Association between Disgust Sensitivity during Pregnancy and Endogenous Steroids: A Longitudinal Study
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
20-16698S
Czech Science Foundation
DRO (Institute of Endocrinology-EÚ, 00023761
Czech Ministry of Health
PubMed
38999978
PubMed Central
PMC11241696
DOI
10.3390/ijms25136857
PII: ijms25136857
Knihovny.cz E-zdroje
- Klíčová slova
- 7α/β-hydroxy-androgens, DHEA, androstenediol, behavioral immune system, cortisol, disgust, estrogens, pregnancy, steroids, testosterone,
- MeSH
- dospělí MeSH
- lidé MeSH
- longitudinální studie MeSH
- mladý dospělý MeSH
- odpor * MeSH
- prospektivní studie MeSH
- první trimestr těhotenství MeSH
- steroidy krev MeSH
- těhotenství MeSH
- třetí trimestr těhotenství krev MeSH
- Check Tag
- dospělí MeSH
- lidé MeSH
- mladý dospělý MeSH
- těhotenství MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- steroidy MeSH
The emotion of disgust protects individuals against pathogens, and it has been found to be elevated during pregnancy. Physiological mechanisms discussed in relation to these changes include immune markers and progesterone levels. This study aimed to assess the association between steroids and disgust sensitivity in pregnancy. Using a prospective longitudinal design, we analyzed blood serum steroid concentrations and measured disgust sensitivity via text-based questionnaires in a sample of 179 pregnant women during their first and third trimesters. We found positive correlations between disgust sensitivity and the levels of C19 steroids (including testosterone) and its precursors in the Δ5 pathway (androstenediol, DHEA, and their sulfates) and the Δ4 pathway (androstenedione). Additionally, positive correlations were observed with 5α/β-reduced C19 steroid metabolites in both trimesters. In the first trimester, disgust sensitivity was positively associated with 17-hydroxypregnanolone and with some estrogens. In the third trimester, positive associations were observed with cortisol and immunoprotective Δ5 C19 7α/β-hydroxy-steroids. Our findings show that disgust sensitivity is positively correlated with immunomodulatory steroids, and in the third trimester, with steroids which may be related to potential maternal-anxiety-related symptoms. This study highlights the complex relationship between hormonal changes and disgust sensitivity during pregnancy.
Zobrazit více v PubMed
Schaller M., Duncan L.A. The behavioral immune system: Its evolution and social psychological implications. In: Forgas J.P., Haselton M.G., von Hippel W., editors. Evolution and the Social Mind: Evolutionary Psychology and Social Cognition. Routledge/Taylor & Francis Group; Abingdon, UK: 2007. pp. 293–307. DOI
Curtis V., Aunger R., Rabie T. Evidence that disgust evolved to protect from risk of disease. Proc. Biol. Sci. 2004;271((Suppl. S4)):S131–S133. doi: 10.1098/rsbl.2003.0144. PubMed DOI PMC
Rozin P., Fallon A.E. A perspective on disgust. Psychol. Rev. 1987;94:23–41. doi: 10.1037/0033-295X.94.1.23. PubMed DOI
Stevenson R.J., Oaten M.J., Case T.I., Repacholi B.M., Wagland P. Children’s response to adult disgust elicitors: Development and acquisition. Dev. Psychol. 2010;46:165–177. doi: 10.1037/a0016692. PubMed DOI
