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Variation of human milk oligosaccharides in relation to milk groups and lactational periods

  • Stephan Thurl (a1), Manfred Munzert (a2), Jobst Henker (a3), Günther Boehm (a4) (a5), Beate Müller-Werner (a4), Jürgen Jelinek (a4) and Bernd Stahl (a4)...


Human milk oligosaccharides, representing the third largest fraction of human milk, have been assigned important protective functions for newborns acting as bifidogenic substrates or as inhibitory agents towards pathogens. Using high-pH anion-exchange chromatography and an enzyme test kit, twenty oligosaccharides and lactose were determined in milk samples of German women from days 3 to 90 postpartum. Twenty-two secretor mothers with Lewis blood group Le(a − b+) synthesised all twenty oligosaccharides, and could be assigned to milk group 1. Five non-secretor mothers (Le(a+b − )) produced all oligosaccharides with the exception of α1,2-fucosylated compounds (milk group 2), whereas three secretor mothers with blood type Le(a − b − ) lacked α1,4-fucosyloligosaccharides, corresponding to milk group 3. Secretor women of milk groups 1 and 3 synthesised significantly higher amounts of total neutral oligosaccharides and of several total core structures (e.g. lacto-N-tetraose) than non-secretor women. Generally, these oligosaccharides significantly decrease during the first 3 months postpartum. By comparing fucosyloligosaccharides within and among the three milk groups, insight into their biosynthesis could be gained. Six acidic oligosaccharides without fucose residues were detected in milk samples of all mothers. Regression analysis confirmed that total acidic oligosaccharides declined threefold during the study period. Milk samples corresponding to the three milk groups exhibited significant qualitative and quantitative differences during the first 3 months of lactation. It can be assumed that particularly milk of non-secretor women (milk group 2) exerts a modified biological protection in the babies in comparison with milks of secretors (groups 1 and 3).

