Adverse childhood experiences, low self-esteem, and salient stimulus response in eating disorders.
anorexia nervosa
biological
bulimia nervosa
neuroimaging
Journal
European eating disorders review : the journal of the Eating Disorders Association
ISSN: 1099-0968
Titre abrégé: Eur Eat Disord Rev
Pays: England
ID NLM: 9436977
Informations de publication
Date de publication:
13 Feb 2024
13 Feb 2024
Historique:
revised:
11
11
2023
received:
07
08
2023
accepted:
09
01
2024
medline:
13
2
2024
pubmed:
13
2
2024
entrez:
13
2
2024
Statut:
aheadofprint
Résumé
Adverse childhood experiences (ACEs) are elevated in individuals with eating disorders (EDs), but how the neurobiology of EDs and ACEs interact is unclear. Women 18-45 years old with anorexia nervosa (AN, n = 38), bulimia nervosa (BN, n = 32), or healthy controls (n = 60) were assessed for ACEs and ED behaviours and performed a taste-conditioning task during brain imaging. Mediation analyses tested relationships between ACE score, self-esteem, and ED behaviours. ACE scores were elevated in EDs and correlated positively with body mass index (p = 0.001), drive for thinness (p = 0.001), and body dissatisfaction (p = 0.032); low self-esteem mediated the relationship between ACEs and body dissatisfaction, drive for thinness, and bulimia severity. ACE scores correlated negatively (FDR-corrected) with unexpected, salient stimulus receipt in AN (substantia nigra) and BN (anterior cingulate, frontal and insular cortex, ventral striatum, and substantia nigra). When ACE scores were included in the model, unexpected stimulus receipt brain response was elevated in EDs in the anterior cingulate and ventral striatum. ACEs attenuate unexpected salient stimulus receipt response, which may be a biological marker for altered valence or hedonic tone perception in EDs. Low self-esteem mediates the relationships between ACEs and ED behaviours. Adverse childhood experiences should be assessed in biological studies, and their effects targeted in treatment.
Sections du résumé
BACKGROUND
BACKGROUND
Adverse childhood experiences (ACEs) are elevated in individuals with eating disorders (EDs), but how the neurobiology of EDs and ACEs interact is unclear.
METHODS
METHODS
Women 18-45 years old with anorexia nervosa (AN, n = 38), bulimia nervosa (BN, n = 32), or healthy controls (n = 60) were assessed for ACEs and ED behaviours and performed a taste-conditioning task during brain imaging. Mediation analyses tested relationships between ACE score, self-esteem, and ED behaviours.
RESULTS
RESULTS
ACE scores were elevated in EDs and correlated positively with body mass index (p = 0.001), drive for thinness (p = 0.001), and body dissatisfaction (p = 0.032); low self-esteem mediated the relationship between ACEs and body dissatisfaction, drive for thinness, and bulimia severity. ACE scores correlated negatively (FDR-corrected) with unexpected, salient stimulus receipt in AN (substantia nigra) and BN (anterior cingulate, frontal and insular cortex, ventral striatum, and substantia nigra). When ACE scores were included in the model, unexpected stimulus receipt brain response was elevated in EDs in the anterior cingulate and ventral striatum.
CONCLUSIONS
CONCLUSIONS
ACEs attenuate unexpected salient stimulus receipt response, which may be a biological marker for altered valence or hedonic tone perception in EDs. Low self-esteem mediates the relationships between ACEs and ED behaviours. Adverse childhood experiences should be assessed in biological studies, and their effects targeted in treatment.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIMH NIH HHS
ID : MH096777
Pays : United States
Organisme : NIMH NIH HHS
ID : MH103436
Pays : United States
Informations de copyright
© 2024 The Authors. European Eating Disorders Review published by Eating Disorders Association and John Wiley & Sons Ltd.