Al-Shawaf L., Lewis D.M.G., Buss D.M. Sex Differences in Disgust: Why Are Women More Easily Disgusted Than Men? Emot. Rev. 2018;10:149–160. doi: 10.1177/1754073917709940. DOI
Stevenson R.J., Case T.I., Oaten M.J. Frequency and recency of infection and their relationship with disgust and contamination sensitivity. Evol. Hum. Behav. 2009;30:363–368. doi: 10.1016/j.evolhumbehav.2009.02.005. DOI
Kankova S., Takács L., Krulova M., Hlavacova J., Nouzova K., Hill M., Vcelak J., Monk C. Disgust sensitivity is negatively associated with immune system activity in early pregnancy: Direct support for the Compensatory Prophylaxis Hypothesis. Evol. Hum. Behav. 2022;43:234–241. doi: 10.1016/j.evolhumbehav.2022.02.001. DOI
Kankova S., Takacs L., Hlavacova J., Calda P., Monk C., Havlicek J. Disgust sensitivity in early pregnancy as a response to high pathogen risk. Front. Psychol. 2023;14:1015927. doi: 10.3389/fpsyg.2023.1015927. PubMed DOI PMC
Fessler D.M., Navarrete C.D. Elevated disgust sensitivity in the first trimester of pregnancy-Evidence supporting prophylaxis the compensatory hypothesis. Evol. Hum. Behav. 2005;26:344–351. doi: 10.1016/j.evolhumbehav.2004.12.001. DOI
Dlouha D., Roberts S.C., Hlavacova J., Nouzova K., Kankova S. Longitudinal changes in disgust sensitivity during pregnancy and the early postpartum period, and the role of recent health problems. Sci. Rep. 2023;13:4752. doi: 10.1038/s41598-023-31060-6. PubMed DOI PMC
Ille R., Schoggl H., Kapfhammer H.P., Arendasy M., Sommer M., Schienle A. Self-disgust in mental disorders–symptom-related or disorder-specific? Compr. Psychiatry. 2014;55:938–943. doi: 10.1016/j.comppsych.2013.12.020. PubMed DOI
Olatunji B.O. Changes in disgust correspond with changes in symptoms of contamination-based OCD: A prospective examination of specificity. J. Anxiety Disord. 2010;24:313–317. doi: 10.1016/j.janxdis.2010.01.003. PubMed DOI
Fessler D.M., Navarrete C.D. Domain-specific variation in disgust sensitivity across the menstrual cycle. Evol. Hum. Behav. 2003;24:406–417. doi: 10.1016/S1090-5138(03)00054-0. DOI
Miyaura H., Iwata M. Direct and indirect inhibition of Th1 development by progesterone and glucocorticoids. J. Immunol. 2002;168:1087–1094. doi: 10.4049/jimmunol.168.3.1087. PubMed DOI
Olatunji B.O., Cox R.C., Li I. Disgust regulation between menstrual cycle phases: Differential effects of emotional suppression and reappraisal. J. Behav. Ther. Exp. Psychiatry. 2020;68:101543. doi: 10.1016/j.jbtep.2019.101543. PubMed DOI
Dlouha D., Ullman J., Takacs L., Nouzova K., Hrbackova H., Seda J., Kankova S. Comparing disgust sensitivity in women in early pregnancy and non-pregnant women in the follicular and luteal phases of the menstrual cycle. Evol. Hum. Behav. 2024;45:164–174. doi: 10.1016/j.evolhumbehav.2024.01.006. DOI
Timmers A.D., Bossio J.A., Chivers M.L. Disgust, sexual cues, and the prophylaxis hypothesis. Evol. Psychol. Sci. 2018;4:179–190. doi: 10.1007/s40806-017-0127-3. DOI
Stern J., Shiramizu V. Hormones, ovulatory cycle phase and pathogen disgust: A longitudinal investigation of the Compensatory Prophylaxis Hypothesis. Horm. Behav. 2022;138:105103. doi: 10.1016/j.yhbeh.2021.105103. PubMed DOI
