Skip to main content
Top
Published in: Arthritis Research & Therapy 1/2018

Open Access 01-12-2018 | Research article

Targeted lipidomics analysis identified altered serum lipid profiles in patients with polymyositis and dermatomyositis

Authors: Joan Raouf, Helena Idborg, Petter Englund, Helene Alexanderson, Maryam Dastmalchi, Per-Johan Jakobsson, Ingrid E. Lundberg, Marina Korotkova

Published in: Arthritis Research & Therapy | Issue 1/2018

Login to get access

Abstract

Background

Polymyositis (PM) and dermatomyositis (DM) are severe chronic autoimmune diseases, characterized by muscle fatigue and low muscle endurance. Conventional treatment includes high doses of glucocorticoids and immunosuppressive drugs; however, few patients recover full muscle function. One explanation of the persistent muscle weakness could be altered lipid metabolism in PM/DM muscle tissue as we previously reported. Using a targeted lipidomic approach we aimed to characterize serum lipid profiles in patients with PM/DM compared to healthy individuals (HI) in a cross-sectional study. Also, in the longitudinal study we compared serum lipid profiles in patients newly diagnosed with PM/DM before and after immunosuppressive treatment.

Methods

Lipidomic profiles were analyzed in serum samples from 13 patients with PM/DM, 12 HI and 8 patients newly diagnosed with PM/DM before and after conventional immunosuppressive treatment using liquid chromatography tandem mass spectrometry (LC-MS/MS) and a gas-chromatography flame ionization detector (GC-FID). Functional Index (FI), as a test of muscle performance and serum levels of creatine kinase (s-CK) as a proxy for disease activity were analyzed.

Results

The fatty acid (FA) composition of total serum lipids was altered in patients with PM/DM compared to HI; the levels of palmitic (16:0) acid were significantly higher while the levels of arachidonic (20:4, n-6) acid were significantly lower in patients with PM/DM. The profiles of serum phosphatidylcholine and triacylglycerol species were changed in patients with PM/DM compared to HI, suggesting disproportionate levels of saturated and polyunsaturated FAs that might have negative effects on muscle performance. After immunosuppressive treatment the total serum lipid levels of eicosadienoic (20:2, n-6) and eicosapentaenoic (20:5, n-3) acids were increased and serum phospholipid profiles were altered in patients with PM/DM. The correlation between FI or s-CK and levels of several lipid species indicate the important role of lipid changes in muscle performance and inflammation.

