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Lower Serum Zinc and Higher CRP Strongly Predict Prenatal Depression and Physio-somatic Symptoms, Which All Together Predict Postnatal Depressive Symptoms

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Abstract

Pregnancy and delivery are associated with activation of immune-inflammatory pathways which may prime parturients to develop postnatal depression. There are, however, few data on the associations between immune-inflammatory pathways and prenatal depression and physio-somatic symptoms. This study examined the associations between serum zinc, C-reactive protein (CRP), and haptoglobin at the end of term and prenatal physio-somatic symptoms (fatigue, back pain, muscle pain, dyspepsia, obstipation) and prenatal and postnatal depressive and anxiety symptoms as measured using the Edinburgh Postnatal Depression Scale (EPDS), Beck Depression Inventory (BDI), Hamilton Depression Rating Scale (HAMD), and Spielberger’s State Anxiety Inventory (STAI). Zinc and haptoglobin were significantly lower and CRP increased at the end of term as compared with non-pregnant women. Prenatal depression was predicted by lower zinc and lifetime history of depression, anxiety, and premenstrual tension syndrome (PMS). The latter histories were also significantly and inversely related to lower zinc. The severity of prenatal EDPS, HAMD, BDI, STAI, and physio-somatic symptoms was predicted by fatigue in the first and second trimesters, a positive life history of depression, anxiety, and PMS, and lower zinc and higher CRP. Postnatal depressive symptoms are predicted by prenatal depression, physio-somatic symptoms, zinc and CRP. Prenatal depressive and physio-somatic symptoms have an immune-inflammatory pathophysiology, while postnatal depressive symptoms are highly predicted by prenatal immune activation, prenatal depression, and a lifetime history of depression and PMS. Previous episodes of depression, anxiety disorders, and PMS may prime pregnant females to develop prenatal and postnatal depressive symptoms via activated immune pathways.

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References

  1. Maes M, Bosmans E, Suy E, Vandervorst C, DeJonckheere C, Raus J (1991) Depression-related disturbances in mitogen-induced lymphocyte responses and interleukin-1 beta and soluble interleukin-2 receptor production. Acta Psychiatr Scand 84:379–386

    Article  CAS  PubMed  Google Scholar 

  2. Maes M (1995) Evidence for an immune response in major depression: a review and hypothesis. Prog Neuropsychopharmacol Biol Psychiatry 19(1):11–38

    Article  CAS  PubMed  Google Scholar 

  3. Maes M, Stevens WJ, Declerck LS, Bridts CH, Peeters D, Schotte C, Cosyns P (1993) Significantly increased expression of T-cell activation markers (interleukin-2 and HLA-DR) in depression: further evidence for an inflammatory process during that illness. Prog Neuropsychopharmacol Biol Psychiatry 17(2):241–255

    Article  CAS  PubMed  Google Scholar 

  4. Maes M, Bosmans E, Meltzer HY (1995) Immunoendocrine aspects of major depression. relationships between plasma interleukin-6 and soluble interleukin-2 receptor, prolactin and cortisol. Eur Arch Psychiatry Clin Neurosci 245(3):172–178

    Article  CAS  PubMed  Google Scholar 

  5. Maes M, Scharpe S, Bosmans E, Vandewoude M, Suy E, Uyttenbroeck W, Cooreman W, Vandervorst C, Raus J (1992) Disturbances in acute phase plasma proteins during melancholia: additional evidence for the presence of an inflammatory process during that illness. Prog Neuropsychopharmacol Biol Psychiatry 16(4):501–515

    Article  CAS  PubMed  Google Scholar 

  6. Maes M, Scharpé S, Van Grootel L, Uyttenbroeck W, Cooreman W, Cosyns P, Suy E (1992) Higher alpha 1-antitrypsin, haptoglobin, ceruloplasmin and lower retinol binding protein plasma levels during depression: further evidence for the existence of an inflammatory response during that illness. J Affect Disord 24(3):183–192

    Article  CAS  PubMed  Google Scholar 

  7. Sluzewska A, Rybakowski J, Bosmans E, Sobieska M, Berghmans R, Maes M, Wiktorowicz K (1996) Indicators of immune activation in major depression. Psychiatry Res 64(3):161–167

    Article  CAS  PubMed  Google Scholar 

  8. Lopresti AL, Maker GL, Drummund PD (2014) A review of peripheral biomarkers in major depression: the potential of inflammatory and oxidative stress biomarkers. Prog Neuro-Psychopharmacol Biol Psychiatry 48:102–111