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Corresponding author

*Corresponding author: S. Thurl, fax +49 661 9640 505, email


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1 Montreuil, J & Mullet, S (1960) Étude des variations des constituents glucidiques du lait de femme au cours de la lactation (Study of changes in carbohydrate constituents of human breast milk during lactation). Bull Soc Chim Biol 42, 365377.
2 Viverge, D, Grimmonprez, L, Cassanas, G, et al. (1985) Variations of lactose and oligosaccharides in milk from women of blood types secretor A or H, secretor Lewis, and secretor H/nonsecretor Lewis during the course of lactation. Ann Nutr Metab 29, 111.
3 Coppa, GV, Gabrielli, O, Pierani, P, et al. (1993) Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics 91, 637641.
4 Stahl, B, Thurl, S, Zeng, J, et al. (1994) Oligosaccharides from human milk as revealed by matrix-assisted laser desorption/ionization mass spectrometry. Anal Biochem 223, 218226.
5 Kobata, A, Yamashita, K & Tachibana, Y (1978) Oligosaccharides from human milk. Methods Enzymol 50, 216220.
6 Bruntz, R, Dabrowski, U, Dabrowski, J, et al. (1988) Fucose-containing oligosaccharides from human milk from a donor of blood group O Le(a) nonsecretor. Biol Chem Hoppe-Seyler 369, 257273.
7 Haeuw-Fievre, S, Wieruszeski, JM, Plancke, Y, et al. (1993) Primary structure of human milk octa-, dodeca- and tridecasaccharides determined by a combination of 1H-NMR spectroscopy and fast-atom bombardment mass spectrometry. Eur J Biochem 215, 361371.
8 Boehm, G & Stahl, B (2003) Oligosaccharides. In Functional Dairy Products, pp. 203243 [Mattila-Sandholm, T and Scarela, M, editors]. Boca Raton: CRC Press.
9 Henry, SM, Oriol, R & Samuelsson, BE (1994) Detection and characterization of Lewis antigens in plasma of Lewis-negative individuals. Vox Sang 67, 387396.
10 Oriol, R, Le Pendu, J & Mollicone, R (1986) Genetics of ABO, H, Lewis, X and related antigens. Vox Sang 51, 161171.
11 Ma, B, Simala-Grant, JL & Taylor, DE (2006) Review: fucosylation in prokaryotes and eukaryotes. Glycobiology 16, 158R184R.
12 Watkins, WM, Greenwell, P, Yates, AD, et al. (1988) Regulation of expression of carbohydrate blood group antigens. Biochimie 70, 15971611.
13 Kobata, A (1977) Milk glycoproteins and oligosaccharides. In The Glycoconjugates, vol. 1, pp. 423440 [Horowitz, M and Pigman, W, editors]. New York: Academic Press.
14 Thurl, S, Henker, J, Siegel, M, et al. (1997) Detection of four human milk groups with respect to Lewis blood group dependent oligosaccharides. Glycoconjugate J 14, 795799.
15 Coppa, GV, Pierani, P, Zampini, L, et al. (1999) Oligosaccharides in human milk during different phases of lactation. Acta Paediatr Suppl 430, 8994.
16 Grönberg, G, Lipniunas, P, Lundgren, T, et al. (1992) Structural analysis of five new monosialylated oligosaccharides from human milk. Arch Biochem Biophys 296, 597610.
17 Donovan, SM (2009) Invited Commentary: human milk oligosaccharides – the plot thickens. Br J Nutr 101, 12671269.
18 Bode, L (2009) Human milk oligosaccharides: prebiotics and beyond. Nutr Rev 67, Suppl. 2, S183S191.
19 Ruiz-Palacios, MG, Cervantes, LE, Ramos, P, et al. (2003) Campylobacter jejuni binds intestinal H(O) antigen (Fuc α1, 2Galβ1,4GlcNAc), and fucosyloligosaccharides from human milk inhibit its binding and infection. J Biol Chem 278, 1411214120.
20 Kunz, C, Rudloff, S, Baier, W, et al. (2000) Oligosaccarides in human milk: structural, functional and metabolic aspects. Annu Rev Nutr 20, 699722.
21 György, P, Norris, RF & Rose, CS (1954) Bifidus factor. I. A variant of Lactobacillus bifidus requiring a special growth factor. Arch Biochem Biophys 48, 193202.
22 Gauhe, A, György, P, Hoover, JRE, et al. (1954) Bifidus factor. IV. Preparations obtained from human milk. Arch Biochem Biophys 48, 214224.
23 Coppa, GV, Zampini, L, Galeazzi, T, et al. (2006) Prebiotics in human milk: a review. Dig Liver Dis 38, Suppl. 2, S291S294.
24 Viverge, D, Grimmonprez, L, Cassanas, G, et al. (1990) Discriminant carbohydrate components of human milk according to donor secretor types. J Pediatr Gastroenterol Nutr 11, 365370.
25 Erney, RM, Malone, WT, Skelding, MB, et al. (2000) Variability of human milk neutral oligosaccharides in a diverse population. J Pediatr Gastroenterol Nutr 30, 181192.
26 Chaturvedi, P, Warren, CD, Altaye, M, et al. (2001) Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology 11, 365372.
27 Sumiyoshi, W, Urashima, T, Nakamura, T, et al. (2003) Determination of each neutral oligosaccharide in the milk of Japanese women during the course of lactation. Br J Nutr 89, 6169.
28 Newburg, DS, Ruiz-Palacios, GM, Altaye, M, et al. (2004) Innate protection conferred by fucosylated oligosaccharides of human milk against diarrhea in breastfed infants. Glycobiology 14, 253263.
29 Martín-Sosa, S, Martín, MJ, García-Prado, LA, et al. (2003) Sialyloligosaccharides in human and bovine milk and in infant formulas: variations with the progression of lactation. J Dairy Sci 86, 5259.
30 Asakuma, S, Akahori, M, Kimura, K, et al. (2007) Sialyl oligosaccharides of human colostrum: changes in concentration during the first three days of lactation. Biosci Biotechnol Biochem 71, 14471451.
