Embryological, clinical and ultrastructural study of human oocytes presenting indented zona pellucida

Abstract

Human oocyte dysmorphisms attain a large proportion of retrieved oocytes from assisted reproductive technology (ART) treatment cycles. Extracytoplasmic defects involve abnormal morphology of the zona pellucida (ZP), perivitelline space and first polar body. The aim of the present study was to describe a novel dysmorphism affecting the ZP, indented ZP. We also evaluated the clinical, embryological and ultrastructural features of these cases. We evaluated all ART treatment cycles during 7 consecutive years and found 13 treatment cycles (six patients) with all oocytes presenting an indented ZP. In addition, these oocytes presented total or partial absence of the perivitelline space, absence of resistance to ZP and oolemma penetration during microinjection, and low ooplasm viscosity during aspiration. This novel described dysmorphism was recurrent and attained all oocytes in three cases that had more than one treatment cycle. When compared with controls, data showed significant low oocyte maturity (42% versus 81.6%) and high cycle cancellation (30.8% versus 8.5%) rates, normal degeneration (3.4% versus 6.3%) and fertilization rates (69% versus 69.5%), and low pregnancy (15.4% versus 33.3%) and live-birth delivery (7.7% versus 27.7%) rates per cycle. Ultrastructure analysis revealed a zona pellucida structure with large empty electrolucent regions, an outer ZP layer with an indented surface with protuberances and a thick inner ZP that obliterated the perivitelline space. There was evidence of exocytosis of ZP material by the oocyte. In conclusion, oocytes with this novel described dysmorphism (indented ZP) are associated with low maturity, pregnancy and live-birth delivery rates.

Fertilization and embryo quality of mature oocytes with specific morphological abnormalities

“…Extracytoplasmic defects include abnormal morphology of the ZP, the PVS, and first PB. Morphological abnormalities of the ZP include a thick, indented, or dark ZP, and can emerge differently in different IVF cycles with the same woman [ 16 28 29 ]. This type of oocyte presents with a total or partial absence of the PVS, an absence of resistance to ZP and oolemma penetration during ICSI, and low ooplasm viscosity during aspiration [ 16 ].…”

“…Pregnancy rates from oocytes with specific single abnormalities are difficult to assess because a typical embryo transfer includes mixed embryos generated from normal and dysmorphic oocytes. Nonetheless, a poor pregnancy rate has been reported in oocytes with cytoplasmic granularity [ 14 ], cytoplasmic inclusions [ 8 9 10 14 ], an indented ZP [ 16 ], oval shape [ 30 31 ], a dark ZP [ 11 ], and an abnormal ZP [ 16 ], compared with those without such anomalies.…”

“…Poor FR has been reported in oocytes with cytoplasmic inclusions [ 8 9 10 ], vacuoles [ 6 10 ], refractile bodies [ 1 6 ], dark ZP [ 11 ], a large PVS [ 6 12 13 ], and abnormal PB [ 6 7 ]. Nonetheless, a relatively good FR was also reported in oocytes exhibiting cytoplasmic inclusions [ 14 ], refractile bodies [ 10 ], a dark ZP [ 10 15 ], a large PVS [ 16 ], debris in the PVS [ 15 17 ], and an abnormal PB [ 15 18 19 ].…”

Embryological Characteristics and Clinical Outcomes of Oocytes with Heterogeneous Zona Pellucida During Assisted Reproduction Treatment: A Retrospective Study

“…Mei Li et al found that the immaturity rate is significantly higher in the abnormal ZP group compared with controls [ 18 ]. Recently, Sousa et al also showed oocytes with indented ZP appear to have only a 42% maturity rate, versus 81.2% for normal oocytes [ 27 ]. It appears that oocytes fail to reach the MII stage because of 4 main reasons: (1) genetic defects, (2) abnormal meiotic recombination, (3) abnormal microfilament action, and (4) failure to produce key cell cycle regulating factors [ 28 ].…”

Ultrastructural and cytogenetic analyses of mature human oocyte dysmorphisms with respect to clinical outcomes

“…cytoplasmic and nuclear maturity [4][5][6][7][8]. Therefore, numerous factors have been referred as relevant for oocyte competence such as zona pellucida (ZP) morphology [9][10][11][12]; polar body morphology, and chromosome constitution [13][14][15][16][17][18]; metaphase spindle [19][20][21]; chromosome constitution [1,2,7,22]; oocyte DNA damage and repair [22]; cytoplasmic viscosity and resistance to membrane penetration during intracytoplasmic sperm injection (ICSI) [7,23,24]; oocyte shape [7,25,26]; mitochondria aggregation patterns [27,28]; diverse extracytoplasmic and intracytoplasmic inclusions [5][6][7][8]; and abnormal expressed genes [29][30][31][32].…”