Foundation Trust, Guy’s Hospital 7 UCL Centre for PGD, Department of Obstetrics and Gynecology, University College London, London, UK 8 Laboratory of Medical Genetics, University of Athens, St. Sophia’s Children’s Hospital, Athens, Greece 9 Sanatorium Repromeda, Brno, Czech Republic and 10 Melbourne IVF, East Melbourne VIC, Australia
11 To whom correspondence should be addressed at: Centre for Medical Genetics, University Hospital and Medical School of the Dutch-speaking Brussels Free University (Vrije Universiteit Brussel, VUB), Laarbeeklaan 101, 1090 Brussels, Belgium. E-mail: karen.sermon{at}az.vub.ac.be
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Abstract |
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The sixth report of the ESHRE PGD Consortium is presented, relating to cycles collected for the calendar year 2003 and follow-up of the pregnancies and babies born up to October 2004. Since the beginning of the data collections, there has been a steady rise in the number of cycles, pregnancies and babies reported. For this report, 50 centres participated, reporting on 2984 cycles, 501 pregnancies and 373 babies born. Five hundred and twenty-nine cycles were reported for chromosomal abnormalities, 516 cycles were reported for monogenic diseases, 137 cycles were reported for sexing for X-linked diseases, 1722 cycles were reported for preimplantation genetic screening (PGS) and 80 cycles were reported for social sexing. Data VI is compared to the cumulative data for data collections I–V.
Key words: PGD/preimplantation genetic screening/fluorescence in-situ hybridization/PCR/ESHRE PGD Consortium
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary materialsReferences |
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Since 1999, the ESHRE PGD Consortium has reported on a regular basis on the current practice of PGD, as reported by their members (ESHRE PGD Consortium Steering Committee, 1999
, 2000, 2002; Sermon et al., 2005; Harper et al., 2006). The data analysed previously included referral and clinical data on the patients consulting for PGD, the cycles they underwent, the pregnancies that ensued from these cycles and the babies born. Because the analysis of the referral and clinical data was biased by several factors, e.g. the underreporting of couples who did not come through for PGD, this analysis is left out for the current report.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary materialsReferences |
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Data were collected using a FileMaker Pro 5 database consisting of files for cycle records, frozen cycle records, pregnancies and babies. A first general round of correction was carried out, requesting corrections from participating centres, followed by a more in-depth correction by expert co-authors. Cycles with insufficient data, e.g. with no cycle or patient identification or no clear indication, cycles from the wrong time period, or reported after the closure of the collection period, were eliminated from the calculations.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary materialsReferences |
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The membership has increased steadily, and while in the first report data on sixteen centres were included (ESHRE PGD Consortium Committee, 1999), that figure has now increased to 50. This has also led to a steady increase in the number of cycles reported, from 392 in the first report to 3929 in the current report.
The results are represented in tables according to a now set layout. Accompanying text is limited to the minimum, and seven tables are only available in an electronic version: Supplementary Table IIc with the list of abnormal karyotypes, Supplementary Table IIIc with the list of X-linked diseases for which sexing was carried out, Supplementary Table IVc with the list of monogenic diseases for which PGD was carried out, Supplementary Tables VIIIa (data I–V) and VIIIb (data VI) with the complications of pregnancy and Supplementary Tables XIIa (data I–V) and XIIb (data VI) with the congenital malformations and the neonatal complications.
An overview of all cycles collected previously in data collections I–V can be found in Table Ia, whereas an overview of the current data collection can be found in Table Ib.
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PGD cycles for chromosomal abnormalities
Tables IIa and IIb summarize the 1207 and 529 cycles collected for data collection I–V and VI, respectively. Overall, there was very little difference between the two data collections. Reciprocal translocation was the most frequent class of chromosome aberration; ICSI was the predominant mode of fertilization; acid Tyrodes with cleavage aspiration was the predominant sampling method. A global average of 14.3 and 14.0 cumulus oocyte complexes (COCs) per oocyte retrieval (OR) cycle was collected for the I–V and VI data collections, respectively; the fertilization rate (74 and 70%), the proportion of successfully biopsied embryos which gave a diagnosis (91 and 92%), the proportion of successfully biopsied embryos with a transferable result (25 and 25%) and the clinical pregnancy rate per OR (15 and 14%) were similar.
