Childhood adversity impact on gut microbiota and inflammatory response to stress during pregnancy
Open accessAbstract
Background Adverse childhood experiences (ACEs), such as abuse or chronic stress, program an exaggerated adult inflammatory response to stress. Emerging rodent research suggests that the gut microbiome may be a key mediator in the association between early life stress and dysregulated glucocorticoid-immune response. However, ACE impact on inflammatory response to stress, or on the gut microbiome, have not been studied in human pregnancy, when inflammation increases risk of poor outcomes. The aim of this study was to assess the relationships among ACE, the gut microbiome, and cytokine response to stress in pregnant women.Methods Physically and psychiatrically healthy adult pregnant women completed the Adverse Childhood Experiences Questionnaire (ACE-Q) and gave a single stool sample between 20 and 26 weeks gestation. Stool DNA was isolated and 16S sequencing was performed. Three 24-hour food recalls were administered to assess dietary nutrient intake. A subset of women completed the Trier Social Stress Test (TSST) at 22-34 weeks gestation; plasma interleukin-6 (IL-6), interleukin-1β (IL-1β), high sensitivity C-reactive protein (hsCRP), tumor necrosis factor α (TNF-α), and cortisol were measured at four timepoints pre and post stressor, and area under the curve (AUC) was calculated.Results Forty-eight women completed the ACE-Q and provided stool; 19 women completed the TSST. Women reporting 2 or more ACEs (high ACE) had greater differential abundance of gut Prevotella than low ACE participants (q = 5.7 × 10^-13). Abundance of several gut taxa were significantly associated with cortisol, IL-6, TNF-α and CRP AUCs regardless of ACE status. IL-6 response to stress was buffered among high ACE women with high intake of docosahexaenoic acid (DHA) (p = 0.03) and eicosapentaenoic acid (EPA) (p = 0.05).Discussion Our findings suggest that multiple childhood adversities are associated with changes in gut microbiota composition during pregnancy, and such changes may contribute to altered inflammatory and glucocorticoid response to stress. While preliminary, this is the first study to demonstrate an association between gut microbiota and acute glucocorticoid-immune response to stress in a clinical sample. Finally, exploratory analyses suggested that high ACE women with high dietary intake of ω-3 polyunsaturated fatty acids (PUFAs) had a dampened inflammatory response to acute stress, suggesting potentially protective effects of ω-3s in this high-risk population. Given the adverse effects of inflammation on pregnancy and the developing fetus, mechanisms by which childhood adversity influence the gut-brain axis and potential protective factors such as diet should be further explored.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Maternal stress during pregnancy is associated with a distinct fecal microbiota profile.
“In addition, maternal stress during pregnancy display a distinct fecal microbiota profile (Hantsoo et al., 2019;Hechler et al., 2019), that has generational consequences.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Hantsoo et al., 2019
The Results (Gut Microbiome) report higher fecal Prevotella abundance in pregnant women with multiple adverse childhood experiences, supporting an association between earlier stress and a microbiota difference measured during pregnancy. But the exposure was childhood adversity, not maternal stress during pregnancy, and the study found no overall differences in microbiota diversity or community composition between groups. (LLM, conf=0.87)
Experimental — accuracy not yet measuredOther factors, such as epimutations, fetal reprogramming, and gut microbiome transfer, may induce intergenerational phenotypic changes.
