Research Article
BibTex RIS Cite

The Effects of Refrigerated Storage Time on Sialic Acid and Nitric Oxide Levels and Oxidant Antioxidant System of Human Milk

Year 2023, , 243 - 250, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1293969

Abstract

Objective: Human milk (HM) is a marvelous nutrition that serves all the needs of infants in the first six months with the vitamins, minerals, proteins, carbohydrates, and lipids it contains. For the first 4-6 months of a baby’s life, Nursing is accepted as the most beneficial and recommended feeding method. The greatest technique for providing nutrition in the absence of breastfeeding is through expressed HM. In this case, milk storage conditions become critical. The proper storage of HM is essential for preserving the nutritional and antioxidant properties of HM. This study aims to examine the effects of storing HM in the refrigerator.

Materials and Methods: The effects of storing HM in the refrigerator were examined for four days with regard to the protein profile oxidant-antioxidant balance and nitric oxide (NO) and sialic acid (SA) levels.

Results: Total protein (TP) levels decreased gradually over the four days. In the SDS-PAGE electrophoresis method, the heavy chain sIgA and 𝜅-casein bands also disappeared in HM. While glutathione-S-transferase and superoxide dismutase activities decreased significantly during the first two days, their activities fell below the detection limit in the last two days. While the glutathione level and catalase activity also decreased gradually over the four days, the malondialdehyde, SA, and NO levels increased significantly.

Conclusion: HM can be safely stored in the refrigerator for two days due to the TP, SA, and NO levels, as well as the antioxidant enzyme activities, remaining unchanged from the first day of expressing HM.

Supporting Institution

Marmara University

Project Number

TDK-2021-10306

Thanks

This research was financially supported by TUBITAK (Project ID:321S097) and Marmara University Scientific Research Project Department (Project ID: TDK-2021-10306) which are gratefully acknowledged.

