Comparing disgust sensitivity in women in early pregnancy and non-pregnant women in the follicular and luteal phases of the menstrual cycle

Behavioral immune system (BIS) is considered an important mechanism protecting individuals against pathogens. It makes people avoid other individuals or objects displaying pathogen cues (Schaller & Duncan, 2007). The affective part of the BIS, which triggers the avoidant reaction, is the emotion of disgust.

Examining the function of BIS, Fessler and Navarrete (2003) formulated the Compensatory Prophylaxis Hypothesis (CPH), which they first proposed in the context of hormonal changes during the menstrual cycle. As the levels of progesterone, a hormone that has been shown to have immunosuppressive effects (Miyaura & Iwata, 2002), peak in the luteal phase of the menstrual cycle (Farage, Neill, & MacLean, 2009), the authors expected disgust sensitivity to be elevated in this phase to compensate for the insufficient immune system activity. Nevertheless, they observed no difference in disgust sensitivity between the follicular and luteal phases based on the self-reported date of the last menstruation (Fessler & Navarrete, 2003).

Further research testing the CPH provided conflicting results. In line with Fessler and Navarrete (2003), several other studies found no support for the CPH, including a longitudinal study by Timmers, Bossio, and Chivers (2018) based on sexual video stimuli of pathogen-related disgust, and a cross-sectional study by Olatunji, Cox, and Li (2020) using disgust-inducing video stimuli. Similarly to Fessler and Navarrete (2003), both these studies used the date of the last menstruation to determine the cycle phase. Moreover, the CPH was not supported by a recent longitudinal study, which used ovulation tests to determine the cycle phase and tested the women five times throughout the cycle (Stern & Shiramizu, 2022).

On the other hand, there are studies which did find support for the CPH. Two longitudinal studies using ovulation tests to determine the cycle phase observed higher disgust sensitivity in the luteal phase compared to menstruation (Żelaźniewicz, Borkowska, Nowak, & Pawłowski, 2016) or to the follicular phase (Miłkowska, Galbarczyk, Klimek, Zabłocka-Słowińska and Jasienska, 2021). In addition, a cross-sectional study showed that in women who recently had an infection, women in the luteal phase had higher disgust sensitivity than women in the follicular phase (Miłkowska, Galbarczyk, & Jasienska, 2019).

While comparing disgust sensitivity at different phases of the menstrual cycle is one way to test the CPH, other authors adopted a more direct approach, examining the association between progesterone and disgust sensitivity levels in naturally cycling women. In their cross-sectional study, Fleischman and Fessler (2011) found a positive correlation between salivary progesterone levels and disgust sensitivity measured at different phases of the menstrual cycle. In addition, a longitudinal study by Żelaźniewicz et al. (2016) observed a positive correlation between serum progesterone levels and disgust sensitivity in the luteal phase of the cycle but not during menstruation. However, multiple studies report no association between salivary progesterone and disgust sensitivity, using a longitudinal (Jones et al., 2018; Stern & Shiramizu, 2022; Timmers et al., 2018) and cross-sectional (Rafiee, Jones, & Shiramizu, 2022) design.

The inconsistencies in the existing research may be attributed to several methodological factors. While most studies compared disgust sensitivity in the follicular and luteal phases, some compared the luteal phase with menstruation (Żelaźniewicz et al., 2016). The method of determining the cycle phase may also play a role; some studies used only calendar-based methods, determining the cycle phase based on the date of the last menstruation (Fessler & Navarrete, 2003; Olatunji et al., 2020; Timmers et al., 2018). However, the calendar-based methods have been found to be inaccurate, and should therefore not be used as the sole indicator of the cycle phase (Wideman, Montgomery, Levine, Beynnon, & Shultz, 2013). Also, the methods used to measure disgust sensitivity vary across the studies, with some studies using questionnaires such as the Disgust Scale-Revised (Fessler & Navarrete, 2003; Żelaźniewicz et al., 2016) or the Three Domains of Disgust Scale (Jones et al., 2018; Miłkowska et al., 2019; Miłkowska et al., 2021; Rafiee et al., 2022; Stern & Shiramizu, 2022), while others using visual (image) (Fleischman & Fessler, 2011) or video stimuli (Olatunji et al., 2020; Timmers et al., 2018). Different methods for measuring disgust sensitivity may elicit varying intensities of the disgust response, which may lead to inconsistent results. Additionally, a majority of longitudinal studies (Miłkowska et al., 2021; Stern & Shiramizu, 2022; Żelaźniewicz et al., 2016) used questionnaires to measure disgust; however, questionnaires may have lower accuracy when administered repeatedly in a short period of time.