    Article  Google Scholar 

  9. Pasko JA, Nicolson GC, Williams LJ, Jacka FN, Henry MJ, Kotowicz MA (2010) Association of high-sensitivity C-reactive protein with de novo depression. Br J Psychiatry 197(5):372–377

    Article  Google Scholar 

  10. Liu Y (2012) RC-M Ho, Mak A: Interleukin (IL)-6, tumour necrosis factor alpha (TNF-α) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: a meta-analysis and meta-regression. J Affect Disord 139:230–239

    Article  CAS  PubMed  Google Scholar 

  11. Mikova O, Yakimova R, Bosmans E, Kenis G, Maes M (2001) Increased serum tumor necrosis factor alpha concentrations in major depression and multiple sclerosis. Eur Neuropsychopharmacol 11(3):203–208

    Article  CAS  PubMed  Google Scholar 

  12. Valkanova V, Ebmeier KP, Allan CL (2013) CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. J Affect Disord 150(3):736–744

    Article  CAS  PubMed  Google Scholar 

  13. Solomons NW (1988) Zinc and copper. In: Shils ME, Young VR (eds) Modern nutrition in health and disease. Lea & Febiger, Philadelphia, pp 238–262

    Google Scholar 

  14. Mussalo-Rauhamaa H, Konttinen YT, Lehto J, Honkanen V (1988) Predictive clinical and laboratory parameters for serum zinc and copper in rheumatoid arthritis. Ann Rheum Dis 47(10):816–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Maes M, D’Haese PC, Scharpé S, D’Hondt P, Cosyns P, De Broe ME (1994) Hypozincemia in depression. J Affect Disord 31(2):135–140

    Article  CAS  PubMed  Google Scholar 

  16. Maes M, Vandoolaeghe E, Neels H, Demedts P, Wauters A, Meltzer HY, Altamura C, Desnyder R (1997) Lower serum zinc in major depression is a sensitive marker of treatment resistance and of the immune/inflammatory response in that illness. Biol Psychiatry 42(5):349–358

    Article  CAS  PubMed  Google Scholar 

  17. Siwek M, Szewczyk B, Dudek D, Styczeń K, Sowa-Kućma M, Młyniec K, Siwek A, Witkowski L, Pochwat B, Nowak G (2013) Zinc as a marker of affective disorders. Pharmacol Rep 65(6):1512–1518

    Article  CAS  PubMed  Google Scholar 

  18. Swardfager W, Herrmann N, Mazereeuw G, Goldberger K, Harimoto T, Lanctôt KL (2013) Zinc in depression: a meta-analysis. Biol Psychiatry 74(12):872–878

    Article  CAS  PubMed  Google Scholar 

  19. Siwek M, Dudek D, Schlegel-Zawadzka M, Morawska A, Piekoszewski W, Opoka W, Zięba A, Popik P, Pilc A, Nowak G (2010) Serum zinc level in depressed patients during zinc supplementation of imipramine treatment. J Affective Disorders 126:447–452

    Article  CAS  Google Scholar 

  20. Maes M, De Vos N, Demedts P, Wauters A, Neels H (1999) Lower serum zinc in major depression in relation to changes in serum acute phase proteins. J Affect Disord 56(2–3):189–194

    Article  CAS  PubMed  Google Scholar 

  21. Nowak G, Kubera M, Maes M (2000) Neuroimmunological aspects of the alterations in zinc homeostasis in the pathophysiology and treatment of depression. Acta Neuropsychiatrica 12(2):49–53

    Article  CAS  PubMed  Google Scholar 

  22. Aggett PJ, Harries JT (1979) Current status of zinc in health and disease states. Arch Dis Child 54(12):909–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Maes M, Galecki P, Chang YS, Berk M (2011) A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry 35(3):676–692

    Article  CAS  PubMed  Google Scholar 

  24. Leonard B, Maes M (2012) Mechanistic explanations how cell-mediated immune activation, inflammation and oxidative and nitrosative stress pathways and their sequels and concomitants play a role in the pathophysiology of unipolar depression. Neurosci Biobehav Rev 36(2):764–785

    Article  CAS  PubMed  Google Scholar 

  25. Maes M, Ombelet W, Libbrecht II, Stevens K, Kenis G, De Jongh R, Lin AH, Cox J, Bosmans E (1999) Effects of pregnancy and delivery on serum concentrations of Clara Cell Protein (CC16), an endogenous anticytokine: lower serum CC16 is related to postpartum depression. Psychiatry Res 87(2–3):117–127