References

  • Kim JH, Froh EB. What nurses need to know regarding nutri-tional and immunobiological properties of human milk. J Obstet Gynecol Neonatal Nurs. 2012;41(1):122-137. google scholar
  • Yi D, Kim S. Human breast milk composition and function in hu-man health: From nutritional components to microbiome and Mi-croRNAs. Nutrients. 2021;13(9):3094. doi:10.3390/nu13093094 google scholar
  • Hendricks G, Guo M. Bioactive components in human milk. Hu-man milk biochemistry and infant formula manufacturing tech-nology. Elsevier; 2014:33-54. google scholar
  • Donovan SM. Human milk proteins: Composition and physiolog-ical significance. nestle Nutr Inst Workshop Ser. 2019;90:93-101. google scholar
  • Marinkovic V, Rankovic-Janevski M, Spasic S, et al. Antioxida-tive activity of colostrum and human milk: Effects of Pasteuriza-tion and storage. J Pediatr Gastroenterol Nutr. 2016;62(6):901-906. google scholar
  • Paduraru L, Dimitriu DC, Avasiloaiei AL, Moscalu M, Zonda GI, Stamatin M. Total antioxidant status in fresh and stored hu-man milk from mothers of term and preterm neonates. Pediatr Neonatol. 2018;59(6):600-605. google scholar
  • Ankrah NA, Appiah-Opong R, Dzokoto C. Human breast-milk storage and the glutathione content. J Trop Pediatr. 2000;46(2):111-113. google scholar
  • Nakano T, Sugawara M, Kawakami H. Sialic acid in hu-man milk: Composition and functions. Acta Paediatr Taiwan. 2001;42(1):11-17. google scholar
  • Ruhaak LR, Stroble C, Underwood MA, Lebrilla CB. Detection of milk oligosaccharides in plasma of infants. Anal Bioanal Chem. 2014;406(24):5775-5784. google scholar
  • Açar Y, Yassibaş E. Anne sütü oligosakkaritleri ve sağlık üzerine etkileri. Gazi Sağlık Bilimleri Dergisi. 2021;6(1):22-33. google scholar
  • Newburg DS. Oligosaccharides in human milk and bacterial col-onization. J Pediatr Gastroenterol Nutr. 2000;30:S8-S17. google scholar
  • Liu F, Simpson AB, D’Costa E, Bunn FS, van Leeuwen SS. Sialic acid, the secret gift for the brain. Crit Rev Food Sci Nutr. 2022:1-20. doi:10.1080/10408398.2022.2072270 google scholar
  • Jantscher-Krenn E, Bode L. Human milk oligosaccharides and their potential benefits for the breast-fed neonate. Minerva Pediatr. 2012;64(1):83-99. google scholar
  • Wang B. Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr. 2009;29:177-222. google scholar
  • Brignon G, Chtourou A, Ribadeau-Dumas B. Preparation and amino acid sequence of human K-casein. FEBS Letters. 1985;188(1):48-54. google scholar
  • Martin HM, Hancock JT, Salisbury V, Harrison R. Role of xan-thine oxidoreductase as an antimicrobial agent. Infect Immun. 2004;72(9):4933-4939. google scholar
  • Stevens CR, Millar TM, Clinch JG, Kanczler JM, Bodamyali T, Blake DR. Antibacterial properties of xanthine oxidase in human milk. The Lancet. 2000;356(9232):829-830. google scholar
  • Yuksel S, Yigit AA, Cinar M, Atmaca N, Onaran Y. Oxidant and antioxidant status of human breast milk during lactation period. Dairy Sci & Technol. 2015;95(3):295-302. google scholar
  • Ulukaya B. Storage of human milk: Effect of temperature and storage conditions on microbiota. Karabük University, Institute of Graduate Programs, Department of Midwifery, Master Thesis, 2022. google scholar
  • Iqbal M, Lestari LA, Kurdanti W, Mardiyati NL. Effect of tem-perature and storage duration on lactose, protein and fat content of breast milk. presented at: International Conference on Health and Well-Being; 2016. google scholar
  • Li X, Gu Y, He S, et al. Influence of pasteurization and storage on dynamic in vitro gastric digestion of milk proteins: Quan-titative insights based on peptidomics. Foods. 2020;9(8):998. doi:10.3390/foods9080998 google scholar
  • Meng F, Uniacke-Lowe T, Ryan AC, Kelly AL. The composition and physico-chemical properties of human milk: A review. Trends Food Sci Technol. 2021;112:608-621. google scholar
  • Miranda KM, Espey MG, Wink DA. A rapid, simple spectropho-tometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide. 2001;5(1):62-71. google scholar
  • Miller EM, Aiello MO, Fujita M, Hinde K, Milligan L, Quinn EA. Field and laboratory methods in human milk research. Am J Hum Biol. 2013;25(1):1-11. google scholar
  • Ledwozyw A, Michalak J, Stepien A, Kadziolka A. The relation-ship between plasma triglycerides, cholesterol, total lipids and lipid peroxidation products during human atherosclerosis. Clin Chim Acta. 1986;155(3):275-283. google scholar
  • Habig WH, Jakoby WB. Assays for differentiation of glutathione S-transferases. Methods Enzymol. 1981;77:398-405. google scholar
  • Aebi H. Catalase. Methods of enzymatic analysis. Elsevier; 1974:673-684. google scholar
  • Mylroie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol. 1986;82(3):512-520. google scholar
  • Beutler E. Reduced Glutathione. In: Bergmeyen HV, ed. Glu-tathione in red blood cell metabolism: A manuel of biochemical methods. Grune and Stratton; 1975:112-114. google scholar
  • Warren L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959;234(8):1971-1975. google scholar
  • Lowry O, Rosebrough N, Farr A, Randall R. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193(1):265-275. google scholar
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680-685. google scholar
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods. 2012;9(7):671-675. google scholar
  • Chang YC, Chen CH, Lin MC. The macronutrients in human milk change after storage in various containers. Pediatr Neonatol. 2012;53(3):205-209. google scholar
  • Abramovich M. Human Milk Storage Conditions in regard to safety and optimal preservation of nutritional properties. Univer-sity of Manitoba (Canada); 2011. google scholar
  • Place M. Donor Breast Milk Banks: The Operation of Donor Milk Bank Services. London: National Institute for Health and Clinical Excellence (NICE); February 2010. google scholar
  • schberger K, Castello P, Hoekstra E, et al. Bisphenol A and baby bottles: Challenges and perspectives. Luxembourg: Publications Office of the European Union. 2010;10:5-50. google scholar
  • Wang B. Sialic acid is an essential nutrient for brain development and cognition. Annu Review Nutr. 2009;29:177-222. google scholar
  • Hauser J, Pisa E, Arias Vasquez A, et al. Sialylated human milk oligosaccharides program cognitive development through a non-genomic transmission mode. Mol Psychiatry. 2021;26(7):2854-2871. google scholar
  • Fernandes JO, Tella SOC, Ferraz IS, Ciampo LAD, Tanus-Santos JE. Assessment of nitric oxide metabolites concentrations in plasma, saliva, and breast milk and their relationship in lactat-ing women. Mol Cell Biochem. 2021;476(2):1293-1302. google scholar
  • Silvestre D, Löpez M, March L, Plaza A, Martinez-Costa C. Bac-tericidal activity of human milk: Stability during storage. Br J Biomed Sci. 2006;63(2):59-62. google scholar
Year 2023, , 243 - 250, 21.12.2023
https://doi.org/10.26650/EurJBiol.2023.1293969