Rafiee Y., Jones B.C., Shiramizu V. Is pathogen disgust increased on days of the menstrual cycle when progesterone is high? Evidence from a between-subjects study using estimated progesterone levels. Adapt. Hum. Behav. Physiol. 2023;9:26–36. doi: 10.1007/s40750-022-00208-5. DOI
Zelazniewicz A., Borkowska B., Nowak J., Pawlowski B. The progesterone level, leukocyte count and disgust sensitivity across the menstrual cycle. Physiol. Behav. 2016;161:60–65. doi: 10.1016/j.physbeh.2016.04.002. PubMed DOI
Milkowska K., Galbarczyk A., Klimek M., Zablocka-Slowińska K., Jasienska G. Pathogen disgust, but not moral disgust, changes across the menstrual cycle. Evol. Hum. Behav. 2021;42:402–408. doi: 10.1016/j.evolhumbehav.2021.03.002. DOI
Milkowska K., Galbarczyk A., Jasienska G. Disgust sensitivity in relation to menstrual cycle phase in women with and without an infection. Am. J. Hum. Biol. 2019;31:e23233. doi: 10.1002/ajhb.23233. PubMed DOI
Liu M., Zhang X., He Z., Liang Y., Zou B., Ma X., Gu S., Wang F. Opposite effects of estradiol and progesterone on woman’s disgust processing. Front. Psychiatry. 2023;14:1161488. doi: 10.3389/fpsyt.2023.1161488. PubMed DOI PMC
Fleischman D.S., Fessler D.M. Progesterone’s effects on the psychology of disease avoidance: Support for the compensatory behavioral prophylaxis hypothesis. Horm. Behav. 2011;59:271–275. doi: 10.1016/j.yhbeh.2010.11.014. PubMed DOI
Conway C.A., Jones B.C., DeBruine L.M., Welling L.L., Law Smith M.J., Perrett D.I., Sharp M.A., Al-Dujaili E.A. Salience of emotional displays of danger and contagion in faces is enhanced when progesterone levels are raised. Horm. Behav. 2007;51:202–206. doi: 10.1016/j.yhbeh.2006.10.002. PubMed DOI
Kamboj S.K., Krol K.M., Curran H.V. A specific association between facial disgust recognition and estradiol levels in naturally cycling women. PLoS ONE. 2015;10:e0122311. doi: 10.1371/journal.pone.0122311. PubMed DOI PMC
Kavaliers M., Bishnoi I.R., Ossenkopp K.P., Choleris E. Differential effects of progesterone on social recognition and the avoidance of pathogen threat by female mice. Horm. Behav. 2021;127:104873. doi: 10.1016/j.yhbeh.2020.104873. PubMed DOI
Bressan P., Kramer P. Progesterone does raise disgust. Horm. Behav. 2022;137:104937. doi: 10.1016/j.yhbeh.2021.104937. PubMed DOI
Jones B., Hahn A., Fisher C., Wang H., Kandrik M., Lee A., Tybur J., DeBruine L. Hormonal correlates of pathogen disgust: Testing the compensatory prophylaxis hypothesis. Evol. Hum. Behav. 2018;39:166–169. doi: 10.1016/j.evolhumbehav.2017.12.004. DOI
Zelazniewicz A., Pawlowski B. Disgust in pregnancy and fetus sex–longitudinal study. Physiol. Behav. 2015;139:177–181. doi: 10.1016/j.physbeh.2014.11.032. PubMed DOI
Racicot K., Kwon J.Y., Aldo P., Silasi M., Mor G. Understanding the complexity of the immune system during pregnancy. Am. J. Reprod. Immunol. 2014;72:107–116. doi: 10.1111/aji.12289. PubMed DOI PMC
Hove C., Trumble B.C., Anderson A.S., Stieglitz J., Kaplan H., Gurven M.D., Blackwell A.D. Immune function during pregnancy varies between ecologically distinct populations. Evol. Med. Public Health. 2020;2020:114–128. doi: 10.1093/emph/eoaa022. PubMed DOI PMC
