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The use of blastocysts developing from nonpronuclear and monopronuclear zygotes can be considered in PGT-SR: a retrospective cohort study

BMC Pregnancy and Childbirth volume 25, Article number: 530 (2025) Cite this article

Abstract

Background

While zygotes lacking pronuclei (0PN) or exhibiting a single pronucleus (1PN) may theoretically yield diploid embryos with developmental potential, current clinical protocols predominantly exclude these embryos from use. In the population undergoing preimplantation genetic testing for structural rearrangements (PGT-SR), there is a high rate of chromosomal aneuploidy abnormalities and needs a large number of embryos to obtain euploid embryos, so we will explore whether 0PN and 1PN embryos can be an option for them.

Methods

This retrospective analysis examined pronuclear development in 4,868 zygotes derived from 4,902 injected metaphase II (MII) oocytes across 422 assisted reproductive cycles. In a subset of 54 cycles (12.8%), preimplantation genetic testing for structural rearrangements (PGT-SR) was implemented for blastocysts originating from 0PN and 1PN embryos that progressed to Day 5/6 development stage prior to vitrification. Comprehensive genomic haplotyping was performed on 343 embryos within this subgroup, including 33 0PN-derived, 36 1PN-derived, and 274 conventional 2PN-derived specimens. The investigation’s primary endpoint focused on neonatal survival outcomes, while secondary assessments evaluated both embryo transfer suitability and chromosomal normality rates.

Results

Compared to 2PN embryos, the proportion of 0PN and 1PN embryos developing into blastocysts is significantly lower (5.41%, 21.56% vs. 56.51%, p-value < 0.001); the euploid rate of 0PN blastocysts is not statistically different from that of 2PN blastocysts (18.18% vs. 33.21%, p-value = 0.111), but significantly lower for 1PN blastocysts (11.11% vs. 33.21%, p-value = 0.004). In 54 cycles involving 0PN and 1PN blastocysts, the inclusion of 0PN and 1PN embryos resulted in an increase in the number of frozen embryos (5.81 ± 3.55 vs. 7.09 ± 3.52, p-value = 0.063), transferable embryos (1.59 ± 1.25 vs. 1.78 ± 1.30, p-value = 0.452), embryos transferred (0.98 ± 0.76 vs. 1.07 ± 0.75, p-value = 0.526), and patients undergoing transfer (74.07% vs. 79.63%, p-value = 0.494), although these changes were not statistically significant. The five 0PN and 1PN embryos transferred resulted in three live births, which was not a significant increase (56.36% vs. 56.67%, p-value = 0.974).

Conclusion

Chromosome abnormalities did not increase the occurrence of abnormal fertilization. There were already a large number of embryos in the PGT-SR population, and routine inclusion of 0PN and 1PN embryos in the PGT-SR cycle is not recommended in this study. Priority should be given to the transfer of 2PN embryos. If a couple receives fewer than three 2PN embryos, or no 2PN embryos at all, it may be considered to include 0PN and 1PN embryos, with preference given to the use of 0PN. Furthermore, genome-wide ploidy and haplotyping are recommended for detection, and aneuploid and ploidy abnormalities are excluded.

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Introduction

In assisted reproductive technology, effective oocyte-sperm fertilization is indicated by the appearance of two pronuclei (2PN) 16–18 h after insemination [1, 2]. However, embryos with no pronuclei (0PN) or only one pronucleus (1PN) are occasionally discovered, with reported frequency of 11.3-20% [3]and 1.6-7.7% [4], respectively. These embryos are generally deemed defective and inappropriate for clinical use; moreover, the European Society of Human Reproduction and Embryology (ESHRE) does not recommend the use of 0PN and 1PN embryos in in vitro fertilisation (IVF) practices [5]; thus, they are usually discarded.

These embryos may cleave in the same way that typically fertilized 2PN-derived embryos do [6,7,8]. Chromosomal analysis revealed that a few 1PN- and 0PN-derived embryos had normal chromosomal structure [9, 10]. Furthermore, in cycles with only 0PN-derived embryos, the transfer of these embryos resulted in pregnancies and healthy newborns [11,12,13,14]. Like 0PN, successful development to full term has been reported following the transfer of 1PN-derived embryos [4, 15,16,17,18]. For some patients, this will provide them with the only clinically available embryo, resulting in the only chance of a pregnancy in a particular cycle.