    Article  CAS  PubMed  Google Scholar 

  26. Maes M, Lin AH, Ombelet W, Stevens K, Kenis G, De Jong R, Cox J, Bosmans E (2000) Immune activation in the early puerperium is related to postpartum axiety and depressive symptoms. Psychoneuroendocrinology 25:121–137

    Article  CAS  PubMed  Google Scholar 

  27. Maes M, Libbrecht I, Lin A, Goossens F, Ombelet W, Stevens K, Bosmans E, Altamura C, Cox J, de Jongh R et al (2000) Effects of pregnancy and delivery on serum prolyl endopeptidase (PEP) activity: alterations in serum PEP are related to increased anxiety in the early puerperium and to postpartum depression. J Affect Disord 57(1–3):125–137

    Article  CAS  PubMed  Google Scholar 

  28. Maes M, Verkerk R, Bonaccorso S, Ombelet W, Bosmans E, Scharpé S (2002) Depressive and anxiety symptoms in the early puerperium are related to increased degradation of tryptophan into kynurenine, a phenomenon which is related to immune activation. Life Sci 71(16):1387–1348

    Article  Google Scholar 

  29. Christian LM, Franco A, Glaser R, Iams J (2009) Depressive symptoms are associated with elevated serum proinflammatory cytokines among pregnant women. Brain Behav Immun 23:750–754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Azar R, Mercer D (2013) Mild depressive symptoms are associated with elevated C-reactive protein and proinflammatory cytokine levels during early to midgestation: a prospective pilot study. J Womens Health (Larchmt) 22(4):385–389

    Article  Google Scholar 

  31. Cassidy-Bushrow AE, Peters RM, Johnson DA, Templin TN (2012) Association of depressive symptoms with inflammatory biomarkers among pregnant African-American women. J Reprod Immunol 94(2):202–209

    Article  CAS  PubMed  Google Scholar 

  32. Shelton MM, Schminkey DL, Groer MW (2015) Relationships among prenatal depression, plasma cortisol, and inflammatory cytokines. Biol Res Nurs 17(3):295–302

    Article  CAS  PubMed  Google Scholar 

  33. Roy A, Evers SE, Avison WR, Campbell MK (2010) Higher zinc intake buffers the impact of stress on depressive symptoms in pregnancy. Nutr Res 30(10):695–704

    Article  CAS  PubMed  Google Scholar 

  34. Wójcik J, Dudek D, Schlegel-Zawadzka M, Grabowska M, Marcinek A, Florek E, Piekoszewski W, Nowak RJ, Opoka W, Nowak G (2006) Antepartum/postpartum depressive symptoms and serum zinc and magnesium levels. Pharmacol Rep 58(4):571–576

    PubMed  Google Scholar 

  35. Etebary S, Nikseresht S, Sadeghipour HR, Zarrindast MR (2010) Postpartum depression and role of serum trace elements. Iran J Psychiatr 5(2):40–46

    Google Scholar 

  36. Maes M, Mihaylova I, Leunis JC (2005) In chronic fatigue syndrome, the decreased levels of omega-3 poly-unsaturated fatty acids are related to lowered serum zinc and defects in T cell activation. Neuro Endocrinol Lett 26(6):745–751

    CAS  PubMed  Google Scholar 

  37. Maes M, Twisk FN, Johnson C (2012) Myalgic Encephalomyelitis (ME), Chronic Fatigue Syndrome (CFS), and Chronic Fatigue (CF) are distinguished accurately: results of supervised learning techniques applied on clinical and inflammatory data. Psychiatry Res 200(2-3):754–760

    Article  PubMed  Google Scholar 

  38. Maes M, Ombelet W, De Jongh R, Kennis G, Bosman E (2001) The inflammatory response following delivery is amplified in women who previously suffered from major depression, suggesting that major depression is accompanied by a sensitization of the inflammatory response system. J Affect Disord 63:85–92

    Article  CAS  PubMed  Google Scholar 

  39. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–23

    PubMed  Google Scholar 

  40. Kittirathanapaiboon P, Khamwongpin M (2005) The Validity of the Mini International Neuropsychiatric Interview (M.I.N.I.) Thai Version: Suanprung Hospital, Department of Mental Health

