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Table 4 The results and conclusions of the 24 studies included in the review

From: Effect of the time interval between oocyte retrieval and ICSI on embryo development and reproductive outcomes: a systematic review

Study Items Results Conclusions
Velde et al. (1998) [21] OPU-DN No difference in MOR, FR, and GER between groups ICSI should be delayed until the noon hour to observe fertilization in the following morning
DN-ICSI No difference in MOR, FR, and GER between groups
Yanagida et al. (1998) [22] OPU-DN The MOR, FR, CR, and PR were similar between groups. When incubated for > 9 h, the MOR was significantly decreased, while the PR showed a downward trend ICSI is performed at any time within 1–9 h following oocyte retrieval
Rienzi et al. (1998) [23] OPU-DN No differences in MOR, CR, and PR between groups. The FR and GER of the group with incubation time of < 3 h were significantly lower than those with incubation time of > 3 h The optimum time range between 3 and 12 h following oocyte retrieval can improve the fertilization rate and embryo quality
Andrews et al. (2001) [24] OPU-ICSI No differences in FR and LBR. The CR of the group incubated for < 3 h was superior to that incubated for > 5 h The shorter incubation durations (<  3 h) generally seemed to produce better results than longer ones (>  5 h)
Hassan et al. (2001) [2] OPU-DN The MOR, FR, BFR, and PR were significantly higher in the 4-h incubation group than those in the immediate DN group Aspects of nuclear, cytoplasmic maturation, and oolemma properties were improved when oocytes were preincubated with intact cumulus before DN rather than after DN
DN-ICSI No differences in FR, BFR, and PR between ICSI group without incubation and those 4 h following incubation.
Jacobs et al. (2001) [25] OPU-DN No significant differences in FR, GER, IR, and PR among all groups Incubation durations of 30 min to 6 h prior to ICSI did not improve the ICSI results. Should ICSI are needed in advance, no incubation is needed.
Ho et al. (2003) [26] OPU-DN The MOR in the group with an incubation time of < 2.5 h was significantly lower than that of > 2.5 h. No differences in FR, GER, and PR among all groups. Nuclear maturity of the oocytes with hCG administration 34 h earlier could be increased by incubation for 2.5 h before DN
Isiklar et al. (2004) [15] OPU-DN The MOR, FR, and GER of 2–4 h incubation group before DN were significantly higher than those of no incubation group. However, no differences in IR and PR between the two groups Pre-incubation of oocytes prior to ICSI is associated with improved maturation of oocytes, fertilization, and embryo quality
Falcone et al. (2008) [3] DN-ICSI With the extension of OPU-ICSI, the FR and CR were gradually increased, peaking at 5–6 h (3–4 h for DN-ICSI), and then gradually decreased with the extension of OPU-ICSI The most appropriate incubation time for mature oocytes before ICSI is 5–6 h
Boldi et al. (2010) [27] DN-ICSI No significant difference in FR between the two groups, however the GER, IR, and PR in the group within 1 h of DN-ICSI were significantly higher than those with 1–3 h of DN-ICSI Oocytes should be injected as soon as possible following cumulus removal to improve the ICSI outcome
Aletebi (2011) [4] OPU-DN
DN-ICSI
The MOR and FR of the 2-h group were significantly higher than those of the 1-h group; no incubation group before and after DN.
The PR of the 2-h group and 1-h group was similar and significantly higher than that of the no incubation group
It is preferable to allow an interval between oocyte retrieval and sperm injection
Patrat et al. (2012) [17] OPU-DN The total time of OPU-DN within 3 h had no effect on the MOR and GER. The FR gradually increased, the IR peaked at 1.5–2 h, and the PR reached a high value at approximately 2 h Incubation of oocytes approximately 2 h before DN may not increase MOR, however may lead to the optimal combination of FR and IR. Meanwhile, the sperm injection should be achieved without any delay following oocyte denudation to maintain good fertilization results
DN-ICSI DN-ICSI had no effect on MOR, GER, IR, and PR, however, FR gradually decreased within 3 h.