Références
Afifi, T. O., Sareen, J., Fortier, J., Taillieu, T., Turner, S., Cheung, K., & Henriksen, C. A. (2017). Child maltreatment and eating disorders among men and women in adulthood: Results from a nationally representative United States sample. International Journal of Eating Disorders, 50(11), 1281-1296. https://doi.org/10.1002/eat.22783
Bhushan, D., Kotz, K., McCall, J., Wirtz, S., Gilgoff, R., Dube, S. R., Powers, C., Olson-Morgan, J., Galeste, M., Patterson, K., Harris, L., Mills, A., Bethel, C., & Burke, H. N. (2020). The roadmap for resilience: The California surgeon general’s report on adverse childhood experiences, toxic stress, and health. Office of the California Surgeon General. https://doi.org/10.48019/PEAM8812
Brewerton, T. D. (2022). Mechanisms by which adverse childhood experiences, other traumas and PTSD influence the health and well-being of individuals with eating disorders throughout the life span. Journal of Eating Disorders, 10(1), 162. https://doi.org/10.1186/s40337-022-00696-6
Brewerton, T. D., Gavidia, I., Suro, G., Perlman, M. M., Genet, J., & Bunnell, D. W. (2021). Provisional post-traumatic stress disorder is associated with greater severity of eating disorder and comorbid symptoms in adolescents treated in residential care. European Eating Disorders Reviews: The Journal of the Eating Disorders Association, 29(6), 910-923. https://doi.org/10.1002/erv.2864
Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., & Rosen, B. R. (2002). Dorsal anterior cingulate cortex: A role in reward-based decision making. Proceedings of the National Academy of Sciences of the United States of America, 99(1), 523-528. https://doi.org/10.1073/pnas.012470999
Castellini, G., Lelli, L., Cassioli, E., Ciampi, E., Zamponi, F., Campone, B., Monteleone, A. M., & Ricca, V. (2018). Different outcomes, psychopathological features, and comorbidities in patients with eating disorders reporting childhood abuse: A 3-year follow-up study. European Eating Disorders Reviews: The Journal of the Eating Disorders Association, 26(3), 217-229. https://doi.org/10.1002/erv.2586
Chesney, E., Goodwin, G. M., & Fazel, S. (2014). Risks of all-cause and suicide mortality in mental disorders: A meta-review. World Psychiatry: Official Journal of the World Psychiatrc Association (WPA), 13(2), 153-160. https://doi.org/10.1002/wps.20128
Crouch, E., Radcliff, E., Strompolis, M., & Srivastav, A. (2018). Safe, stable, and nurtured: Protective factors against poor physical and mental health outcomes following exposure to adverse childhood experiences (ACEs). Journal of Child & Adolescent Trauma, 12(2), 165-173. https://doi.org/10.1007/s40653-018-0217-9
DeGuzman, M., Shott, M. E., Yang, T. T., Riederer, J., & Frank, G. K. W. (2017). Association of elevated reward prediction error response with weight gain in adolescent anorexia nervosa. American Journal of Psychiatry, 174(6), 557-565. https://doi.org/10.1176/appi.ajp.2016.16060671
de Vries, S. K., & Meule, A. (2016). Food addiction and bulimia nervosa: New data based on the yale food addiction Scale 2.0. European Eating Disorders Review, 24(6), 518-522. https://doi.org/10.1002/erv.2470
Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., Koss, M. P., & Marks, J. S. (1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. American Journal of Preventive Medicine, 14(4), 245-258. https://doi.org/10.1016/s0749-3797(98)00017-8
Ferrell, E. L., Russin, S. E., & Flint, D. D. (2022). Prevalence estimates of comorbid eating disorders and post-traumatic stress disorder: A quantitative synthesis. Journal of Aggression, Maltreatment & Trauma, 31(2), 264-282. https://doi.org/10.1080/10926771.2020.1832168
Forrest, L. N., Grilo, C. M., & Udo, T. (2021). Suicide attempts among people with eating disorders and adverse childhood experiences: Results from a nationally representative sample of adults. International Journal of Eating Disorders, 54(3), 326-335. https://doi.org/10.1002/eat.23457
Frank, G. K., Kaye, W. H., Carter, C. S., Brooks, S., May, C., Fissell, K., & Stenger, V. (2003). The evaluation of brain activity in response to taste stimuli--a pilot study and method for central taste activation as assessed by event-related fMRI. Journal of Neuroscience Methods, 131(1-2), 99-105. https://doi.org/10.1016/s0165-0270(03)00240-1
Frank, G. K. W., Reynolds, J. R., Shott, M. E., Jappe, L., Yang, T. T., Tregellas, J. R., & O'Reilly, R. C. (2012). Anorexia nervosa and obesity are associated with opposite brain reward response. Neuropsychopharmacology: Officially Publication of the American College of Neuropsychopharmacology, 37(9), 2031-2046. https://doi.org/10.1038/npp.2012.51
Frank, G. K. W., Shott, M. E., & DeGuzman, M. C. (2019). The neurobiology of eating disorders. Child and Adolescent Psychiatric Clinics of North America, 28(4), 629-640. https://doi.org/10.1016/j.chc.2019.05.007
Frank, G. K. W., Shott, M. E., Pryor, T., Swindle, S., Nguyen, T., & Stoddard, J. (2023). Trait anxiety is associated with amygdala expectation and caloric taste receipt response across eating disorders. Neuropsychopharmacology, 48(2), 380-390. https://doi.org/10.1038/s41386-022-01440-z
Frank, G. K. W., Shott, M. E., Stoddard, J., Swindle, S., & Pryor, T. L. (2021). Association of brain reward response with body mass index and ventral striatal-hypothalamic circuitry among young women with eating disorders. JAMA Psychiatry, 78(10), 1123-1133. https://doi.org/10.1001/jamapsychiatry.2021.1580
Garner, D. (2004). The eating disorder inventory-3: Professional manual. Psychological Assessment Resources.