“Importantly, in addition to epigenetic modifications, other factors, such as epimutations (an mutation occur at the epigenetic level), fetal reprogramming (266), and even gut microbiome transfer (267) may induce intergenerational phenotypic changes.”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [267]
The Conclusions report that childhood adversity was associated with differences in pregnant women’s gut microbiota, but do not address microbiome transfer or intergenerational phenotypic changes. Searches for maternal-to-offspring microbial transmission, microbiota transfer, and intergenerational effects found no passage establishing the point attributed to citation 267. (LLM, conf=0.74)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research
Buysse, D. J., Reynolds, C. F., Monk, T. H., Berman, S. R., & Kupfer, D. J. (1989) · Psychiatry Research · doi:10.1016/0165-1781(89)90047-4 · Cited by 35,234 · see citing works
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
A Global Measure of Perceived Stress
Cohen, S., Kamarck, T., & Mermelstein, R. (1983) · Journal of Health and Social Behavior · doi:10.2307/2136404 · Cited by 32,807 · see citing works
Search and clustering orders of magnitude faster than BLAST
Edgar, R. C. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq461 · Cited by 20,617 · see citing works
Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., Koss, M. P., & Marks, J. S. (1998) · American Journal of Preventive Medicine · doi:10.1016/s0749-3797(98)00017-8 · Cited by 18,943 · cited 1× · see citing works
“The ACE-Q is a well validated scale that has been used in numerous studies to assess exposure to adversity before the age of 18 and associations with later health outcomes (Felitti et al., 1998).”
MethodFastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
Price, M. N., Dehal, P. S., & Arkin, A. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009490 · Cited by 14,894 · see citing works
Detection of Postnatal Depression: Development of the 10-item Edinburgh Postnatal Depression Scale
Cox, J. L., Holden, J. M., & Sagovsky, R. (1987) · British Journal of Psychiatry · doi:10.1192/bjp.150.6.782 · Cited by 14,183 · see citing works
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
Lozupone, C., & Knight, R. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8228-8235.2005 · Cited by 8,227 · see citing works
Linking long-term dietary patterns with gut microbial enterotypes
Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.-Y., Keilbaugh, S. A., Bewtra, M., Knights, D., Walters, W. A., Knight, R., et al. (2011) · Science · doi:10.1126/science.1208344 · Cited by 6,513 · see citing works
Self-citationKirschbaum, C., Pirke, K.-M., & Hellhammer, D. H. (2008) · Neuropsychobiology · doi:10.1159/000119004 · Cited by 6,093 · see citing works
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J.-J., Blugeon, S., Bridonneau, C., Furet, J.-P., Corthier, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804812105 · Cited by 4,413 · see citing works
Host Remodeling of the Gut Microbiome and Metabolic Changes during Pregnancy
Koren, O., Goodrich, J. K., Cullender, T. C., Spor, A., Laitinen, K., Kling Bäckhed, H., Gonzalez, A., Werner, J. J., Angenent, L. T., Knight, R., et al. (2012) · Cell · doi:10.1016/j.cell.2012.07.008 · Cited by 2,165 · see citing works
Miller, G. E., Chen, E., & Parker, K. J. (2011) · Psychological Bulletin · doi:10.1037/a0024768 · Cited by 1,785 · see citing works
Childhood maltreatment predicts adult inflammation in a life-course study
Danese, A., Pariante, C. M., Caspi, A., Taylor, A., & Poulton, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610362104 · Cited by 1,264 · see citing works
The maternal microbiota drives early postnatal innate immune development
Gomez de Agüero, M., Ganal-Vonarburg, S. C., Fuhrer, T., Rupp, S., Uchimura, Y., Li, H., Steinert, A., Heikenwalder, M., Hapfelmeier, S., Sauer, U., et al. (2016) · Science · doi:10.1126/science.aad2571 · Cited by 1,231 · see citing works
