Background/Aims: The aim of the present study was to identify and quantify the polyamine levels in human milk obtained from different countries and through different modes of delivery, and to investigate their association with breast milk microbes. Methods: Mature breast milk samples were obtained from 78 healthy mothers after 1 month of lactation from 4 different geographical locations: Finland, Spain (Europe); South Africa (Africa); and China (Asia). Polyamines were determined using HPLC after dansyl derivatization and milk microbiota was obtained by 16S rRNA gene sequencing. Results: The mean values of polyamines in breast milk were 70.0, 424.2, and 610.0 nmol/dL for putrescine, spermidine and spermine, respectively, and 1,170.9 nmol/dL of total polyamines. The levels of putrescine were significantly higher in Spain (p < 0.05) and spermidine levels were significantly higher in Finland (p < 0.05) compared with other countries. Cesarean delivery had an impact on polyamine levels and it was related to an increase in the putrescine concentration being significant in Spanish samples (p < 0.01). Furthermore, putrescine levels were correlated positively with Gammaproteobacteria (r = 0.46, p < 0.001), especially with Pseudomonas fragi (r = 0.40, p < 0.001). Conclusions: The results demonstrate significant effect of geographical variations in human milk polyamine concentrations, being correlated with human milk microbiota composition. These differences may have an impact on infant development during lactation.

Keywords:
Polyamines, Putrescine, Spermidine, Spermine, Caesarean, Breast milk, Microbiota, Proteobacteria
1.
Michael AJ: Polyamines in eukaryotes, bacteria, and archaea. J Biol Chem 2016;291:14896-14903.
2.
Pegg AE: Functions of polyamines in mammals. J Biol Chem 2016;291:14904-14912.
3.
Atiya Ali M, Strandvik B, Sabel KG, Palme Kilander C, Strömberg R, Yngve A: Polyamine levels in breast milk are associated with mothers' dietary intake and are higher in preterm than full-term human milk and formulas. J Hum Nutr Diet 2014;27:459-467.
4.
Buts JP, De keyser N, De Raedemaeker L, Collette E, Sokal EM: Polyamine profiles in human milk, infant artificial formulas, and semi-elemental diets. J Pediatr Gastroenterol Nutr 1995;21:44-49.
5.
Romain N, Dandrifosse G, Jeusette F, Forget P: Polyamine concentration in rat milk and food, human milk, and infant formulas. Pediatr Res 1992;32:58-63.
6.
Rezaei R, Wu Z, Hou Y, Bazer FW, Wu G: Amino acids and mammary gland development: nutritional implications for milk production and neonatal growth. J Anim Sci Biotechnol 2016;7:20.
7.
Rillema JA, Collins S, Williams CH: Prolactin stimulation of iodide uptake and incorporation into protein is polyamine-dependent in mouse mammary gland explants. Proc Soc Exp Biol Med 2000;224:41-44.
8.
Loser C: Polyamines in human and animal milk. Br J Nutr 2000;84(suppl 1):S55-S58.
9.
Dandrifosse G, Peulen O, El Khefif N, Deloyer P, Dandrifosse AC, Grandfils C: Are milk polyamines preventive agents against food allergy? Proc Nutr Soc 2000;59:81-86.
10.
Sabater-Molina M, Larqué E, Torrella F, Plaza J, Lozano T, Muñoz A, Zamora S: Effects of dietary polyamines at physiologic doses in early-weaned piglets. Nutrition 2009;25:940-946.
11.
Peulen O, Deloyer P, Grandfils C, Loret S, Dandrifosse G: Intestinal maturation induced by spermine in young animals. Livestock Prod Sci 2000;66:109-120.
12.
Gómez-Gallego C, Frias R, Pérez-Martínez G, Bernal MJ, Periago MJ, Salminen S, Ros G, Collado MC: Polyamine supplementation in infant formula: influence on lymphocyte populations and immune system-related gene expression in a Balb/cOlaHsd mouse model. Food Res Int 2014;59:8-15.
13.
Perez-Cano FJ, Gonzalez-Castro A, Castellote C, Franch A, Castell M: Influence of breast milk polyamines on suckling rat immune system maturation. Dev Comp Immunol 2010;34:210-218.
14.
Gómez-Gallego C, Collado MC, Pérez G, Ilo T, Jaakkola UM, Bernal MJ, Periago MJ, Frias R, Ros G, Salminen S: Resembling breast milk: influence of polyamine-supplemented formula on neonatal BALB/cOlaHsd mouse microbiota. Br J Nutr 2014;111:1050-1058.