Grant, M. M., Cannistraci, C., Hollon, S. D., Gore, J., & Shelton, R. (2011). Childhood trauma history differentiates amygdala response to sad faces within MDD. Journal of Psychiatric Research, 45(7), 886-895. https://doi.org/10.1016/j.jpsychires.2010.12.004
Guillaume, S., Jaussent, I., Maimoun, L., Ryst, A., Seneque, M., Villain, L., Hamroun, D., Lefebvre, P., Renard, E., & Courtet, P. (2016). Associations between adverse childhood experiences and clinical characteristics of eating disorders. Scientific Reports, 6(1), 35761. https://doi.org/10.1038/srep35761
Hanson, J. L., Williams, A. V., Bangasser, D. A., & Peña, C. J. (2021). Impact of early life stress on reward circuit function and regulation. Frontiers in Psychiatry, 12, 12. https://doi.org/10.3389/fpsyt.2021.744690. Accessed 24 February 2022.
Heather Hsu, C. C., Rolls, E. T., Huang, C. C., Chong, S. T., Zac Lo, C. Y., Feng, J., & Lin, C. P. (2020). Connections of the human orbitofrontal cortex and inferior frontal Gyrus. Cerebral Cortex, 30(11), 5830-5843. https://doi.org/10.1093/cercor/bhaa160
Hendrikse, C. J., du Plessis, S., Luckhoff, H. K., Vink, M., van den Heuvel, L. L., Scheffler, F., Phahladira, L., Smit, R., Asmal, L., Seedat, S., & Emsley, R. (2022). Childhood trauma exposure and reward processing in healthy adults: A functional neuroimaging study. Journal of Neuroscience Research, 100(7), 1452-1462. https://doi.org/10.1002/jnr.25051
Herzog, J. I., & Schmahl, C. (2018). Adverse childhood experiences and the consequences on neurobiological, psychosocial, and somatic conditions across the lifespan. Frontiers in Psychiatry, 9, 420. https://doi.org/10.3389/fpsyt.2018.00420
Khalsa, S. S., Craske, M. G., Li, W., Vangala, S., Strober, M., & Feusner, J. D. (2015). Altered interoceptive awareness in anorexia nervosa: Effects of meal anticipation, consumption and bodily arousal. International Journal of Eating Disorders, 48(7), 889-897. https://doi.org/10.1002/eat.22387
Lloyd, A., McKay, R. T., & Furl, N. (2022). Individuals with adverse childhood experiences explore less and underweight reward feedback. Proceedings of the National Academy of Sciences of the United States of America, 119(4), e2109373119. https://doi.org/10.1073/pnas.2109373119
Mahmood, S., Li, Y., & Hynes, M. (2022). Adverse childhood experiences and obesity: A one-to-one correlation? Clinical Child Psychology and Psychiatry, 28(2), 785-794. Published online August 12. https://doi.org/10.1177/13591045221119001
Mason, S. M., Flint, A. J., Roberts, A. L., Agnew-Blais, J., Koenen, K. C., & Rich-Edwards, J. W. (2014). Post-traumatic stress disorder symptoms and food addiction in women by timing and type of trauma exposure. JAMA Psychiatry, 71(11), 1271-1278. https://doi.org/10.1001/jamapsychiatry.2014.1208
McLaughlin, K. A., Weissman, D., & Bitrán, D. (2019). Childhood adversity and neural development: A systematic review. Annual Review of Development Psychology, 1, 277-312. https://doi.org/10.1146/annurev-devpsych-121318-084950
Merrick, M. T., Ports, K. A., Ford, D. C., Afifi, T. O., Gershoff, E. T., & Grogan-Kaylor, A. (2017). Unpacking the impact of adverse childhood experiences on adult mental health. Child Abuse & Neglect, 69, 10-19. https://doi.org/10.1016/j.chiabu.2017.03.016
Mirman, A., Bick, A. S., Kalla, C., Canetti, L., Segman, R., Dan, R., Ben Yehuda, A., Levin, N., & Bonne, O. (2021). The imprint of childhood adversity on emotional processing in high functioning young adults. Human Brain Mapping, 42(3), 615-625. https://doi.org/10.1002/hbm.25246
Mitchell, K. S., Mazzeo, S. E., Schlesinger, M. R., Brewerton, T. D., & Smith, B. N. (2012). Comorbidity of partial and subthreshold ptsd among men and women with eating disorders in the national comorbidity survey-replication study. International Journal of Eating Disorders, 45(3), 307-315. https://doi.org/10.1002/eat.20965