Conclusions

Serum lipids profiles are significantly altered in patients with PM/DM compared to HI. Moreover, immunosuppressive treatment in patients newly diagnosed with PM/DM significantly affected serum lipid profiles. These findings provide new evidence of the dysregulated lipid metabolism in patients with PM/DM that could possibly contribute to low muscle performance.
Appendix
Available only for authorised users
Literature
1.
go back to reference Tieu J, Lundberg IE, Limaye V. Idiopathic inflammatory myositis. Best Pract Res Clin Rheumatol. 2016;30(1):149–68.CrossRefPubMed Tieu J, Lundberg IE, Limaye V. Idiopathic inflammatory myositis. Best Pract Res Clin Rheumatol. 2016;30(1):149–68.CrossRefPubMed
2.
go back to reference Zong M, Lundberg IE. Pathogenesis, classification and treatment of inflammatory myopathies. Nat Rev Rheumatol. 2011;7(5):297–306.CrossRefPubMed Zong M, Lundberg IE. Pathogenesis, classification and treatment of inflammatory myopathies. Nat Rev Rheumatol. 2011;7(5):297–306.CrossRefPubMed
3.
go back to reference Moran EM, Mastaglia FL. Cytokines in immune-mediated inflammatory myopathies: cellular sources, multiple actions and therapeutic implications. Clin Exp Immunol. 2014;178(3):405–15.CrossRefPubMedPubMedCentral Moran EM, Mastaglia FL. Cytokines in immune-mediated inflammatory myopathies: cellular sources, multiple actions and therapeutic implications. Clin Exp Immunol. 2014;178(3):405–15.CrossRefPubMedPubMedCentral
4.
go back to reference De Paepe B. Interferons as components of the complex web of reactions sustaining inflammation in idiopathic inflammatory myopathies. Cytokine. 2015;74(1):81–7.CrossRefPubMed De Paepe B. Interferons as components of the complex web of reactions sustaining inflammation in idiopathic inflammatory myopathies. Cytokine. 2015;74(1):81–7.CrossRefPubMed
5.
go back to reference Korotkova M, Helmers SB, Loell I, Alexanderson H, Grundtman C, Dorph C, Lundberg IE, Jakobsson PJ. Effects of immunosuppressive treatment on microsomal prostaglandin E synthase 1 and cyclooxygenases expression in muscle tissue of patients with polymyositis or dermatomyositis. Ann Rheum Dis. 2008;67(11):1596–602.CrossRefPubMed Korotkova M, Helmers SB, Loell I, Alexanderson H, Grundtman C, Dorph C, Lundberg IE, Jakobsson PJ. Effects of immunosuppressive treatment on microsomal prostaglandin E synthase 1 and cyclooxygenases expression in muscle tissue of patients with polymyositis or dermatomyositis. Ann Rheum Dis. 2008;67(11):1596–602.CrossRefPubMed
6.
go back to reference Loell I, Alemo Munters L, Pandya J, Zong M, Alexanderson H, Fasth AE, Stahl Hallengren C, Radmark O, Lundberg IE, Jakobsson PJ, et al. Activated LTB4 pathway in muscle tissue of patients with polymyositis or dermatomyositis. Ann Rheum Dis. 2013;72(2):293–9.CrossRefPubMed Loell I, Alemo Munters L, Pandya J, Zong M, Alexanderson H, Fasth AE, Stahl Hallengren C, Radmark O, Lundberg IE, Jakobsson PJ, et al. Activated LTB4 pathway in muscle tissue of patients with polymyositis or dermatomyositis. Ann Rheum Dis. 2013;72(2):293–9.CrossRefPubMed
7.
go back to reference Nagaraju K, Lundberg IE. Polymyositis and dermatomyositis: pathophysiology. Rheum Dis Clin N Am. 2011;37(2):159–71. vCrossRef Nagaraju K, Lundberg IE. Polymyositis and dermatomyositis: pathophysiology. Rheum Dis Clin N Am. 2011;37(2):159–71. vCrossRef
8.
