Linking the reversal of gestational insulin resistance to postpartum depression.
Gestational diabetes mellitus (GDM)
Glucose
Insulin
Insulin resistance (IR)
Postpartum depression (PPD)
Pregnancy
Journal
BMC medicine
ISSN: 1741-7015
Titre abrégé: BMC Med
Pays: England
ID NLM: 101190723
Informations de publication
Date de publication:
08 Oct 2024
08 Oct 2024
Historique:
received:
12
03
2024
accepted:
26
09
2024
medline:
9
10
2024
pubmed:
9
10
2024
entrez:
8
10
2024
Statut:
epublish
Résumé
Postpartum depression (PPD) constitutes a significant mental health disorder affecting almost one fifth of pregnancies globally. Despite extensive research, the precise etiological mechanisms underlying PPD remain elusive. However, several risk factors like genetic predisposition, hormonal fluctuations, and stress-related environmental and psychosocial triggers have been found to be implicated in its development. MAIN: Recently, an increased risk of PPD has been reported to be associated with gestational diabetes mellitus (GDM), which is characterized by the disruption of glucose metabolism, primarily attributed to the emergence of insulin resistance (IR). While IR during pregnancy seems to be an evolutionary adaptative mechanism to handle the profound metabolic alterations during pregnancy, its subsequent resolution following delivery necessitates a reconfiguration of the metabolic landscape in both peripheral tissues and the central nervous system (CNS). Considering the pivotal roles of energy metabolism, particularly glucose metabolism, in CNS functions, we propose a novel model that such pronounced changes in IR and the associated glucose metabolism seen postpartum might account for PPD development. This concept is based on the profound influences from insulin and glucose metabolism on brain functions, potentially via modulating neurotransmitter actions of dopamine and serotonin. Their sudden postpartum disruption is likely to be linked to mood changes, as observed in PPD. The detailed pathogenesis of PPD might be multifactorial and still remains to be fully elucidated. Nevertheless, our hypothesis might account in part for an additional etiological factor to PPD development. If our concept is validated, it can provide guidance for future PPD prevention, diagnosis, and intervention.
Sections du résumé
BACKGROUND
BACKGROUND
Postpartum depression (PPD) constitutes a significant mental health disorder affecting almost one fifth of pregnancies globally. Despite extensive research, the precise etiological mechanisms underlying PPD remain elusive. However, several risk factors like genetic predisposition, hormonal fluctuations, and stress-related environmental and psychosocial triggers have been found to be implicated in its development. MAIN: Recently, an increased risk of PPD has been reported to be associated with gestational diabetes mellitus (GDM), which is characterized by the disruption of glucose metabolism, primarily attributed to the emergence of insulin resistance (IR). While IR during pregnancy seems to be an evolutionary adaptative mechanism to handle the profound metabolic alterations during pregnancy, its subsequent resolution following delivery necessitates a reconfiguration of the metabolic landscape in both peripheral tissues and the central nervous system (CNS). Considering the pivotal roles of energy metabolism, particularly glucose metabolism, in CNS functions, we propose a novel model that such pronounced changes in IR and the associated glucose metabolism seen postpartum might account for PPD development. This concept is based on the profound influences from insulin and glucose metabolism on brain functions, potentially via modulating neurotransmitter actions of dopamine and serotonin. Their sudden postpartum disruption is likely to be linked to mood changes, as observed in PPD.
CONCLUSIONS
CONCLUSIONS
The detailed pathogenesis of PPD might be multifactorial and still remains to be fully elucidated. Nevertheless, our hypothesis might account in part for an additional etiological factor to PPD development. If our concept is validated, it can provide guidance for future PPD prevention, diagnosis, and intervention.
Identifiants
pubmed: 39379948
doi: 10.1186/s12916-024-03659-7
pii: 10.1186/s12916-024-03659-7
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
433Informations de copyright
© 2024. The Author(s).