In a recent study, Destouni, A. et al. (2018) demonstrated that Haplarithmisis allows the inclusion of both 0PN and 1PN embryos by simultaneously excluding the presence of mutant haplotypes and confirming biparental diploidy across the embryonic genome in preimplantation genetic testing for a monogenic disorder (PGT-M) cycles [19].

Balanced translocation is one of the most common reasons for preimplantation genetic testing (PGT), with an incidence ranging from 1/500 to 1/625 in the general population and up to 1/20 in patients with a history of repeated IVF failure or recurrent miscarriages [20]. Although they frequently exhibit normal phenotypes, the possibility of creating imbalanced gametes is substantial (usually about 70%) due to abnormal segregation of rearranged chromosomes during meiosis [21, 22]. Unbalanced gametes can cause infertility, recurrent miscarriages, and other congenital abnormalities [23,24,25]. Due to the lower probability of whole chromosomal rearrangements in embryos carried by patients with balanced translocations, a larger number of embryos are required to boost the chance of successful transplantation.

PGT-SR has previously been widely used to select embryos free of chromosomal copy number variations (CNV) from chromosome balanced translocation carriers. However, effectively distinguishing between balanced and physically normal chromosomes in embryos remains challenging. Zhang et al. addressed this issue using genome-wide ploidy and haplotyping. Single-nucleotide polymorphisms (SNP) information of family members and embryos was analyzed to distinguish balanced and structurally normal chromosomes efficiently [26].

This study used haplotype analysis to detect embryos with 0PN and 1PN in PGT-SR patients to confirm whether PGT-SR patients can increase the number of transplantable embryos by using 0PN and 1PN embryos.

Methods

Study population

We enrolled 357 translocation carrier families that would undergo assisted reproductive at the Centre for Reproductive Medicine, Shandong Provincial Hospital Affiliated with Shandong University from October 2018 to December 2020.

The Institutional Review Board of Reproductive Medicine at Shandong University provided ethical approval for the usage and analysis of information and data from patients who underwent PGT-SR.

IVF, pronuclear scoring and embryo handling

Ovarian stimulation was performed according to the clinical routine in the Centre for Reproductive Medicine, Shandong Provincial Hospital Affiliated to Shandong University. After oocyte aspiration, Intracytoplasmic sperm injection (ICSI) was performed on metaphase II (MII) oocytes. Zygotes were cultured until the blastocyst stage.

All oocytes were inseminated by intracytoplasmic sperm injection and the embryos were cryopreserved through vitrification. The embryo scoring was conducted by morphologic criteria [27]. Briefly, blastocysts were graded on a 1–6 scale determined by the degree of expansion and hatching status. The inner cell mass (ICM) was scored according to the number of cells. Many ICM cells packed together tightly represented the best grade (A), whereas grade B showed several ICM cells loosely grouped. The worst grade (C) was when there were very few ICM cells. In parallel, trophectoderm (TE) was considered of good quality if many cells formed a cohesive epithelium. Many TE cells forming multiple epithelial layers represented the best grade (A). Grade B showed few TE cells consisting of a loose epithelium and very few large TE cells represented the worst grade (C). Three experienced embryologists scored the blastocysts using consistent lab conditions and scoring criteria. In addition, embryonic scoring was checked by the section director. Poor-quality blastocysts were not biopsied.

Good-quality blastocysts were drilled, and 4–6 trophoblast cells were biopsied [28]. The biopsied cells were placed into polymerase chain reaction tubes with an alkaline denaturation buffer for cell lysis. Whole genomic amplification (WGA) was performed by the multiple displacement amplification (MDA) method. Isothermal DNA amplification with phi 29 DNA polymerase was performed (Repli-g single cell kit, QIAGEN GmbH, Hilden, Germany) as described in the manufacturers’ protocol. The isothermal amplification was performed at 30 °C for 8 h and the reaction was stopped by incubation at 65 °C for 3 min.

