Review Preimplantation testing for chromosome aneuploidy
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1 Review 2008;10: /toag The Obstetrician & Gynaecologist Review Preimplantation testing for chromosome aneuploidy Author Caroline Mackie Ogilvie Key content: Around 50% of cleavage stage human embryos obtained by in vitro fertilisation (IVF) have an abnormal number of chromosomes. Aneuploidy testing has been introduced at some IVF centres with the aim of identifying and removing abnormal embryos and increasing pregnancy success rates. Randomised controlled trials have indicated that pregnancy and live birth rates are lower for women undergoing aneuploidy testing. Learning objectives: To understand the nature and frequency of chromosome abnormalities in cleavage stage human embryos. To understand the rationale underlying aneuploidy testing. To understand the results of research on aneuploidy testing. Ethical issues: Should aneuploidy testing be offered, when randomised trials indicate either that it has no effect or that it results in fewer ongoing pregnancies and live births? Keywords aneuploidy testing / comparative genomic hybridisation / fluorescence in situ hybridisation / in vitro fertilisation / preimplantation genetic diagnosis Please cite this article as: Ogilvie CM. Preimplantation testing for chromosome aneuploidy. The Obstetrician & Gynaecologist 2008;10: Author details Caroline Mackie Ogilvie DPhil Consultant Clinical Scientist Guy s and St Thomas Centre for Preimplantation Genetic Diagnosis and Cytogenetics Department, 5th floor, Tower Wing, Guy s and St Thomas NHS Foundation Trust, St Thomas Street, London SE1 9RT, UK caroline.ogilvie@genetics.kcl.ac.uk (corresponding author) 88
2 The Obstetrician & Gynaecologist 2008;10:88 92 Review Introduction In vitro fertilisation (IVF) centres are constantly seeking to improve their pregnancy success rates to minimise the emotional trauma and invasive burden of repeated cycles. The European Society of Human Reproduction & Embryologye (ESHRE) 1 quotes success rates of around 30% per embryo transfer on average, although these rates vary considerably between centres and with maternal age. Efforts to achieve high pregnancy rates have, in some countries, resulted in the replacement of several embryos in each cycle. This, in turn, has given rise to a dramatic increase in multiple pregnancies, with the associated risks for mothers and fetuses. The UK s regulatory body, the Human Fertilisation and Embryology Authority (HFEA) 2 strongly discourages the transfer of more than two embryos for women under 40 years of age and more than three for those over 40. Nevertheless, the rate of twin pregnancies remains high and the holy grail for most professionals involved in IVF is the transfer of a single embryo per cycle with an associated high chance of a healthy singleton pregnancy and live birth. Improvements in culture media; assessment of embryo morphology; and culture and transfer at the blastocyst stage 3 have gone some way to increasing success rates but there is still considerable room for improvement. Preimplantation genetic diagnosis Assessment of the genetic status of a preimplantation embryo by biopsy and testing of a single cell is now an accepted option for carriers of genetic anomalies, such as single gene defects and chromosome rearrangements. 4 This technology, known as preimplantation genetic diagnosis (PGD), was developed in the early 1990s 5 and is practised at a number of centres worldwide. The aim of PGD is to reduce substantially the risk of an abnormal pregnancy, which can be 25% for autosomal recessive disorders such as cystic fibrosis and spinal muscular atrophy, or 50% for some chromosome rearrangements and autosomal dominant single gene defects such as Huntington disease. The residual risk of abnormality following testing depends on the specific test used and varies from case to case. Mutations in single genes can be detected by a range of techniques, including direct amplification using the polymerase chain reaction and minisequencing. Alternatively, the mutated chromosome can be tracked using a haplotyping approach, with or without prior amplification of the whole genome. 