31 Bao, Y, Zhu, L & Newburg, DS (2007) Simultaneous quantification of sialyloligosaccharides from human milk by capillary electrophoresis. Anal Biochem 370, 206214.
32 Thurl, S, Müller-Werner, B & Sawatzki, G (1996) Quantification of individual oligosaccharide compounds from human milk using high-pH anion-exchange chromatography. Anal Biochem 235, 202206.
33 Thurl, S, Henker, J, Siegel, M, et al. (1998) Lewis blood groups of breastfeeding women tested serologically and by chromatographic analysis of human milk oligosaccharides. Milchwissenschaft 53, 127129.
34 Viverge, D, Grimmonprez, L, Cassanas, G, et al. (1986) Diurnal variations and within the feed in lactose and oligosaccharides of human milk. Ann Nutr Metab 30, 196209.
35 Neville, MC, Keller, RP, Casey, CE, et al. (1984) Studies on human lactation. I. Within-feed and between-breast variation in selected components of human milk. Am J Clin Nutr 40, 635646.
36 Thurl, S, Henker, J, Taut, H, et al. (1993) Variations of neutral oligosaccharides and lactose in human milk during the feeding. Z Ernährungswiss 32, 262269.
37 Wiederschain, GY & Newburg, DS (2001) Glycoconjugate stability in human milk: glycosidase activities and sugar release. J Nutr Biochem 12, 559564.
38 Bertino, E, Coppa, GV, Giuliani, F, et al. (2008) Effects of Holder pasteurization on human milk oligosaccharides. Int J Immunopathol Pharmacol 21, 381385.
39 Beutler, HO (1984) Lactose and d-galactose. In Methods in Enzymatic Analysis, vol. 6, pp. 104112 [Bergmeyer, HU, editor]. Weinheim, Deerfield Beach, Basel: Verlag Chemie.
40 SAS Institute Inc (2002–2003) SAS/STAT. Release 9.1. Cary, NC: SAS Institute, Inc.
41 Musumeci, M, Simpore, J, D'Agata, A, et al. (2006) Oligosaccharides in colostrum of Italian and Burkinabe women. J Pediatr Gastroenterol Nutr 43, 372378.
42 Kobata, A (2004) Minireview: the third chains of living organisms – a trail of glycobiology that started from the third floor of building 4 in NIH. Arch Biochem Biophys 426, 107121.
43 Kumazaki, T & Yoshida, A (1984) Biochemical evidence that secretor gene, Se, is a structural gene encoding a specific fucosyltransferase. Proc Natl Acad Sci U S A 81, 41934197.
44 Costache, M, Apoil, PA, Cailleau, A, et al. (1997) Evolution of fucosyltransferase genes in vertebrates. J Biol Chem 272, 2972129728.
45 Mollicone, R, Gibaud, A, Francois, A, et al. (1990) Acceptor specificity and tissue distribution of three human α-3-fucosyltransferases. Eur J Biochem 191, 169176.
46 Johnson, PH, Donald, ASR, Feeney, J, et al. (1992) Reassessment of the acceptor specificity and general properties of the Lewis blood-group gene associated α-3/4-fucosyltransferases purified from human milk. Glycoconjugate J 9, 251264.
47 Costa, J, Grabenhorst, E, Nimtz, M, et al. (1997) Stable expression of the golgi form and secretory variants of human fucosyltransferase III from BHK-21 cells. J Biol Chem 272, 1161311621.
48 Legaigneur, P, Breton, C, Battari, AE, et al. (2001) Exploring the acceptor substrate recognition of the human ß-galactoside α2,6-sialyltransferase. J Biol Chem 276, 2160821617.
49 Harduin-Lepers, A, Vallejo-Ruiz, V, Krzewinski-Recchi, MA, et al. (2001) The human sialyltransferase family. Biochimie 83, 727737.
50 Engfer, MB, Stahl, B, Finke, B, et al. (2000) Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract. Am J Clin Nutr 71, 15891596.
51 Gnoth, MJ, Kuntz, C, Kinne-Saffran, E, et al. (2000) Human milk oligosaccharides are minimally ingested in vitro. J Nutr 130, 30143020.
52 Wada, J, Ando, T, Kiyohara, M, et al. (2008) Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl Environ Microbiol 74, 39964004.
53 Neville, MC, Keller, R, Seacat, J, et al. (1988) Studies in human lactation: milk volumes in lactating women during the onset of lactation and full lactation. Am J Clin Nutr 48, 13751386.
54 Cravioto, A, Tello, A, Villafán, H, et al. (1991) Inhibition of localized adhesion of enteropathogenic Escherichia coli to Hep-2 cells by immunoglobulin and oligosaccharide fractions of human colostrum and breast milk. J Infect Dis 163, 12471255.
55 Jiang, X, Huang, P, Zhong, W, et al. (2004) Human milk contains elements that block binding of noroviruses to human histo-blood group antigens in saliva. J Infect Dis 190, 18501859.
56 Sinclair, HR, Smejkal, CW, Glister, C, et al. (2008) Sialyloligosaccharides inhibit cholera toxin binding to the GM1 receptor. Carbohydrate Res 343, 25892594.
57 Obermeier, S, Rudloff, S, Pohlentz, G, et al. (1999) Secretion of 13C-labelled oligosaccharides into human milk and infant's urine after oral [13]galactose load. Isotopes Environ Health Stud 35, 119125.
58 Bode, L, Rudloff, S, Kunz, C, et al. (2004) Human milk oligosaccharides reduce platelet–neutrophil complex formation leading to a decrease in neutrophil ß 2 integrin expression. J Leukoc Biol 76, 820826.
59 Bode, L, Kunz, C, Muhly-Reinholz, M, et al. (2004) Inhibition of monocyte, lymphocyte, and neutrophil adhesion to endothelial cells by human milk oligosaccharides. Thromb Haemost 92, 14021410.


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