Linking the Human Gut Microbiome to Inflammatory Cytokine Production Capacity
Schirmer, M., Smeekens, S. P., Vlamakis, H. C., Jaeger, M., Oosting, M., Franzosa, E. A., ter Horst, R., Jansen, T., Jacobs, L., Bonder, M. J., et al. (2016) · Cell · doi:10.1016/j.cell.2016.10.020 · Cited by 1,159 · see citing works
Temporal and spatial variation of the human microbiota during pregnancy
DiGiulio, D. B., Callahan, B. J., McMurdie, P. J., Costello, E. K., Lyell, D. J., Robaczewska, A., Sun, C. L., Goltsman, D. S. A., Wong, R. J., Shaw, G., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1502875112 · Cited by 1,129 · see citing works
Bailey, M. T., Dowd, S. E., Galley, J. D., Hufnagle, A. R., Allen, R. G., & Lyte, M. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.023 · Cited by 1,123 · see citing works
Kubany, E. S., Leisen, M. B., Kaplan, A. S., Watson, S. B., Haynes, S. N., Owens, J. A., & Burns, K. (2000) · Psychological Assessment · doi:10.1037/1040-3590.12.2.210 · Cited by 1,102 · cited 4× · see citing works
“Participants completed additional rating scales including Traumatic Life Events Questionnaire (TLEQ) (Kubany et al., 2000), Spielberger State Trait Anxiety Inventory (STAI; State -”
MethodInfluentialO'Mahony, S. M., Marchesi, J. R., Scully, P., Codling, C., Ceolho, A.-M., Quigley, E. M. M., Cryan, J. F., & Dinan, T. G. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.06.026 · Cited by 1,069 · see citing works
Suganami, T., Nishida, J., & Ogawa, Y. (2005) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000183883.72263.13 · Cited by 1,056 · see citing works
Caughey, G. E., Mantzioris, E., Gibson, R. A., Cleland, L., & James, M. (1996) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/63.1.116 · Cited by 860 · see citing works
IBD—what role do Proteobacteria play?
Mukhopadhya, I., Hansen, R., El-Omar, E. M., & Hold, G. L. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.14 · Cited by 810 · see citing works
Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers.
Ferrucci, L., Cherubini, A., Bandinelli, S., Bartali, B., Corsi, A., Lauretani, F., Martin, A., Andres-Lacueva, C., Senin, U., & Guralnik, J. M. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1303 · Cited by 696 · see citing works
Gut microbiome composition is linked to whole grain-induced immunological improvements
Martínez, I., Lattimer, J. M., Hubach, K. L., Case, J. A., Yang, J., Weber, C. G., Louk, J. A., Rose, D. J., Kyureghian, G., Peterson, D. A., et al. (2013) · The ISME Journal · doi:10.1038/ismej.2012.104 · Cited by 614 · see citing works
Marzi, M., Viganò, M., Trabattoni, D., Villa, M. L., SALVAGGIO, A., Clerici, E., & Clerici, M. (1996) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1996.d01-809.x · Cited by 613 · see citing works
Carpenter, L. L., Carvalho, J. P., Tyrka, A. R., Wier, L. M., Mello, A. F., Mello, M. F., Anderson, G. M., Wilkinson, C. W., & Price, L. H. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.05.002 · Cited by 564 · see citing works
Schommer, N. C., Hellhammer, D. H., & Kirschbaum, C. (2003) · Psychosomatic Medicine · doi:10.1097/01.psy.0000035721.12441.17 · Cited by 561 · see citing works
Optimizing methods and dodging pitfalls in microbiome research
Kim, D. J., Hofstaedter, C. E., Zhao, C., Mattei, L. M., Tanes, C., Clarke, E., Lauder, A. P., Sherrill-Mix, S. A., Chehoud, C., Kelsen, J. R., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0267-5 · Cited by 536 · see citing works
Self-citationGanesh, B. P., Klopfleisch, R., Loh, G., & Blaut, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074963 · Cited by 522 · see citing works
Narayan, A. J., Rivera, L. M., Bernstein, R. E., Harris, W. W., & Lieberman, A. (2017) · International Journal of Child Abuse & Neglect · doi:10.1016/j.chiabu.2017.09.022 · Cited by 512 · see citing works
The microbiome: a key regulator of stress and neuroinflammation
Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.03.001 · Cited by 508 · see citing works
Association between plasma IL-6 response to acute stress and early-life adversity in healthy adults