15.
Gómez-Gallego C, Collado MC, Ilo T, Jaakkola UM, Bernal MJ, Periago MJ, Salminen S, Ros G, Frias R: Infant formula supplemented with polyamines alters the intestinal microbiota in neonatal BALB/cOlaHsd mice. J Nutr Biochem 2012;23:1508-1513.
16.
Bardocz S: Polyamines in food and their consequences for food quality and human health. Trends Food Sci Technol 1995;6:341-346.
17.
Peulen O, Dewe W, Dandrifosse G, Henrotay I, Romain N: The relationship between spermine content of human milk during the first postnatal month and allergy in children. Public Health Nutr 1998;1:181-184.
18.
Martin V, Maldonado-Barragan A, Moles L, Rodriguez-Banos M, del Campo R, Fernandez L, Rodriguez JM, Jimenez E: Sharing of bacterial strains between breast milk and infant feces. J Hum Lact 2012;28:36-44.
19.
Cabrera-Rubio R, Mira-Pascual L, Mira A, Collado MC: Impact of mode of delivery on the milk microbiota composition of healthy women. J Dev Orig Health Dis 2016;7:54-60.
20.
Kumar H, du Toit E, Kulkarni A, Aakko J, Linderborg KM, Zhang Y, Nicol MP, Isolauri E, Yang B, Collado MC, Salminen S: Distinct patterns in human milk microbiota and fatty acid profiles across specific geographic locations. Front Microbiol 2016;7:1619.
21.
Khodayar-Pardo P, Mira-Pascual L, Collado MC, Martinez-Costa C: Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J Perinatol 2014;34:599-605.
22.
Wortham BW, Patel CN, Oliveira MA: Polyamines in bacteria: pleiotropic effects yet specific mechanisms. Adv Exp Med Biol 2007;603:106-115.
23.
Di Martino ML, Campilongo R, Casalino M, Micheli G, Colonna B, Prosseda G: Polyamines: emerging players in bacteria-host interactions. Int J Med Microbiol 2013;303:484-491.
24.
Orlando A, Linsalata M, Notarnicola M, Tutino V, Russo F: Lactobacillus GG restoration of the gliadin induced epithelial barrier disruption: the role of cellular polyamines. BMC Microbiol 2014;14:19.
25.
Gomez-Gallego C, Recio I, Gomez-Gomez V, Ortuno I, Bernal MJ, Ros G, Periago MJ: Effect of processing on polyamine content and bioactive peptides released after in vitro gastrointestinal digestion of infant formulas. J Dairy Sci 2016;99:924-932.
26.
Galitsopoulou A, Michaelidou AM, Menexes G, Alichanidis E: Polyamine profile in ovine and caprine colostrum and milk. Food Chem 2015;173:80-85.
27.
Dorhout B, van Beusekom CM, Huisman M, Kingma AW, de Hoog E, Boersma ER, Muskiet FA: Estimation of 24-hour polyamine intake from mature human milk. J Pediatr Gastroenterol Nutr 1996;23:298-302.
28.
Pollack PF, Koldovsky O, Nishioka K: Polyamines in human and rat milk and in infant formulas. Am J Clin Nutr 1992;56:371-375.
29.
Abdulhussein AA, Wallace HM: Polyamines and membrane transporters. Amino Acids 2014;46:655-660.
30.
Jimenez E, Ladero V, Chico I, Maldonado-Barragan A, Lopez M, Martin V, Fernandez L, Fernandez M, Alvarez MA, Torres C, Rodriguez JM: Antibiotic resistance, virulence determinants and production of biogenic amines among enterococci from ovine, feline, canine, porcine and human milk. BMC Microbiol 2013;13:288.
31.
Hamana K, Matsuzaki S: Polyamine distribution patterns serve as a phenotypic marker in the chemotaxonomy of the proteobacteria. Can J Microbiol 1993;39:304-310.
32.
Perez M, Ladero V, Redruello B, del Rio B, Fernandez L, Miguel Rodriguez J, Cruz Martin M, Fernandez M, Alvarez MA: Mastitis modifies the biogenic amines profile in human milk, with significant changes in the presence of histamine, putrescine and spermine. PLoS One 2016;11:e0162426.
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2017
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