Differences in human meibum lipid composition with meibomian gland dysfunction using NMR and principal component analysis

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 1, 2012, Pages 337-347

  Borchman, Douglas ^a   Foulks, Gary N ^b   Yappert, Marta C ^a   Milliner, Sarah E ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL ESTER; TERPENOID; TRIACYLGLYCEROL; WAX; LIPID;

ADOLESCENT; ADULT; AGED; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; EYELID DISEASE; FEMALE; HUMAN; INFANT; LIPID COMPOSITION; LIPID OXIDATION; MALE; MEIBOMIAN GLAND DYSFUNCTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; AGING; CHEMISTRY; LIPID METABOLISM; MEIBOMIAN GLAND; METABOLISM; METHODOLOGY; MIDDLE AGED; PHYSIOLOGY; PRESCHOOL CHILD; SEBUM;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; CHILD; CHILD, PRESCHOOL; EYELID DISEASES; FEMALE; HUMANS; INFANT; LIPID METABOLISM; LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MEIBOMIAN GLANDS; MIDDLE AGED; PRINCIPAL COMPONENT ANALYSIS; SEBUM; YOUNG ADULT;

EID: 84859245910     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-8551     Document Type: Article

References (91)

1. Brown SI, Dervichian DG. The oils of the meibomian glands: physical and surface characteristics. Arch Ophthalmol. 1969;82: 537-540.
2. Yokoi N, Takehisa Y, Kinoshita S. Correlation of tear lipid layer interference patterns with the diagnosis and severity of dry eye. Am J Ophthalmol. 1996:122;818-824.
3. Hamano H, Hamano T, Hori M, Kawabe H, Mitsunga S. Observations of the precorneal tear film of Sjögren's syndrome by a bio differential interference microscope. Folia Ophthalmol Jpn. 1980; 31:753-755.
4. Matsumoto Y, Dogru M, Goto E, I et al. Efficacy of a new warm moist air device on tear functions of patients with simple meibomian gland dysfunction. Cornea. 2006;25:644-650.
5. Liu DT, Di Pascuale MA, Sawai J, Gao YY, Tseng SC. Tear film dynamics in floppy eyelid syndrome. Invest Ophthalmol Vis Sci. 2005;46:1188-1194.
6. Yokoi N, Komuro A. Non-invasive methods of assessing the tear film. Exp Eye Res. 2004;78:399-407.
7. Shimazaki J, Sakata M, Tsubota K. Ocular surface changes and discomfort in patients with meibomian gland dysfunction. Arch Ophthalmol. 1995;113:1266-1270.
8. Mathers WD. Ocular evaporation in meibomian gland dysfunction and dry eye. Ophthalmology. 1993;100:347-351.
9. Craig JP, Blades K, Patel S. Tear lipid layer structure and stability following expression of the meibomian glands. Ophthalmic Physiol Opt. 1995;15:569-574.
10. McCulley JP, Sciallis GF. Meibomian keratoconjunctivitis. Am J Ophthalmol. 1977;84:788-793.
11. Young G, Efron N. Characteristics of the pre-lens tear film during hydrogel contact lens wear. Ophthalmic Physiol Opt. 1991;11:53-58.
12. Korb DR, Greiner JV, Glonek T. Tear film lipid layer formation: Implications for contact lens wear. Opt Vis Sci. 1996;73:189-192.
13. Norm MS. Tear break-up time: a review. In: Holly FJ, ed. The Preocular Tear Film in Health, Disease, and Contact Lens Wear. Lubbock, TX: Dry Eye Institute;1986:52-55.
14. Foulks GN. The evolving treatment of dry eye. Ophthalmol Clin North Am. 2003;16:29-35.
15. Paranjpe DR, Foulks GN. Therapy for meibomian gland disease. Ophthalmol Clin North Am. 2003;16:37-42.
16. Bron AJ, Tiffany JM. The meibomian glands and tear film lipids: structure, function, and control. Adv Exp Med Biol. 1998;438:281-295.
17. Foulks GN. The correlation between the tear film lipid layer and dry eye disease. Surv Ophthalmol. 2007;52:369-374.
18. Green-Church KB, Butovich I, Willcox M, et al. The international workshop on meibomian gland dysfunction: report of the subcommittee on tear film lipids and lipid-protein interactions in health and disease. Invest Ophthalmol Vis Sci. 2011;52:1979-1993.
