@ CIC Edizioni Internazionali. The impact of Italian legislative amendments on delivery rate: a matched case control study. Introduction.
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1 Original article The impact of Italian legislative amendments on delivery rate: a matched case control study Roberta Maggiulli 1 Antonio Capalbo 1,2 Stefania Romano 1 Laura Albricci 1 Catello Scarica 1 Silvia Colamaria 1 Fabio Sapienza 1 Maddalena Giuliani 2 Laura Rienzi 1 Filippo Maria Ubaldi 1 1 GENERA Centre for Reproductive Medicine, Valle Giulia Clinic, Rome, Italy 2 GENETYX Molecular Genetics Laboratory, Vicenza, Italy Address for correspondence: Roberta Maggiulli GENERA Centre for Reproductive Medicine, Valle Giulia Clinic Via G. De Notaris 2b Rome, Italy Tel.: Fax: maggiulli@generaroma.it Summary In May 2009, the Italian Constitutional Court declared unconstitutional the 40/2004 restrictive law of the Italian Parliament, granting the physician the possibility to define the optimal number of oocytes to be inseminated, the number of embryos to be transferred and allowing cryopreservation of embryos. To investigate the effect of suspension of the restrictive human ART law in Italy on the characteristics and efficiency of a routine infertility program, a one-to-one matched case-control study was conducted before and after the Court sentence (182 cycles for both s, respectively). Mean number of inseminated oocytes was 2.9 and 7.5 in the pre- and postsentence s, respectively (p< 0,001). A lower mean number of embryos per patient was transferred in the post-sentence (2.5 vs 2.1; p< 0.001). Although comparable cumulative delivery rates were obtained in both periods, fewer cycles per patient were performed in the post-sentence (mean: 1.6 vs 1.4; p<0.01). In conclusion, inseminating more than 3 oocytes and performing embryo selection allows a reduction in the number of embryos to be transferred and/or cryopreserved while maintaining the same chance to obtain a delivery. KEY WORDS: Italian law, delivery rates, live birth rates. Introduction The laboratory part use of human assisted reproduction is continuously subject of debates all over the world. The intensity and specific subject of these debates is related to the cultural, religious and/or historical background of the given society and has a significant influence on the implemented legal frames. However, another factor, the actual intentions of the governing political power may have an equally important, or even more decisive role in establishment of the relevant legal frames. Accordingly, the scale of permitted vs prohibited procedures and practices varies widely even within a relatively homogenous of countries including the European Union. Moreover, profound changes may also occur in relation to the intentions of a newly elected government, or as the result of the debates between various institutions involved in constitutional and legislation issues. In the majority of the cases, these changes do not reflect authentically the intentions of the population they are applied on. From this point of view the situation in Italy Current Trends in Clinical Embryology 2016; 3 (2):
2 R. Maggiulli et al. during the past decade is usually regarded as the most extreme example. Radical changes of the legal frames have caused considerable tensions, required adaptations from both professionals and patients, and resulted in profound theoretical as well as practical changes in the everyday infertility treatment. The Law 40/2004 ( Norms on the matter of medically assisted procreation ) referred the sanctity of human life from its inception. On this basis, embryo cryopreservation and suppression were forbidden, accordingly the rights of specialists to select and apply the optimal treatment, and the rights of patients to decide about the use of their embryos were seriously restricted. For the latter, the law has also created (and acknowledged) a serious contradiction with the relatively liberal abortion law implemented in 1978 and confirmed also in the ominous Law 40/2004. The practical consequences of the restrictive law on the clinical practice were the following: no more than three oocytes per treatment cycle could be fertilized; and the transfer of all three possible embryos was mandated. Cryopreservation