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The relatively low pregnancy rates are likely to reflect that the low proportion of embryos with a transferable result limits the choice of embryo for transfer (24% of embryos biopsied for all classes of chromosome aberration and only 17% of embryos for reciprocal translocation cycles in particular for the data collection VI).
PGD cycles for sexing for X-linked diseases
Table IIIa summarizes data I-V and Table IIIb summarizes the data from collection VI for sexing only for X-linked disease using the PCR or fluorescent in-situ hybridization (FISH). A total number of 137 cycles were collected in this group, with 134 cycles using FISH and three cycles using PCR.
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The biopsy was successful in 98% of embryos biopsied and 92% of the embryos successfully biopsied were diagnosed. A transfer was achieved in 76% of the cycles with an average of 1.7 embryos transferred in each cycle. The overall clinical pregnancy rate was 22% per OR and 30% per embryo transfer (ET) procedure, with an implantation rate of 21%.
Supplementary Table IIIc summarizes the list of 36 indications. The most common indication was Duchenne muscular dystrophy (n = 33; 25%), haemophilia (n = 25; 19%), retinitis pigmentosa (n = 6), adrenoleukodystophy (n = 6), Alport syndrome (n = 5) and non-fragile X, X-linked mental retardation (n = 5).
Overall, these data are quite unremarkable and very comparable to previous data collections (I–V). In contrast to other indication groups, the number of cycles for sexing for X-linked diseases remains stable.
PGD for monogenic diseases
Amongst PGD cycles initiated for single-gene disorders between January and December 2003, the most common autosomal recessive diseases were cystic fibrosis, 
-thalassemia (with or without HLA typing), spinal muscular atrophy and sickle cell anaemia. The most common autosomal dominant diseases were Huntington disease, myotonic dystrophy, adenomatous polyposis coli and Marfans syndrom. The most common specific diagnosis of X-linked diseases was for Duchenne and Becker muscular dystrophy, fragile X and haemophilia. PGD cycles for an additional 47 monogenic diseases were initiated in 104 cycles, included under ‘other’ in Table IVb, listed in Supplementary Table IVc.
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An average of 13.8 oocytes were collected per OR, biopsy was successful in 98% of embryos, diagnosis was achieved in 86% of embryos successfully biopsied, and 75% of cycles to OR had an ET, with 667 embryos transferred. Overall, 20% of cycles that reached the stage of OR resulted in a clinical pregnancy (or 27% clinical pregnancy rate per ET).
As recommended (Thornhill et al., 2005), 434 cycles had ICSI and 11 cycles had ICSI and frozen (two of which were just frozen embryos). Two cycles were noted as IVF and frozen and 3 cycles as IVF and ICSI. Laser drilling was used for zona breaching in 64% of biopsy cycles, with cleavage aspiration accounting for 85% of biopsy procedures. In addition 17 cycles (4%) used trophectoderm biopsy in blastocysts; representing the first time, blastocyst biopsy has been reported to ESHRE for clinical PGD cycles.
Overall, the number of PGD cycles performed for monogenic disorders between January and December 2003 represents the largest number performed in a single year so far. The assisted reproduction techniques (ART) and embryology procedures applied reflect accumulated experience and expertise, along with technological developments, e.g. laser drilling and blastocyst biopsy.
With respect to the progress and outcome of cycles, including the embryology, rates of diagnosis and clinical outcome such as clinical pregnancy and embryo implantation rates, there are no apparent changes compared to previous data collections (Table IVa and Supplementary Table IVc).
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Preimplantation genetic screening
The cumulative data for preimplantation genetic screening (PGS) from collections I–V are summarized in Table Va. Table Vb summarizes the data from collection VI. It is clear that the number of PGS cycles continues to rise. In last year’s data collection (data V), 1211 PGS cycles were performed (Harper et al., 2006
), whereas this year 1722 cycles were reported, which represents a 42% increase. The largest increase was seen in cycles for repeated implantation failures (RIF) (275–462; 68% increase) and in cycles for severe male factor (101–188; 86% increase).