The CPH has also been tested in the context of immune system changes during pregnancy. The authors of the first study that tested the CPH in a sample of pregnant women hypothesized that disgust sensitivity would be elevated in the first trimester (Fessler, Eng, & Navarrete, 2005), as early pregnancy was then considered a period of immunosuppression, necessary to tolerate the semi-allogeneic fetus. They indeed observed higher disgust sensitivity in the first trimester compared to other trimesters (Fessler et al., 2005). In line with their results, Żelaźniewicz and Pawłowski (2015) found that disgust sensitivity was highest in the first trimester compared to other pregnancy phases and the postpartum period in their longitudinal study. Nevertheless, the view of early pregnancy as a state of immunosuppression has since been challenged by the evidence that the first trimester is characterized by immunomodulation rather than immunosuppression (Hedman et al., 2020; Peterson et al., 2020; Racicot, Kwon, Aldo, Silasi, & Mor, 2014). Moreover, the assumption that disgust sensitivity is highest in the first trimester has been called into question as well. For example, a recent longitudinal study found that disgust sensitivity increased throughout pregnancy (Dlouhá, Roberts, Hlaváčová, Nouzová, & Kaňková, 2023). This study however provided support for the CPH with the finding that in the first trimester, women who recently had an infection experienced higher disgust sensitivity than those who had not.

A recent study by Kaňková et al. (2022) examined the associations between disgust sensitivity and immune system activity in pregnancy directly by linking disgust to cytokine levels. The authors found that disgust sensitivity was negatively correlated with both pro- and anti-inflammatory serum cytokine levels in the first trimester, suggesting that disgust may compensate for insufficient immune modulation in early pregnancy. In line with these findings, Kaňková et al. (2023) reported significant negative correlations between disgust sensitivity and free β-human chorionic gonadotropin (hCG) levels. This hormone plays a role in establishing pregnancy-induced immune tolerance (Schumacher et al., 2013); for example, it has been shown to have a positive effect on the increase of regulatory T-cells (Furcron et al., 2016). Therefore, it is possible that due to their insufficient immunomodulation, pregnant women with lower hCG levels might need increased protection for their more vulnerable fetus, which is manifested in their increased disgust sensitivity.

Although it seems that the first trimester is not characterized by mere immunosuppression, but rather by modulations of the immune response, disgust sensitivity may still have a protective function during the first trimester, a period crucial for organogenesis and extremely sensitive to negative disruptions (Fessler et al., 2005; Miao et al., 2021; Weinhold, 2009). In line with this assumption, a study by Kaňková et al. (2023) showed that women in the first trimester displayed higher disgust sensitivity when exposed to a greater pathogen risk, such as the Covid-19 pandemic.

While a number of studies focused on disgust sensitivity in pregnant or non-pregnant women, no study has compared disgust levels between pregnant and non-pregnant women so far. Nevertheless, in order to examine the ability to recognize pathogen threat, Jones et al. (2005) compared pregnant and non-pregnant women, as well as non-pregnant women in the follicular and luteal phases, in terms of their attraction to faces based on their apparent health. The authors found that women in the luteal phase were more attracted to healthy faces than women in the follicular phase, and pregnant women were more attracted to healthy faces than non-pregnant women.

To fill the gap in the previous research, this study aimed to compare pregnant and non-pregnant women in terms of their disgust sensitivity, while examining whether disgust sensitivity differs in the luteal and follicular phases in non-pregnant women, using the ultrasound method to determine the phase of the cycle. As the above-mentioned inconsistencies in the previous research might be due to the different methods for measuring disgust, we employed the two most frequently used questionnaires (the Disgust Scale-Revised and the Three Domains of Disgust Scale) to be able to compare the results obtained by these questionnaires. In line with the CPH, we hypothesized that pregnant women in the first trimester would experience higher disgust sensitivity than non-pregnant controls, as they need increased protection in this period critical for organogenesis. In addition, we expected that women in the luteal phase of the menstrual cycle would display higher disgust sensitivity compared to those in the follicular phase, because the luteal phase is associated with both higher progesterone levels and with the preparation of the body for potential pregnancy.

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