Human colostrum action against Giardia lamblia infection influenced by hormones and advanced maternal age

  • Queli Lisiane Castro Pereira
  • Cristiane de Castro Pernet Hara
  • Rubian Trindade Silva Fernandes
  • Danny Laura Gomes Fagundes
  • Aline do Carmo França-Botelho
  • Maria Aparecida Gomes
  • Eduardo Luzía França
  • Adenilda Cristina Honorio-França
Original Paper
First Online:
Received:
Accepted:
  • 25 Downloads

Abstract

Children are more susceptible to Giardia lamblia infection. Cells and hormones contained in human colostrum have an immunoprotective action against giardiasis, but the effects of advanced maternal age on these components are poorly understood. This study analyzed the colostrum of older women to determine melatonin and cortisol levels besides the participation of these hormones on the functional activity of phagocytes against G. lamblia. Colostrum samples were collected from younger (18 to 35 years old) and older (over 36 years old) lactating women. Colostrum samples were subjected to melatonin and cortisol determination, immunophenotyping, quantification of superoxide release, and assessment of phagocytic rate and microbicidal activity of phagocytes treated with hormones and in the presence of G. lamblia. Colostrum from mothers of advanced age contained higher melatonin and cortisol levels and a lower rate of cells expressing CD14+ and CD15+. In the colostru of these older mothers, melatonin increased superoxide release by phagocytes. In both groups, superoxide release by phagocytes treated with cortisol was higher in the presence of G. lamblia. In colostrum from mothers of advanced age, mononuclear (MN) phagocytes treated with melatonin showed higher phagocytosis of G. lamblia and higher microbicidal index. In younger mothers, MN and polymorphonuclear (PMN) colostrum phagocytes exhibited higher rates of G. lamblia elimination when treated with both melatonin and cortisol. In older mothers, cortisol and melatonin regulation for the functional activity of colostrum phagocytes against G. lamblia may represent an additional defense mechanism, relevant for the protection and treatment of parasitic infections in breastfed children.

Keywords

Giardia lamblia Colostrum Climacteric Phagocytes Hormones 
This is a preview of subscription content, log in to check access

Notes

Acknowledgments

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil; Fundação de Apoio a Pesquisa de Mato Grosso (FAPEMAT), Brazil; and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES, Brazil.

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflict of interest.