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As for the previous data collections, there was an underreporting of cycles that were cancelled before OR. Only 9 of 1722 cycles were reported to be cancelled, whereas in general cancellation rates are in the range of 5–10%. As a result, the outcome of PGS can only be presented as clinical pregnancy rate per OR or per ET but not per cycle started. This may partly be explained by the fact that many reporting centres only receive the blastomeres for analysis, while the IVF cycle is done elsewhere, making accurate reporting of cycles more difficult and as a result incomplete.
For data collection VI, 9496 embryos were biopsied, and a result was obtained for 8795 embryos (93% of biopsied embryos). Of 3193 embryos diagnosed as transferable (34% of all biopsied embryos), 2277 were transferred and 454 were frozen. In total, 384 embryos implanted (17% implantation rate).
The overall clinical pregnancy rate was 18% per OR and 24% per ET. These results are similar to the results from collection V (16 and 23% clinical pregnancy rate per OR and ET, respectively). The clinical pregnancy rate per OR ranged from 9% for advanced maternal age (AMA) + recurrent miscarriage to 31% for ‘other indications’. These differences in results between various indications reflect at least in part differences in patient and cycle specific data. For instance, in women treated with PGS for AMA (12% clinical pregnancy rate per OR), the mean age was 41 years and the average number of oocytes obtained per OR was 9.8. For couples treated with PGS for severe male factor (28% clinical pregnancy rate per OR), the mean age was only 33 years and the average number of oocytes obtained was 14.6.
PGD cycles for social sexing
Table VIb summarizes the data from collection VI for social sexing cases using FISH and PCR. Social sexing for male embryos made up 76% of the cycles (n = 61) while sexing for females made up 24% (n = 19). A total of 80 cycles were collected in this group, with 79 cycles going to OR and an average of 15.4 oocytes per retrieval. The embryos in this group were mainly diagnosed using FISH (91%). The biopsy was successful in 96% of embryos biopsied and 93% of the embryos biopsied were diagnosed. A transfer was achieved in 60% of the cycles which went through PGD, with an average of 2.0 embryos transferred in each cycle. The overall clinical pregnancy rate was 19% per OR and 32% per ET, with an implantation rate [fetal heart beat (FHB)/embryos transferred] of 23%. These data are very comparable to the I–V set (Table VIa).
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Pregnancies and babies
The cumulative data for collection I–V is summarized in Tables VIIa
http://humrep.oxfordjournals.org/cgi/data/del402/DC1/4http://humrep.oxfordjournals.org/cgi/data/del402/DC1/5–XIIa. It is becoming apparent that PGD babies are very comparable to ICSI babies in every respect, e.g. complications of pregnancy, characteristics at birth and major and minor malformations.
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Of the 666 cycles ending in a positive hCG, no pregnancy was reported in 186 cases: for 89 pregnancies, no information was given by the centres. For 89 further cycles with a positive hCG, no pregnancy was reported because there was no positive heartbeat (these are not the same as the 46 subclinical pregnancies that were reported, Table VIIb). A further eight cycles ending in a positive hCG were lost to follow-up. No cycle was reported for 21 pregnancies. This results in the reporting of 501 pregnancies. Five hundred and one pregnancies ended in 373 reported deliveries, leading to the birth of 453 babies (295 singletons, 152 twins and 6 triplets). Two pregnancies were terminated because of an encephalocele and spina bifida diagnosed on ultrasound. Sixty-nine of 403 ongoing pregnancies (17%) presented with complications, mainly bleeding and emesis. One hundred and five of 373 pregnancies were delivered prematurely (28%), 48 singleton pregnancies (16%), 55 twin pregnancies (72%) and 2 triplet pregnancies (100%). As before, all parameters e.g. weight, length and head circumference were comparable to those of ICSI babies (Bonduelle et al., 2002
) and previous PGD Consortium reports (Harper et al., 2006). Seventeen babies were born with malformations (4%), eleven of which were major malformations.
Two hundred and fifty-seven of the 564 fetal sacs were tested prenatally (46%), whereas 203 of 564 fetal sacs were tested post-natally (36%). These figures cannot be added, as some fetal sacs were tested both prenatally and post-natally. Abnormalities were found in 13 instances: four prenatally, two of which ended in a termination of pregnancy (TOP) and nine post-natally. Eight abnormalities were found in miscarriage material, whereas one abnormal karyotype was found at birth.