  41. Biggs WS, Demuth RH (2011) Premenstrual syndrome and premenstrual dysphoric disorder. Am Fam Physician 84(8):918–924

    PubMed  Google Scholar 

  42. Hamilton M (2000) Hamilton rating scale for depression (Ham-D). in: handbook of psychiatric measures. APA, Washington DC, pp 526–528

    Google Scholar 

  43. Vacharaporn K, Pitanupong J, Samangsri N (2003) Development of the Edinburgh Postnatal Depression Scale Thai Version. J Mental Health Thai 11(3):164–169

    Google Scholar 

  44. Pitanupong J, Liabsuetrakul T, Vittayanont A (2007) Validation of the Thai Edinburgh Postnatal Depression Scale for screening postpartum depression. Psychiatry Res 149(1–3):253–259

    Article  PubMed  Google Scholar 

  45. Beck AT, Steer RA, Garbin MGJ (1988) Psychometric properties of the Beck Depression Inventory twenty-five years of evaluation. Clin Psych Rev 8:77–100

    Article  Google Scholar 

  46. Spielberger CD, Vagg PR (1984) Psychometric properties of the STAI: a reply to Ramanaiah, Franzen, and Schill. J Pers Assess 48(1):95–97

    Article  CAS  PubMed  Google Scholar 

  47. Maes M, Bosmans E, De Jongh R, Kenis G, Vandoolaeghe E, Neels H (1997) Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment resistant depression. Cytokine 9:853–858

    Article  CAS  PubMed  Google Scholar 

  48. Maes M, Song C, Lin A, Gabriels L, De Jongh R, Van Gastel A, Kenis G, Bosmans E, De Meester I, Benoyt I et al (1998) The effects of psychological stress on humans: increased production of proinflammatory cytokines and a Th-1-like response in stress-induced anxiety. Cytokine 10:313–318

    Article  CAS  PubMed  Google Scholar 

  49. Anderson G, Maes M (2013) Postpartum depression: psychoneuroimmunological underpinnings and treatment. Neuropsychiatr Dis Treat 9:277–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Nowak G (1998) Alterations in zinc homeostasis in depression and antidepressant therapy. Pol J Pharmacol 50(1):1–4

    Article  CAS  PubMed  Google Scholar 

  51. Nowak G, Szewczyk B (2002) Mechanisms contributing to antidepressant zinc actions. Pol J Pharmacol 54:587–592

    CAS  PubMed  Google Scholar 

  52. Bourre JM (2006) Effects of nutrients (in food) on the structure and function of the nervous system: update on dietary requirements for brain. Part 1: micronutrients. J Nutr Health Aging 10(5):377–385

    CAS  PubMed  Google Scholar 

  53. Huang EP (1997) Metal ions and synaptic transmission: think zinc. Proc Natl Acad Sci U S A 94(25):13386–13387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Frederickson CJ, Won Suh S, Silva D, Frederickson CJ, Thomson RB (2000) Importance of zinc in the central nervous system: the zinc-containing neuron. J Nutr 130:1471s–1483s

    CAS  PubMed  Google Scholar 

  55. Maes M, Christophe A, Delanghe J, Altamura C, Neels H, Meltzer HY (1999) Lowered omega3 polyunsaturated fatty acids in serum phospholipids and cholesteryl esters of depressed patients. Psychiatry Res 85(3):275–291

    Article  CAS  PubMed  Google Scholar 

  56. De Vriese SR, Christophe AB, Maes M (2003) Fatty acid composition of phospholipids and cholesteryl esters in maternal serum in the early puerperium. Prostaglandins Leukot Essent Fatty Acids 68(5):331–335

    Article  PubMed  Google Scholar 

  57. Szewczyk B, Pochwat B, Rafało A, Palucha-Poniewiera A, Domin H, Nowak G (2015) Activation of mTOR dependent signaling pathway is a necessary mechanism of antidepressant-like activity of zinc. Neuropharmacology 19(99):517–526

    Article  Google Scholar 

  58. Szewczyk B, Poleszak E, Sowa-Kućma M, Wróbel A, Słotwiński S, Listos J et al (2010) The involvement of NMDA and AMPA receptors in the mechanism of antidepressant-like action of zinc in the forced swim test. Amino Acids 39(1):205–217

    Article  CAS  PubMed  Google Scholar 

  59. Takeda A, Tamano H (2009) Insight into zinc signaling from dietary zinc deficiency. Brain Res Rev 62:33–44

    Article  CAS  PubMed  Google Scholar 

  60. Szewczyk B, Kubera M, Nowak G (2011) The role of zinc in neurodegenerative inflammatory pathways in depression. Prog Neuropsychopharmacol Biol Psychiatry 35(3):693–701