Genome-wide ploidy and haplotyping

The isolated DNA and WGA products were treated according to the manufacturer’s instructions (Illumina, San Diego, CA, USA), which were then scanned using an Illumina iScan Bead Array Reader. The microarray scanning results were processed using the B allele frequency and Log R Ratio of Genome Studio software (Illumina) and Karyo Studio software (Illumina) to analyze the copy number of the chromosomes. Genome wide preimplantation genetic haplotyping (PGH) analysis based on Illumina Human Karyomap-12 V1.0 microarray was performed as our previous description.

Embryo transfer

Blastocysts determined to have no detectable abnormalities (normal or balanced for the translocated chromosomes) were warmed and transferred as single embryos. Genomewide aberrations, such as chaotic copy number signatures spanning the entire genome (gross aneuploidy), and anomalies of embryonic ploidy (triploidy, haploidy) are also indications for designating an embryo as unsuitable for transfer.

Statistical analysis

Continuous variables were presented as mean and standard deviation (SD) or median and interquartile range (IQR), as appropriate based on normality of the data. Categorical variables were presented as counts and proportions. T tests or Wilcoxon rank sum tests were performed for continuous variables comparison, and Chi-squared test or Fisher exact tests were used for categorical variables comparison. p-value < 0.05 was considered statistically significant. All analyses were conducted using STATA software.

Results

0PN and 1PN embryos have a low development potential

The outcomes of embryos classified as 0PN, 1PN and 2PN at fertilization check were analysed. There were 610 0PN, 167 1PN and 4091 2PN embryos in culture representing 12.44%, 3.41% and 83.46% of the 4902 successfully injected MIIs in the study (Table 1). Significantly less 0PNs and 1PNs develop into good quality blastocysts compared to 2PNs (5.41%, 21.56% vs. 56.51%, p-value < 0.001) (Table 1). PGT-SR was performed in 33 0PN and 36 1PN embryos in 54 of the 422 initiated cycles (12.8%) (Fig. 1). Basic information about the patients included in the study are shown in Table S1. By comparing the patients’ baseline information, we found that the most important characteristics of patients with PGT-SR compared to those with PGT-A and PGT-M are the younger age of the patients, the lower number of pregnancies, and the higher AMH (Supplementary Table 1, Additional File 1).

Table 1 Proportion of cultured embryos developing from 0PN, 1PN and 2PN zygotes
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Fig. 1
figure 1

Flow diagram of the study

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0PN and 1PN embryos have poor blastocyst ratings

As shown in Table 2, there is no significant distinction in Blastocyst expansion and inner cell mass between 0PN and 2PN (p-value = 0.4172; p-value = 0.1853) and between 1PN and 2PN (p-value = 0.6899; p-value = 0.4174).

Table 2 The day of embryo culture and blastocyst score
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On the day of embryo culture, compared with 2PN embryos, 0PN embryos developed to Day5 blastocysts more quickly (p-value = 0.01), more 1PN embryos arrived at the blastocyst at Day6, compared with 2PN, there were significant differences (p-value = 0.0002).

On trophectoderm development, there was no significant difference between 0PN and 2PN (p-value = 0.7558), but the score of trophectoderm development of 1PN embryo was significantly lower than that of 2PN embryo (p-value = 0.0092).

Genome-wide ploidy and haplotyping outcomes in 0PN, 1PN and 2PN derived embryos

In 54 cycles with either 0PN or 1PN embryos, a total of 33 0PN embryos, 36 1PN embryos, and 274 2PN embryos were tested successfully. The abnormal group included embryos with signatures of bi-maternal triploidy, gynogenesis, and aneuploidy, without these defects are considered Euploid embryos.

Of the 36 analysed 1PN embryos, 14 were found to be gynogenetic (38.89%), 18 to be aneuploidy (50.00%), and 4 to be Euploid (11.11%). Of the 33 analysed 0PN embryos, only one was gynogenetic (3.03%), 26 were aneuploidy (78.79%), and 6 were Euploid (18.18%). Of the 274 analysed 2PN embryos, none were gynogenetic, but two were triploid (0.73%), 181 were aneuploidy (66.06%), and 91 were euploid (33.21%) (Table 3).