Molendijk, M. L., Hoek, H. W., Brewerton, T. D., & Elzinga, B. M. (2017). Childhood maltreatment and eating disorder pathology: A systematic review and dose-response meta-analysis. Psychological Medicine, 47(8), 1402-1416. https://doi.org/10.1017/S0033291716003561
O’Doherty, J., Dayan, P., Schultz, J., Deichmann, R., Friston, K., & Dolan, R. J. (2004). Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science, 304(5669), 452-454. https://doi.org/10.1126/science.1094285
O’Doherty, J. P., Dayan, P., Friston, K., Critchley, H., & Dolan, R. J. (2003). Temporal difference models and reward-related learning in the human brain. Neuron, 38(2), 329-337. https://doi.org/10.1016/s0896-6273(03)00169-7
O’Doherty, J. P., Hampton, A., & Kim, H. (2007). Model-based fMRI and its application to reward learning and decision making. Annals of the New York Academy of Sciences, 1104(1), 35-53. https://doi.org/10.1196/annals.1390.022
Osadchiy, V., Mayer, E. A., Bhatt, R., Labus, J. S., Gao, L., Kilpatrick, L. A., Liu, C., Tillisch, K., Naliboff, B., Chang, L., & Gupta, A. (2019). History of early life adversity is associated with increased food addiction and sex-specific alterations in reward network connectivity in obesity. Obesity Science & Practice, 5(5), 416-436. https://doi.org/10.1002/osp4.362
Pang, Y., Zhao, S., Li, Z., Yu, J., Zhang, R., Lu, F., Chen, H., Wu, F., Zheng, W., Gao, J., Yang, Y., Wu, H., & Wang, J. (2022). Enduring effect of abuse: Childhood maltreatment links to altered theory of mind network among adults. Human Brain Mapping, 43(7), 2276-2288. https://doi.org/10.1002/hbm.25787
Pechtel, P., Lyons-Ruth, K., Anderson, C. M., & Teicher, M. H. (2014). Sensitive periods of amygdala development: The role of maltreatment in preadolescence. NeuroImage, 97, 236-244. https://doi.org/10.1016/j.neuroimage.2014.04.025
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54(5), 504-514. https://doi.org/10.1016/s0006-3223(03)00168-9
Quevedo, K., Ng, R., Scott, H., Smyda, G., Pfeifer, J. H., & Malone, S. (2017). The neurobiology of self-processing in abused depressed adolescents. Development and Psychopathology, 29(3), 1057-1073. https://doi.org/10.1017/S0954579416001024
Reyes-Rodríguez, M. L., Von Holle, A., Ulman, T. F., Thornton, L. M., Klump, K. L., Brandt, H., Crawford, S., Fichter, M. M., Halmi, K. A., Huber, T., Johnson, C., Jones, I., Kaplan, A. S., Mitchell, J. E., Strober, M., Treasure, J., Woodside, D. B., Berrettini, W. H., Kaye, W. H., & Bulik, C. M. (2011). Post traumatic stress disorder in anorexia nervosa. Psychosomatic Medicine, 73(6), 491-497. https://doi.org/10.1097/PSY.0b013e31822232bb
Rienecke, R. D., Johnson, C., Le Grange, D., Manwaring, J., Mehler, P. S., Duffy, A., McClanahan, S., & Blalock, D. V. (2022). Adverse childhood experiences among adults with eating disorders: Comparison to a nationally representative sample and identification of trauma profiles. Journal of Eating Disorders, 10(1), 72. https://doi.org/10.1186/s40337-022-00594-x
Ruigrok, S. R., Kotah, J. M., Kuindersma, J. E., Speijer, E., van Irsen, A., la Fleur, S., & Korosi, A. (2021). Adult food choices depend on sex and exposure to early-life stress: Underlying brain circuitry, adipose tissue adaptations and metabolic responses. Neurobiology of Stress, 15, 100360. https://doi.org/10.1016/j.ynstr.2021.100360
Sanchez, E. O., & Bangasser, D. A. (2022). The effects of early life stress on impulsivity. Neuroscience & Biobehavioral Reviews, 137, 104638. https://doi.org/10.1016/j.neubiorev.2022.104638