of embryos was only permitted in exceptional situation where the health status of the woman does not allow fresh transfer, and this situation was unpredictable at the time of creation of the embryo. On the other hand, the law permitted, and to some extent encouraged the cryopreservation of male and female gametes. To save the considerable achievements in infertility treatment, and to maintain (or at least avoid the catastrophic decrease of) the overall efficiency, considerable efforts have been performed in two distinct areas. One of the crucial changes was the improvement and widespread application of oocyte cryopreservation, first by traditional freezing (1, 2), then by vitrification. Recently the latter approach has become highly successful and evolved as a competitive alternative of embryo cryopreservation (3-6). Another tendency performed by several clinics was the application of mild stimulation approaches, as collection of a high amount of MII phase oocytes has become unreasonable. As a possible consequence, the overall quality of recovered oocytes and that of embryos derived of them has increased, and in spite of the lack of possibility to select the best embryo(s) for transfer, the overall pregnancy rates did not decrease dramatically (7). The less disturbed hormonal status of the recipients might have also contributed in this achievement. On the other hand, the selection of the best oocytes for fertilization followed by the transfer of all available embryos irrespective to their quality did not result in the expected improvement (3, 8). It should also be mentioned that applications of some recent tendencies in human ART including blastocyst culture and various methods of invasive or non-invasive embryo quality assessment were mostly abandoned as their application would not have any practical consequence on the routine infertility practice. However, the efforts to compensate the restrictions have eventually become successful, although this success does not justify the introduction of Law 40/2004. According to Ragni et al. (9) and La Sala et al. (10), the new legal situation did not reduce the success rates of ART and did not increase the number of multiple births. On the other hand, the lack of possibility to cryopreserve embryos was serious and in most clinics could not be compensated by the increased efficiency of oocyte cryopreservation. Meanwhile, both ART specialists and their legal and laic supporters have intensified their effort in various ways and on different levels to prove the absurdity of the situation that has been evolved, and to achieve changes by using the possibilities offered by the Italian legislation system. A strong international support from IVF specialists all over the world has also contributed in these arguments (11-13, among others). Efforts included a referendum that eventually has failed to achieve the required majority for changing the most important restrictions (14). On the other hand, appeals to lower courts around the country have succeeded to proceed the issue to the Italian Constitutional Court. In the decision published on 8th May, 2009, the Court ruled that part of the 40/2004 Law of the Italian Parliament is unconstitutional (15). This decision has created a special legal situation, as some critical restrictions were eliminated, but creation of a new law is the authority of the Parliament, and is expected in the foreseeable future. In this transitional period certain things remain unclarified, but some critical restrictions were clearly eliminated including the limit of maximum 3 oocytes to be fertilized and the need to transfer all the embryos that have been created. Strict ban of embryo cryopreservation was also declared as unconstitutional, although the 48 Current Trends in Clinical Embryology 2016; 3 (2): 47-53