6 Chromosome imbalance in embryos, resulting from parental chromosome rearrangement, is detected by the application of fluorescently-labelled DNA probes to the nucleus of the biopsied cell, previously fixed on a microscope slide. The copy number of the chromosome segments involved in the rearrangement can be assessed by counting the fluorescent signals in the nucleus, using fluorescence microscopy. 7 This technique is known as fluorescence in situ hybridisation (FISH). The development of FISH technology allowed the investigation of the chromosomal status of preimplantation embryos, which was initially undertaken to follow up embryos unsuitable for replacement or donated for research after PGD cycles. These studies indicated that a high proportion of such embryos had an abnormal number of chromosomes, a condition known as aneuploidy, showing either uniform abnormality, mosaicism (the presence of two or more populations of cells, each with a different chromosome constitution), or chaos (each cell in the embryo showing a different abnormality) It is against this background that the concept of aneuploidy testing (also called aneuploidy screening [AS], PGD-AS, preimplantation genetic screening [PGS] or preimplantation genetic testing [PGT]) to improve IVF success rates has emerged. It is important to understand that PGD for couples at high prior risk of affected pregnancies because of a familial mutation or chromosome rearrangement is effectively a genetic test carried out to avoid genetic disease. In contrast, aneuploidy testing is rooted in the world of assisted conception, with the aim of improving the chances of pregnancy and live birth for couples undergoing IVF. Rationale for aneuploidy testing There are some chromosome aneuploidies, for instance, trisomy 21 (Down syndrome); trisomy 13 (Patau syndrome); and trisomy 18 (Edwards syndrome), that are compatible with survival to term, although the majority of such conceptuses are miscarried. The congenital abnormalities associated with these syndromes lead to neonatal death or lifelong physical and mental disability. Therefore, the removal of embryos carrying these aneuploidies from an IVF cohort would remove the risk of a pregnancy affected by them. In addition, many of the other chromosome abnormalities detected by FISH may not be compatible with embryo development and implantation and, therefore, it seems logical that the transfer of embryos with normal chromosomes should increase the chances of a successful pregnancy, which may be especially important if single embryo transfer becomes normal practice. Strategies There are only five fluorescent tags available with discrete and resolvable excitation and emission wavelengths and it is, therefore, only possible to have unique detectable colours for five chromosome pairs in one hybridisation test. As there are 23 pairs of human chromosomes, 89
3 Review 2008;10:88 92 The Obstetrician & Gynaecologist Table 1 Pregnancy success rates following aneuploidy testing per oocyte retrieval or embryo transfer 20 Success rate Success rate per oocyte per embryo Indication retrieval (%) transfer (%) Raised maternal age Recurrent miscarriage Recurrent implantation failure Severe male factor infertility detection of aneuploidy for only five pairs may not make very much difference to IVF success. For this reason, some centres using aneuploidy testing have adopted a strategy of using more than one sequential hybridisation step, with analysis, then washing, following each step. The maximum number of chromosomes tested for in clinical cycles using this approach is nine. 11 Which subset of chromosomes should be included in an aneuploidy test? If the object is to increase pregnancy success rates, those chromosomes most frequently found to be aneuploid in cleavage stage embryos should be included. If the object, however, is to prevent miscarriage and the birth of children with congenital abnormalities, those chromosomes most frequently found to be aneuploid in products of conception should be included. Comprehensive data are available for the latter group, 12 but only small studies have been published for the former. 