Carpenter, L. L., Gawuga, C. E., Tyrka, A. R., Lee, J. K., Anderson, G. M., & Price, L. H. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.159 · Cited by 464 · see citing works
The Macaque Gut Microbiome in Health, Lentiviral Infection, and Chronic Enterocolitis
McKenna, P. M., Hoffmann, C., Minkah, N. K., Aye, P. P., Lackner, A. A., Liu, Z. Z., Lozupone, C., Hamady, M., Knight, R. D., & Bushman, F. D. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.0040020 · Cited by 438 · see citing works
Fava, F., Gitau, R., Griffin, B. A., Gibson, G. R., Tuohy, K. M., & Lovegrove, J. A. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.33 · Cited by 435 · see citing works
Kiecolt-Glaser, J. K., Gouin, J.-P., Weng, N.-P., Malarkey, W. B., Beversdorf, D. Q., & Glaser, R. (2011) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31820573b6 · Cited by 430 · see citing works
Early-life adversity and cortisol response to social stress: a meta-analysis
Bunea, I. M., Szentágotai-Tătar, A., & Miu, A. C. (2017) · Translational Psychiatry · doi:10.1038/s41398-017-0032-3 · Cited by 392 · see citing works
Fast food fever: reviewing the impacts of the Western diet on immunity
Myles, I. A. (2014) · Nutrition Journal · doi:10.1186/1475-2891-13-61 · Cited by 390 · see citing works
López‐García, E., Schulze, M. B., Manson, J. E., Meigs, J. B., Albert, C. M., Rifai, N., Willett, W. C., & Hu, F. B. (2004) · Journal of Nutrition · doi:10.1093/jn/134.7.1806 · Cited by 378 · see citing works
Stressful early life experiences and immune dysregulation across the lifespan
Fagundes, C. P., Glaser, R., & Kiecolt-Glaser, J. K. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.06.014 · Cited by 371 · see citing works
Ajuwon, K. M., & Spurlock, M. E. (2005) · The Journal of Nutrition · doi:10.1093/jn/135.8.1841 · Cited by 343 · see citing works
Jašarević, E., Howerton, C. L., Howard, C. D., & Bale, T. L. (2015) · Endocrinology · doi:10.1210/en.2015-1177 · Cited by 329 · see citing works
Self-citationLovallo, W. R. (2013) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2012.10.006 · Cited by 315 · see citing works
Taylor, S. E., Lehman, B. J., Kiefe, C. I., & Seeman, T. E. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.016 · Cited by 296 · see citing works
Rallidis, L. S., Paschos, G., Liakos, G. K., Velissaridou, A. H., Anastasiadis, G., & Zampelas, A. (2003) · Atherosclerosis · doi:10.1016/s0021-9150(02)00427-6 · Cited by 288 · see citing works
Kato-Kataoka, A., Nishida, K., Takada, M., Kawai, M., Kikuchi-Hayakawa, H., Suda, K., Ishikawa, H., Gondo, Y., Shimizu, K., Matsuki, T., et al. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.04134-15 · Cited by 288 · see citing works
Lovallo, W., Farag, N. H., Sorocco, K., Cohoon, A. J., & Vincent, A. S. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.018 · Cited by 274 · see citing works
Christian, L. M., & Porter, K. M. (2014) · Cytokine · doi:10.1016/j.cyto.2014.06.018 · Cited by 268 · see citing works
Jašarević, E., Howard, C. D., Misic, A. M., Beiting, D. P., & Bale, T. L. (2017) · Scientific Reports · doi:10.1038/srep44182 · Cited by 262 · see citing works
Self-citationConnection Between BMI-Related Plasma Metabolite Profile and Gut Microbiota
Ottosson, F. A., Brunkwall, L., Ericson, U., Nilsson, P. M., Almgren, P., Fernandez, C., Melander, O., & Orho‐Melander, M. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-02114 · Cited by 246 · see citing works
Kiecolt-Glaser, J. K., Belury, M. A., Andridge, R., Malarkey, W. B., Hwang, B. S., & Glaser, R. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.05.011 · Cited by 233 · see citing works
Pusceddu, M. M., El Aidy, S., Crispie, F., O’Sullivan, O., Cotter, P., Stanton, C., Kelly, P., Cryan, J. F., & Dinan, T. G. (2015) · PLOS ONE · doi:10.1371/journal.pone.0139721 · Cited by 214 · see citing works
Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.12.021 · Cited by 213 · see citing works
Depressive symptoms, omega-6:omega-3 fatty acids, and inflammation in older adults.