3 The impact of Italian legislative amendments on delivery rate: a matched case control study application areas remain limited. The purpose of this work was to analyze the effect of the legal situation that has been evolved after the decision of the Italian Constitutional Court on the practice and efficiency on the routine infertility work in Italy. We conducted a one-to-one matched case-control study with good responder patients of our centre undergoing ICSI treatment before and after the Court ruling in order to evaluate the impact of the changes to the restrictive Italian law on assisted reproduction. Materials and methods All fresh cycles performed between September 2008 and May 2009 for the pre-sentence and between September 2010 and May 2011 for the post-sentence at GENERA Centre for Reproductive Medicine have been analyzed retrospectively. We exclude from the study patients with less than 6 MII retrieved oocytes and patients undergoing PGD/PGS cycles. Only patients with supernumerary oocytes available for cryopreservation were included in the pre-sentence. A single fresh attempt was included for each patient. A total of 182 fresh cycles performed before the Italian Constitutional Court decision were individually and sequentially matched according to maternal age, basal FSH, number of mature oocytes retrieved and sperm characteristics with 182 cycles performed after the revision to the restrictions. Cumulative delivery rates per ovum pick-up and delivery rates per fresh and warmed cycles as well as time to pregnancy (number of cycles performed per obtained delivery) was regarded as primary and secondary outcome measures, respectively. The ovulation induction, laboratory and embryo transfer protocols applied by the individual clinics did not differ in the two investigation periods. No significant change in the laboratory and medical staff has happened in the centre during the pre- and post-sentence period. During the pre-sentence period, a maximum 3 oocytes were inseminated by in vitro fertilization or intracytoplasmic injection, and all cleaved embryos without serious morphological alterations were transferred. In the post-sentence period, according to the international standards and also the guidelines of the Italian Fertility Societies the number of oocytes to be subjected to insemination and the number of embryos transferred was determined on the basis of the age of the female partner, the quality of the sperm and the infertility history of the patients. All couples enrolled in the post-sentence programs were asked to sign a consent form for a personalised number of oocytes to be used, number of embryos to be transferred and for cryopreservation of nontransferred leftover embryos. Embryos were transferred 48 to 72 hours after oocyte retrieval. Oocyte and embryo vitrification were performed as described earlier (4). Clinical pregnancy was determined by ultrasound demonstration of gestational sac at 7 weeks. Miscarriage was classified as early (before 12 weeks) or late (after 12 weeks; 16). Delivery rate was defined as number of delivery per embryo transfer. Implantation rate and live birth rate were defined as number of gestational sacs and number of live birth per transferred embryo, respectively. Approval for the study was obtained from the local institutional review board, and patients were asked to provide and informed consent to the anonymous use of clinical data for statistical evaluation and research purposes. Statistical analysis: Continuous data and categorical variables are reported as mean and percentage frequency with standard deviations and 95% confidence intervals, respectively. Fisher s exact test was used to test the categorical variable. Student s t-test was used to test continuous variables between s. Alpha was set at Results Characteristics of the started cycles of investigated patients are summarized in Table 1. Mean value comparisons confirmed that the 182 corresponding pairs were similar for the matching criteria i.e. age, basal FSH level and number of retrieved MII oocytes. However, the number of the inseminated oocytes was significantly higher after the restrictions were eliminated. In terms, more fertilized oocytes and more good quality embryos were obtained in the post-sentence. Oocyte cryopreservation was performed in all the pre-sentence cycles, while in the post-sentence oocytes and/or embryos cryopreservation was performed only in selected cases. Importantly, a significantly lower number Current Trends in Clinical Embryology 2016; 3 (2):