13,14 Comparative genomic hybridisation Ideally, the whole chromosome set should be analysed. Comparative genomic hybridisation (CGH) achieves this by using amplified DNA from a single biopsied cell. This DNA is labelled with a fluorescent tag, mixed with control DNA labelled with a different tag, then hybridised onto fixed control chromosome spreads (chromosome CGH), 15,16 or to microarrays (array CGH). 17 Chromosome CGH has been used in clinical cycles but requires freezing of embryos prior to diagnosis and transfer because of the time-frame of the test. Array CGH is less time consuming but has not yet been sufficiently developed and validated to be used clinically. Application Aneuploidy testing was first reported in It is an expensive and time-consuming test, for which couples are charged in addition to their IVF costs at those centres where it is offered. The benefits to them should, therefore, be clear, as couples desperate for children can be swayed by the technological imperative into agreeing to tests of unproven value. In general, four groups of patients have been targeted for aneuploidy testing, although there has been a suggestion that this test should be part of routine IVF care. The four groups generally targeted are: older women, as they have an empirically higher risk of chromosomally abnormal fetuses women who have suffered repeated IVF failure, as these failures may be the result of a high prevalence of abnormal embryos in each cohort women who have had recurrent miscarriages, as they may be caused by chromosome aneuploidy couples with severe male factor infertility, as empirical data suggests that embryos from such cycles have a high prevalence of aneuploidy. 19 There is a considerable body of published data from the centres where aneuploidy testing is carried out. The most recent data collection 20 by the ESHRE PGD Consortium reports that aneuploidy testing is now the most common reason for embryo biopsy, with 1722 cycles submitted to the data collection for the period January December Pregnancy success rates for these cycles per oocyte retrieval and per embryo transfer for the different targeted groups are presented in Table 1. Published studies Three recent reviews have summarised the studies on aneuploidy testing for raised maternal age published prior to Both non-randomised and randomised studies were reviewed. The nonrandomised studies reported increased pregnancy rates and reduced miscarriage rates. 11,24,25 The authors of the reviews, however, concluded that there were insufficient data, based on the results of the randomised controlled trials, 26,27 to determine whether aneuploidy testing was an effective strategy in terms of improving live birth rates per cycle started. Some methodological problems with the randomised controlled trials were mentioned in the reviews; further trials were recommended. Further criticism of the methodology of the trials (for instance, two cells biopsied rather than one, suboptimal protocols for cell nucleus spreading) has been put forward by supporters of aneuploidy testing from the larger centres offering this service. 28 Mastenbroek et al. 29 have since published the results of a multicentre, randomised double-blind controlled trial on aneuploidy testing for raised maternal age. This trial found that the ongoing pregnancy and live birth rate was significantly lower in the women who had aneuploidy testing than in the control group. Thus, while previous randomised studies had shown no improvement in outcome for women undergoing aneuploidy testing, this study is the first to demonstrate that it results in lower success rates, in terms of both ongoing pregnancy and live birth. No prospective randomised trials for indications other than raised maternal age have been published. 90
