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Milk Fermented by Lactic Acid Bacteria Enhances the Absorption of Dietary Sphingomyelin in Rats

  • Original Article
  • Published:
Lipids

Abstract

Supplementation with sphingomyelin has been reported to prevent disease and maintain good health. However, intact sphingomyelin and ceramides are poorly absorbed compared with glycerolipids. Therefore, if the bioavailability of dietary sphingomyelin can be increased, supplementation would be more effective at lower doses. The aim of this study in rats was to evaluate the effect of fermented milk on the bioavailability of dietary sphingomyelin in rats. After the rats had fasted for 15 h, test solutions were administrated orally. Blood samples were collected from the tail vein before and 90, 180, 270, and 360 min after administration. Compared with sphingomyelin/milk phospholipids concentrate (MPL) alone, co-ingestion of sphingomyelin/MPL with fermented milk caused an approximate twofold significant increase in serum ceramides containing d16:1 sphingosine with 16:0, 22:0, 23:0 and 24:0 fatty acids, which was derived from the ingested sphingomyelin. While nonfat milk also increased the serum levels of these ceramides, fermented milk was more effective. Co-ingestion of the upper layer of fermented milk or exopolysaccharide concentrate prepared from fermented milk significantly increased serum ceramide levels. X-ray diffraction analysis also showed addition of fermented milk or EPS concentrate to sphingomyelin eliminated the characteristic peak of sphingomyelin. This study demonstrated for the first time that co-ingestion of dietary sphingomyelin and fermented milk, compared with ingestion of dietary sphingomyelin alone, caused a significant increase in the absorption of sphingomyelin. Our results indicate exopolysaccharides in fermented milk may contribute to inhibition of sphingomyelin crystallization, resulting in enhanced absorption of dietary sphingomyelin in rats.

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Abbreviations

AUC:

The area under the serum concentration–time curve

EPS:

Exopolysaccharide

HPLC–MS/MS:

High-performance liquid chromatography–tandem mass spectrometry

LOQ:

Limit of quantification

MPL:

Milk phospholipids concentrate

MRM:

Multiple-reaction-monitoring

XRD:

X-ray diffraction

References

  1. Vesper H, Schmelz EM, Nikolova-Karakashian MN, Dillehay DL, Lynch DV, Merrill AH Jr (1999) Sphingolipids in food and the emerging importance of sphingolipids to nutrition. J Nutr 129:1239–1250

    CAS  PubMed  Google Scholar 

  2. Zeisel SH, Char D, Sheard NF (1986) Choline, phosphatidylcholine and sphingomyelin in human and bovine milk and infant formulas. J Nutr 116:50–58

    CAS  PubMed  Google Scholar 

  3. Zeisel SH, Mar MH, Howe JC, Holden JM (2003) Concentrations of choline-containing compounds and betaine in common foods. J Nutr 133:1302–1307

    CAS  PubMed  Google Scholar 

  4. Watanabe S, Takahashi T, Tanaka L, Haruta Y, Shiota M, Hosokawa M, Miyashita K (2011) The effect of milk polar lipids separated from butter serum on the lipid levels in the liver and the plasma of obese-model mouse (KK-Ay). J Funct Foods 3:313–320

    Article  CAS  Google Scholar 

  5. Schmelz EM, Dillehay DL, Webb SK, Reiter A, Adams J, Merrill AH Jr (1996) Sphingomyelin consumption suppresses aberrant colonic crypt foci and increases the proportion of adenomas versus adenocarcinomas in CF1 mice treated with 1,2-dimethylhydrazine: implications for dietary sphingolipids and colon carcinogenesis. Cancer Res 56:4936–4941

    CAS  PubMed  Google Scholar 

  6. Schmelz EM, Bushnev AS, Dillehay DL, Liotta DC, Merrill AH Jr (1997) Suppression of aberrant colonic crypt foci by synthetic sphingomyelins with saturated or unsaturated sphingoid base backbones. Nutr Cancer 28:81–85

    Article  CAS  PubMed  Google Scholar 

  7. Haruta Y, Kato K, Yoshioka T (2008) Dietary phospholipid concentrate from bovine milk improves epidermal function in hairless mice. Biosci Biotechnol Biochem 72:2151–2157

    Article  CAS  PubMed  Google Scholar 

  8. Haruta-Ono Y, Setoguchi S, Ueno HM, Higurashi S, Ueda N, Kato K, Saito T, Matsunaga K, Takata J (2012) Orally administered sphingomyelin in bovine milk is incorporated into skin sphingolipids and is involved in the water-holding capacity of hairless mice. J Dermatol Sci 68:56–62