4 R. Maggiulli et al. Table 1 - Baseline patient s characteristics and fresh cycles outcomes. of embryos was transferred in the post-sentence. However, no differences were observed in the clinical outcomes obtained. In Table 2 the results obtained in the warming cycles are described. Interestingly, no differences were observed in clinical pregnancy rates, implantation rates, delivery rates and live birth rates when oocytes were warmed in the pre- and post- sentence s compared to embryos. Overall, a comparable cumulative delivery rate per patient was obtained after fresh and warming cycles in both periods, however a significantly lower number of cycles per patient was performed in the post-sentence (p<0.01; Table 3). Multiple pregnancy rate was also similar in both s (15,3 vs 13,6%, respectively). Importantly, the cumulative live birth rate was significantly improved by embryo selection in the post sentence (Table 3). In other terms, a mean number of 3.1 and 2.7 cycles was necessary to obtain a delivery in the pre- and post- sentence, respectively (P<0.01). Pre-sentence 95%CI Post-sentence 95%CI P N patients Mean age (mean ± SD) 35.8 ± ± 3.9 Mean basal FSH (mean ± SD) 6.5 ± ± 1.9 Agonist protocol (%) 143/182 (78.6) /182 (74.2) Antagonist protocol (%) 39/182 (21.4) /182 (25.8) COC (mean ± SD) 12.8 ± ± 4.9 MII (mean ± SD) 10.1 ± ± 3.5 Inseminated MII (mean ± SD) 2.9 ± ± 2.6 P< PN (mean ± SD) 2.6 ± ± 2.2 P<0.001 Top quality embryos (mean ± SD) 1.5 ± ± 1.8 P<0.001 Embryo transferred (mean ± SD) 2.5 ± ± 0.5 P<0.001 Oocyte vitrified (mean ± SD) 6.2 ± ± 3.6 P<0.001 Embryo vitrified (mean ± SD) 0 2.1± 1.7 P<0.001 N of ET (%) 172/182 (94.5) /182 (92.8) Clinical PR per cycle (%) 77/182 (42.3) /182 (48.3) Clinical PR per ET (%) 77/172 (44.8) /169 (52.1) Implantation rate (%) 101/435 (23.2) /370 (30.0) Early and late abortion rate (%) 9/77 (11.7) /88 (19.3) Delivery rate per fresh cycle (%) 68/182 (37.4) /182 (39.0) Live birth rate (%) 90/435 (20.7) /370 (24.6) COC: cumulus-oocyte-complexes. Discussion During the past ten years, Italy has deserved well the attention of human embryologist, reproductive biologists and lawmakers dealing with this special area. Drastic changes implemented forth and back in this country in the legislation are without precedent all over the world in the 30 years history of human assisted reproduction. Although these changes have caused serious problems to both professionals and patients, they also created an exceptional possibility to investigate how infertility clinics can adapt to the changing situations. After the initial, extremely restrictive Law 40/2004 of the Italian Parliament, several reviews have analysed the attempts of Italian IVF specialist to overcome the problems, minimize the effect and avoid sharp decline in the overall efficiency (7-10, 17-21), and special strategies were also published to overcome special problems (2-6). As discussed earlier, the adaptation 50 Current Trends in Clinical Embryology 2016; 3 (2): 47-53
5 The impact of Italian legislative amendments on delivery rate: a matched case control study Table 2 - Warmed cycles (oocytes and embryos) laboratory and clinical outcomes. Pre sentence (oocytes) 95%CI Post sentence (oocytes) 95%CI Post sentence (embryos) N of cycles Number of oocytes/embryos warmed Survival rate (%) 437/487 (89.7) N of ET (%) 111/ (96.5) 99.0 Clinical PR per cycle (%) 35/ (30.4) 39.7 Clinical PR per ET (%) 35/ (31.5) 41.0 Implantation rate (%) 43/ (16.1) 21.1 Abortion rate (%) 6/35 (17.1) Delivery rate per warmed cycle (%) 29/ (25.2) 34.2 Live birth rate (%) 35/ (13.2) 17.8 ET: Embryo transfer. PR: Pregnancy rate. Table 3 - Cumulative clinical outcomes. 95%CI 78/91(85.7) /20 (90.0) /20 (35.0) /18 (38.9) /33 (21.2) /7 (14.2) /20 (30.0) /33 (18.2) / (94.4) /56 (98.2) /56 (37.5) /55 (38.2) /117 (17.9) /20 (15.0) /56 (32.1) /117 (15.4) Pre-sentence Post-sentence 95%CI 95%CI P Fresh cycle delivery rate (% per patient) 68/182 (37.4) /182 (39.0) Number of cycles per patient (mean ±SD) 182 (1±0) 182 (1±0) I warming I warming delivery rate (% per cycle) 26/104 (25.0) /60 (33.3) I warming cumulative delivery rate (% per patient) 94/182 (51.6) /182 (50.0) Number of cycles per patient (mean ±SD) 286 (1.57±0.7) 242 (1.32±0,5) 0.01 II warming II warming delivery rate (% per cycle) 3/11 (27.2) /16 (25) II warming cumulative delivery rate (% per patient) 97/182 (53.3) /182 (52.2) Number of cycles per patient (mean ±SD) 297 (1.63±0.6) 258 (1.41±0,6) 0.01 Cumulative live birth rate (%) 144/701 (20.5) 139/520 (26.7) P Current Trends in Clinical Embryology 2016; 3 (2):
