DOI QR코드

DOI QR Code

Associations among plasma vitamin C, epidermal ceramide and clinical severity of atopic dermatitis

  • Shin, Jihye (Department of Medical Nutrition, Graduate School of East-West Medical Science, Kyung Hee University) ;
  • Kim, You Jin (Department of Nutritional Science and Food Management, College of Health Sciences, Ewha Womans University) ;
  • Kwon, Oran (Department of Nutritional Science and Food Management, College of Health Sciences, Ewha Womans University) ;
  • Kim, Nack-In (Department of Dermatology, College of Medicine, Kyung Hee University) ;
  • Cho, Yunhi (Department of Medical Nutrition, Graduate School of East-West Medical Science, Kyung Hee University)
  • Received : 2015.10.13
  • Accepted : 2016.02.25
  • Published : 2016.08.01

Abstract

BACKGROUND/OBJECTIVES: Atopic dermatitis (AD), a chronic inflammatory skin disease, is accompanied by disruption of the epidermal lipid barrier, of which ceramide (Cer) is the major component. Recently it was reported that vitamin C is essential for de novo synthesis of Cer in the epidermis and that the level of vitamin C in plasma is decreased in AD. The objective of this study was to determine the associations among clinical severity, vitamin C in either plasma or epidermis, and Cer in the epidermis of patients with AD. SUBJECTS/METHODS: A total of 17 patients (11 male and 6 female) aged 20-42 years were enrolled. The clinical severity of AD was assessed according to the SCORAD (SCORing Atopic Dermatitis) system. Levels of vitamin C were determined in plasma and biopsies of lesional epidermis. Levels of epidermal lipids, including Cer, were determined from tape-stripped lesional epidermis. RESULTS: The clinical severity of patients ranged between 0.1 and 45 (mild to severe AD) based on the SCORAD system. As the SCORAD score increased, the level of vitamin C in the plasma, but not in the epidermis, decreased, and levels of total Cer and Cer2, the major Cer species in the epidermis, also decreased. There was also a positive association between level of vitamin C in the plasma and level of total Cer in the epidermis. However, levels of epidermal total lipids including triglyceride, cholesterol, and free fatty acid (FFA) were not associated with either SCORAD score or level of vitamin C in the plasma of all subjects. CONCLUSIONS: As the clinical severity of AD increased, level of vitamin C in the plasma and level of epidermal Cer decreased, and there was a positive association between these two parameters, implying associations among plasma vitamin C, epidermal Cer, and the clinical severity of AD.