Of the misdiagnosis: a trisomy 13 was found in miscarriage material after PGD for 45,XY,der(13;14)(q10;q10). Although difficult to trace, the centre where this misdiagnosis occurred seem to attribute it to a human error without discarding a FISH error or embryonic mosaicism, because the diagnosis was established on one cell. The trisomy 16 found in miscarriage material after PGS for AMA and RIF occurred after first polar body biopsy only, in which clearly two signals for chromosome 16 had been found. The second trisomy 16 found in miscarriage material occurred after PGS at the cleavage stage. Re-probing of the fixed blastomere clearly showed two signals for chromosome 16. Although a FISH error seems unlikely, the cause of this error (mosaicism of the embryo, human error) cannot be traced anymore.
Seventeen misdiagnoses have been reported in six reports, ten for PCR and seven for FISH. Except for one misdiagnosis for a reciprocal translocation where an inappropriate probe scheme was used (Sermon et al., 2005; Mackie Ogilvie and Scriven, 2004; Kyu Lim et al., 2004), the reason for the misdiagnoses is difficult to establish.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary materialsReferences |
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This sixth report of the ESHRE PGD Consortium reports on an ever-increasing number of cycles, pregnancies and babies, from a still increasing number of participating centres. For this report, the referrals are not included, because it was felt from previous reports that the data were biased and incomplete. Indeed, only few centres reported all referrals, i.e. referrals for patients who did not come through for PGD because either it was technically impossible to help them, or for ethical reasons, or reasons related to IVF e.g. AMA.
An interesting feature is the relative increase in the number of PGS cycles. This reflects the fact that many IVF laboratories offer PGS, and PGS only, as an additional method to select the best embryo for transfer. The ESHRE PGD Consortium Steering Committee would like to emphasize that they feel that there is a need for large randomized controlled trials to investigate the (cost-)effectiveness of PGS for well-defined indications. Currently, there are insufficient data that demonstrate that PGS is indeed a cost-effective alternative for standard IVF (Staessen et al., 2004; Twisk et al., 2006).
PGD for monogenic diseases and chromosomal abnormalities have also been steadily increasing, whereas sexing (both for X-linked diseases and for social sexing) remains stable. For the sexing for X-linked diseases, this reflects the fact that more and more specific PGD at the DNA level is offered. For social sexing, only two centres offer it, and this has remained the same for the last three reports. To be able to offer PGD for monogenic diseases or chromosomal abnormalities, a close collaboration between an IVF centre and a genetic laboratory is mandatory. The higher technical expertise needed for this type of diagnosis explains why less centres are able to offer it.
It becomes obvious that at birth PGD babies have characteristics that are comparable to those of ICSI babies. No pregnancy complication or malformation at birth is particularly occurring in the PGD population. The characteristics of the babies at birth are also comparable, and the main complication remains multiple pregnancies leading to morbidity and mortality in PGD offspring.
The ESHRE PGD Consortium has been active during the past year: the PGD Consortium guidelines for PGD and PGS were published in 2005 (Thornhill et al., 2005), and recently, a joint report of the European Society for Human Genetics (ESHG) and ESHRE was published (Soini et al., 2006). This report discusses the interface between genetics and assisted reproductive technology regarding technical, sociological, ethical and legal issues and deals not only with PGD but also with other topics such as screening of gamete donors and reproductive tourism.
The ESHRE PGD Consortium also aims at constantly improving the data collection and its processing. A major reorganization of the database is planned, and better follow-up of data submission is now reassured by a permanent staff member at ESHRE. Quality assessment of captured FISH images is planned, as well as retrospective analysis of the children born after PGD, as a preliminary study for the long-term child follow-up. With these measures, ESHRE hopes to help IVF and genetic centres to bring PGD up to today’s standards of good laboratory and clinical practice.
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Supplementary materials |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary materialsReferences |
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Supplementary data are available at http://humrep.oxfordjournals.org/.
Table IIc. Chromosomal abnormalities analysed, data VI.
Table IIIc. List of indications for which sexing has been performed, data collection VI.