19. Butovich IA, Millar TJ, Ham BM. Understanding and analyzing meibomian lipids: a review. Curr Eye Res. 2008;33:405-420.
20. Nicolaides N, Santos EC. The di- and triesters of the lipids of steer and human meibomian glands. Lipids. 1985;20:454-467.
21. Borchman D, Foulks GN, Yappert MC. Confirmation of changes in human meibum lipid infrared spectra with age using principal component analysis. Curr Eye Res. 2010;35:778-786.
22. Borchman D, Foulks GN, Yappert MC. Changes in human meibum lipid with meibomian gland dysfunction using principal component analysis. Exp Eye Res. 2010;91:246-256.
23. Borchman D, Foulks GN, Yappert MC, Milliner SE. Changes in human meibum lipid composition with age using NMR Spectroscopy. Invest Ophthalmol Vis Sci. In press.
24. 1H-NMR Spectroscopy. Invest Ophthalmol Vis Sci. 2011;52:7350-7358.
25. Oshima Y, Sato H, Zaghloul A, Foulks GN, Yappert MC, Borchman D. Characterization of human meibum lipid using Raman spectroscopy. Curr Eye Res. 2009;34:824-835.
26. Shine WE, McCulley JP. The role of cholesterol in chronic blepharitis. Invest Ophthalmol Vis Sci. 1991;32:2272-2280.
27. Shine WE, McCulley JP. Meibomian gland triglyceride fatty acid differences in chronic blepharitis patients. Cornea. 1996;15:340-346.
28. Shine WE, McCulley JP. Association of meibum oleic acid with meibomian seborrhea. Cornea. 2000;19:72-74.
29. Joffre C, Souchier M, Leclere L, et al. Branched-chain fatty acids, increased in tears of blepharitis patients, are not toxic for conjunctival cells. Br J Ophthalmol. 2009;93:1391-1395.
30. Shine WE, McCulley JP. Keratoconjunctivitis sicca associated with meibomian secretion polar lipid abnormality. Arch Ophthalmol. 1998;116:849-852.
31. Shine WE, McCulley JP. Meibomianitis: polar lipid abnormalities. Cornea. 2004;23:781-783.
32. Butovich IA, Uchiyama E, Di Pascuale MA, et al. Liquid chromatography- mass spectrometric analysis of lipids present in human meibomian gland secretions. Lipids. 2007;42:765-776.
33. Butovich IA, Uchiyama E, McCulley JP. Lipids of human meibum: mass-spectrometric analysis and structural elucidation. J Lipid Res. 2007;48:2220-2235.
34. Butovich IA. On the lipid composition of human meibum and tears: comparative analysis of nonpolar lipids. Invest Ophthalmol Vis Sci. 2008;49:3779-3789.
35. Butovich IA, Wojtowicz JC, Molai M. Human tear film and meibum: very long chain wax esters and (O-acyl)-omega-hydroxy fatty acids of meibum. J Lipid Res. 2009;50:2471-2485.
36. Butovich IA. Cholesteryl esters as a depot for very long chain fatty acids in human meibum. J Lipid Res. 2009;50:501-513.
37. Foulks GN, Borchman D, Yappert MC, Kim S, McKay JW. Topical azithromycin therapy of meibomian gland dysfunction: clinical response and lipid alterations. Cornea. 2010;29:781-788.
38. Borchman D, Foulks GN, Yappert MC, et al. Human meibum lipid conformation and thermodynamic changes with meibomian-gland dysfunction. Invest Ophthalmol Vis Sci. 2011;52:3805-3817.
39. Foulks GN, Borchman D. Meibomian gland dysfunction: the past, the present, the future. Eye Contact Lens. 2010;36:249-253.
40. Borchman D, Foulks GN, Yappert MC, et al. Physical changes in human meibum with age as measured by infrared spectroscopy. Ophthalmic Res. 2010;44:34-42.
41. Borchman D, Foulks GN, Yappert MC, Tang D, Ho DV. Spectroscopic evaluation of human tear lipids. Chem Phys Lipids. 2007; 147:87-102.
42. Borchman D, Foulks GN, Yappert MC, Ho DV. Temperature-induced conformational changes in human tear lipids hydrocarbon chains. Biopolymers. 2007;87:124-133.
43. Huang L, Grami V, Marrero Y, et al. Human lens phospholipid changes with age and cataract. Invest Ophthalmol Vis Sci. 2005; 46:1682-1689.