4 The Obstetrician & Gynaecologist 2008;10:88 92 Review Problems associated with aneuploidy testing The rationale underpinning aneuploidy testing is seductively logical: remove abnormal embryos from an IVF cohort and there is an increased likelihood that a successful pregnancy will ensue. There are, however, two factors that may explain why the randomised trials published show either no effect or a detrimental effect of aneuploidy testing. The first concerns the limitations of FISH analysis. Even in the larger and most experienced centres, no more than nine chromosomes have been tested and it may be that those aneuploidies most likely to cause pregnancy failure have not been targeted. In addition, FISH, although generally robust in experienced hands, can result in, for instance, failure of probes to hybridise or overlapping signals, which can cause false normal and abnormal results in some embryos. The apparently abnormal embryos will be excluded from consideration for transfer, even if of good morphological quality, thus reducing the chance of pregnancy. Women of raised maternal age produce fewer eggs and, therefore, have fewer embryos than younger women; this reduction in embryo cohort is likely to be significant in terms of pregnancy success. Indeed, a study by Munne et al. 11 showed that women with fewer than eight zygotes did not benefit from aneuploidy testing. The second limitation to the efficacy of aneuploidy testing is the biological phenomenon of mosaicism, which may result in the cell tested not being representative of the embryo as a whole. Abnormal cells may be generated and then lost or selected against as part of the normal process of embryo development. 30,31 Aneuploidy testing may, therefore, result in embryos not being transferred that could otherwise develop normally and establish a successful pregnancy. Controversies Supporters of aneuploidy testing in general, those who are already using it in clinical practice maintain that in their hands it is of benefit to couples, not just in terms of pregnancy success rates but by allowing childless couples to reach closure if most of their embryos are found to be abnormal. 32 For women with recurrent miscarriage, there are data to indicate that their chances of successful delivery following miscarriage are much higher when using natural conception than the published figure for success rates following IVF and aneuploidy testing. 33,34 The ethics of subjecting them to these procedures, with their associated financial and physical costs is, therefore, understandably viewed with scepticism. The largest body of data for aneuploidy testing is for women of raised maternal age. Reports of nonrandomised studies for this group have concluded, for instance, that: and: Some patients can take real advantage from the chromosome analysis of in vitro fertilisation-generated embryos 24 If replacements are limited to two embryos [PGD] should benefit most IVF patients of advanced maternal age 11 the greatest numerical impact of PGD is in standard assisted reproduction practices, where improved in vitro fertilisation efficiency through aneuploidy screening is surely evolving to become the standard. 35 Even prior to the publication of Mastenbroek s paper, however, a number of professionals had cast doubt on the ethics of offering this test outside the context of a randomised trial. For example, one paper is titled PGD for aneuploidy screening: an expensive hoax?. 36 Other papers state: and: randomised controlled trials with large patient populations are needed before PGD can routinely be recommended as a means for increasing pregnancy rates The use of healthy delivery as the primary outcome, rather than implantation rate, is critical to evaluate the real impact of PGD. 21 more properly conducted randomised controlled trials are needed. Until such trials have been performed [preimplantation genetic screening] should not be used in routine patient care. 22 Mastenbroek s study provides additional weight to the arguments against the use of aneuploidy testing as a clinical service, although the design and execution of the Mastenbroek trial have been criticised by those with experience of aneuploidy testing as a clinical service, who suggest that these flaws were responsible for the adverse outcome reported. 37,38 The future There is an urgent need for further data on the efficacy of aneuploidy testing in the targeted groups. The most suitable setting for these trials would be large centres where aneuploidy testing is already in place and where there is considerable experience and expertise to be found. Whether such trials are ever set up remains to be seen. In the meantime, technology may overtake the debate. 91