Kiecolt-Glaser, J. K., Belury, M. A., Porter, K., Beversdorf, D. Q., Lemeshow, S., & Glaser, R. (2007) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3180313a45 · Cited by 212 · see citing works
The microbiome in posttraumatic stress disorder and trauma-exposed controls: an exploratory study
Hemmings, S. M. J., Malan-Müller, S., van den Heuvel, L. L., Demmitt, B. A., Stanislawski, M. A., Smith, D. G., Bohr, A. D., Stamper, C. E., Hyde, E. R., Morton, J. T., et al. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000512 · Cited by 208 · see citing works
Knowles, S. R., Nelson, E. A., & Palombo, E. A. (2008) · Biological Psychology · doi:10.1016/j.biopsycho.2007.09.010 · Cited by 192 · see citing works
Slopen, N., Lewis, T. T., Gruenewald, T. L., Mujahid, M. S., Ryff, C. D., Albert, M. A., & Williams, D. R. (2010) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181e9c16f · Cited by 190 · see citing works
Pace, T. W. W., Wingenfeld, K., Schmidt, I., Meinlschmidt, G., Hellhammer, D. H., & Heim, C. M. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2011.07.232 · Cited by 184 · see citing works
Early childhood adversity and pregnancy outcomes
Smith, M. V., Gotman, N., & Yonkers, K. A. (2016) · Maternal and Child Health Journal · doi:10.1007/s10995-015-1909-5 · Cited by 175 · see citing works
Microbiome, HPA Axis and Production of Endocrine Hormones in the Gut
Sudo, N. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0897-4_8 · Cited by 167 · see citing works
Sorokin, Y., Romero, R., Mele, L., Wapner, R., Iams, J., Dudley, D., Spong, C., Peaceman, A., Leveno, K., Harper, M., et al. (2010) · American Journal of Perinatology · doi:10.1055/s-0030-1249366 · Cited by 154 · see citing works
Fatigue, Inflammation, and ω-3 and ω-6 Fatty Acid Intake Among Breast Cancer Survivors
Alfano, C. M., Imayama, I., Neuhouser, M. L., Kiecolt‐Glaser, J. K., Smith, A. W., Meeske, K., McTiernan, A., Bernstein, L., Baumgartner, K. B., Ulrich, C. M., et al. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2011.36.4109 · Cited by 153 · see citing works
Poole, J. C., Dobson, K. S., & Pusch, D. (2017) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.03.047 · Cited by 145 · see citing works
Childhood adversities and distress - The role of resilience in a representative sample
Beutel, M. E., Tibubos, A. N., Klein, E. M., Schmutzer, G., Reiner, I., Kocalevent, R., & Brähler, E. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173826 · Cited by 145 · see citing works
Macfarlane, S., Cleary, S., Bahrami, B., Reynolds, N., & Macfarlane, G. T. (2013) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.12453 · Cited by 144 · see citing works
Voellmin, A., Winzeler, K., Hug, E., Wilhelm, F. H., Schaefer, V., Gaab, J., La Marca, R., Pruessner, J. C., & Bader, K. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.09.008 · Cited by 144 · see citing works
Haghiac, M., Yang, X.-H., Presley, L. H., Smith, S., Dettelback, S., Minium, J., Belury, M. A., Catalano, P. M., & Mouzon, S. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137309 · Cited by 140 · see citing works
González, A., Jenkins, J. M., Steiner, M. S., & Fleming, A. S. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.08.012 · Cited by 136 · see citing works
Lindsay, K. L., Buß, C., Wadhwa, P. D., & Entringer, S. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.021 · Cited by 135 · see citing works
Childhood Abuse and Inflammatory Responses to Daily Stressors
Gouin, J.-P., Glaser, R., Malarkey, W. B., Beversdorf, D., & Kiecolt-Glaser, J. K. (2012) · Annals of Behavioral Medicine · doi:10.1007/s12160-012-9386-1 · Cited by 130 · see citing works
Adverse childhood experiences are associated with spontaneous preterm birth: a case-control study