6 R. Maggiulli et al. to the new situation was unpredictably and unexpectedly successful and the overall efficiency did not drop considerably compared to the previous period in Italy and also compared to the efficiency in countries with similar technological level and extend of application of IVF technologies, but without restrictive law in the given period. According to our knowledge, the present paper is the first case control study to deal with the effect of the latest legal situation that has arisen with the sentence of the Italian Constitutional Court (1st April, 2009) that has declared some restrictions of the Law 20/2004 were unconstitutional. This sentence has created a new, although not entirely clarified legal situation and provided more autonomy to specialist to determine the appropriate number of embryos to transfer. The practical consequences of the sentence were the following: in contrast to the previous situation, the number of the oocytes subjected to fertilization in one cycle was not restricted to maximum three, i.e. could be increased, and more embryos could be obtained; the obligation to transfer all viable embryos was abolished, accordingly the number of transferred embryos could be determined due to the given situation to achieve maximal efficiency and to decrease risks including multiple pregnancies transfer of unselected embryos to patients could be minimized; also the number of transfers with no, or maximum one unselected embryos could be decreased. The sentence of the Constitutional Court also allowed with certain restrictions the cryopreservation of the created embryos. The accumulated knowledge and new approaches during the restrictive period could theoretically result in a considerable increase of overall efficiency under the new conditions where more freedom is provided to select the optimal treatment. In the initial period, however, the expected marked improvement of efficiency i.e. an increase in the delivery rates after fresh cycles, and decrease of multiple pregnancies did not occur. It should be considered that the investigated post-sentence period has started only 1 year after the introduction of the new legislation and was relatively short. Adaptation to the new situation may require more time and experience from both ART specialists and patients. The lack of significant difference in terms of cumulative delivery rate during the two periods can also be explained with the introduction of vitrification that has eliminated the difference between the overall outcome of oocyte and embryo cryo - preservation (also documented by 5 and 6). This one-to-one matched case-control study shows that embryo selection is useful to optimize clinical outcomes per transferred embryo. Moreover, cryopreserving only in selected cases significantly benefits the patient in terms of time to pregnancy. In other terms, a mean of 3.1 vs 2.7 cycles were necessary to obtain a delivery and a mean of 4.9 vs 3.7 embryos had to be transferred to obtain a live birth in the pre- and post- sentence, respectively (P<0.01). In latest year, the improvements obtained with the introduction of vitrification and with the employment of more reliable embryo selection methods, such as blastocyst culture and PGD-A, have had several important clinical implications. In particular, when embryo selection in enhanced, single embryo transfer policy can be adopted without affecting the total efficacy of IVF treatment but increasing efficiency and safety (22). Acknowledgements The Authors acknowledge all the team of the GENERA Centre for Reproductive Medicine of Rome for the collaboration in performing this study. References 1. Porcu E, Venturoli S. Progress with oocyte cryopreservation. Curr Opin Obstet Gynecol. 2006;18: Borini A, Bianchi V, Bonu MA, Sciajno R, Sereni E, Cattoli M, Mazzone S, Trevisi MR, Iadarola I, Distratis V, Nalon M, Coticchio G. Evidence-based clinical outcome of oocyte slow cooling. Reprod Biomed Online. 2007; 15; Rienzi L, Romano S, Albricci L, Maggiulli R, Capalbo A, Baroni E, Colamaria S, Sapienza F, Ubaldi F. Embryo development of fresh versus vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study. Hum Reprod. 2010;25: Ubaldi F, Anniballo R, Romano S, Baroni E, Albricci L, Colamaria S, Capalbo A, Sapienza F, Vajta G, Rienzi L. Cumulative ongoing pregnancy rate achieved with oocyte vitrification and cleavage stage transfer without embryo selection in a standard infertility program. Hum Reprod. 2010;25: Rienzi L, Cobo A, Paffoni A, Scarduelli C, Capalbo A, Vajta G, Remohi J, Ragni G, Ubaldi FM. Consistent and 52 Current Trends in Clinical Embryology 2016; 3 (2): 47-53