    Article  CAS  PubMed  Google Scholar 

  9. Morifuji M, Oba C, Ichikawa S, Ito K, Kawahata K, Asami Y, Ikegami S, Itoh H, Sugawara T (2015) A novel mechanism for improvement of dry skin by dietary milk phospholipids: effect on epidermal covalently bound ceramides and skin inflammation in hairless mice. J Dermatol Sci 78:224–231

    Article  CAS  PubMed  Google Scholar 

  10. Nilsson A (1968) Metabolism of sphingomyelin in the intestinal tract of the rat. Biochim Biophys Acta 164:575–584

    Article  CAS  PubMed  Google Scholar 

  11. Schmelz EM, Crall KJ, Larocque R, Dillehay DL, Merrill AH Jr (1994) Uptake and metabolism of sphingolipids in isolated intestinal loops of mice. J Nutr 124:702–712

    CAS  PubMed  Google Scholar 

  12. Nilsson Å, Duan R-D (2006) Absorption and lipoprotein transport of sphingomyelin. J Lipid Res 47:154–171

    Article  CAS  PubMed  Google Scholar 

  13. Morifuji M, Higashi S, Oba C, Ichikawa S, Kawahata K, Yamaji T, Itoh H, Manabe Y, Sugawara T (2015) Milk phospholipids enhance lymphatic absorption of dietary sphingomyelin in lymph-cannulated rats. Lipids 50:987–996

    Article  CAS  PubMed  Google Scholar 

  14. Ohlsson L, Hertervig E, Jonsson BA, Duan RD, Nyberg L, Svernlov R, Nilsson A (2010) Sphingolipids in human ileostomy content after meals containing milk sphingomyelin. Am J Clin Nutr 91:672–678

    Article  CAS  PubMed  Google Scholar 

  15. Fuller R (1991) Probiotics in human medicine. Gut 32:439–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22:659–661

    Article  CAS  PubMed  Google Scholar 

  17. Byrdwell WC, Perry RH (2007) Liquid chromatography with dual parallel mass spectrometry and 31P nuclear magnetic resonance spectroscopy for analysis of sphingomyelin and dihydrosphingomyelin. II. Bovine milk sphingolipids. J Chromatogr A 1146:164–185

    Article  CAS  PubMed  Google Scholar 

  18. Duan RD, Nyberg L, Nilsson A (1995) Alkaline sphingomyelinase activity in rat gastrointestinal tract: distribution and characteristics. Biochim Biophys Acta 1259:49–55

    Article  PubMed  Google Scholar 

  19. Cerning J (1995) Production of exopolysaccharides by lactic acid bacteria and dairy propionibacteria. Lait 75:463–472

    Article  CAS  Google Scholar 

  20. Carey MC, Small DM (1978) The physical chemistry of cholesterol solubility in bile. Relationship to gallstone formation and dissolution in man. J Clin Invest 61:998–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hegardt FG, Dam H (1971) The solubility of cholesterol in aqueous solutions of bile salts and lecithin. Z Ernahrungswiss 10:223–233

    Article  CAS  PubMed  Google Scholar 

  22. Dickinson E (2009) Hydrocolloids as emulsifiers and emulsion stabilizers. Food Hydrocoll 23:1473–1482

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Food Science Research Labs, Meiji Co. Ltd., 540 Naruda, Odawara-shi, Kanagawa, 250-0862, Japan

    Masashi Morifuji, Masami Kitade, Chisato Oba, Tomoyuki Fukasawa, Keiko Kawahata & Taketo Yamaji

  2. Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kitashirakawaoiwakecho, Sakyo-ku, Kyoto-shi, Kyoto, 606-8502, Japan

    Yuki Manabe & Tatsuya Sugawara

Authors
  1. Masashi Morifuji
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  2. Masami Kitade
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  3. Chisato Oba
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  4. Tomoyuki Fukasawa
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  5. Keiko Kawahata
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  6. Taketo Yamaji
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  7. Yuki Manabe
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  8. Tatsuya Sugawara
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Correspondence to Masashi Morifuji.

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Morifuji, M., Kitade, M., Oba, C. et al. Milk Fermented by Lactic Acid Bacteria Enhances the Absorption of Dietary Sphingomyelin in Rats. Lipids 52, 423–431 (2017). https://doi.org/10.1007/s11745-017-4247-0

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  • DOI: https://doi.org/10.1007/s11745-017-4247-0

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