Abstract

Project Number

TDK-2021-10306

References

  • Kim JH, Froh EB. What nurses need to know regarding nutri-tional and immunobiological properties of human milk. J Obstet Gynecol Neonatal Nurs. 2012;41(1):122-137. google scholar
  • Yi D, Kim S. Human breast milk composition and function in hu-man health: From nutritional components to microbiome and Mi-croRNAs. Nutrients. 2021;13(9):3094. doi:10.3390/nu13093094 google scholar
  • Hendricks G, Guo M. Bioactive components in human milk. Hu-man milk biochemistry and infant formula manufacturing tech-nology. Elsevier; 2014:33-54. google scholar
  • Donovan SM. Human milk proteins: Composition and physiolog-ical significance. nestle Nutr Inst Workshop Ser. 2019;90:93-101. google scholar
  • Marinkovic V, Rankovic-Janevski M, Spasic S, et al. Antioxida-tive activity of colostrum and human milk: Effects of Pasteuriza-tion and storage. J Pediatr Gastroenterol Nutr. 2016;62(6):901-906. google scholar
  • Paduraru L, Dimitriu DC, Avasiloaiei AL, Moscalu M, Zonda GI, Stamatin M. Total antioxidant status in fresh and stored hu-man milk from mothers of term and preterm neonates. Pediatr Neonatol. 2018;59(6):600-605. google scholar
  • Ankrah NA, Appiah-Opong R, Dzokoto C. Human breast-milk storage and the glutathione content. J Trop Pediatr. 2000;46(2):111-113. google scholar
  • Nakano T, Sugawara M, Kawakami H. Sialic acid in hu-man milk: Composition and functions. Acta Paediatr Taiwan. 2001;42(1):11-17. google scholar
  • Ruhaak LR, Stroble C, Underwood MA, Lebrilla CB. Detection of milk oligosaccharides in plasma of infants. Anal Bioanal Chem. 2014;406(24):5775-5784. google scholar
  • Açar Y, Yassibaş E. Anne sütü oligosakkaritleri ve sağlık üzerine etkileri. Gazi Sağlık Bilimleri Dergisi. 2021;6(1):22-33. google scholar
  • Newburg DS. Oligosaccharides in human milk and bacterial col-onization. J Pediatr Gastroenterol Nutr. 2000;30:S8-S17. google scholar
  • Liu F, Simpson AB, D’Costa E, Bunn FS, van Leeuwen SS. Sialic acid, the secret gift for the brain. Crit Rev Food Sci Nutr. 2022:1-20. doi:10.1080/10408398.2022.2072270 google scholar
  • Jantscher-Krenn E, Bode L. Human milk oligosaccharides and their potential benefits for the breast-fed neonate. Minerva Pediatr. 2012;64(1):83-99. google scholar
  • Wang B. Sialic acid is an essential nutrient for brain development and cognition. Annu Rev Nutr. 2009;29:177-222. google scholar
  • Brignon G, Chtourou A, Ribadeau-Dumas B. Preparation and amino acid sequence of human K-casein. FEBS Letters. 1985;188(1):48-54. google scholar
  • Martin HM, Hancock JT, Salisbury V, Harrison R. Role of xan-thine oxidoreductase as an antimicrobial agent. Infect Immun. 2004;72(9):4933-4939. google scholar
  • Stevens CR, Millar TM, Clinch JG, Kanczler JM, Bodamyali T, Blake DR. Antibacterial properties of xanthine oxidase in human milk. The Lancet. 2000;356(9232):829-830. google scholar
  • Yuksel S, Yigit AA, Cinar M, Atmaca N, Onaran Y. Oxidant and antioxidant status of human breast milk during lactation period. Dairy Sci & Technol. 2015;95(3):295-302. google scholar
  • Ulukaya B. Storage of human milk: Effect of temperature and storage conditions on microbiota. Karabük University, Institute of Graduate Programs, Department of Midwifery, Master Thesis, 2022. google scholar
  • Iqbal M, Lestari LA, Kurdanti W, Mardiyati NL. Effect of tem-perature and storage duration on lactose, protein and fat content of breast milk. presented at: International Conference on Health and Well-Being; 2016. google scholar
  • Li X, Gu Y, He S, et al. Influence of pasteurization and storage on dynamic in vitro gastric digestion of milk proteins: Quan-titative insights based on peptidomics. Foods. 2020;9(8):998. doi:10.3390/foods9080998 google scholar