44. 31P NMR and MALDI-MS. Biochim Biophys Acta. 2010; 1798:303-311.
45. Ferguson-Yankey S, Borchman D, Taylor KG, DuPre DB, Yappert MC. Conformational Studies of sphingolipids by NMR spectroscopy, I: dihydrosphingomyelin. Biochim Biophys Acta. 2000; 1467:307-325.
46. Borchman D, Byrdwell WC, Yappert MC. Regional and age-dependent differences in the phospholipid composition of human lens membranes. Invest Ophthalmol Vis Sci. 1994;35:3938-3942.
47. Byrdwell WC, Borchman D, Porter RA, Taylor KG, Yappert MC. Separation and characterization of the unknown phospholipid in human lens membranes. Invest Ophthalmol Vis Sci. 1994;35:4333-4343.
48. Merchant TE, Lass JH, Meneses P, Greiner JV, Glonek T. Human crystalline lens phospholipid analysis with age. Invest Ophthalmol Vis Sci. 1991;32:549-555.
49. Robosky LC, Wade K, Woolson D, et al. Quantitative evaluation of sebum lipid components with nuclear magnetic resonance. J Lipid Res. 2008;49:686-692.
50. Tulloch AP. Solvent effects on the nuclear magnetic resonance spectra of methyl hydroxysterates. J Am Oil Chem Soc. 1966;43: 670-674.
51. Verardo G, Pagani E, Geatti P. A thorough study of the surface wax of apple fruits. Anal Biochem. 2003;376:659-667.
52. Frost DJ, Barzilay J. Proton magnetic resonance identification of nonconjugated cis-unsatureated fatty acids and esters. Anal Chem. 1971;43:1316-1318.
53. 13C NMR studies of melon and head blubber of the striped dolphin (Stenella coeruleoalba). Lipids. 2006;41:1039-1048.
54. Tulloch AP. Beeswax: structure of the esters and their component hydroxyl acids and diols. Chem Phys Lipids. 1971;6:235-265.
55. Wineburg JP, Swern D. NMR chemical shift reagents in structural determination of lipid derivatives, II: methyl petroselinate and methyl oleate. J Am Oil Chem Soc. 1971;49:267-273.
56. KE PJ, Ackman RG. NMR determination of wax esters in marine lipids. Anal Chem Acta. 1974;69:253-258.
57. Purcell JM, Morris SG, Susi H. Proton magnetic resonance spectra of unsaturated fatty acids. Anal Chem. 1966;38:588-592.
58. Johnson LF, Shoolery JN. Determination of unsaturation and average molecular weight of natural fats by nuclear magnetic resonance. Anal Chem. 1962;34:1136-1139.
59. Glass CA, Dutton HJ. Determination of beta-olefinic methyl groups in esters of fatty acids by nuclear magnetic resonance. Anal Chem. 1964;36:2401-2404.
60. Foulks GN, Bron AJ. Meibomian-gland dysfunction: a clinical scheme for description, diagnosis, classification and grading. Ocul Surf. 2003;1:17-36.
61. Mahalanobis PC. On the generalized distance in statistics. Proc Natl Inst Sci India. 1936;2:49-55.
62. 34 methylated squalenes from a Bolivian strain of Botryococcus braunii. Phytochemistry. 2004;65:3159-3165.
63. Corcelli A, Lattanzio VMT, Mascolo G, Papadia P, Fanizzi F. Lipidprotein stoichiometries in a crystalline biological membrane: NMR quantitative analysis of the lipid extract of the purple membrane. J Lipid Res. 2002;43:132-140.
64. Quang DN, Hashimoto T, Tanaka M, et al. Concentoils B, C and D, three squalene-type triterpenoids from the ascomycete Daldinia concentrica. Phytochemistry. 2002;61:345-353.
65. D'Imperio M, Gobbing M, Picanza A, Costanzo S, Della Corte A, Mannina L. Influence of harvest method and period on olive oil composition: an NMR and statistical study. J Agric Food Chem. 2010;58:11043-11051.
66. Haywood RM, Claxson AW, Hawkes GE, et al. Detection of aldehydes and their conjugated hydroperoxydiene precursors in thermally- stressed culinary oils and fats: investigations using high resolution proton NMR spectroscopy. Free Radic Res. 1995;22:441-482.
67. 1H nuclear magnetic resonance. J Sci Food Agric. 2005;85:2413-2420.