References

  1. Bilenko N, Ghosh R, Levy A, Deckelbaum RJ, Fraser D (2008) Partial breastfeeding protects Bedouin infants from infection and morbidity: prospective cohort study. Asia Pac J Clin Nutr 17:243–249PubMedGoogle Scholar
  2. Brandtzaeg P (2010) The mucosal immune system and its integration with the mammary glands. J Pediatr 156:8–15CrossRefGoogle Scholar
  3. Caetano MR, Couto E, Passini Junior R, Simoni RZ, Barini R (2006) Gestational prognostic factors in women with recurrent spontaneous abortion. São Paulo Med J 124:181–185CrossRefPubMedGoogle Scholar
  4. Caspari GR (1993) The influence of colostral leukocytes on the couse of an experimental Escherichia coli infection and serum antibodies in neonatal calves. Vet Immunol Immunopathol 35:275–288CrossRefGoogle Scholar
  5. Cecatti JG, De Aquino MMA (1998) Causes and factors associated to fetal death. Rev Ciênc Méd 7:43–48Google Scholar
  6. Cohen WR (2014) Does maternal age affect pregnancy outcome? BJOG 121:252–254CrossRefPubMedGoogle Scholar
  7. Fagundes DLG, França EL, Hara CCP, Honorio-França AC (2012) Immunomodulatory effects of poly (ethylene glycol) microspheres adsorbed with cortisol on activity of colostrum phagocytes. Int J Pharmacol 8:510–518CrossRefGoogle Scholar
  8. Fagundes DLG, França EL, Morceli G, Rudge MVC, Calderon IPM, Honorio-França AC (2013) The role of cytokines in the functional activity of phagocytes in blood and colostrum of diabetic mothers. Clin Dev Immunol 2013:590190:1–8CrossRefGoogle Scholar
  9. Fagundes DLG, França EL, Fernandes RTS, Hara CCP, Morceli G, Honorio-França AC, Calderon IMP (2016) Changes in T cell phenotype and cytokines profile in maternal blood, cord blood and colostrum of diabetic mothers. J Matern Fetal Neonatal Med 29:998–1004CrossRefGoogle Scholar
  10. Foligne B, Aissaoui F, Senegal-Balas F, Cayuela C, Bernard P, Antoine JM (2001) Changes in cell proliferation and differentiation of adult rat small intestine epithelium after adrenalectomy. Dig Dis Sci 46:1236–1246CrossRefPubMedGoogle Scholar
  11. França EL, Nicomedes TR, Calderon IMP, Honorio-França AC (2010) Time-dependent alterations of soluble and cellular components in human milk. Biol Rhythm Res 41:333–347CrossRefGoogle Scholar
  12. França EL, Bitencourt RV, Fujimori M, Moraes TC, Calderon IMP, Honorio-França AC (2011a) Human colostral phagocytes eliminate enterotoxigenic Escherichia coli opsonized by colostrum supernatant. J Microbiol Immunol Infect 44:1–7CrossRefPubMedGoogle Scholar
  13. França EL, Morceli G, Fagundes DLG, Calderon IMP, Honorio-França AC (2011b) Secretory IgA-Fc alpha receptor interaction modulating phagocytosis and microbicidal activity by phagocytes in human colostrum of diabetics. APMIS 119:710–719CrossRefPubMedGoogle Scholar
  14. Franca EL, Calderon IMP, Vieira EL, Morceli G, Honorio-França AC (2012) Transfer of maternal immunity to newborns of diabetic mothers. Clin Dev Immunol 2012: 928187:1–7CrossRefGoogle Scholar
  15. França-Botelho AC, Honorio-França AC, França EL, Gomes MA, Costa-Cruz JM (2006) Phagocytosis of Giardia lamblia trophozoites by human colostral leukocytes. Acta Paediatr 95:438–443CrossRefPubMedGoogle Scholar
  16. França-Botelho ACF, França JL, Oliveira FC, França EL, Honorio-França AC, Caliari MV, Gomes MA (2011) Melatonin reduces the severity of experimental amoebiasis. Parasit Vectors 4:62–67CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fujimori M, França EL, Moraes TC, Fiori V, Abreu LC, Honorio-Franca AC (2017) Cytokine and adipokine are biofactors can act in blood and colostrum of obese mothers. Biofactors 23:45–51Google Scholar
  18. Garofalo R (2010) Cytokines in human milk. J Pediatr 156:S36–S40CrossRefPubMedGoogle Scholar