Table IVc. List of indications under ‘others’ for monogenic diseases with PCR, data VI.
Table VIIIa. Complications in clinical pregnancies, data I–V.
Table VIIIb. Complications in clinical pregnancies, data VI.
Table XIIa. Congenital malformations and neonatal complications at birth, data collection I–V.
TableXIIb. Congenital malformations and neonatal complications at birth, data collection VI.
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References |
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Bonduelle M, Liebaers I, Deketelaere V, Derde M-P, Camus M, Devroey P, Van Steirteghem A. (2002) Neonatal data on a cohort of 2889 infants born after ICSI (1991–1999) and of 1995 infants born after IVF (1983–1999). Hum Reprod 17:671–694.
ESHRE PGD Consortium Steering Committee. (1999) ESHRE preimplantation genetic diagnosis (PGD) consortium: preliminary assessment of data from January 1997 to September 1998. Hum Reprod 14:3138–3148.
ESHRE PGD Consortium Steering Committee. (2000) ESHRE preimplantation genetic diagnosis (PGD) consortium: data collection II (May 2000). Hum Reprod 15:2673–2683.
ESHRE PGD Consortium Steering Committee. (2002) ESHRE preimplantation genetic diagnosis consortium: data collection III (May 2001). Hum Reprod 17:233–246.
Harper JC, Boelaert K, Geraedts J, Harton G, Kearns WG, Moutou C, Muntjewerff N, Repping S, SenGupta S, Scriven PN, et al. (2006) ESHRE PGD Consortium data collection V: cycles from January to December 2002 with pregnancy follow-up to October 2003. Hum Reprod 21:3–21.
Kyu Lim C, Hyun Jun J, Mi Min D, Lee HS, Young Kom J, Koong MK, Kang IS. (2004) Efficacy and clinical outcome of preimplantation genetic diagnosis using FISH for couples of reciprocal and Robertsonian translocations; the Korean experience. Prenat Diagn 24:556–561.[CrossRef][Web of Science][Medline]
Mackie Ogilvie C and Scriven PN. (2004) Preimplantation genetic diagnosis (PGD) for reciprocal translocations. Prenat Diagn 24:553–555.[CrossRef][Web of Science][Medline]
Sermon K, Moutou C, Harper J, Geraedts J, Scriven P, Wilton L, Magli MC, Michiels A, Viville S, De Die C. (2005) ESHRE PGD consortium data collection IV: May–December 2001. Hum Reprod 20:19–34.
Soini S, Ibarreta D, Anastasiadou V, Ayme S, Braga S, Cornel M, Coviello DA, Evers-Kiebooms G, Geraedts J, Gianaroli L, et al. (2006) The interface between assisted reproductive technologies and genetics: technical, social, ethical and legal issues. Eur J Hum Genet 14:588–645.[CrossRef][Web of Science][Medline]
Staessen C, Platteau P, Van Assche E, Michiels A, Tournaye H, Camus M, Devroey P, Liebaers I, Van Steirteghem A. (2004) Comparison of blastocyst transfer with or without preimplantation genetic diagnosis for aneuploidy screening in couples with advanced maternal age: a prospective randomized controlled trial. Hum Reprod 19:2849–2858.
Thornhill AR, deDie-Smulders CE, Geraedts JP, Harper JC, Harton GL, Lavery SA, Moutou C, Robinson MD, Schmutzler AG, Scriven PN, et al. (2005) ESHRE PGD consortium ‘Best practice guidelines for clinical preimplantation genetic diagnosis (PGD) and preimplantation genetic screening (PGS)’. Hum Reprod 20:35–48.
Twisk M, Mastenbroek S, van Wely M, Heineman MJ, Van der Veen F, Repping S. (2006) Preimplantation genetic screening for abnormal number of chromosomes (aneuploidies) in in vitro fertilisation or intracytoplasmic sperm injection. Cochrane Database Syst Rev 25:CD005291.
Submitted on August 21, 2006; accepted on August 31, 2006.
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J. A. Collins Preimplantation Genetic Screening in Older Mothers N. Engl. J. Med., July 5, 2007; 357(1): 61 - 63. [Full Text] [PDF]
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