Références
American Psychiatric Association, DSM-5 Task Force. (2013). Diagnostic and statistical manual of mental disorders: DSM-5™ (5th ed.). American Psychiatric Publishing, Inc.. https://doi.org/10.1176/appi.books.9780890425596 .
O’Hara MW, McCabe JE. Postpartum depression: current status and future directions. Annu Rev Clin Psychol. 2013;9:379–407.
pubmed: 23394227
doi: 10.1146/annurev-clinpsy-050212-185612
Gavin NI, Gaynes BN, Lohr KN, Meltzer-Brody S, Gartlehner G, Swinson T. Perinatal depression: a systematic review of prevalence and incidence. Obstet Gynecol. 2005;106(5 Pt 1):1071–83.
pubmed: 16260528
doi: 10.1097/01.AOG.0000183597.31630.db
Slomian J, Honvo G, Emonts P, Reginster JY, Bruyere O. Consequences of maternal postpartum depression: a systematic review of maternal and infant outcomes. Womens Health (Lond). 2019;15:1745506519844044.
pubmed: 31035856
doi: 10.1177/1745506519844044
Leboffe EN, Pietragallo HC, Liu G, Ba D, Leslie D, Chuang CH. The impact of the 2015 ACOG screening guidelines on the diagnosis of postpartum depression among privately insured women. J Affect Disord. 2023;328:103–7.
pubmed: 36764363
doi: 10.1016/j.jad.2023.02.020
Wang Z, Liu J, Shuai H, Cai Z, Fu X, Liu Y, Xiao X, Zhang W, Krabbendam E, Liu S, et al. Mapping global prevalence of depression among postpartum women. Transl Psychiatry. 2021;11(1):543.
pubmed: 34671011
pmcid: 8528847
doi: 10.1038/s41398-021-01663-6
Swart T, Shandley K, Huynh M, Brown CM, Austin DWB J. Pregnancy complications and their association with postpartum depression symptoms: a retrospective study. Aust J Psychol. 2023;75(1):1–7.
Zhao XH, Zhang ZH. Risk factors for postpartum depression: an evidence-based systematic review of systematic reviews and meta-analyses. Asian J Psychiatr. 2020;53.
doi: 10.1016/j.ajp.2020.102353
Bloch M, Daly RC, Rubinow DR. Endocrine factors in the etiology of postpartum depression. Compr Psychiatry. 2003;44(3):234–46.
pubmed: 12764712
doi: 10.1016/S0010-440X(03)00034-8
Kim S, Soeken TA, Cromer SJ, Martinez SR, Hardy LR, Strathearn L. Oxytocin and postpartum depression: delivering on what’s known and what’s not. Brain Res. 2014;1580:219–32.
pubmed: 24239932
doi: 10.1016/j.brainres.2013.11.009
Azami M, Badfar G, Soleymani A, Rahmati S. The association between gestational diabetes and postpartum depression: a systematic review and meta-analysis. Diabetes Res Clin Pract. 2019;149:147–55.
pubmed: 30735772
doi: 10.1016/j.diabres.2019.01.034
Benton D, Nabb S. Carbohydrate, memory, and mood. Nutr Rev. 2003;61(5 Pt 2):S61–7.
pubmed: 12828194
doi: 10.1301/nr.2003.may.S61-S67
Alonge KM, D’Alessio DA, Schwartz MW. Brain control of blood glucose levels: implications for the pathogenesis of type 2 diabetes. Diabetologia. 2021;64(1):5–14.
pubmed: 33043401
doi: 10.1007/s00125-020-05293-3
Nakabeppu Y. Origins of brain insulin and its function. Adv Exp Med Biol. 2019;1128:1–11.
pubmed: 31062322
doi: 10.1007/978-981-13-3540-2_1
McNay EC, Pearson-Leary J. GluT4: a central player in hippocampal memory and brain insulin resistance. Exp Neurol. 2020;323:113076.