Abu-Raya B., Michalski C., Sadarangani M., Lavoie P.M. Maternal Immunological Adaptation During Normal Pregnancy. Front. Immunol. 2020;11:575197. doi: 10.3389/fimmu.2020.575197. PubMed DOI PMC
Kankova S., Hlavacova J., Roberts K., Benesova J., Havlicek J., Calda P., Dlouha D., Roberts S.C. Associations between nausea and vomiting in pregnancy, disgust sensitivity, and first-trimester maternal serum free beta-hCG and PAPP-A. Horm. Behav. 2023;152:105360. doi: 10.1016/j.yhbeh.2023.105360. PubMed DOI
Gerdes A.B., Uhl G., Alpers G.W. Spiders are special: Fear and disgust evoked by pictures of arthropods. Evol. Hum. Behav. 2009;30:66–73. doi: 10.1016/j.evolhumbehav.2008.08.005. DOI
Cisler J.M., Olatunji B.O., Lohr J.M. Disgust sensitivity and emotion regulation potentiate the effect of disgust propensity on spider fear, blood-injection-injury fear, and contamination fear. J. Behav. Ther. Exp. Psychiatry. 2009;40:219–229. doi: 10.1016/j.jbtep.2008.10.002. PubMed DOI PMC
Marzillier S., Davey G. Anxiety and disgust: Evidence for a unidirectional relationship. Cogn. Emot. 2005;19:729–750. doi: 10.1080/02699930441000436. DOI
Silva M.M.J., Nogueira D.A., Clapis M.J., Leite E. Anxiety in pregnancy: Prevalence and associated factors. Rev. Esc. Enferm. USP. 2017;51:e03253. doi: 10.1590/s1980-220x2016048003253. PubMed DOI
Fava G.A., Grandi S., Michelacci L., Saviotti F., Conti S., Bovicelli L., Trombini G., Orlandi C. Hypochondriacal fears and beliefs in pregnancy. Acta Psychiatr. Scand. 1990;82:70–72. doi: 10.1111/j.1600-0447.1990.tb01358.x. PubMed DOI
Odent M. Fear of death during labour. Midwifery Today Int. Midwife. 2003;67:20–22. doi: 10.1080/02646839108403655. PubMed DOI
Shlomi Polachek I., Huller Harari L., Baum M., Strous R.D. Postpartum anxiety in a cohort of women from the general population: Risk factors and association with depression during last week of pregnancy, postpartum depression and postpartum PTSD. Isr. J. Psychiatry Relat. Sci. 2014;51:128–134. PubMed
Sterzl I., Hill M., Starka L., Velikova M., Kanceva R., Jemelkova J., Czernekova L., Kosztyu P., ZadraZil J., Matousovic K., et al. Patients with IgA nephropathy have altered levels of immunomodulatory C19 steroids. Glucocorticoid therapy with addition of adrenal androgens may be the choice. Physiol. Res. 2017;66:S433–S442. doi: 10.33549/physiolres.933732. PubMed DOI
Honcu P., Hill M., Bicikova M., Jandova D., Velikova M., Kajzar J., Kolatorova L., Bestak J., Macova L., Kancheva R., et al. Activation of Adrenal Steroidogenesis and an Improvement of Mood Balance in Postmenopausal Females after Spa Treatment Based on Physical Activity. Int. J. Mol. Sci. 2019;20:3687. doi: 10.3390/ijms20153687. PubMed DOI PMC
Olatunji B.O., Williams N.L., Tolin D.F., Abramowitz J.S., Sawchuk C.N., Lohr J.M., Elwood L.S. The Disgust Scale: Item analysis, factor structure, and suggestions for refinement. Psychol. Assess. 2007;19:281–297. doi: 10.1037/1040-3590.19.3.281. PubMed DOI
Tybur J., Lieberman D., Griskevicius V. Microbes, Mating, and Morality: Individual Differences in Three Functional Domains of Disgust. Psychiatry Investig. 2009;12:538–544. doi: 10.1037/a0015474. PubMed DOI