5 Review 2008;10:88 92 The Obstetrician & Gynaecologist Alternative testing strategies, such as array comparative genomic hybridisation, may replace traditional FISH and result in more effective embryo selection, although any technique that tests single cells for aneuploidy is likely to be limited in its efficacy by the incidence of mosaicism in preimplantation embryos. There is some evidence that gentle stimulation protocols can result in embryos with fewer chromosome abnormalities, 39 reducing the need for aneuploidy testing. Finally, new, highly effective culture media and techniques may in the future achieve satisfactory pregnancy rates without the need for the additional costs of aneuploidy testing. Until then, efforts should continue to establish other ways of assessing and improving the implantation potential of embryos, with a view to moving towards single embryo transfer and reducing the incidence of multiple pregnancy. References 1 European Society of Human Reproduction & Embryology (ESHRE) [ 2 Human Fertilisation and Embryology Authority. Revised Code of Practice (6th Edition) [ 3 KhalafY, El-Toukhy T, Coomarasamy A, Kamal A, Bolton V, Braude P. Selective single blastocyst transfer reduces the multiple pregnancy rate and increases pregnancy rates: a pre- and postintervention study. BJOG 2008;115: doi: /j x 4 Braude P, Pickering S, Flinter F, Ogilvie CM. Preimplantation genetic diagnosis. Nat Rev Genet 2002;3: doi: /nrg953 5 Handyside AH, Kontogianni EH, Hardy K, Winston RM. Pregnancies from biopsied human preimplantation embryos sexed by Y-specific DNA amplification. Nature 1990;344: doi: /344768a0 6 Renwick P, Ogilvie CM. Preimplantation genetic diagnosis for monogenic diseases: overview and emerging issues. Expert Rev Mol Diagn 2007;7: doi: / Scriven PN, Handyside AH, Ogilvie CM. Chromosome translocations: segregation modes and strategies forpreimplantation genetic diagnosis. Prenat Diagn 1998;18: doi: /(sici) (199812)18: 13<1437::AID-PD497>3.0.CO;2-P 8 Kuo HC, Ogilvie CM, Handyside AH. Chromosomal mosaicism in cleavage-stage human embryos and the accuracy of single-cell genetic analysis. J Assist Reprod Genet 1998;15: doi: /a: Delhanty JD, Harper JC, Ao A, Handyside AH, Winston RM. Multicolour FISH detects frequent chromosomal mosaicism and chaotic division in normal preimplantation embryos from fertile patients. Hum Genet 1997;99: doi: /s Delhanty JD, Griffin DK, Handyside AH, Harper J, Atkinson GH, Pieters MH, et al. Detection of aneuploidy and chromosomal mosaicism in human embryos during preimplantation sex determination by fluorescent in situ hybridisation, (FISH). Hum Mol Genet 1993;2: doi: /hmg/ Munné S, Sandalinas M, Escudero T, Velilla E, Walmsley R, Sadowy S, et al. Improved implantation after preimplantation genetic diagnosis of aneuploidy. Reprod Biomed Online 2003;7: Hassold T, Chen N, Funkhouser J, Jooss T, Manuel B, Matsuura J, et al. A cytogenetic study of 1000 spontaneous abortions. Ann Hum Genet 1980;44: doi: /j tb00955.x 13 Wells D, Delhanty JD. Comprehensive chromosomal analysis of human preimplantation embryos using whole genome amplification and single cell comparative genomic hybridization. Mol Hum Reprod 2000;6: doi: /molehr/ Trussler JL, Pickering SJ, Ogilvie CM. Investigation of chromosomal imbalance in human embryos using comparative genomic hybridization. Reprod Biomed Online 2004;8: Wells D, Escudero T, Levy B, Hirschhorn K, Delhanty JD, Munné S. First clinical application of comparative genomic hybridization and polar body testing for preimplantation genetic diagnosis of aneuploidy. Fertil Steril 2002;78: doi: /s (02) Wilton L, Voullaire L, Sargeant P, Williamson R, McBain J. Preimplantation aneuploidy screening using comparative genomic hybridization or fluorescence in situ hybridization of embryos from patients with recurrent implantation failure. Fertil Steril 2003;80: doi: /s (03) Le Caignec C, Spits C, Sermon K, De Rycke M, Theinpont B, Debrock S, et al. Single-cell chromosomal imbalances detection by array CGH. Nucleic Acids Res 2006;34:e68. doi: /nar/gkl Munné S, Lee A, Rosenwaks Z, Grifo J, Cohen J. Diagnosis of major chromosome aneuploidies in human