Esbert et al. (2013) [28] OPU-DN Compared with the 4-h incubation group before DN, the MOR in the 2-h incubation group was significantly lower, while the FR, GER, IR, and PR remained unchanged. Delaying denudation procedure resulted in a higher MOR, although did not influence clinical outcomes
Garor et al. (2015) [5] OPU-DN No impact on the FR and PR regardless of the hCG–OPU interval. Delaying oocyte denudation or sperm injection did not compensate for insufficient exposure to the follicular environment after hCG triggers before ovulatory oocyte maturation.
DN-ICSI No impact on the FR and PR regardless of the hCG–OPU interval.
Terasawa et al. (2016) [29] OPU-DN The FR in the DN group within 2 h of OPU was significantly higher than that in DN group of > 2 h Cumulus-oocyte complexes are recommended to be denuded soon after OPU in the case of ICSI
Ishikawa et al. (2016) [30] OPU-DN No significant differences in the MOR, FR, and BFR between the two groups, however, the rate of high-quality blastocysts was significantly increased after 2 h of incubation Oocyte culturing with cumulus cells for 2 h or longer improved the resulting blastocyst quality
Pereira et al. (2016) [31] OPU-DN The time of OPU-DN in the fertilization group was significantly longer than that in the non-fertilization group Modulating time intervals between OPU, DN, and ICSI to grant fertilization seems feasible
Bárcena et al. (2016) [19] OPU-DN No differences in FR, GER, PR, and LBR among all groups High-quality oocytes may withstand ageing in vitro to a certain extent, allowing for easier planning of laboratory workflow without a detrimental effect on the outcomes
DN-ICSI No differences in FR, GER, PR, and LBR among all groups
Pujol et al. (2018) [20] OPU-DN No effect on PR, continued pregnancy rate and LBR The PR diminishing was progressive as time OPU-ICSI increases. ICSI should not be delayed whenever possible.
DN-ICSI The PR decreased by 7.9%, when the DN-ICSI time was increased by 1 h, with no effect on LBR.
Mizuno et al. (2018) [16] OPU-DN No significant differences in MOR, FR, BFR, PR, and LBR between the two groups, but the high-quality blastocyst rate was significantly increased Intact cumulus cells should be maintained during the preincubation period, since they are essential to embryonic development post fertilization
Naji et al. (2018) [32] OPU-DN No significant difference, in MOR, FR, BFR, IR, PR, and LBR between different groups Oocyte denudation within 2 h or 2–5 h results in a comparable outcome, permitting more efficiency and flexibility in scheduling laboratory workload
Zhang et al. (2020) [33] DN-ICSI The FR increased with longer DN-ICSI interval within 5 h and declined with DN-ICSI interval > 5 h. The PR was significantly higher in DN-ICSI interval of < 4 h compared to that of > 4 h The optimal time for ICSI is within 4 h following oocyte denudation for excellent outcomes in ICSI cycles
Azizi et al. (2020) [34] OPU-DN Be was associated with cytoplasmic granulation and extended PVS of oocytes The time intervals in the ICSI cycle alters oocyte quality, with no significant impact on the reproductive outcomes
DN-ICSI The DN-ICSI was associated with oocytes cytoplasmic granulation. The FR, CR, and PR were not associated with the time intervals in ICSI cycles.
Maggiulli al. (2020) [35] IO-DN No effect on MOR, however, the BFR was decreased while IO-DN increased. IO-DN did not affect the cumulative live birth rate, but affected the BFR.
  1. IO Induction of ovulation, MOR Mature Oocyte Rate, FR Fertilisation Rate, CR Cleavage Rate, GER Good Embryo Rate, BFR Blastocyst Formation Rate, IR Implantation Rate, PR Pregnancy Rate, LBR Live Birth Rate