Erbay L.G., Kartalci S. Neurosteroid Levels in Patients with Obsessive-Compulsive Disorder. Psychiatry Investig. 2015;12:538–544. doi: 10.4306/pi.2015.12.4.538. PubMed DOI PMC
Luu-The V. Assessment of steroidogenesis and steroidogenic enzyme functions. J. Steroid Biochem. Mol. Biol. 2013;137:176–182. doi: 10.1016/j.jsbmb.2013.05.017. PubMed DOI
Lephart E.D. Brain 5alpha-reductase: Cellular, enzymatic, and molecular perspectives and implications for biological function. Mol. Cell Neurosci. 1993;4:473–484. doi: 10.1006/mcne.1993.1059. PubMed DOI
Celotti F., Melcangi R.C., Martini L. The 5 alpha-reductase in the brain: Molecular aspects and relation to brain function. Front. Neuroendocrinol. 1992;13:163–215. PubMed
Coutinho A.E., Chapman K.E. The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol. Cell Endocrinol. 2011;335:2–13. doi: 10.1016/j.mce.2010.04.005. PubMed DOI PMC
Bottasso O., Bay M.L., Besedovsky H., del Rey A. The immuno-endocrine component in the pathogenesis of tuberculosis. Scand. J. Immunol. 2007;66:166–175. doi: 10.1111/j.1365-3083.2007.01962.x. PubMed DOI
Du C., Khalil M.W., Sriram S. Administration of dehydroepiandrosterone suppresses experimental allergic encephalomyelitis in SJL/J mice. J. Immunol. 2001;167:7094–7101. doi: 10.4049/jimmunol.167.12.7094. PubMed DOI
Rontzsch A., Thoss K., Petrow P.K., Henzgen S., Brauer R. Amelioration of murine antigen-induced arthritis by dehydroepiandrosterone (DHEA) Inflamm. Res. 2004;53:189–198. doi: 10.1007/s00011-003-1244-y. PubMed DOI
Tan X.D., Dou Y.C., Shi C.W., Duan R.S., Sun R.P. Administration of dehydroepiandrosterone ameliorates experimental autoimmune neuritis in Lewis rats. J. Neuroimmunol. 2009;207:39–44. doi: 10.1016/j.jneuroim.2008.11.011. PubMed DOI
Choi I.S., Cui Y., Koh Y.A., Lee H.C., Cho Y.B., Won Y.H. Effects of dehydroepiandrosterone on Th2 cytokine production in peripheral blood mononuclear cells from asthmatics. Korean J. Intern. Med. 2008;23:176–181. doi: 10.3904/kjim.2008.23.4.176. PubMed DOI PMC
Sudo N., Yu X.N., Kubo C. Dehydroepiandrosterone attenuates the spontaneous elevation of serum IgE level in NC/Nga mice. Immunol. Lett. 2001;79:177–179. doi: 10.1016/S0165-2478(01)00285-1. PubMed DOI
Kasperska-Zajac A., Brzoza Z., Rogala B. Dehydroepiandrosterone and dehydroepiandrosterone sulphate in atopic allergy and chronic urticaria. Inflammation. 2008;31:141–145. doi: 10.1007/s10753-008-9059-1. PubMed DOI
Sterzl I., Hampl R., Sterzl J., Votruba J., Starka L. 7 β-OH-DHEA counteracts dexamethasone induced suppression of primary immune response in murine spleenocytes. J. Steroid Biochem. Mol. Biol. 1999;71:133–137. doi: 10.1016/S0960-0760(99)00134-X. PubMed DOI
Romagnani S., Kapsenberg M., Radbruch A., Adorini L. Th1 and Th2 cells. Res. Immunol. 1998;149:871–873. doi: 10.1016/S0923-2494(99)80016-9. PubMed DOI
Pratschke S., von Dossow-Hanfstingl V., Dietz J., Schneider C.P., Tufman A., Albertsmeier M., Winter H., Angele M.K. Dehydroepiandrosterone modulates T-cell response after major abdominal surgery. J. Surg. Res. 2014;189:117–125. doi: 10.1016/j.jss.2014.02.002. PubMed DOI
Pettersson H., Lundqvist J., Norlin M. Effects of CYP7B1-mediated catalysis on estrogen receptor activation. Biochim. Biophys. Acta. 2010;1801:1090–1097. doi: 10.1016/j.bbalip.2010.05.011. PubMed DOI