Table 3 Chromosomal status of the blastocysts
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Euploid frequencies change considerably between 1PNs and 2PNs (11.11% vs. 33.21%, p-value = 0.004), but not between 0PNs and 2PNs (18.18% vs. 33.21%, p-value = 0.111). The rates of gynogenetic or triploid only change considerably between 1PNs and 2PNs (38.89% vs. 0.73%, p-value < 0.001), but not between 0PNs and 2PNs (3.03% vs. 0.73%, p-value = 0.290). We found that aneuploidy embryo rates do not differ significantly between the 0PN, 1PN, and 2PNs (78.79% 0PN, 50.00% 1PN, and 66.06% 2PN, p-value > 0.05) (Table 3). Developmental and morphological characteristics of 0PN/1PN embryos and subsequently transferred embryos have been provided in Supplementary Tables 2 and Supplementary Table 3, Additional File 1. The types of chromosome abnormalities and the information of embryos transferred for PGT-SR patient are shown in Table S1 and Table S2.

Cycle outcomes following the inclusion of 0PN and 1PN

The addition of 1PN and 0PN embryos increased the number of frozen embryos (p-value = 0.0629), transferable embryos (p-value = 0.4522), transplanted embryos (p-value = 0.5262), and transferred patients (p-value = 0.494) in the 54 cycles, but there was no significant change. After including 0PN and 1PN, there were three more live births, however, there was no significant increase (56.36% vs. 56.67%, p-value = 0.974) (Table 4).

Table 4 Cycle outcomes following the with or without of 0PN and 1PN
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At least one-fifth of the analyzed embryos developed from 0PN and 1PN zygotes in the 54 cycles. In one cycle, only 0PN embryos were available for genetic analysis. Unaffected embryos were transferred in 37 of the 42 cycles (88.09%) (Fig. 2A). Only because 0PN and 1PN embryos were diagnosed as unaffected, 5 of the 42 PGT-M cycles (11.90%) could reach embryo transfer. Four cycles (9.52%) proceeded to embryo transfer with 0PNs only. Five cycles (unavailable for analysis), which would not have the chance to transfer embryo, had 0PN and 1PN blastocysts (Fig. 2B).

Fig. 2
figure 2

Distribution of 0PN, 1PN and 2PN embryos in the PGT-SR cycles

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Discussion

The study showed that genome-wide haplotyping of 0PN and 1PN embryos that were developmentally competent prevented their routine inclusion in PGT-SR cycles. While transplantable euploid embryos were found in both types of embryos and live births were achieved after transplantation, including 0PN and 1PN embryos did not significantly increase the number of transplantable embryos. Additionally, there were already a large number of embryos in the PGT-SR population, making it unnecessary to select 0PN and 1PN embryos for implantation.

In this study, 10 embryos out of 36 1PN blastocysts and 33 0PN blastocysts were transplantable (14.49%), which was much lower than the rate for 2PN embryos (33.21%). This result indicates that in the PGT-SR population, 0PN and 1PN embryos need to pay more than twice the number of embryos to obtain transplantable embryos.

The present study contributes the first genome-wide dataset regarding the parental ploidy of 0PN, 1PN and 2PN embryos in PGT-SR cycles. In 38.89% of 1PN embryos, 3.03% of 0PN embryos, and none of the 2PN embryos, gynogenesis took place. This study’s incidence of gynogenesis was lower than that of previous studies, which found that the incidence of gynogenesis in 1PN after ICSI was 45.5% [29] and 57.14% [19]. This difference in incidence may be the result of an increase in the aneuploidy rate, which has been linked to a decrease in gynogenesis incidence. One embryo (3.33%) out of the 33 0PN embryos underwent gynogenesis; no triploid development took place. This finding differs from earlier research, which found that in Aspasia Destouni’s study, 2% of 0PN embryos developed triploidly. Of the 274 2PN embryos, 2 embryos (0.73%) developed Triploid, and no gynogenesis occurred. This suggests that the number of prokaryotes cannot be used by 0PN blastocysts as a proxy for proper fertilization, 0PN embryogenesis may be due to missing the prokaryotic observation period, and the probability of normal fertilization in 0PN blastocysts is the same as that in 2PN blastocysts.