Christiaens, I., Hegadoren, K., & Olson, D. M. (2015) · BMC Medicine · doi:10.1186/s12916-015-0353-0 · Cited by 130 · see citing works
Adverse childhood experiences and chronic hypothalamic–pituitary–adrenal activity
Kalmakis, K. A., Meyer, J. S., Chiodo, L. M., & Leung, K. (2015) · Stress · doi:10.3109/10253890.2015.1023791 · Cited by 129 · see citing works
Röytiö, H., Mokkala, K., Vahlberg, T., & Laitinen, K. (2017) · British Journal Of Nutrition · doi:10.1017/s0007114517002100 · Cited by 128 · see citing works
Shea, A. K., Streiner, D. L., Fleming, A. S., Kamath, M. V., Broad, K., & Steiner, M. S. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.07.006 · Cited by 118 · see citing works
Maes, M., Christophe, A., Bosmans, E., Lin, A., & Neels, H. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00268-1 · Cited by 118 · see citing works
García‐Ródenas, C. L., Bergonzelli, G. E., Nutten, S., Schumann, A., Cherbut, C., Turini, M., Ornstein, K., Rochat, F., & Corthésy‐Theulaz, I. (2006) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/01.mpg.0000226376.95623.9f · Cited by 114 · see citing works
Stress-Induced Inflammatory Responses in Women
Christian, L. M., Glaser, R., Porter, K. M., & Iams, J. D. (2013) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31829bbc89 · Cited by 111 · see citing works
Suzuki, A., Poon, L., Papadopoulos, A. S., Kumari, V., & Cleare, A. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.09.007 · Cited by 102 · see citing works
Lower subjective social status exaggerates interleukin-6 responses to a laboratory stressor
Derry, H. M., Fagundes, C. P., Andridge, R., Glaser, R., Malarkey, W. B., & Kiecolt‐Glaser, J. K. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.026 · Cited by 102 · see citing works
Bublitz, M. H., & Stroud, L. R. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.01.009 · Cited by 88 · see citing works
Maki, P. M., Mordecai, K. L., Rubin, L. H., Sundermann, E., Savarese, A., Eatough, E., & Drogos, L. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.023 · Cited by 87 · cited 1× · see citing works
“Cortisol responder status was also calculated as a secondary measure of HPA axis response (Herbison et al., 2016; Maki et al., 2015; Schommer et al., 2003); cortisol responders were defined as those participants with a positive change from baseline to peak.”
Measures of adiposity predict interleukin-6 responses to repeated psychosocial stress
McInnis, C. M., Thoma, M. V., Gianferante, D., Hanlin, L. C., Chen, X., Breines, J. G., Hong, S., & Rohleder, N. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.07.018 · Cited by 87 · see citing works
Ehrlich, K. B., Ross, K. M., Chen, E., & Miller, G. E. (2016) · Development and Psychopathology · doi:10.1017/s0954579416000845 · Cited by 84 · see citing works
Kumsta, R., Schlotz, W., Golm, D., Moser, D., Kennedy, M., Knights, N., Kreppner, J., Maughan, B., Rutter, M. L., & Sonuga-Barke, E. J. S. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.09.021 · Cited by 78 · see citing works
Childhood abuse is associated with increased hair cortisol levels among urban pregnant women
Schreier, H. M. C., Enlow, M. B., Ritz, T., Gennings, C., & Wright, R. J. (2015) · Journal of Epidemiology & Community Health · doi:10.1136/jech-2015-205541 · Cited by 74 · see citing works
Gillespie, S. L., Porter, K. M., & Christian, L. M. (2016) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2016.02.001 · Cited by 73 · see citing works
Miller, G. E., Culhane, J. F., Grobman, W. A., Simhan, H. N., Williamson, D. E., Adam, E. K., Buß, C., Entringer, S., Kim, K. A., García‐España, J. F., et al. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.04.018 · Cited by 61 · see citing works