7 The impact of Italian legislative amendments on delivery rate: a matched case control study predictable delivery rates after oocyte vitrification: an observational longitudinal cohort multicentric study. Hum. Reprod. 2012;27: Rienzi L, Gracia C, Maggiulli R, LaBarbera AR, Kaser DJ, Ubaldi FM, Vanderpoel S, Racowsky C. Oocyte, embryo and blastocyst cryopreservation in ART: systematic review and meta-analysis comparing slow-freezing versus vitrification to produce evidence for the development of global guidance. Hum Reprod Update Nov 8. [Epub ahead of print] 7. Levi Setti PE, Albani E, Novara P, Cesana A, Negri L. Results of in vitro fertilization in Italy after the introduction of a new law. Fertil Steril. 2008;90: La Sala GB, Nicoli A, Villani MT, Di Girolamo R, Capodanno F, Blickstein I. The effect of selecting oocytes for insemination and transferring all resultant embryos without selection on outcomes of assisted reproduction. Fertil Steril. 2009;91; Ragni G, Allegra A, Anserini P, Causio F, Ferraretti AP, Greco E, Palermo R, Somigliana E.The 2004 Italian legislation regulating assisted reproduction technology: a multicentre survey on the results of IVF cycles. Hum Reprod. 2005;20: La Sala GB, Villani MT, Nicoli A, Valli B, Iannotti F, Blickstein I. The effect of legislation on outcomes of assisted reproduction technology: lessons from the 2004 Italian law. Fertil Steril. 2008;89: Pellicer A. The Italian law on assisted reproduction: a view from Spain. Reprod Biomed Online. 2005;11: Kahraman S, Findikli N. Effect of Italian referendum on global IVF: a comment from Turkey. Reprod Biomed Online. 2005;11: Sauer M. Italian Law 40/2004: a view from the Wild West. Reprod Biomed Online. 2006;12: Benagiano G. The four referendums attempting to modify the restrictive Italian IVF legislation failed to reach the required quorum. Reprod Biomed Online. 2005;11: Corte Costituzionale, Sentenza 151/09 nei giudizi di legittimità costituzionale dell articolo 6, comma 3, e dell - articolo 14, commi1, 2, 3 e 4, della legge 19 febbraio 2004, n. 40 (Norme in materia di procreazione medicalmente assistita) Farquharson RG, Jauniaux E, Exalto N. ESHRE Special Interest Group for Early Pregnancy (SIGEP). Updated and revised nomenclature for description of early pregnancy events. Hum Reprod. 2005;20: Ciriminna R, Papale ML, Artini PG, Costa M, De Santis L, Gandini L, Parmegiani L, Ragni G, Revelli A, Rienzi L. Italian Society of Embriology, Reproduction and Research Barbaro R, Cela V, Cino I, Colia D, D Ambrogio G, Diotallevi L, Dusi M, Filicori M, Genazzani AR, Giuffrida G, Lombardo F, Paffoni A, Racca C, Greco E. Impact of Italian legislation regulating assisted reproduction techniques on ICSI outcomes in severe male factor infertility: a multicentric survey. Hum Reprod. 2007;22: La Sala GB, Gallinelli A, Nicoli A, Villani MT, Nucera G. Pregnancy loss and assisted reproduction: preliminary results after the law 40/2004 in Italy. Reprod Biomed Online. 2006;13: Caserta D, Marci R, Tatone C, Schimberni M, Vaquero E, Lazzarin N, Fazi A, Moscarini M. IVF pregnancies: neonatal outcomes after the new Italian law on assisted reproduction technology (law 40/2004). Acta Obstet Gynecol Scand. 2008;87: Turillazzi E, Fineschi V. Assisted reproductive technology: official data on the application of the Italian law. Reprod Biomed Online. 2008;16(S1): Ubaldi FM, Capalbo A, Colamaria S, Ferrero S, Maggiulli R, Vajta G, Sapienza F, Cimadomo D, Giuliani M, Gravotta E, Vaiarelli A, Rienzi L. Reduction of multiple pregnancies in the advanced maternal age population after implementation of an elective single embryo transfer policy coupled with enhanced embryo selection: pre- and post-intervention study. Hum Reprod. 2015;30(9): Current Trends in Clinical Embryology 2016; 3 (2):
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