  19. Gravena AAF, Sass A, Marcon SS, Pelloso SM (2012) Outcomes in late-age pregnancies. Rev Esc Enferm USP 46:15–21CrossRefPubMedGoogle Scholar
  20. Hara CCP, Honorio-França AC, Fagundes DLG, Guimarães PCL, França EL (2013) Melatonin nanoparticles adsorbed to polyethylene glycol microspheres as activators of human colostrum macrophages. J Nanomater 2:1–8CrossRefGoogle Scholar
  21. Hernandes MRG, Moraes LCA, Ribeiro EB, Fagundes DLG, Honorio-França AC, França EL (2017) In vitro immunomodulatory effects of microemulsions with levamisole delivery systems on blood phagocytes interacting with Giardia lamblia. Parasitol Int 66:299–304CrossRefPubMedGoogle Scholar
  22. Hill DR, Pearson RD (1987) Ingestion of Giardia lamblia trophozoites by human mononuclear phagocytes. Infect Immun 55:3155–3161PubMedPubMedCentralGoogle Scholar
  23. Honorio-França AC, Carvalho MP, Isaac L, Trabulsi LR, Carneiro-Sampaio MMS (1997) Colostral mononuclear phagocytes are able to kill Enteropathogenic Escherichia coli opsonized with colostral IgA. Scand J Immunol 46:59–66CrossRefPubMedGoogle Scholar
  24. Honorio-França AC, Launay P, Carneiro-Sampaio MM, Monteiro RC (2001) Colostral neutrophils express Fc alpha receptors (CD89) lacking gamma chain association and mediate noninflammatory properties of secretory IgA. J Leukoc Biol 69:289–296PubMedGoogle Scholar
  25. Honorio-França AC, Hara CCP, Ormonde JVS, Nunes GT, França EL (2013) Human colostrum melatonin exhibits a day-night variation and modulates the activity of colostral phagocytes. J Appl Biomed 11:153–162CrossRefGoogle Scholar
  26. Hugaes A, Brock JH, Parrott DMV, Cockburn F (1988) The interaction of infant formula with macrophages: effect on phagocytic activity, relationship to expression of class II MHC antigen and survival of orally administered macrophages in the neonatal gut. Immunology 64:213–218Google Scholar
  27. Ignatius R, Gahutu JG, Klotz C, Steininger C, Shyirambere C, Lyng M, Musemakweri A, Aebischer T, Martus P, Harms G, Mockenhaup FP (2012) High prevalence of Giardia duodenalis Assemblage B infection and association with underweight in Rwandan children. PLoS Negl Trop Dis 6:e1677Google Scholar
  28. Jouana PN, Pouliotb Y, Gauthiera SF, Laforest JP (2006) Hormones in bovine milk and milk products. Int Dairy J 16:1408–1414CrossRefGoogle Scholar
  29. Keister DB (1983) Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77:487–488CrossRefPubMedGoogle Scholar
  30. Kohut ML, Martin AE, Senchina DS, Lee W (2005) Glucocorticoids produced during exercise may be necessary for optimal virus-induced IL-2 and cell proliferation whereas both catecholamines and glucocorticoids may be required for adequate immune defense to viral infection. Brain Behav Immun 19:423–435CrossRefPubMedGoogle Scholar
  31. Kreutner AK, Del Bene VE, Amstey MS (1981) Giardiasis in pregnancy. Am J Obstet Gynecol 140:895–901CrossRefPubMedGoogle Scholar
  32. Kunz-Ebrecht SR, Mohamed-Ali V, Feldman PJ, Kirschbaum C, Steptoe A (2003) Cortisol responses to mild psychological stress are inversely associated with proinflammatory cytokines. Brain Behav Immun 17:373–383CrossRefPubMedGoogle Scholar
  33. Lim HY, Muller N, Herold MJ, Van Den Brandt J, Reichardt HM (2007) Glucocorticoids exert opposing effects on macrophage function dependent on their concentration. Immunology 122:47–53CrossRefPubMedPubMedCentralGoogle Scholar
  34. Maestroni GS (2001) The immunotherapeutic potential of melatonin. Expert Opin Investig Drugs 10:467–476CrossRefPubMedGoogle Scholar
  35. Mahmud MA, Chappell CL, Hossain MM, Chappell M, Hossain M, Huang DB, Habib M, Dupont HL (2001) Impact of breast-feeding on Giardia lamblia infections in Bilbeis. Egypt. Am J Trop Med Hyg 65:257–260CrossRefPubMedGoogle Scholar