go back to reference Lightfoot AP, Nagaraju K, McArdle A, Cooper RG. Understanding the origin of non-immune cell-mediated weakness in the idiopathic inflammatory myopathies - potential role of ER stress pathways. Curr Opin Rheumatol. 2015;27(6):580–5.CrossRefPubMed Lightfoot AP, Nagaraju K, McArdle A, Cooper RG. Understanding the origin of non-immune cell-mediated weakness in the idiopathic inflammatory myopathies - potential role of ER stress pathways. Curr Opin Rheumatol. 2015;27(6):580–5.CrossRefPubMed
10.
go back to reference Loell I, Raouf J, Chen YW, Shi R, Nennesmo I, Alexanderson H, Dastmalchi M, Nagaraju K, Korotkova M, Lundberg IE. Effects on muscle tissue remodeling and lipid metabolism in muscle tissue from adult patients with polymyositis or dermatomyositis treated with immunosuppressive agents. Arthritis Res Ther. 2016;18(1):136.CrossRefPubMedPubMedCentral Loell I, Raouf J, Chen YW, Shi R, Nennesmo I, Alexanderson H, Dastmalchi M, Nagaraju K, Korotkova M, Lundberg IE. Effects on muscle tissue remodeling and lipid metabolism in muscle tissue from adult patients with polymyositis or dermatomyositis treated with immunosuppressive agents. Arthritis Res Ther. 2016;18(1):136.CrossRefPubMedPubMedCentral
11.
go back to reference Lipina C, Hundal HS. Lipid modulation of skeletal muscle mass and function. J Cachexia Sarcopenia Muscle. 2017;8(2):190–201.CrossRefPubMed Lipina C, Hundal HS. Lipid modulation of skeletal muscle mass and function. J Cachexia Sarcopenia Muscle. 2017;8(2):190–201.CrossRefPubMed
12.
go back to reference Bruni P, Donati C. Pleiotropic effects of sphingolipids in skeletal muscle. Cell Mol Life Sci. 2008;65(23):3725–36.CrossRefPubMed Bruni P, Donati C. Pleiotropic effects of sphingolipids in skeletal muscle. Cell Mol Life Sci. 2008;65(23):3725–36.CrossRefPubMed
13.
go back to reference Korotkova M, Lundberg IE. The skeletal muscle arachidonic acid cascade in health and inflammatory disease. Nat Rev Rheumatol. 2014;10(5):295–303.CrossRefPubMed Korotkova M, Lundberg IE. The skeletal muscle arachidonic acid cascade in health and inflammatory disease. Nat Rev Rheumatol. 2014;10(5):295–303.CrossRefPubMed
14.
go back to reference Funai K, Lodhi IJ, Spears LD, Yin L, Song H, Klein S, Semenkovich CF. Skeletal muscle phospholipid metabolism regulates insulin sensitivity and contractile function. Diabetes. 2016;65(2):358–70.CrossRefPubMed Funai K, Lodhi IJ, Spears LD, Yin L, Song H, Klein S, Semenkovich CF. Skeletal muscle phospholipid metabolism regulates insulin sensitivity and contractile function. Diabetes. 2016;65(2):358–70.CrossRefPubMed
15.
go back to reference Henry R, Peoples GE, McLennan PL. Muscle fatigue resistance in the rat hindlimb in vivo from low dietary intakes of tuna fish oil that selectively increase phospholipid n-3 docosahexaenoic acid according to muscle fibre type. Br J Nutr. 2015;114(6):873–84.CrossRefPubMed Henry R, Peoples GE, McLennan PL. Muscle fatigue resistance in the rat hindlimb in vivo from low dietary intakes of tuna fish oil that selectively increase phospholipid n-3 docosahexaenoic acid according to muscle fibre type. Br J Nutr. 2015;114(6):873–84.CrossRefPubMed
16.
go back to reference Blondelle J, Ohno Y, Gache V, Guyot S, Storck S, Blanchard-Gutton N, Barthelemy I, Walmsley G, Rahier A, Gadin S, et al. HACD1, a regulator of membrane composition and fluidity, promotes myoblast fusion and skeletal muscle growth. J Mol Cell Biol. 2015;7(5):429–40.CrossRefPubMedPubMedCentral Blondelle J, Ohno Y, Gache V, Guyot S, Storck S, Blanchard-Gutton N, Barthelemy I, Walmsley G, Rahier A, Gadin S, et al. HACD1, a regulator of membrane composition and fluidity, promotes myoblast fusion and skeletal muscle growth. J Mol Cell Biol. 2015;7(5):429–40.CrossRefPubMedPubMedCentral
17.