68. Borchman D, Yappert MC. Lipids and the Ocular Lens. J Lipid Res. 2010;51:2473-2488.
69. Lamba OP, Lal S, Yappert MC, Borchman D. Spectroscopic detection of lipid peroxidation products and structural changes in a sphingomyelin model system. Biochem Biophys Acta. 1991;1081: 181-187.
70. 3+: A site-specific catalyzed oxidation. Free Rad Biol Med. 1994;16:591-601.
71. Ashraf Z, Pasha U, Greenstone V, et al. Quantification of human sebum on skin and human meibum on the eye lid margin using sebum tape, spectroscopy and chemical analysis. Curr Eye Res. 2011;36:553-562.
72. Huang Z, Poulter CD. Tetramethylsqualene, a triterpene from Botryococcus braunii var. show A. Phytochemistry. 1989;28: 1467-1470.
73. Pogliani L, Ceruti M, Ricchiardi G, Viterbo D. An NMR and molecular mechanics study of squalene and squalene derivatives. Chem Phys Lipids. 1994;70:21-34.
74. Huang MT, Ho CT, Wang ZY, et al. Inhibition of skin tumorigenesis by rosemary and its constituents carnosol and ursolic acid. Cancer Res. 1994;54:701-708.
75. Palozza P, Parrone N, Simone RE, Catalano A. Lycopene in atherosclerosis prevention: an integrated scheme of the potential mechanisms of action from cell culture studies. Arch Biochem Biophys. 2010;504:26-33.
76. Noro J, Barrows LR, Gideon J, et al. Tetrahydroxysqualene from Rhus taitensis shows antimycobacterial activity against Mycobacterium tuberculosis. J Nat Prod. 2008;71:1623-1624.
77. Namitha KK, Megi PS. Chemistry and biotechnology of carotenoids. Crit Rev Food Sci Nutr. 2010;50:728-760.
78. N.I. Krinsky. The biological properties of carotenoids. Pure Appl Chem. 1994;66:1003-1010.
79. JL Schwartz. In vitro biological methods for determination of carotenoid activity. Methods Enzymol. 1993;214:226-256.
80. Mayne ST. Beta-carotene, carotenoids, and disease prevention in humans. FASEB J. 1996;10:690-701.
81. Bara A, Socaciu C, Neamtu G. Effects of some carotenoids on proliferation and nucleotide turnover in Ehrlich ascites. Radioter Oncol Med. 1995;2:16-21.
82. DiMascio P, Kaiser S, Sies H. Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys. 1989;274:532-538.
83. Mishra NN, Liu GY, Yeaman MR, et al. Carotenoid-related alteration of cell membrane fluidity impacts Staphylococcus aureus susceptibility to host defense peptides. Antimicrob Agents Chemother. 2011;55:526-531.
84. Subczynski WK, Markowska E, Gruszecki WI, Sielewiesiuk J. Effects of polar carotenoids on dimyristoylphosphatidylcholine membranes: a spin-label study. Biochim Biophys Acta. 1992;1105: 97-108.
85. Strzałka K, Gruszecki WI. Effect of beta-carotene on structural and dynamic properties of model phosphatidylcholine membranes, I: an EPR spin label study. Biochim Biophys Acta. 1994;1194:138-142.
86. Socaciu C, Jessel R, Diehl HA. Competitive carotenoid and cholesterol incorporation into liposomes: effects on membrane phase transition, fluidity, polarity and anisotropy. Chem Phys Lipids. 2000;106:79-88.
87. Wisniewska A, Widomska J, Subczynski WK. Carotenoid-membrane interactions in liposomes: effect of dipolar, monopolar, and nonpolar carotenoids. Acta Biochim Pol. 2006;53:475-484.
88. Socaciu C, Jessel R, Diehl HA. Carotenoid incorporation into microsomes: yields, stability and membrane dynamics. Spectrochim Acta A Mol Biomol Spectrosc. 2000;56:2799-2809.
89. Rohmer M, Bouvier P, Ourisson G. Molecular evolution of biomembranes: structural equivalents and phylogenetic precursors of sterols. Proc Natl Acad Sci U S A. 1979;76:847-851.
90. Blackie CA, Korb DR, Knop E, Bedi R, Knop N, Holland EJ. Nonobvious obstructive meibomian gland dysfunction. Cornea. 2010;29:1333-1345.
91. Korb DR, Blackie CA. Meibomian gland diagnostic expressibility: correlation with dry eye symptoms and gland location. Cornea. 2008;27:1142-1147.