Schulte, E. M., Yokum, S., Jahn, A., & Gearhardt, A. N. (2019). Food cue reactivity in food addiction: A functional magnetic resonance imaging study. Physiology & Behavior, 208, 112574. https://doi.org/10.1016/j.physbeh.2019.112574
Seeley, W. W. (2019). The salience network: A neural system for perceiving and responding to homeostatic demands. Journal of Neuroscience: The Officially Journal of the Society for Neuroscience, 39(50), 9878-9882. https://doi.org/10.1523/JNEUROSCI.1138-17.2019
Seidemann, R., Duek, O., Jia, R., Levy, I., & Harpaz-Rotem, I. (2021). The reward system and post-traumatic stress disorder: Does trauma affect the way we interact with positive stimuli? Chronic Stress, 5, 2470547021996006. https://doi.org/10.1177/2470547021996006
Simon, J. J., Stopyra, M. A., & Friederich, H. C. (2019). Neural processing of disorder-related stimuli in patients with anorexia nervosa: A narrative review of brain imaging studies. Journal of Clinical Medicine, 8(7), 1047. https://doi.org/10.3390/jcm8071047
Szczepanik, J. E., Reed, J. L., Nugent, A. C., Ballard, E. D., Evans, J. W., Lejuez, C. W., & Zarate, C. A. (2019). Mapping anticipatory anhedonia: An fMRI study. Brain Imaging Behavior, 13(6), 1624-1634. https://doi.org/10.1007/s11682-019-00084-w
Teicher, M. H., & Samson, J. A. (2016). Annual Research Review: Enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry, 57(3), 241-266. https://doi.org/10.1111/jcpp.12507
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273-289. https://doi.org/10.1006/nimg.2001.0978
Val-Laillet, D., Aarts, E., Weber, B., Ferrari, M., Quaresima, V., Stoeckel, L., Alonso-Alonso, M., Audette, M., Malbert, C., & Stice, E. (2015). Neuroimaging and neuromodulation approaches to study eating behavior and prevent and treat eating disorders and obesity. NeuroImage Clinical, 8, 1-31. https://doi.org/10.1016/j.nicl.2015.03.016
van Hoeken, D., & Hoek, H. W. (2020). Review of the burden of eating disorders: Mortality, disability, costs, quality of life, and family burden. Current Opinion in Psychiatry, 33(6), 521-527. https://doi.org/10.1097/YCO.0000000000000641
Vartanian, L. R., Nicholls, K., & Fardouly, J. (2023). Testing the identity disruption model among adolescents: Pathways connecting adverse childhood experiences to body dissatisfaction. Journal of Youth and Adolescence, 52(1), 134-148. https://doi.org/10.1007/s10964-022-01683-5
Wendler-Bödicker, C., Kische, H., Voss, C., & Beesdo-Baum, K. (2023). The association between childhood maltreatment and body (dis)satisfaction in adolescents and young adults from the general population. Journal of Trauma Dissociation: Official Journal of the International Society for the Study of Dissociation ISSD, 25, 1-16. Published online July 5. https://doi.org/10.1080/15299732.2023.2231927
White, S. F., Costanzo, M. E., Blair, J. R., & Roy, M. J. (2015). PTSD symptom severity is associated with increased recruitment of top-down attentional control in a trauma-exposed sample. NeuroImage Clinical, 7, 19-27. https://doi.org/10.1016/j.nicl.2014.11.012
Wilkinson, M. P., Slaney, C. L., Mellor, J. R., & Robinson, E. S. J. (2021). Investigation of reward learning and feedback sensitivity in non-clinical participants with a history of early life stress. PLoS One, 16(12), e0260444. https://doi.org/10.1371/journal.pone.0260444
Wiss, D. A., & Brewerton, T. D. (2020). Adverse childhood experiences and adult obesity: A systematic review of plausible mechanisms and meta-analysis of cross-sectional studies. Physiology & Behavior, 223, 112964. https://doi.org/10.1016/j.physbeh.2020.112964
Wolf, N. M., & Elklit, A. (2020). Child maltreatment and disordered eating in adulthood: A mediating role of PTSD and self-esteem? Journal of Child & Adolescent Trauma, 13(1), 21-32. https://doi.org/10.1007/s40653-018-0224-x