Bowers, K. A., Ding, L., Gregory, S. M., Yolton, K. A., Ji, H., Meyer, J. S., Ammerman, R. T., Ginkel, J. B. V., & Folger, A. T. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.05.024 · Cited by 59 · see citing works
Biomarkers of inflammation and placental dysfunction are associated with subsequent preterm birth
Bastek, J. A., Brown, A. G., Anton, L., Srinivas, S. K., D'addio, A., & Elovitz, M. A. (2010) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2010.511340 · Cited by 56 · see citing works
Self-citationPreadolescent Adversity Programs a Disrupted Maternal Stress Reactivity in Humans and Mice
Morrison, K. E., Epperson, C. N., Sammel, M. D., Ewing, G., Podcasy, J., Hantsoo, L. V., Kim, D. R., & Bale, T. L. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.08.027 · Cited by 54 · see citing works
Self-citationAttachment security moderates the link between adverse childhood experiences and cellular aging
Dagan, O., Asok, A., Steele, H., Steele, M., & Bernard, K. (2017) · Development and Psychopathology · doi:10.1017/s0954579417001705 · Cited by 50 · see citing works
Herbison, C. E., Henley, D., Marsh, J. A., Atkinson, H. C., Newnham, J. P., Matthews, S. G., Lye, S. J., & Pennell, C. E. (2016) · Stress · doi:10.3109/10253890.2016.1146672 · Cited by 49 · see citing works
Christian, L. M., Blair, L. M., Porter, K. M., Lower, M., Cole, R. M., & Belury, M. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148752 · Cited by 46 · see citing works
Association Between Fatty Acid Supplementation and Prenatal Stress in African Americans
Keenan, K. E., Hipwell, A. E., Bortner, J., Hoffmann, A. M., & McAloon, R. L. (2014) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000000559 · Cited by 42 · see citing works
Pearce, B. D., Grove, J., Bonney, E. A., Bliwise, N. G., Dudley, D. J., Schendel, D., & Thorsen, P. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000284949 · Cited by 42 · see citing works
Gouin, J., Caldwell, W., Woods, R., & Malarkey, W. B. (2017) · Annals of Behavioral Medicine · doi:10.1007/s12160-017-9891-3 · Cited by 41 · see citing works
Mitchell, A. M., Porter, K. M., & Christian, L. M. (2017) · Health Psychology · doi:10.1037/hea0000559 · Cited by 39 · see citing works
Lager, S., Ramirez, V. I., Acosta, O. M., Meireles, C. L., Miller, E., Gaccioli, F., Rosario, F. J., Gelfond, J. A. L., Hakala, K. W., Weintraub, S. T., et al. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-01384 · Cited by 39 · see citing works
Childhood stress and birth timing among African American women: cortisol as biological mediator
Gillespie, S. L., Christian, L. M., Alston, A. D., & Salsberry, P. J. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.06.009 · Cited by 38 · cited 1× · see citing works
“, 2016), and recent work suggests maternal cortisol (Gillespie et al., 2017) or elevated baseline interleukin (IL)-6 (Miller et al.”
BackgroundBublitz, M. H., Parade, S. H., & Stroud, L. R. (2014) · Biological Psychology · doi:10.1016/j.biopsycho.2014.08.014 · Cited by 38 · see citing works
Atta, D. S., Girbash, E. F., Abdelwahab, S. M., Abdeldayem, H. M., Ibrahim, T., & Ghonaim, R. A. (2015) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2015.1127342 · Cited by 25 · see citing works
Tell, D., Mathews, H. L., Burr, R. L., & Janusek, L. W. (2018) · Stress · doi:10.1080/10253890.2018.1424132 · Cited by 17 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- First MB, Spitzer RL, Gibbon M, Williams JBW, 2002 Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-patient Edition (SCID-I/NP) Biometrics Research, New York State Psychiatric Institute, New York.
- Spielberger C, Gorsuch R, Lushene R, 1983 The State-Trait Anxiety. Inventory: Test manual. Consulting Psychologist Press.