pubmed: 31614121
doi: 10.1016/j.expneurol.2019.113076
Wang T, Wang J, Hu X, Huang XJ, Chen GX. Current understanding of glucose transporter 4 expression and functional mechanisms. World J Biol Chem. 2020;11(3):76–98.
pubmed: 33274014
pmcid: 7672939
doi: 10.4331/wjbc.v11.i3.76
Koepsell H. Glucose transporters in brain in health and disease. Pflugers Arch. 2020;472(9):1299–343.
pubmed: 32789766
pmcid: 7462931
doi: 10.1007/s00424-020-02441-x
Gray SM, Barrett EJ. Insulin transport into the brain. Am J Physiol Cell Physiol. 2018;315(2):C125–36.
pubmed: 29847142
pmcid: 6139500
doi: 10.1152/ajpcell.00240.2017
Begg DP. Insulin transport into the brain and cerebrospinal fluid. Vitam Horm. 2015;98:229–48.
pubmed: 25817871
doi: 10.1016/bs.vh.2014.12.007
Rhea EM, Rask-Madsen C, Banks WA. Insulin transport across the blood-brain barrier can occur independently of the insulin receptor. J Physiol. 2018;596(19):4753–65.
pubmed: 30044494
pmcid: 6166047
doi: 10.1113/JP276149
Csajbok EA, Tamas G. Cerebral cortex: a target and source of insulin? Diabetologia. 2016;59(8):1609–15.
pubmed: 27207082
doi: 10.1007/s00125-016-3996-2
Mazucanti CH, Liu QR, Lang D, Huang N, O’Connell JF, Camandola S, Egan JM. Release of insulin produced by the choroid plexis is regulated by serotonergic signaling. JCI Insight. 2019;4(23):e131682. https://doi.org/10.1172/jci.insight.131682 .
Lee MK, Graham SN, Gold PE. Memory enhancement with posttraining intraventricular glucose injections in rats. Behav Neurosci. 1988;102(4):591–5.
pubmed: 3166734
doi: 10.1037/0735-7044.102.4.591
Lee SH, Zabolotny JM, Huang H, Lee H, Kim YB. Insulin in the nervous system and the mind: functions in metabolism, memory, and mood. Mol Metab. 2016;5(8):589–601.
pubmed: 27656397
pmcid: 5021669
doi: 10.1016/j.molmet.2016.06.011
Lyra E, Silva NM, Lam MP, Soares CN, Munoz DP, Milev R, De Felice FG. Insulin resistance as a shared pathogenic mechanism between depression and type 2 diabetes. Front Psych. 2019;10:1–8.
Kleinridders A, Pothos EN. Impact of brain insulin signaling on dopamine function, food intake, reward, and emotional behavior. Current nutrition reports. 2019;8(2):83–91.
pubmed: 31001792
doi: 10.1007/s13668-019-0276-z
Reagan LP, Cowan HB, Woodruff JL, Piroli GG, Erichsen JM, Evans AN, Burzynski HE, Maxwell ND, Loyo-Rosado FZ, Macht VA, et al. Hippocampal-specific insulin resistance elicits behavioral despair and hippocampal dendritic atrophy. Neurobiol Stress. 2021;15.
pubmed: 34258333
pmcid: 8252121
doi: 10.1016/j.ynstr.2021.100354
Smith VA, Maciejewski ML, Berkowitz TSZ, Mitchell JE, Liu CF, Bradley KA, Olsen MK, Livingston EL, Arterburn DE. The effect of bariatric surgery on long-term depression treatment in patients with obesity. Ann Surg. 2022;276(2):318–23.
pubmed: 36036992
doi: 10.1097/SLA.0000000000005520
Kheirvari M, Anbara T. Changes in clinical depression following sleeve gastrectomy. Endocrinol Diabetes Metab. 2021;4(4): e00282.
