Abstract

Mammalian olfaction and reproduction are tightly linked, a link less explored in humans. Here, we asked whether human unexplained repeated pregnancy loss (uRPL) is associated with altered olfaction, and particularly altered olfactory responses to body-odor. We found that whereas most women with uRPL could identify the body-odor of their spouse, most control women could not. Moreover, women with uRPL rated the perceptual attributes of men's body-odor differently from controls. These pronounced differences were accompanied by an only modest albeit significant advantage in ordinary, non-body-odor-related olfaction in uRPL. Next, using structural and functional brain imaging, we found that in comparison to controls, most women with uRPL had smaller olfactory bulbs, yet increased hypothalamic response in association with men's body-odor. These findings combine to suggest altered olfactory perceptual and brain responses in women experiencing uRPL, particularly in relation to men's body-odor. Whether this link has any causal aspects to it remains to be explored.

Highlights

  • A remarkable ~50% of all human conceptions, and ~15% of documented human pregnancies, end in spontaneous miscarriage (Rai and Regan, 2006)

  • Consistent with the two former studies, as a group, control women were unable to identify their spouse above chance levels (chance = 33.3%, mean control = 28% ± 34%, Shapiro-Wilk test of normality (SW) = 0.77, p < 0.001, difference from chance: Wilcoxon W = 206, p = 0.18, effect size estimated by rank biserial correlation (RBC) = 1.17 (parametric comparison: t(32) = 0.88, p = 0.39, Cohen’s d = 0.15))

  • We found that women who experience unexplained repeated pregnancy loss (RPL) have an overwhelming advantage over controls at recognizing their spouse by smell, yet only a slight trend at most towards a general olfactory advantage

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Summary

Introduction

A remarkable ~50% of all human conceptions, and ~15% of documented human pregnancies, end in spontaneous miscarriage (Rai and Regan, 2006). Bruce-like effects have been hypothesized, not verified by manipulation, in lions (Bertram, 1975; Packer and Pusey, 1983), wild horses (Berger, 1983), dogs (Bartos et al, 2016), and primates (Pereira, 1983; Mori and Dunbar, 1985; Agoramoorthy et al, 1988; Colmenares and Gomendio, 1988). Of the latter, a comprehensive study observed pregnancy termination in ~80% of gelada baboon females following replacement of the dominant male (Roberts et al, 2012). We hypothesized that the olfactory system, and responses to men's body-odor, may be involved in human spontaneous miscarriage as well

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