Keywords

References

  1. Addor FA, Takaoka R, Rivitti EA, Aoki V. Atopic dermatitis: correlation between non-damaged skin barrier function and disease activity. Int J Dermatol 2012;51:672-6. https://doi.org/10.1111/j.1365-4632.2011.05176.x
  2. Darlenski R, Kazandjieva J, Hristakieva E, Fluhr JW. Atopic dermatitis as a systemic disease. Clin Dermatol 2014;32:409-13. https://doi.org/10.1016/j.clindermatol.2013.11.007
  3. Elias PM. Epidermal lipids, barrier function, and desquamation. J Invest Dermatol 1983;80 Suppl:44s-49s.
  4. Weerheim A, Ponec M. Determination of stratum corneum lipid profile by tape stripping in combination with high-performance thin-layer chromatography. Arch Dermatol Res 2001;293:191-9. https://doi.org/10.1007/s004030100212
  5. Di Nardo A, Wertz P, Giannetti A, Seidenari S. Ceramide and cholesterol composition of the skin of patients with atopic dermatitis. Acta Derm Venereol 1998;78:27-30. https://doi.org/10.1080/00015559850135788
  6. Imokawa G, Abe A, Jin K, Higaki Y, Kawashima M, Hidano A. Decreased level of ceramides in stratum corneum of atopic dermatitis:an etiologic factor in atopic dry skin? J Invest Dermatol 1991;96:523-6. https://doi.org/10.1111/1523-1747.ep12470233
  7. Matsumoto M, Umemoto N, Sugiura H, Uehara M. Difference in ceramide composition between "dry" and "normal" skin in patients with atopic dermatitis. Acta Derm Venereol 1999;79:246-7. https://doi.org/10.1080/000155599750011183
  8. Merrill AH Jr. De novo sphingolipid biosynthesis: a necessary, but dangerous, pathway. J Biol Chem 2002;277:25843-6. https://doi.org/10.1074/jbc.R200009200
  9. Garner WL, Oyatsu Y, Zuccaro C, Rodriquez JL, Smith DJ, Marcelo CL. The effect of essential fatty acid supplementation on keratinocyte replication. Prostaglandins Leukot Essent Fatty Acids 1995;52:349-55. https://doi.org/10.1016/0952-3278(95)90037-3
  10. Zineb R, Zhor B, Odile W, Marthe RR. Distinct, tissue-specific regulation of vitamin D receptor in the intestine, kidney, and skin by dietary calcium and vitamin D. Endocrinology 1998;139:1844-52. https://doi.org/10.1210/endo.139.4.5903
  11. Hennings H, Michael D, Cheng C, Steinert P, Holbrook K, Yuspa SH. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 1980;19:245-54. https://doi.org/10.1016/0092-8674(80)90406-7
  12. Uchida Y, Behne M, Quiec D, Elias PM, Holleran WM. Vitamin C stimulates sphingolipid production and markers of barrier formation in submerged human keratinocyte cultures. J Invest Dermatol 2001;117:1307-13. https://doi.org/10.1046/j.0022-202x.2001.01555.x
  13. Ponec M, Weerheim A, Kempenaar J, Mulder A, Gooris GS, Bouwstra J, Mommaas AM. The formation of competent barrier lipids in reconstructed human epidermis requires the presence of vitamin C. J Invest Dermatol 1997;109:348-55. https://doi.org/10.1111/1523-1747.ep12336024
  14. Sivaranjani N, Rao SV, Rajeev G. Role of reactive oxygen species and antioxidants in atopic dermatitis. J Clin Diagn Res 2013;7:2683-5.
  15. Leveque N, Robin S, Muret P, Mac-Mary S, Makki S, Humbert P. High iron and low ascorbic acid concentrations in the dermis of atopic dermatitis patients. Dermatology 2003;207:261-4. https://doi.org/10.1159/000073087
  16. Macheleidt O, Kaiser HW, Sandhoff K. Deficiency of epidermal protein-bound omega-hydroxyceramides in atopic dermatitis. J Invest Dermatol 2002;119:166-73. https://doi.org/10.1046/j.1523-1747.2002.01833.x
  17. Shindo Y, Witt E, Han D, Epstein W, Packer L. Enzymic and nonenzymic antioxidants in epidermis and dermis of human skin. J Invest Dermatol 1994;102:122-4. https://doi.org/10.1111/1523-1747.ep12371744
  18. Kunz B, Oranje AP, Labreze L, Stalder JF, Ring J, Taieb A. Clinical validation and guidelines for the SCORAD index: consensus report of the European Task Force on Atopic Dermatitis. Dermatology 1997;195:10-9.
  19. Wollenberg A, Zoch C, Wetzel S, Plewig G, Przybilla B. Predisposing factors and clinical features of eczema herpeticum: a retrospective analysis of 100 cases. J Am Acad Dermatol 2003;49:198-205. https://doi.org/10.1067/S0190-9622(03)00896-X
  20. Benzie I, Strain JJ. Effect of vitamin C supplementation on concentrations of vitamins C and E in fasting plasma. Asia Pac J Clin Nutr 1999;8:207-10. https://doi.org/10.1046/j.1440-6047.1999.00114.x
  21. Dhariwal KR, Hartzell WO, Levine M. Ascorbic acid and dehydroascorbic acid measurements in human plasma and serum. Am J Clin Nutr 1991;54:712-6. https://doi.org/10.1093/ajcn/54.4.712
  22. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.
  23. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957;226:497-509.
  24. Uchida Y, Hara M, Nishio H, Sidransky E, Inoue S, Otsuka F, Suzuki A, Elias PM, Holleran WM, Hamanaka S. Epidermal sphingomyelins are precursors for selected stratum corneum ceramides. J Lipid Res 2000;41:2071-82.
  25. Kim H, Lee J, Cho Y. Dietary sericin enhances epidermal levels of glucosylceramides and ceramides with up-regulating protein expressions of glucosylceramide synthase, beta-glucocerebrosidase and acidic sphingomyelinase in NC/Nga mice. Nutr Res 2012;32:956-64. https://doi.org/10.1016/j.nutres.2012.09.006
  26. Chen H, Mendelsohn R, Rerek ME, Moore DJ. Fourier transform infrared spectroscopy and differential scanning calorimetry studies of fatty acid homogeneous ceramide 2. Biochim Biophys Acta 2000;1468:293-303. https://doi.org/10.1016/S0005-2736(00)00271-6
  27. Benzie IF. Vitamin C: prospective functional markers for defining optimal nutritional status. Proc Nutr Soc 1999;58:469-76. https://doi.org/10.1017/S0029665199000610
  28. Angelova-Fischer I, Mannheimer AC, Hinder A, Ruether A, Franke A, Neubert RH, Fischer TW, Zillikens D. Distinct barrier integrity phenotypes in filaggrin-related atopic eczema following sequential tape stripping and lipid profiling. Exp Dermatol 2011;20:351-6. https://doi.org/10.1111/j.1600-0625.2011.01259.x
  29. Hara J, Higuchi K, Okamoto R, Kawashima M, Imokawa G. Highexpression of sphingomyelin deacylase is an important determinant of ceramide deficiency leading to barrier disruption in atopic dermatitis. J Invest Dermatol 2000;115:406-13. https://doi.org/10.1046/j.1523-1747.2000.00072.x
  30. Tawada C, Kanoh H, Nakamura M, Mizutani Y, Fujisawa T, Banno Y, Seishima M. Interferon-${\gamma}$ decreases ceramides with long-chain fatty acids: possible involvement in atopic dermatitis and psoriasis. J Invest Dermatol 2014;134:712-8. https://doi.org/10.1038/jid.2013.364
  31. Pinnel SR, Murad S, Darr D. Induction of collagen synthesis by ascorbic acid. A possible mechanism. Arch Dermatol 1987;123:1684-6. https://doi.org/10.1001/archderm.1987.01660360122023