pubmed: 34505417
pmcid: 8502213
doi: 10.1002/edm2.282
Bai X, Liu Z, Li Z, Yan D. The association between insulin therapy and depression in patients with type 2 diabetes mellitus: a meta-analysis. BMJ Open. 2018;8(11): e020062.
pubmed: 30498035
pmcid: 6278799
doi: 10.1136/bmjopen-2017-020062
Li JR, Cao J, Wei J, Geng W. Case Report: Semaglutide-associated depression: a report of two cases. Front Psychiatry. 2023;14:1238353.
pubmed: 37706035
pmcid: 10495976
doi: 10.3389/fpsyt.2023.1238353
Chen W, Cai P, Zou W, Fu Z. Psychiatric adverse events associated with GLP-1 receptor agonists: a real-world pharmacovigilance study based on the FDA Adverse Event Reporting System database. Front Endocrinol (Lausanne). 2024;15:1330936.
pubmed: 38390214
doi: 10.3389/fendo.2024.1330936
Schell M, Wardelmann K, Kleinridders A. Untangling the effect of insulin action on brain mitochondria and metabolism. J Neuroendocrinol. 2021;33(4):1–14.
doi: 10.1111/jne.12932
Markus CR. Effects of carbohydrates on brain tryptophan availability and stress performance. Biol Psychol. 2007;76(1–2):83–90.
pubmed: 17689173
doi: 10.1016/j.biopsycho.2007.06.003
Lyons PM, Truswell AS. Serotonin precursor influenced by type of carbohydrate meal in healthy adults. Am J Clin Nutr. 1988;47(3):433–9.
pubmed: 3279747
doi: 10.1093/ajcn/47.3.433
Barbour LA, McCurdy CE, Hernandez TL, Kirwan JP, Catalano PM, Friedman JE. Cellular mechanisms for insulin resistance in normal pregnancy and gestational diabetes. Diabetes Care. 2007;30(Suppl 2):S112–119.
pubmed: 17596458
doi: 10.2337/dc07-s202
Ryan EA. Hormones and insulin resistance during pregnancy. Lancet. 2003;362(9398):1777–8.
pubmed: 14654313
doi: 10.1016/S0140-6736(03)14942-2
Sonagra AD, Biradar SMKD, Murthy DSJ. Normal pregnancy- a state of insulin resistance. J Clin Diagn Res. 2014;8(11):01–3.
Satoh T. Bird evolution by insulin resistance. Trends Endocrinol Metab. 2021;32(10):803–13.
pubmed: 34446347
doi: 10.1016/j.tem.2021.07.007
Soeters MR, Soeters PB. The evolutionary benefit of insulin resistance. Clin Nutr. 2012;31(6):1002–7.
pubmed: 22682085
doi: 10.1016/j.clnu.2012.05.011
Chechko N, Dukart J, Tchaikovski S, Enzensberger C, Neuner I, Stickel S. The expectant brain-pregnancy leads to changes in brain morphology in the early postpartum period. Cereb Cortex. 2022;32(18):4025–38.
pubmed: 34942007
doi: 10.1093/cercor/bhab463
Hillerer KM, Jacobs VR, Fischer T, Aigner L. The maternal brain: an organ with peripartal plasticity. Neural Plast. 2014;2014: 574159.
pubmed: 24883213
pmcid: 4026981
doi: 10.1155/2014/574159
Hoekzema E, van Steenbergen H, Straathof M, Beekmans A, Freund IM, Pouwels PJW, Crone EA. Mapping the effects of pregnancy on resting state brain activity, white matter microstructure, neural metabolite concentrations and grey matter architecture. Nat Commun. 2022;13(1):6931.
pubmed: 36414622
pmcid: 9681770
doi: 10.1038/s41467-022-33884-8
Skajaa GO, Fuglsang J, Knorr S, et al. Changes in insulin sensitivity and insulin secretion during pregnancy and post partum in women with gestational diabetes. BMJ Open Diabetes Res Care. 2020;8:e001728. https://doi.org/10.1136/bmjdrc-2020-001728 .