    Article  CAS  PubMed  Google Scholar 

  61. Chen CJ, Liao SL (2003) Neurotrophic and neurotoxic effects of zinc on neonatal cortical neurons. Neurochem Int 42:471–479

    Article  CAS  PubMed  Google Scholar 

  62. Mocchegiani E, Freddari CB, Marcellini F, Malavota M (2005) Brain, aging and neurodegeneration: role of zinc ion availability. Prog Neurobiol 75:367–390

    Article  CAS  PubMed  Google Scholar 

  63. Barrondo S, Sallés J (2009) Allosteric modulation of 5-HT(1A) receptors by zinc: binding studies. Neuropharmacology 56(2):455–462

    Article  CAS  PubMed  Google Scholar 

  64. Szewczyk B, Poleszak E, Wlaź P, Wróbel A, Blicharska E, Cichy A et al (2009) The involvement of serotonergic system in the antidepressant effect of zinc in the forced swim test. Prog Neuropsychopharmacol Biol Psychiatry 33(2):323–329

    Article  CAS  PubMed  Google Scholar 

  65. Lai J, Moxey A, Nowak G, Vashum K, Bailey K (2012) M. M: The efficacy of zinc supplementation in depression: systematic review of randomised controlled trials. J Affect Disord 136(1–2):e31–e39

    Article  CAS  PubMed  Google Scholar 

  66. Nowak G (2015) Zinc, future mono/adjunctive therapy for depression: mechanisms of antidepressant action. Pharmacol Rep 67(3):659–662

    Article  CAS  PubMed  Google Scholar 

  67. Leung BM, Kaplan BJ (2009) Perinatal depression: prevalence, risks, and the nutrition link--a review of the literature. J Am Diet Assoc 109(9):1566–1575

    Article  CAS  PubMed  Google Scholar 

  68. Scrandis DA, Langenberg P, Tonelli LH, Sheikh TM, Manogura AC, Alberico LA, Hermanstyne T, Fuchs D, Mighty H, Hasday JD et al (2008) Prepartum depressive symptoms correlate positively with C-reactive protein levels and negatively with tryptophan levels: a preliminary report. Int J Child Health Hum Dev 1(2):167–174

    PubMed  PubMed Central  Google Scholar 

  69. Verduijn J, Milaneschi Y, Schoevers RA, van Hemert AM, Beekman AT, Penninx BW (2015) Pathophysiology of major depressive disorder: mechanisms involved in etiology are not associated with clinical progression. Transl Psychiatr 29(5):e649

    Article  Google Scholar 

  70. Howren MB, Lamkin DM, Suls J (2009) Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom Med 71:171–186

    Article  CAS  PubMed  Google Scholar 

  71. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK et al (2010) A meta-analysis of cytokines in major depression. Biol Psychiatry 67:446–457

    Article  CAS  PubMed  Google Scholar 

  72. Kroenke KM, Spitzer RLM, Williams JBD (2001) The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med 16:606–613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. de Oliveira LC, Franco-Sena AB, Rebelo F, Farias DR, Lepsch J, Lima Nda S, Kac G (2015) Factors associated with maternal serum C-reactive protein throughout pregnancy: a longitudinal study in women of Rio de Janeiro. Brazil Nutrit 31(9):1103–1108

    Google Scholar 

  74. Coussons-Read ME, Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 21:343–350

    Article  CAS  PubMed  Google Scholar 

  75. Miller GE, Freedland KE, Carney RM, Stetler CA, Banks WA (2003) Pathways linking depression, adiposity, and inflammatory markers in healthy young adults. Brain Behav Immun 17:276–285

    Article  CAS  PubMed  Google Scholar 

  76. Madan JC, Davis JM, Craig WY, Collins M, Allan W, Quinn R et al (2009) Maternal obesity and markers of inflammation in pregnancy. Cytokine 47:61–64

    Article  CAS  PubMed  Google Scholar 

  77. Copeland WE, Shanahan L, Worthman C, Angold A, Costello EJ (2012) Cumulative depression episodes predict later C-reactive protein levels: a prospective analysis. Biol Psychiatry 71(1):15–21

    Article  CAS  PubMed  Google Scholar 

  78. Maes M (2009) “Functional” or “psychosomatic” symptoms, e.g. a flu-like malaise, aches and pain and fatigue, are major features of major and in particular of melancholic depression. Neuro Endocrinol Lett 30(5):564–573