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
The HPA axis dysregulation in severe mental illness: Can we shift the blame to gut microbiota?
Misiak, B., Łoniewski, I., Marlicz, W., Frydecka, D., Szulc, A., Rudzki, L., & Samochowiec, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109951 · Cited by 343 · see citing works
Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma
Jiang, S., Postovit, L., Cattaneo, A., Binder, E. B., & Aitchison, K. J. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00808 · Cited by 288 · see citing works
Braveman, P., Dominguez, T. P., Burke, W., Dolan, S. M., Stevenson, D. K., Jackson, F. M., Collins, J. W., Driscoll, D. A., Haley, T., Acker, J., et al. (2021) · Frontiers in Reproductive Health · doi:10.3389/frph.2021.684207 · Cited by 189 · see citing works
Cowan, C. S. M., Dinan, T. G., & Cryan, J. F. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13156 · Cited by 176 · see citing works
Spichak, S., Bastiaanssen, T. F. S., Berding, K., Vlckova, K., Clarke, G., Dinan, T. G., & Cryan, J. F. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.044 · Cited by 127 · see citing works
Neurodevelopmental pathways in bipolar disorder
Kloiber, S., Rosenblat, J. D., Husain, M. I., Ortiz, A., Berk, M., Quevedo, J., Vieta, E., Maes, M., Birmaher, B., Soares, J. C., et al. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.005 · Cited by 122 · see citing works
A preliminary study of gut microbiome variation and HPA axis reactivity in healthy infants
Rosin, S., Xia, K., Azcarate-Peril, M. A., Carlson, A. L., Propper, C. B., Thompson, A. L., Grewen, K., & Knickmeyer, R. C. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.105046 · Cited by 74 · see citing works
Robinson, J. M., & Breed, M. F. (2020) · Science of The Total Environment · doi:10.1016/j.scitotenv.2020.137626 · Cited by 30 · see citing works
Zhang, X., Wang, H., Kilpatrick, L. A., Dong, T. S., Gee, G. C., Labus, J. S., Osadchiy, V., Beltran-Sanchez, H., Wang, M. C., Vaughan, A., et al. (2023) · Nature Mental Health · doi:10.1038/s44220-023-00134-9 · Cited by 20 · see citing works
- Authors
- Hantsoo, L., Jašarević, E., Criniti, S., McGeehan, B., Tanes, C., Sammel, M. D., Elovitz, M. A., Compher, C., Wu, G., & Epperson, C. N.
- Affiliations
- University of Pennsylvania (US)
- University of Maryland, Baltimore (US)
- Children's Hospital of Philadelphia (US)
- Corresponding author
- Hantsoo, Liisa
- ORCID
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2019-01
- Volume
- 75
- Pages
- 240-250
- ISSN
- 0889-1591 (ISSN-L)
- PMC
- PMC6349044
- OpenAlex
- W2898944101
- Cited by
- 156
- References
- 102
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 23 · 2023: 24 · 2022: 21 · 2021: 26 · 2020: 22 · 2019: 12
- FWCI
- 5.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Pennsylvania Health System
- National Institute of Mental Health (P50MH099910, K23MH107831)
- National Institute of Nursing Research (R01NR014784)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12HD085848)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- adverse childhood experiences, gut microbiota, pregnancy, cytokines, interleukin-6, omega-3 polyunsaturated fatty acids, docosahexaenoic acid, eicosapentaenoic acid, dietary intake, Prevotella, cortisol, C-reactive protein, Trier Social Stress Test, early life stress
- MeSH terms
- Gastrointestinal Microbiome, Adverse Childhood Experiences, Adult, C-Reactive Protein, Diet, Fatty Acids, Unsaturated, Feces, Female, Humans, Hydrocortisone, Inflammation, Pregnancy, RNA, Ribosomal, 16S, Stress, Psychological, Tumor Necrosis Factor-alpha, Fatty Acids, Omega-3, Interleukin-6, Cytokines, Interleukin-1beta
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