Kirwan JP, Varastehpour A, Jing M, Presley L, Shao J, Friedman JE, Catalano PM. Reversal of insulin resistance postpartum is linked to enhanced skeletal muscle insulin signaling. J Clin Endocrinol Metab. 2004;89(9):4678–84.
pubmed: 15356080
doi: 10.1210/jc.2004-0749
Ryan EA, O’Sullivan MJ, Skyler JS. Insulin action during pregnancy. Studies with the euglycemic clamp technique. Diabetes. 1985;34(4):380–9.
pubmed: 3882502
doi: 10.2337/diab.34.4.380
Wu CH, Gau ML, Cheng SF, Chen TL, Wu CJ. Excessive gestational weight gain and emotional eating are positively associated with postpartum depressive symptoms among taiwanese women. BMC Womens Health. 2023;23(1):464.
pubmed: 37658388
pmcid: 10474696
doi: 10.1186/s12905-023-02625-4
Qiu X, Zhang S, Yan J. Gestational weight gain and risk of postpartum depression: a meta-analysis of observational studies. Psychiatry Res. 2022;310: 114448.
pubmed: 35227990
doi: 10.1016/j.psychres.2022.114448
Herring SJ, Rich-Edwards JW, Oken E, Rifas-Shiman SL, Kleinman KP, Gillman MW. Association of postpartum depression with weight retention 1 year after childbirth. Obesity (Silver Spring). 2008;16(6):1296–301.
pubmed: 18369338
doi: 10.1038/oby.2008.71
Okun ML. Disturbed sleep and postpartum depression. Curr Psychiatry Rep. 2016;18(7):66.
pubmed: 27222140
doi: 10.1007/s11920-016-0705-2
Pope CJ, Mazmanian D. Breastfeeding and postpartum depression: an overview and methodological recommendations for future research. Depress Res Treat. 2016;2016:4765310.
pubmed: 27148457
pmcid: 4842365
Henshaw EJ. Breastfeeding and postpartum depression: a review of relationships and potential mechanisms. Curr Psychiatry Rep. 2023;25(12):803–8.
pubmed: 37906349
doi: 10.1007/s11920-023-01471-3
Tanner HL, Dekker Nitert M, Callaway LK, Barrett HL. Ketones in pregnancy: why is it considered necessary to avoid them and what is the evidence behind their perceived risk? Diabetes Care. 2021;44(1):280–9.
pubmed: 33444162
doi: 10.2337/dc20-2008
Fischer S, Morales-Suárez-Varela M. The Bidirectional Relationship between Gestational Diabetes and Depression in Pregnant Women: A Systematic Search and Review. Healthcare. 2023;11(3):404. https://doi.org/10.3390/healthcare11030404 .
OuYang H, Chen B, Abdulrahman AM, Li L, Wu N. Associations between gestational diabetes and anxiety or depression: a systematic review. J Diabetes Res. 2021;2021:9959779.
pubmed: 34368368
pmcid: 8337159
doi: 10.1155/2021/9959779
Gilbert L, Nikolaou A, Quansah DY, Rossel JB, Horsch A, Puder JJ. Mental health and its associations with glucose-lowering medication in women with gestational diabetes mellitus. A prospective clinical cohort study. Psychoneuroendocrinology. 2021;124:105095.
pubmed: 33321330
doi: 10.1016/j.psyneuen.2020.105095
Nicklas JM, Miller LJ, Zera CA, Davis RB, Levkoff SE, Seely EW. Factors associated with depressive symptoms in the early postpartum period among women with recent gestational diabetes mellitus. Matern Child Health J. 2013;17(9):1665–72.
pubmed: 23124798
doi: 10.1007/s10995-012-1180-y