preimplantation embryos. Hum Reprod 1993;8: Platteau P, Staessen C, Michiels A, Tournaye H, Van Steirteghem A, Liebaers I, et al. Comparison of the aneuploidy frequency in embryos derived from testicular sperm extraction in obstructive and nonobstructive azoospermic men. Hum Reprod 2004;19: doi: /humrep/deh Sermon KD, Michiels A, Harton G, Moutou C, Repping S, Scriven PN, et al. ESHRE PGD Consortium data collection VI: cycles from January to December 2003 with pregnancy follow-up to October Hum Reprod 2007;22: Shahine LK, Cedars MI. Preimplantation genetic diagnosis does not increase pregnancy rates in patients at risk for aneuploidy. Fertil Steril 2006;85:51 6. doi: /j.fertnstert Twisk M, Mastenbroek S, van Wely M, Heineman MJ, Van derveen F, Repping S. Preimplantation genetic screening for abnormal number of chromosomes (aneuploidies) in in vitro fertilisation or intracytoplasmic sperm injection. Cochrane Database Syst Rev 2006(1):CD Donoso P, Staessen C, Fauser BC, Devroey P. Current value of preimplantation genetic aneuploidy screening in IVF. Hum Reprod Update 2007;13: doi: /humupd/dml Gianaroli L, Magli MC, Ferraretti AP, Munné S. Preimplantation diagnosis for aneuploidies in patients undergoing in vitro fertilization with a poor prognosis: identification of the categories for which it should be proposed. Fertil Steril 1999;72: doi: /s (99) Munné S, Fischer J, Warner A, Chen S, Zouves C, Cohen J; Referring Centres PGD Group. Preimplantation genetic diagnosis significantly reduces pregnancy loss in infertile couples: a multicenter study. Fertil Steril 2006;85: doi: /j.fertnstert Staessen C, Platteau P, Van Assche E, Michiels A, Tournaye H, Camus M, et al. 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 2004;19: doi: /humrep/deh Stevens J, Wale P, Surrey ES, SchoolcraftW, Gardner D. Is aneuploidy screening for patients aged 35 or over beneficial? A prospective randomized trial. Fertil Steril 2004;82 suppl 2:249. doi: /j.fertnstert Cohen J, Wells D, Munné S. Removal of 2 cells from cleavage stage embryos is likely to reduce the efficacy of chromosomal tests that are used to enhance implantation rates. Fertil Steril 2007;87: doi: /j.fertnstert MastenbroekS, Twisk M, van Echten-Arends J, Sikkema-RaddatzB, Korevaar JC, Verhoeve HR, et al. In vitro fertilization with preimplantation genetic screening. N Engl J Med 2007;357:9 17. doi: /nejmoa Munné S, Velilla E, Colls P, Garcia BermudezM, Vemuri MC, Steuerwald N, et al. Self-correction of chromosomally abnormal embryos in culture and implications for stem cell production. Fertil Steril 2005;84: doi: /j.fertnstert Gonzalez-Merino E, Emiliani S, Vassart G, Van den Bergh M, Vannin AS, AbramowiczM, et al. Incidence of chromosomal mosaicism in human embryos at different developmental stages analyzed by fluorescence in situ hybridization. Genet Test 2003;7: doi: / Platteau P, Staessen C, Michiels A, van Steirteghem A, Liebaers I, Devroey P. Preimplantation genetic diagnosis for aneuploidy screening in women older than 37years. Fertil Steril 2005;84: doi: /j.fertnstert Christiansen OB, Nybo Andersen AM, Bosch E, Daya S, Delves PJ, Hviid TV, et al. Evidence-based investigations and treatments of recurrent pregnancy loss. Fertil Steril 2005;83: doi: /j.fertnstert MastenbroekS, Twisk M, Goddijn M, Van derveen F, Repping S, Bossuyt PM, et al. PGD-a model to evaluate efficacy? Fertil Steril 2006;85: doi: /j.fertnstert Verlinsky Y, Cohen J, Munné S, Gianaroli L, Simpson JL, Ferraretti AP, et al. Over a decade of experience with preimplantation genetic diagnosis. Fertil Steril 2004;82: doi: /j.fertnstert Donoso P, Devroey P. PGD for aneuploidy screening: an expensive hoax? Best Pract Res Clin Obstet Gynaecol 2007;21: doi: /j.bpobgyn Munné S, Cohen J, Simpson JL. In vitro fertilization with preimplantation genetic screening. N Engl J Med 2007;357: doi: /nejmc Handyside AH, Thornhill AR. In vitro fertilization with preimplantation genetic screening. N Engl J Med 2007;357(17): Baart EB, Martini E, Eijkemans MJ, Van Opstal D, Beckers NG, Verhoeff A, et al. Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial. Hum Reprod 2007;22: doi: /humrep/del484 92
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