  36. Medeiros SF, Maitelli A, Nince APB (2007) Effects of the menopause hormone therapy on the immune system. Rev Bras Ginecol Obstet 29:593–601Google Scholar
  37. Moraes LCA, França EL, Pessoa RS, Fagundes DL, Gomes MA, Honorio-França AC (2015) The effect of IFN-γ and TGF-β in the functional activity of mononuclear cells in the presence of Entamoeba histolytica. Parasit Vectors 8:413CrossRefPubMedPubMedCentralGoogle Scholar
  38. Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IMP, Honorio França A (2011) Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 100:550–556CrossRefPubMedGoogle Scholar
  39. Morceli G, Honorio-França AC, Fagundes DLG, Calderon IMP, Franca EL (2013) Antioxidant effect of melatonin on the functional activity of colostral phagocytes in diabetic women. PLoS One 8:569–571CrossRefGoogle Scholar
  40. Pandi-Perumal SR, Trakht I, Srinivasan V, Spence DW, Maestroni GJ, Zisapel N, Cardinali DP (2008) Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Prog Neurobiol 85:335–353CrossRefPubMedGoogle Scholar
  41. Pick E, Mizel D (1981) Rapid microassays for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using an automatic enzyme immunoassay reader. J Immunol Methods 46:211–226CrossRefPubMedGoogle Scholar
  42. Quihui L, Morales GG, Mendez RO, Leyva JG, Romero JE, Valencia ME (2010) Could giardiasis be a risk factor for low zinc status in schoolchildren from northwestern Mexico? A cross-sectional study with longitudinal follow-up. BMC Public Health 10:85–91CrossRefPubMedPubMedCentralGoogle Scholar
  43. Rady MY, Johnson DJ, Patel B, Larson J, Helmers R (2005) Cortisol levels and corticosteroid administration fail to predict mortality in critical illness: the confounding effects of organ dysfunction and sex. Arch Surg 140:661–668CrossRefPubMedGoogle Scholar
  44. Reiner DS, Wang CS, Gillin FD (1986) Human milk kills Giardia lamblia by generating toxic lipolytic products. J Infect Dis 154:825–832CrossRefPubMedGoogle Scholar
  45. Robertson LJK, Hanevik AA, Escobedo K, Mørch N (2010) Langeland, giardiasis—why do the symptoms sometimes never stop? Trends Parasitol 26:75–82CrossRefPubMedGoogle Scholar
  46. Sadeghi H, Borji H (2015) A survey of intestinal parasites in a population in Qazvin, north of Iran. Asian Pac J Trop Dis 5:231–233CrossRefGoogle Scholar
  47. Salazar-Molina A, Klijn TP, Delgado JB (2015) Sexual satisfaction in couples in the male and female climacteric stage Satisfacción sexual en parejas durante el climaterio femenino y masculino Satisfação sexual nos casais durante o climatério feminino e masculino. Cad Saude Publica 31:311–320CrossRefPubMedGoogle Scholar
  48. Sudnikovich EJ, Msksimchik YZ, Zabrodskaya SV, Kubyshin VL, Lapshina EA, Bryszewska M, Reiter RJ, Zavodnik IB (2007) Melatonin attenuates metabolic disordens due to streptozotocin induced diabetes in rats. Eur J Pharmacol 569:180–187CrossRefPubMedGoogle Scholar
  49. Walterspiel JN, Morrow AL, Guerrero L, Ruiz-Palacios GM, Pickering LK (1994) Secretory anti-giardia antibodies in human milk: protective effect against diarrhea. Pediatrics 93:28–31PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Queli Lisiane Castro Pereira
    • 1
    • 2
  • Cristiane de Castro Pernet Hara
    • 1
  • Rubian Trindade Silva Fernandes
    • 1
  • Danny Laura Gomes Fagundes
    • 1
  • Aline do Carmo França-Botelho
    • 3
  • Maria Aparecida Gomes
    • 2
  • Eduardo Luzía França
    • 1
  • Adenilda Cristina Honorio-França
    • 1
  1. 1.Institute of Biological and Health ScienceFederal University of Mato GrossoBarra do GarçasBrazil
  2. 2.Department of Parasitology, Institute of Biological SciencesFederal University of Minas GeraisBelo HorizonteBrazil
  3. 3.Institute of Health SciencesUniversity Center of Planalto de AraxáAraxáBrazil

Personalised recommendations