go back to reference Smith GI, Julliand S, Reeds DN, Sinacore DR, Klein S, Mittendorfer B. Fish oil-derived n-3 PUFA therapy increases muscle mass and function in healthy older adults. Am J Clin Nutr. 2015;102(1):115–22.CrossRefPubMedPubMedCentral Smith GI, Julliand S, Reeds DN, Sinacore DR, Klein S, Mittendorfer B. Fish oil-derived n-3 PUFA therapy increases muscle mass and function in healthy older adults. Am J Clin Nutr. 2015;102(1):115–22.CrossRefPubMedPubMedCentral
18.
go back to reference Rodacki CL, Rodacki AL, Pereira G, Naliwaiko K, Coelho I, Pequito D, Fernandes LC. Fish-oil supplementation enhances the effects of strength training in elderly women. Am J Clin Nutr. 2012;95(2):428–36.CrossRefPubMed Rodacki CL, Rodacki AL, Pereira G, Naliwaiko K, Coelho I, Pequito D, Fernandes LC. Fish-oil supplementation enhances the effects of strength training in elderly women. Am J Clin Nutr. 2012;95(2):428–36.CrossRefPubMed
19.
go back to reference Fang L, Mundra PA, Fan FL, Galvin A, Weir JM, Wong G, Chin-Dusting J, Cicuttini F, Meikle P, Dart AM. Plasma lipidomic profiling in patients with rheumatoid arthritis. Metabolomics. 2016;12(8):136.CrossRef Fang L, Mundra PA, Fan FL, Galvin A, Weir JM, Wong G, Chin-Dusting J, Cicuttini F, Meikle P, Dart AM. Plasma lipidomic profiling in patients with rheumatoid arthritis. Metabolomics. 2016;12(8):136.CrossRef
20.
go back to reference Zeng C, Wen B, Hou G, Lei L, Mei Z, Jia X, Chen X, Zhu W, Li J, Kuang Y, et al. Lipidomics profiling reveals the role of glycerophospholipid metabolism in psoriasis. Gigascience. 2017;6(10):1–11.CrossRef Zeng C, Wen B, Hou G, Lei L, Mei Z, Jia X, Chen X, Zhu W, Li J, Kuang Y, et al. Lipidomics profiling reveals the role of glycerophospholipid metabolism in psoriasis. Gigascience. 2017;6(10):1–11.CrossRef
21.
go back to reference Rhee EP, Cheng S, Larson MG, Walford GA, Lewis GD, McCabe E, Yang E, Farrell L, Fox CS, O'Donnell CJ, et al. Lipid profiling identifies a triacylglycerol signature of insulin resistance and improves diabetes prediction in humans. J Clin Invest. 2011;121(4):1402–11.CrossRefPubMedPubMedCentral Rhee EP, Cheng S, Larson MG, Walford GA, Lewis GD, McCabe E, Yang E, Farrell L, Fox CS, O'Donnell CJ, et al. Lipid profiling identifies a triacylglycerol signature of insulin resistance and improves diabetes prediction in humans. J Clin Invest. 2011;121(4):1402–11.CrossRefPubMedPubMedCentral
22.
go back to reference Pietilainen KH, Sysi-Aho M, Rissanen A, Seppanen-Laakso T, Yki-Jarvinen H, Kaprio J, Oresic M. Acquired obesity is associated with changes in the serum lipidomic profile independent of genetic effects–a monozygotic twin study. PLoS One. 2007;2(2):e218.CrossRefPubMedPubMedCentral Pietilainen KH, Sysi-Aho M, Rissanen A, Seppanen-Laakso T, Yki-Jarvinen H, Kaprio J, Oresic M. Acquired obesity is associated with changes in the serum lipidomic profile independent of genetic effects–a monozygotic twin study. PLoS One. 2007;2(2):e218.CrossRefPubMedPubMedCentral
23.
go back to reference Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR, Grunfeld C. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res. 2004;45(7):1169–96.CrossRefPubMed Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR, Grunfeld C. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res. 2004;45(7):1169–96.CrossRefPubMed
24.
25.
go back to reference Wang H, Tang J, Chen X, Li F, Luo J. Lipid profiles in untreated patients with dermatomyositis. J Eur Acad Dermatol Venereol. 2013;27(2):175–9.CrossRefPubMed Wang H, Tang J, Chen X, Li F, Luo J. Lipid profiles in untreated patients with dermatomyositis. J Eur Acad Dermatol Venereol. 2013;27(2):175–9.CrossRefPubMed