Tang W., Eggertsen G., Chiang J.Y., Norlin M. Estrogen-mediated regulation of CYP7B1: A possible role for controlling DHEA levels in human tissues. J. Steroid Biochem. Mol. Biol. 2006;100:42–51. doi: 10.1016/j.jsbmb.2006.02.005. PubMed DOI
Ahlem C.N., Page T.M., Auci D.L., Kennedy M.R., Mangano K., Nicoletti F., Ge Y., Huang Y., White S.K., Villegas S., et al. Novel components of the human metabolome: The identification, characterization and anti-inflammatory activity of two 5-androstene tetrols. Steroids. 2011;76:145–155. doi: 10.1016/j.steroids.2010.10.005. PubMed DOI
Reading C.L., Frincke J.M., White S.K. Molecular targets for 17alpha-ethynyl-5-androstene-3beta,7beta,17beta-triol, an anti-inflammatory agent derived from the human metabolome. PLoS ONE. 2012;7:e32147. doi: 10.1371/journal.pone.0032147. PubMed DOI PMC
Hill M., Parizek A., Cibula D., Kancheva R., Jirasek J.E., Jirkovska M., Velikova M., Kubatova J., Klimkova M., Paskova A., et al. Steroid metabolome in fetal and maternal body fluids in human late pregnancy. J. Steroid Biochem. Mol. Biol. 2010;122:114–132. doi: 10.1016/j.jsbmb.2010.05.007. PubMed DOI
AbdulHussain G., Azizieh F., Makhseed M., Raghupathy R. Effects of Progesterone, Dydrogesterone and Estrogen on the Production of Th1/Th2/Th17 Cytokines by Lymphocytes from Women with Recurrent Spontaneous Miscarriage. J. Reprod. Immunol. 2020;140:103132. doi: 10.1016/j.jri.2020.103132. PubMed DOI
Folstad I., Karter A.J. Parasites, bright males, and the immunocompetence handicap. Am. Nat. 1992;139:603–622. doi: 10.1086/285346. DOI
Meulenberg P.M., Hofman J.A. Maternal testosterone and fetal sex. J. Steroid Biochem. Mol. Biol. 1991;39:51–54. doi: 10.1016/0960-0760(91)90012-T. PubMed DOI
Cisler J.M., Olatunji B.O., Lohr J.M. Disgust, fear, and the anxiety disorders: A critical review. Clin. Psychol. Rev. 2009;29:34–46. doi: 10.1016/j.cpr.2008.09.007. PubMed DOI PMC
Olatunji B.O., Armstrong T., Elwood L. Is Disgust Proneness Associated With Anxiety and Related Disorders? A Qualitative Review and Meta-Analysis of Group Comparison and Correlational Studies. Perspect. Psychol. Sci. 2017;12:613–648. doi: 10.1177/1745691616688879. PubMed DOI
Giltay E.J., Enter D., Zitman F.G., Penninx B.W., van Pelt J., Spinhoven P., Roelofs K. Salivary testosterone: Associations with depression, anxiety disorders, and antidepressant use in a large cohort study. J. Psychosom. Res. 2012;72:205–213. doi: 10.1016/j.jpsychores.2011.11.014. PubMed DOI
Soto-Balbuena C., Rodriguez M.F., Escudero Gomis A.I., Ferrer Barriendos F.J., Le H.N., Pmb-Huca G. Incidence, prevalence and risk factors related to anxiety symptoms during pregnancy. Psicothema. 2018;30:257–263. doi: 10.7334/psicothema2017.379. PubMed DOI
Hill M., Hana V., Jr., Velikova M., Parizek A., Kolatorova L., Vitku J., Skodova T., Simkova M., Simjak P., Kancheva R., et al. A method for determination of one hundred endogenous steroids in human serum by gas chromatography-tandem mass spectrometry. Physiol. Res. 2019;68:179–207. doi: 10.33549/physiolres.934124. PubMed DOI
Trygg J., Wold S. Orthogonal projections to latent structures (O-PLS) J. Chemom. 2002;16:119–128. doi: 10.1002/cem.695. DOI