Air pollution exposure in vitrified oocyte donors and male recipient partners in relation to fertilization and embryo quality

Abstract

Background

Studies on air pollution and outcomes of in vitro fertilization (IVF) have focused on couples undergoing autologous IVF, in which it is challenging to disentangle maternal and paternal exposures during gametogenesis. We sought to evaluate the independent associations between air pollution exposure during oogenesis and spermatogenesis on fertilization and embryo quality in non-identified donor oocyte IVF cycles.

Methods

Our study included 500 oocyte donors and 915 male recipient partners who contributed 1,095 oocyte thaw cycles (2008–2019). Daily ambient air pollutant exposure was estimated using spatio-temporal models based on residential address and averaged over folliculogenesis (i.e., three months prior to initiation of controlled ovarian stimulation), controlled ovarian stimulation, and spermatogenesis (i.e., 72 days prior to oocyte thaw). We used multivariable generalized estimating equations to estimate the adjusted odds ratios (aOR) and 95 % confidence intervals (CI) for an interquartile range increase in pollutant exposure in relation to the proportion of oocytes surviving thaw, oocytes fertilized, and usable embryos.

Results

Oocyte donors with higher exposure to organic carbon (OC) (aOR = 0.86 95 %CI 0.79,0.94) and particulate matter < 10 µm (aOR = 0.69 95 %CI 0.54,0.90) during folliculogenesis had a lower proportion of oocytes surviving thaw. During ovarian stimulation, higher particulate matter < 2.5 µm (aOR = 0.78 95 %CI 0.66, 0.91), nitrate (aOR = 0.83 95 % CI 0.69,0.99), and OC (aOR = 0.86 95 % CI 0.80,0.93) exposure was associated with a lower proportion of surviving oocytes while nitrogen dioxide (aOR = 1.11 95 %CI 1.00,1.23) and ozone (aOR = 1.19 95 %CI 1.04,1.37) exposure was associated with a higher proportion of fertilized oocytes and usable embryos. Elemental carbon (aOR = 0.93 95 %CI 0.87,1.00) and OC (aOR = 0.95 95 %CI 0.90,1.00) exposure during spermatogenesis was associated with a slightly lower proportion of usable embryos. On the day of oocyte thaw, higher ambient OC at the IVF clinic was associated with lower oocyte survival and higher ozone was associated with lower fertilization.

Conclusions

Both maternal and paternal air pollution exposures during gametogenesis have independent, largely detrimental, effects on early embryological outcomes.