26.
go back to reference Kozu KT, Silva CA, Bonfa E, Sallum AM, Pereira RM, Viana VS, Borba E, Campos LM. Dyslipidaemia in juvenile dermatomyositis: the role of disease activity. Clin Exp Rheumatol. 2013;31(4):638–44.PubMed Kozu KT, Silva CA, Bonfa E, Sallum AM, Pereira RM, Viana VS, Borba E, Campos LM. Dyslipidaemia in juvenile dermatomyositis: the role of disease activity. Clin Exp Rheumatol. 2013;31(4):638–44.PubMed
27.
go back to reference Bohan A, Peter JB. Polymyositis and dermatomyositis (second of two parts). N Engl J Med. 1975;292(8):403–7.CrossRefPubMed Bohan A, Peter JB. Polymyositis and dermatomyositis (second of two parts). N Engl J Med. 1975;292(8):403–7.CrossRefPubMed
28.
go back to reference Bohan A, Peter JB. Polymyositis and dermatomyositis (first of two parts). N Engl J Med. 1975;292(7):344–7.CrossRefPubMed Bohan A, Peter JB. Polymyositis and dermatomyositis (first of two parts). N Engl J Med. 1975;292(7):344–7.CrossRefPubMed
29.
go back to reference Hozumi H, Fujisawa T, Nakashima R, Johkoh T, Sumikawa H, Murakami A, Enomoto N, Inui N, Nakamura Y, Hosono Y, et al. Comprehensive assessment of myositis-specific autoantibodies in polymyositis/dermatomyositis-associated interstitial lung disease. Respir Med. 2016;121:91–9.CrossRefPubMed Hozumi H, Fujisawa T, Nakashima R, Johkoh T, Sumikawa H, Murakami A, Enomoto N, Inui N, Nakamura Y, Hosono Y, et al. Comprehensive assessment of myositis-specific autoantibodies in polymyositis/dermatomyositis-associated interstitial lung disease. Respir Med. 2016;121:91–9.CrossRefPubMed
30.
go back to reference Mammen AL, Mahoney JA, St Germain A, Badders N, Taylor JP, Rosen A, Spinette S. A novel conserved isoform of the ubiquitin ligase UFD2a/UBE4B is expressed exclusively in mature striated muscle cells. PLoS One. 2011;6(12):e28861.CrossRefPubMedPubMedCentral Mammen AL, Mahoney JA, St Germain A, Badders N, Taylor JP, Rosen A, Spinette S. A novel conserved isoform of the ubiquitin ligase UFD2a/UBE4B is expressed exclusively in mature striated muscle cells. PLoS One. 2011;6(12):e28861.CrossRefPubMedPubMedCentral
31.
go back to reference Alexanderson H, Broman L, Tollback A, Josefson A, Lundberg IE, Stenstrom CH. Functional index-2: Validity and reliability of a disease-specific measure of impairment in patients with polymyositis and dermatomyositis. Arthritis Rheum. 2006;55(1):114–22.CrossRefPubMed Alexanderson H, Broman L, Tollback A, Josefson A, Lundberg IE, Stenstrom CH. Functional index-2: Validity and reliability of a disease-specific measure of impairment in patients with polymyositis and dermatomyositis. Arthritis Rheum. 2006;55(1):114–22.CrossRefPubMed
32.
go back to reference Idborg H, Olsson P, Leclerc P, Raouf J, Jakobsson PJ, Korotkova M. Effects of mPGES-1 deletion on eicosanoid and fatty acid profiles in mice. Prostaglandins Other Lipid Mediat. 2013;107:18–25.CrossRefPubMed Idborg H, Olsson P, Leclerc P, Raouf J, Jakobsson PJ, Korotkova M. Effects of mPGES-1 deletion on eicosanoid and fatty acid profiles in mice. Prostaglandins Other Lipid Mediat. 2013;107:18–25.CrossRefPubMed
33.
go back to reference Evans JD. Straightforward statistics for the behavioral sciences. Pacific Grove: Brooks/Cole Publishing; 1996. Evans JD. Straightforward statistics for the behavioral sciences. Pacific Grove: Brooks/Cole Publishing; 1996.
34.
go back to reference Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem. 2001;276(20):16683–9.CrossRefPubMed Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem. 2001;276(20):16683–9.CrossRefPubMed