  • Meng F, Uniacke-Lowe T, Ryan AC, Kelly AL. The composition and physico-chemical properties of human milk: A review. Trends Food Sci Technol. 2021;112:608-621. google scholar
  • Miranda KM, Espey MG, Wink DA. A rapid, simple spectropho-tometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide. 2001;5(1):62-71. google scholar
  • Miller EM, Aiello MO, Fujita M, Hinde K, Milligan L, Quinn EA. Field and laboratory methods in human milk research. Am J Hum Biol. 2013;25(1):1-11. google scholar
  • Ledwozyw A, Michalak J, Stepien A, Kadziolka A. The relation-ship between plasma triglycerides, cholesterol, total lipids and lipid peroxidation products during human atherosclerosis. Clin Chim Acta. 1986;155(3):275-283. google scholar
  • Habig WH, Jakoby WB. Assays for differentiation of glutathione S-transferases. Methods Enzymol. 1981;77:398-405. google scholar
  • Aebi H. Catalase. Methods of enzymatic analysis. Elsevier; 1974:673-684. google scholar
  • Mylroie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol. 1986;82(3):512-520. google scholar
  • Beutler E. Reduced Glutathione. In: Bergmeyen HV, ed. Glu-tathione in red blood cell metabolism: A manuel of biochemical methods. Grune and Stratton; 1975:112-114. google scholar
  • Warren L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959;234(8):1971-1975. google scholar
  • Lowry O, Rosebrough N, Farr A, Randall R. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193(1):265-275. google scholar
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680-685. google scholar
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods. 2012;9(7):671-675. google scholar
  • Chang YC, Chen CH, Lin MC. The macronutrients in human milk change after storage in various containers. Pediatr Neonatol. 2012;53(3):205-209. google scholar
  • Abramovich M. Human Milk Storage Conditions in regard to safety and optimal preservation of nutritional properties. Univer-sity of Manitoba (Canada); 2011. google scholar
  • Place M. Donor Breast Milk Banks: The Operation of Donor Milk Bank Services. London: National Institute for Health and Clinical Excellence (NICE); February 2010. google scholar
  • schberger K, Castello P, Hoekstra E, et al. Bisphenol A and baby bottles: Challenges and perspectives. Luxembourg: Publications Office of the European Union. 2010;10:5-50. google scholar
  • Wang B. Sialic acid is an essential nutrient for brain development and cognition. Annu Review Nutr. 2009;29:177-222. google scholar
  • Hauser J, Pisa E, Arias Vasquez A, et al. Sialylated human milk oligosaccharides program cognitive development through a non-genomic transmission mode. Mol Psychiatry. 2021;26(7):2854-2871. google scholar
  • Fernandes JO, Tella SOC, Ferraz IS, Ciampo LAD, Tanus-Santos JE. Assessment of nitric oxide metabolites concentrations in plasma, saliva, and breast milk and their relationship in lactat-ing women. Mol Cell Biochem. 2021;476(2):1293-1302. google scholar
  • Silvestre D, Löpez M, March L, Plaza A, Martinez-Costa C. Bac-tericidal activity of human milk: Stability during storage. Br J Biomed Sci. 2006;63(2):59-62. google scholar
There are 41 citations in total.

Details

Primary Language English
Subjects Plant Cell and Molecular Biology, Animal Cell and Molecular Biology
Journal Section Themed Articles - Research Articles
Authors

Begüm Gürel Gökmen 0000-0002-3955-1948

Tuğba Tunalı-akbay 0000-0002-2091-9298

Project Number TDK-2021-10306
Publication Date December 21, 2023
Submission Date May 8, 2023
Published in Issue Year 2023

Cite

AMA Gürel Gökmen B, Tunalı-akbay T. The Effects of Refrigerated Storage Time on Sialic Acid and Nitric Oxide Levels and Oxidant Antioxidant System of Human Milk. Eur J Biol. December 2023;82(2):243-250. doi:10.26650/EurJBiol.2023.1293969