    PubMed  Google Scholar 

  79. Anderson G, Berk M, Maes M (2014) Biological phenotypes underpin the physio-somatic symptoms of somatization, depression, and chronic fatigue syndrome. Acta Psychiatr Scand 129(2):83–97

    Article  CAS  PubMed  Google Scholar 

  80. Wichers MC, Koek GH, Robaeys G, Praamstra AJ, Maes M (2005) Early increase in vegetative symptoms predicts IFN-alpha-induced cognitive-depressive changes. Psychol Med 35(3):433–441

    Article  CAS  PubMed  Google Scholar 

  81. Groer MW, Morgan K (2007) Immune, health and endocrine characteristics of depressed postpartum mothers. Psychoneuroendocrinology 32(2):133–139

    Article  CAS  PubMed  Google Scholar 

  82. Maes M, Mihaylova I, De Ruyter M (2006) Lower serum zinc in Chronic Fatigue Syndrome (CFS): relationships to immune dysfunctions and relevance for the oxidative stress status in CFS. J Affect Disord 90(2–3):141–147

    Article  CAS  PubMed  Google Scholar 

  83. Prasad AS, Fitzgerald JT, Hess JW, Kaplan J, Pelen F, Dardenne M (1993) Zinc deficiency in elderly patients. Nutrition 9:218–224

    CAS  PubMed  Google Scholar 

  84. Vanuytsel T, Vermeire S, Cleynen I (2013) The role of Haptoglobin and its related protein, Zonulin, in inflammatory bowel disease. Tiss Barriers 1(5):e27321

    Article  Google Scholar 

  85. Areekul S, Kitiyanee U, Ukoskit K (1975) Serum haptoglobins in pregnancy. Southeast Asian J Trop Med Public Health 6(4):567–572

    CAS  PubMed  Google Scholar 

  86. Galicia G, Maes W, Verbinnen B, Kasran A, Bullens D, Arredouani M, Ceuppens JL (2009) Haptoglobin deficiency facilitates the development of autoimmune inflammation. Eur J Immunol 39:3404–3412

    Article  CAS  PubMed  Google Scholar 

  87. Van Vlierberghe H, Langlois M, Delanghe J (2004) Haptoglobin polymorphisms and iron homeostasis in health and in disease. Clin Chim Acta 345:35–42

    Article  PubMed  Google Scholar 

  88. Arredouani MS, Kasran A, Vanoirbeek JA, Berger FG, Baumann H, Ceuppens JL (2005) Haptoglobin dampens endotoxin-induced inflammatory effects both in vitro and in vivo. Immunology 114:263–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Bernard D, Christophe A, Delanghe J, Langlois M, De Buyzere M, Comhaire F (2003) The effect of supplementation with an antioxidant preparation on LDL-oxidation is determined by haptoglobin polymorphism. Redox Rep 8(1):41–46

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research has been supported by the Ratchadaphiseksomphot Endowment Fund 2013 of Chulalongkorn University (CU-56-457-HR)

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Authors and Affiliations

  1. Department of Psychiatry, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand

    Chutima Roomruangwong, Buranee Kanchanatawan & Michael Maes

  2. Department of Medicine, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand

    Sunee Sirivichayakul

  3. Laboratory of Biochemistry, Antwerp Hospital Network, Antwerp, Belgium

    Boris Mahieu

  4. Laboratory of Trace Elements Neurobiology, Institute of Pharmacology PAS, Krakow, Poland

    Gabriel Nowak

  5. Department of Pharmacobiology, Jagiellonian University Medical College, Krakow, Poland

    Gabriel Nowak

  6. Department of Psychiatry, Medical University Plovdiv, Plovdiv, Bulgaria

    Michael Maes

  7. Department of Psychiatry, Faculty of Medicine, State University of Londrina, Londrina, Brazil

    Michael Maes

  8. Revitalis Clinic, Waalre, Netherlands

    Michael Maes

  9. IMPACT Strategic Research Center, Barwon Health, Deakin University, Geelong, VIC, Australia

    Michael Maes

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  1. Chutima Roomruangwong
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Roomruangwong, C., Kanchanatawan, B., Sirivichayakul, S. et al. Lower Serum Zinc and Higher CRP Strongly Predict Prenatal Depression and Physio-somatic Symptoms, Which All Together Predict Postnatal Depressive Symptoms. Mol Neurobiol 54, 1500–1512 (2017). https://doi.org/10.1007/s12035-016-9741-5

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