35.
go back to reference Lee JY, Zhao L, Youn HS, Weatherill AR, Tapping R, Feng L, Lee WH, Fitzgerald KA, Hwang DH. Saturated fatty acid activates but polyunsaturated fatty acid inhibits Toll-like receptor 2 dimerized with Toll-like receptor 6 or 1. J Biol Chem. 2004;279(17):16971–9.CrossRefPubMed Lee JY, Zhao L, Youn HS, Weatherill AR, Tapping R, Feng L, Lee WH, Fitzgerald KA, Hwang DH. Saturated fatty acid activates but polyunsaturated fatty acid inhibits Toll-like receptor 2 dimerized with Toll-like receptor 6 or 1. J Biol Chem. 2004;279(17):16971–9.CrossRefPubMed
37.
go back to reference Bryner RW, Woodworth-Hobbs ME, Williamson DL, Alway SE. Docosahexaenoic acid protects muscle cells from palmitate-induced atrophy. ISRN Obes. 2012;2012:647348.PubMedPubMedCentral Bryner RW, Woodworth-Hobbs ME, Williamson DL, Alway SE. Docosahexaenoic acid protects muscle cells from palmitate-induced atrophy. ISRN Obes. 2012;2012:647348.PubMedPubMedCentral
38.
go back to reference Jacobsson L, Lindgarde F, Manthorpe R, Akesson B. Correlation of fatty acid composition of adipose tissue lipids and serum phosphatidylcholine and serum concentrations of micronutrients with disease duration in rheumatoid arthritis. Ann Rheum Dis. 1990;49(11):901–5.CrossRefPubMedPubMedCentral Jacobsson L, Lindgarde F, Manthorpe R, Akesson B. Correlation of fatty acid composition of adipose tissue lipids and serum phosphatidylcholine and serum concentrations of micronutrients with disease duration in rheumatoid arthritis. Ann Rheum Dis. 1990;49(11):901–5.CrossRefPubMedPubMedCentral
39.
go back to reference Lee AL, Park Y. The Association between n-3 polyunsaturated fatty acid levels in erythrocytes and the risk of rheumatoid arthritis in Korean women. Ann Nutr Metab. 2013;63(1–2):88–95.CrossRefPubMed Lee AL, Park Y. The Association between n-3 polyunsaturated fatty acid levels in erythrocytes and the risk of rheumatoid arthritis in Korean women. Ann Nutr Metab. 2013;63(1–2):88–95.CrossRefPubMed
40.
go back to reference Gorska A, Nawrocki A, Urban M, Florys B. Composition of phospholipid fatty acids in erythrocyte membranes of children with chronic juvenile arthritis: clinical and biochemical correlations. Med Sci Monit. 2000;6(1):30–9.PubMed Gorska A, Nawrocki A, Urban M, Florys B. Composition of phospholipid fatty acids in erythrocyte membranes of children with chronic juvenile arthritis: clinical and biochemical correlations. Med Sci Monit. 2000;6(1):30–9.PubMed
41.
go back to reference Macfarlane DP, Forbes S, Walker BR. Glucocorticoids and fatty acid metabolism in humans: fuelling fat redistribution in the metabolic syndrome. J Endocrinol. 2008;197(2):189–204.CrossRefPubMed Macfarlane DP, Forbes S, Walker BR. Glucocorticoids and fatty acid metabolism in humans: fuelling fat redistribution in the metabolic syndrome. J Endocrinol. 2008;197(2):189–204.CrossRefPubMed
42.
go back to reference Morgan SA, Gathercole LL, Simonet C, Hassan-Smith ZK, Bujalska I, Guest P, Abrahams L, Smith DM, Stewart PM, Lavery GG, et al. Regulation of lipid metabolism by glucocorticoids and 11beta-HSD1 in skeletal muscle. Endocrinology. 2013;154(7):2374–84.CrossRefPubMed Morgan SA, Gathercole LL, Simonet C, Hassan-Smith ZK, Bujalska I, Guest P, Abrahams L, Smith DM, Stewart PM, Lavery GG, et al. Regulation of lipid metabolism by glucocorticoids and 11beta-HSD1 in skeletal muscle. Endocrinology. 2013;154(7):2374–84.CrossRefPubMed
43.