The addition of 0PN and 1PN blastocysts enhanced the chance of transplantation by 5 cycles and 3 cycles of live birth out of the 54 cycles containing these blastocysts. Three viable births, with a 60% live birth rate, were achieved from five transplantations of 0PN and 1PN embryos following screening by genome-wide ploidy and haplotyping. This indicates that in cycles with 0PN and 1PN good quality blastocysts, genomewide haplotyping can benefit families in which the number of transferrable embryos is very limited by the underlying genetic status. The results are consistent with previous research [7, 19, 30]. In contrast to previous studies, the inclusion of 0PN and 1PN embryos greatly raised the success rate of PGT-M patients with 0PN and 1PN embryos; however, the success rate of PGT-SR patients was also improved but only slightly. This may be because the aneuploidy rate in PGT-SR patients increased and the number of transplantable embryos decreased, resulting in the inclusion of 0PN and 1PN embryos not significantly helping patients. In addition, the number of embryos obtained by PGT-SR patients was higher, with an average of nearly six 2PN embryos per cycle. Therefore, the inclusion of 0PN and 1PN embryos did not significantly increase the number of embryos detected.

Comparing to other investigations of PGT-A [31] and PGT-M [19] populations, the incidence of 0PN and 1PN embryos in PGT-SR patients, the culture procedure, and the blastocyst culture findings had similar results. We discovered that the prevalence of 0PN, 1PN, and 2PN fertilization is 12.44%, 3.41%, and 83.46%, respectively, through retrospective analysis of 4,902 successfully injected MII embryos. These findings showed that following ICIS fertilization, there was no difference in the frequency of abnormal fertilization between the PGT-SR and PGT-M populations, and that chromosome abnormalities did not increase the occurrence of abnormal fertilization, which are consistent with those from Destouni’s prior study of PGT-M populations [19].

Similar to the earlier study, 1PN and 0PN embryos showed relatively lower blastocyst formation frequencies than 2PN embryos [10, 12, 19, 31]. The growth ability of 0PN embryos was poor throughout the whole culture phase, and only 5.41% of 0PN embryos in this study were cultivated to the blastocyst stage. These data suggest that a significant proportion of 0PN embryos had incomplete or aberrant fertilization. In contrast to 0PN embryos, 74.85% of 1PN embryos could be cultured to Day3, but apoptosis would occur during continued culture. These results are consistent with the developmental characteristics of parthenogenetic oocytes reported in previous studies [32], which suggested there are a large number of parthenogenetic oocytes in 1PN embryos.

Our study presents the theory that patients who have an insufficient number of 2PN embryos obtained in PGT-SR (fewer than three) or who do not have 2PN embryos can be considered for the inclusion of 0PN and 1PN embryos, thus achieving live births and reducing their mental stress. Meanwhile, patients who have a sufficient number of 2PN embryos may not routinely include 0PN and 1PN embryos. Therefore, the results of this study may provide more valuable suggestions for clinical practice.

Conclusion

In summary, chromosome abnormalities did not increase the occurrence of abnormal fertilization. There were already a large number of embryos in the PGT-SR population, and routine inclusion of 0PN and 1PN embryos in the PGT-SR cycle is not recommended in this study. Priority should be given to the transfer of 2PN embryos. If a couple receives fewer than three 2PN embryos, or no 2PN embryos at all, it may be considered to include 0PN and 1PN embryos, with preference given to the use of 0PN. Furthermore, genome-wide ploidy and haplotyping are recommended for detection, and aneuploid and ploidy abnormalities are excluded.

Data availability

Data is provided within the manuscript or supplementary information files.

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Acknowledgements

Not applicable.

