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

Molecular Neurobiology

Volumn 54, Issue 2, 2017, Pages 1500-1512

  Roomruangwong, Chutima ^a   Kanchanatawan, Buranee ^a   Sirivichayakul, Sunee ^a   Mahieu, Boris ^b   Nowak, Gabriel ^c,d   Maes, Michael ^a,e,f,g,h  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b Hospital Network Antwerp   (Belgium)

^c INSTITUTE OF PHARMACOLOGY   (Poland)

^d JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^e MEDICAL UNIVERSITY OF PLOVDIV   (Bulgaria)

^f STATE UNIVERSITY OF LONDRINA   (Brazil)

^g Revitalis   (Netherlands)

^h DEAKIN UNIVERSITY   (Australia)

Author keywords

Chronic fatigue; Cytokines; Immune; Inflammation; PMS; Postnatal; Prenatal

Indexed keywords

C REACTIVE PROTEIN; HAPTOGLOBIN; ZINC; AUTACOID; BIOLOGICAL MARKER;

ADULT; ANXIETY DISORDER; ARTICLE; BACKACHE; BECK DEPRESSION INVENTORY; BODY MASS; CONSTIPATION; CONTROLLED STUDY; DISEASE SEVERITY; DYSPEPSIA; DYSTHYMIA; EDINBURGH POSTNATAL DEPRESSION SCALE; FATIGUE; FEMALE; FIRST TRIMESTER PREGNANCY; HAMILTON DEPRESSION RATING SCALE; HUMAN; IMMUNE ACTIVATION; IMMUNE INFLAMMATORY PATHOPHYSIOLOGY; IMMUNE RESPONSE; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MYALGIA; PATHOPHYSIOLOGY; PERINATAL DEPRESSION; PREDICTION; PREGNANT WOMAN; PREMENSTRUAL SYNDROME; PROTEIN BLOOD LEVEL; PUERPERAL DEPRESSION; SECOND TRIMESTER PREGNANCY; STATE TRAIT ANXIETY INVENTORY; SYMPTOM; ZINC BLOOD LEVEL; BLOOD; MEDICALLY UNEXPLAINED SYMPTOM; METABOLISM; POSTNATAL DEPRESSION; PREDICTIVE VALUE; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL CARE; PROCEDURES; PSYCHOLOGICAL RATING SCALE;

ADULT; BIOMARKERS; C-REACTIVE PROTEIN; DEPRESSION, POSTPARTUM; FATIGUE; FEMALE; HUMANS; INFLAMMATION MEDIATORS; MEDICALLY UNEXPLAINED SYMPTOMS; PREDICTIVE VALUE OF TESTS; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL CARE; PSYCHIATRIC STATUS RATING SCALES; ZINC;

EID: 84957545994     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-016-9741-5     Document Type: Article

References (89)

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
2. Maes M (1995) Evidence for an immune response in major depression: a review and hypothesis. Prog Neuropsychopharmacol Biol Psychiatry 19(1):11–38
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
22. Aggett PJ, Harries JT (1979) Current status of zinc in health and disease states. Arch Dis Child 54(12):909–917
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
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
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
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
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
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
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
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
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
32. Shelton MM, Schminkey DL, Groer MW (2015) Relationships among prenatal depression, plasma cortisol, and inflammatory cytokines. Biol Res Nurs 17(3):295–302
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
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
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
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
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
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
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
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
42. Hamilton M (2000) Hamilton rating scale for depression (Ham-D). in: handbook of psychiatric measures. APA, Washington DC, pp 526–528
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
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
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
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
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
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
49. Anderson G, Maes M (2013) Postpartum depression: psychoneuroimmunological underpinnings and treatment. Neuropsychiatr Dis Treat 9:277–287
50. Nowak G (1998) Alterations in zinc homeostasis in depression and antidepressant therapy. Pol J Pharmacol 50(1):1–4
51. Nowak G, Szewczyk B (2002) Mechanisms contributing to antidepressant zinc actions. Pol J Pharmacol 54:587–592
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
53. Huang EP (1997) Metal ions and synaptic transmission: think zinc. Proc Natl Acad Sci U S A 94(25):13386–13387
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
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
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
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
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
59. Takeda A, Tamano H (2009) Insight into zinc signaling from dietary zinc deficiency. Brain Res Rev 62:33–44
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
61. Chen CJ, Liao SL (2003) Neurotrophic and neurotoxic effects of zinc on neonatal cortical neurons. Neurochem Int 42:471–479
62. Mocchegiani E, Freddari CB, Marcellini F, Malavota M (2005) Brain, aging and neurodegeneration: role of zinc ion availability. Prog Neurobiol 75:367–390
63. Barrondo S, Sallés J (2009) Allosteric modulation of 5-HT(1A) receptors by zinc: binding studies. Neuropharmacology 56(2):455–462
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
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
66. Nowak G (2015) Zinc, future mono/adjunctive therapy for depression: mechanisms of antidepressant action. Pharmacol Rep 67(3):659–662
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
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
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
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
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
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
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
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
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
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
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
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
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
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
81. Groer MW, Morgan K (2007) Immune, health and endocrine characteristics of depressed postpartum mothers. Psychoneuroendocrinology 32(2):133–139
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
83. Prasad AS, Fitzgerald JT, Hess JW, Kaplan J, Pelen F, Dardenne M (1993) Zinc deficiency in elderly patients. Nutrition 9:218–224
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
85. Areekul S, Kitiyanee U, Ukoskit K (1975) Serum haptoglobins in pregnancy. Southeast Asian J Trop Med Public Health 6(4):567–572
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
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
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
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