go back to reference Huang YS, Huang WC, Li CW, Chuang LT. Eicosadienoic acid differentially modulates production of pro-inflammatory modulators in murine macrophages. Mol Cell Biochem. 2011;358(1–2):85–94.CrossRefPubMed Huang YS, Huang WC, Li CW, Chuang LT. Eicosadienoic acid differentially modulates production of pro-inflammatory modulators in murine macrophages. Mol Cell Biochem. 2011;358(1–2):85–94.CrossRefPubMed
44.
go back to reference Miles EA, Calder PC. Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis. Br J Nutr. 2012;107(Suppl 2):S171–84.CrossRefPubMed Miles EA, Calder PC. Influence of marine n-3 polyunsaturated fatty acids on immune function and a systematic review of their effects on clinical outcomes in rheumatoid arthritis. Br J Nutr. 2012;107(Suppl 2):S171–84.CrossRefPubMed
46.
go back to reference Helge JW, Wu BJ, Willer M, Daugaard JR, Storlien LH, Kiens B. Training affects muscle phospholipid fatty acid composition in humans. J Appl Physiol (1985). 2001;90(2):670–7.CrossRef Helge JW, Wu BJ, Willer M, Daugaard JR, Storlien LH, Kiens B. Training affects muscle phospholipid fatty acid composition in humans. J Appl Physiol (1985). 2001;90(2):670–7.CrossRef
47.
go back to reference Jordy AB, Kiens B. Regulation of exercise-induced lipid metabolism in skeletal muscle. Exp Physiol. 2014;99(12):1586–92.CrossRefPubMed Jordy AB, Kiens B. Regulation of exercise-induced lipid metabolism in skeletal muscle. Exp Physiol. 2014;99(12):1586–92.CrossRefPubMed
48.
go back to reference Andersson A, Nalsen C, Tengblad S, Vessby B. Fatty acid composition of skeletal muscle reflects dietary fat composition in humans. Am J Clin Nutr. 2002;76(6):1222–9.CrossRefPubMed Andersson A, Nalsen C, Tengblad S, Vessby B. Fatty acid composition of skeletal muscle reflects dietary fat composition in humans. Am J Clin Nutr. 2002;76(6):1222–9.CrossRefPubMed
49.
go back to reference Lundberg IE, Tjarnlund A, Bottai M, Werth VP, Pilkington C, Visser M, Alfredsson L, Amato AA, Barohn RJ, Liang MH, et al. 2017 European League Against Rheumatism/American College of Rheumatology classification criteria for adult and juvenile idiopathic inflammatory myopathies and their major subgroups. Ann Rheum Dis. 2017;76(12):1955–64.CrossRefPubMed Lundberg IE, Tjarnlund A, Bottai M, Werth VP, Pilkington C, Visser M, Alfredsson L, Amato AA, Barohn RJ, Liang MH, et al. 2017 European League Against Rheumatism/American College of Rheumatology classification criteria for adult and juvenile idiopathic inflammatory myopathies and their major subgroups. Ann Rheum Dis. 2017;76(12):1955–64.CrossRefPubMed
50.
go back to reference Hengstman GJ, ter Laak HJ, Vree Egberts WT, Lundberg IE, Moutsopoulos HM, Vencovsky J, Doria A, Mosca M, van Venrooij WJ, van Engelen BG. Anti-signal recognition particle autoantibodies: marker of a necrotising myopathy. Ann Rheum Dis. 2006;65(12):1635–8.CrossRefPubMedPubMedCentral Hengstman GJ, ter Laak HJ, Vree Egberts WT, Lundberg IE, Moutsopoulos HM, Vencovsky J, Doria A, Mosca M, van Venrooij WJ, van Engelen BG. Anti-signal recognition particle autoantibodies: marker of a necrotising myopathy. Ann Rheum Dis. 2006;65(12):1635–8.CrossRefPubMedPubMedCentral
Metadata
Title
Targeted lipidomics analysis identified altered serum lipid profiles in patients with polymyositis and dermatomyositis
Authors
Joan Raouf
Helena Idborg
Petter Englund
Helene Alexanderson
Maryam Dastmalchi
Per-Johan Jakobsson
Ingrid E. Lundberg
Marina Korotkova
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2018
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-018-1579-y

Other articles of this Issue 1/2018

Arthritis Research & Therapy 1/2018 Go to the issue