Funding

This research was supported by National Key Research and Development Program of China (2022YFC2703200), Guangxi key research and development plan project (No. AB22035080), Guangxi science and technology base and talent project (No. AC22080002), The Innovation Platform for Academicians of Hainan Province (YSPTZX202310), National Key Research and Development Program of China (2021YFC2700500; 2024YFC3406300; 2024YFC2706700; 2023YFC2705500), National Natural Science Foundation of China (82471751; 82171648; 82471701), Key R&D Program of Shandong Province, China (2023CXPT010; 2023ZLGX02), Medical and Health Development Program of Shandong Province (202201030147).

Author information

Author notes

  1. Jingzhen Wang and Hongqiang Xie contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Reproductive Medicine and Offspring Health, Center for Reproductive Medicine, Cheeloo College of Medicine, Institute of Women, Children and Reproductive Health, Shandong University, 157 Jingliu Road, Jinan, 250012, Shandong, China

    Jingzhen Wang, Hongqiang Xie, Yang Zou, Ming Gao, Lijuan Wang, Xiaowei Liu, Se-Xin Huang, Junhao Yan & Yuan Gao

  2. National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, 250012, Shandong, China

    Jingzhen Wang, Hongqiang Xie, Yang Zou, Ming Gao, Lijuan Wang, Xiaowei Liu, Se-Xin Huang, Junhao Yan & Yuan Gao

  3. Key Laboratory of Reproductive Endocrinology (Shandong University), Ministry of Education, Jinan, 250012, Shandong, China

    Jingzhen Wang, Hongqiang Xie, Yang Zou, Ming Gao, Lijuan Wang, Xiaowei Liu, Se-Xin Huang, Junhao Yan & Yuan Gao

  4. Shandong Technology Innovation Center for Reproductive Health, Jinan, 250012, Shandong, China

    Jingzhen Wang, Hongqiang Xie, Yang Zou, Ming Gao, Lijuan Wang, Xiaowei Liu, Se-Xin Huang, Junhao Yan & Yuan Gao

  5. Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, 250012, Shandong, China

    Jingzhen Wang, Hongqiang Xie, Yang Zou, Ming Gao, Lijuan Wang, Xiaowei Liu, Se-Xin Huang, Junhao Yan & Yuan Gao

  6. Shandong Key Laboratory of Reproductive Research and Birth Defect Prevention, Jinan, 250012, Shandong, China

    Jingzhen Wang, Hongqiang Xie, Yang Zou, Ming Gao, Lijuan Wang, Xiaowei Liu, Se-Xin Huang, Junhao Yan & Yuan Gao

  7. Research Unit of Gametogenesis and Health of ART-Offspring, Chinese Academy of Medical Sciences (No.2021RU001), Jinan, 250012, Shandong, China

    Jingzhen Wang, Hongqiang Xie, Yang Zou, Ming Gao, Lijuan Wang, Xiaowei Liu, Se-Xin Huang, Junhao Yan & Yuan Gao

Authors
  1. Jingzhen Wang
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  2. Hongqiang Xie
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  3. Yang Zou
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  4. Ming Gao
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  5. Lijuan Wang
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  6. Xiaowei Liu
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  7. Se-Xin Huang
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  8. Junhao Yan
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  9. Yuan Gao
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Contributions

JW is responsible for writing original draft, review and editing and validation; HX is responsible for formal analysis and data curation; YZ is responsible for Data curation and investigation; MG is responsible for conceptualization; LW is responsible for methodology; XL is responsible for software; SH is responsible for visualization; JY is responsible for funding acquisition; and YG is project administration and responsible for Supervision and resources.

Corresponding authors

Correspondence to Junhao Yan or Yuan Gao.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Ethics Committee of reproductive hospital affiliated to Shandong University. All the participants had the capacity to consent and we obtained the written informed consents. Our study adhered to the Declaration of Helsinki. We informed consent to participate was obtained from all of the participants in the study.

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No individual data is presented, and consent to publication is therefore not applicable.

Competing interests

The authors declare no competing interests.

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Wang, J., Xie, H., Zou, Y. et al. The use of blastocysts developing from nonpronuclear and monopronuclear zygotes can be considered in PGT-SR: a retrospective cohort study. BMC Pregnancy Childbirth 25, 530 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12884-025-07621-0

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12884-025-07621-0

Keywords

BMC Pregnancy and Childbirth

ISSN: 1471-2393

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