Cited by

  1. The Roles of Vitamin C in Skin Health vol.9, pp.8, 2017, https://doi.org/10.3390/nu9080866
  2. Role of Vitamin C in Skin Diseases vol.9, pp.1664-042X, 2018, https://doi.org/10.3389/fphys.2018.00819
  3. Micronutrients in Atopic Dermatitis: A Systematic Review vol.25, pp.6, 2019, https://doi.org/10.1089/acm.2018.0363
  4. Enhanced Triacylglycerol Content and Gene Expression for Triacylglycerol Metabolism, Acyl-Ceramide Synthesis, and Corneocyte Lipid Formation in the Epidermis of Borage Oil Fed Guinea Pigs vol.11, pp.11, 2016, https://doi.org/10.3390/nu11112818
  5. The role of oral vitamins and supplements in the management of atopic dermatitis: a systematic review vol.58, pp.12, 2016, https://doi.org/10.1111/ijd.14404
  6. 12세 미만 아토피 피부염 어린이의 에너지 및 영양소적정섭취 수준 평가: 2013-2015년 국민건강영양조사 자료를 바탕으로 vol.53, pp.2, 2016, https://doi.org/10.4163/jnh.2020.53.2.141
  7. Behavior of Nutritional Supplements Use in Association With Inflammatory Skin Diseases in Chinese College Students vol.8, pp.None, 2016, https://doi.org/10.3389/fnut.2021.615462
  8. Tetrahexyldecyl Ascorbate (THDC) Degrades Rapidly under Oxidative Stress but Can Be Stabilized by Acetyl Zingerone to Enhance Collagen Production and Antioxidant Effects vol.22, pp.16, 2021, https://doi.org/10.3390/ijms22168756