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Applied Microbiology and Biotechnology

, Volume 104, Issue 3, pp 967–979 | Cite as

Calanus oil in the treatment of obesity-related low-grade inflammation, insulin resistance, and atherosclerosis

  • Amin Gasmi
  • Pavan Kumar Mujawdiya
  • Mariia Shanaida
  • Adrien Ongenae
  • Roman Lysiuk
  • Monica Daniela DoşaEmail author
  • Oxana Tsal
  • Salva Piscopo
  • Salvatore Chirumbolo
  • Geir BjørklundEmail author
Mini-Review
  • 103 Downloads

Abstract

Calanus oil (COil) is a natural product extracted from marine zooplankton Calanus finmarchicus found in the North Atlantic Ocean. This oil is rich in wax esters of polyunsaturated fatty acids (PUFAs) and has been projected as the best alternative to fish oil because its production cannot keep pace with the demands from the growing markets. The COil is the only commercially available marine source of wax esters, whereas classic ω-3 PUFAs comes from triglycerides, ethyl esters, and phospholipids. It has, in recent decades, been seen that there is an unprecedented rise in the use of PUFA-rich oil in the aquaculture industry. A simultaneous rise in the demand of PUFAs is also observed in the health care industry, where PUFAs are suggested preventing various disorders related to lifestyles such as obesity, diabetes mellitus, chronic low-grade inflammation, atherosclerosis, and brain and cardiovascular disorders (CVDs). In this review, we will explore the metabolic aspects related to the use of COil as an antioxidant, anticholesterinemic, and anti-inflammatory dietary source and its impact on the prevention and therapy of obesity-related metabolic disorders.

Keywords

Calanus oil Calanus finmarchicus Polyunsaturated fatty acid Wax esters Astaxanthin 

Notes

Author contributions

All authors confirmed they have contributed to the intellectual content of this paper and have met the following three requirements: (a) significant contributions to the conception and design, acquisition of data, or analysis and interpretation of data; (b) drafting or revising the article for intellectual content; and (c) final approval of the published article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Compliance with ethical standards

Conflict of interest

Adrien Ongenae and Salva Piscopo work for Nutrilogics SA, a company producing natural dietary supplements. No one of the other authors has any conflict of interest to declare.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abdali D, Samson SE, Grover AK (2015) How effective are antioxidant supplements in obesity and diabetes? Med Princ Pract 24(3):201–215.  https://doi.org/10.1159/000375305 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abdelhamid AS, Martin N, Bridges C, Brainard JS, Wang X, Brown TJ, Hanson S, Jimoh OF, Ajabnoor SM, Deane KH, Song F, Hooper L (2018) Polyunsaturated fatty acids for the primary and secondary prevention of cardiovascular disease. Cochrane Database Syst Rev 11:CD012345.  https://doi.org/10.1002/14651858.CD012345.pub3 CrossRefPubMedGoogle Scholar
  3. Abdolahi M, Jafarieh A, Sarraf P, Sedighiyan M, Yousefi A, Tafakhori A, Abdollahi H, Salehinia F, Djalali M (2019) The neuromodulatory effects of omega-3 fatty acids and nano-curcumin on the COX-2/ iNOS network in migraines: a clinical trial study from gene expression to clinical symptoms. Endocr Metab Immune Disord Drug Targets 19(6):874–884.  https://doi.org/10.2174/1871530319666190212170140 CrossRefPubMedGoogle Scholar
  4. Abel S, Riedel S, Gelderblom WC (2014) Dietary PUFA and cancer. Proc Nutr Soc 73(3):361–367.  https://doi.org/10.1017/S0029665114000585 CrossRefPubMedGoogle Scholar
  5. Akbar U, Yang M, Kurian D, Mohan C (2017) Omega-3 fatty acids in rheumatic diseases: a critical review. J Clin Rheumatol 23(6):330–339.  https://doi.org/10.1097/RHU.0000000000000563 CrossRefPubMedGoogle Scholar
  6. Alava JJ, Gobas FA (2012) Assessing biomagnification and trophic transport of persistent organic pollutants in the food chain of the Galapagos sea lion (Zalophus wollebaeki): conservation and management implications. In: Romero A, Keith EO (eds) New approaches to the study of marine mammals. InTech, Rijeka, pp 77–108Google Scholar
  7. Albert BB, Cameron-Smith D, Garg ML, Derraik JG, Hofman PL, Cutfielda WS (2016) Marine oils: complex, confusing, confounded? J Nutr Intermed Metab 5:3–10CrossRefGoogle Scholar
  8. AMAP (2002) Arctic pollution 2002: persistent organic pollutants, heavy metals, radioactivity, human health, changing pathways. Arctic Monitoring and Assessment Programme (AMAP), OsloGoogle Scholar
  9. Ambati RR, Phang SM, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Mar Drugs 12(1):128–152.  https://doi.org/10.3390/md12010128 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Andersson M, Van Nieuwerburgh L, Snoeijs P (2003) Pigment transfer from phytoplankton to zooplankton with emphasis on astaxanthin production in the Baltic Sea food web. Mar Ecol Prog Ser 254:213–224.  https://doi.org/10.3354/meps254213 CrossRefGoogle Scholar
  11. Appleton KM, Sallis HM, Perry R, Ness AR, Churchill R (2015) Omega-3 fatty acids for depression in adults. Cochrane Database Syst Rev 11:CD004692.  https://doi.org/10.1002/14651858.CD004692.pub4 CrossRefGoogle Scholar
  12. Aucoin M, Cooley K, Knee C, Fritz H, Balneaves LG, Breau R, Fergusson D, Skidmore B, Wong R, Seely D (2017) Fish-derived omega-3 fatty acids and prostate cancer: a systematic review. Integr Cancer Ther 16(1):32–62.  https://doi.org/10.1177/1534735416656052 CrossRefPubMedGoogle Scholar
  13. Bailey C, McMeans BC, Arts MT, Rush SA, Fisk AT (2012) Seasonal patterns in fatty acids of Calanus hyperboreus (Copepoda, Calanoida) from Cumberland Sound, Baffin Island, Nunavut. Mar Biol 159(5):1095–1105.  https://doi.org/10.1007/s00227-012-1889-6 CrossRefGoogle Scholar
  14. Bazan NG (2005) Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress. Brain Pathol 15(2):159–166CrossRefGoogle Scholar
  15. Bimbo AP (2012) Processing of marine oils. Long-chain omega-3 specialty oils. In: Breivik H (ed) Long-chain omega-3 specialty oils. Woodhead Publishing, Cambridge, pp 77–109CrossRefGoogle Scholar
  16. Bot M, Brouwer IA, Roca M, Kohls E, Penninx B, Watkins E, van Grootheest G, Cabout M, Hegerl U, Gili M, Owens M, Visser M, Moo DPTI (2019) Effect of multinutrient supplementation and food-related behavioral activation therapy on prevention of major depressive disorder among overweight or obese adults with subsyndromal depressive symptoms: the MooDFOOD randomized clinical trial. JAMA 321(9):858–868.  https://doi.org/10.1001/jama.2019.0556 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bowman GL, Silbert LC, Dodge HH, Lahna D, Hagen K, Murchison CF, Howieson D, Kaye J, Quinn JF, Shinto L (2019) Randomized trial of marine n-3 polyunsaturated fatty acids for the prevention of cerebral small vessel disease and inflammation in aging (PUFA trial): rationale, design and baseline results. Nutrients 11(4).  https://doi.org/10.3390/nu11040735 CrossRefGoogle Scholar
  18. Buettner C (2010) GPR120 mediates the benefits of fish oil. Sci Transl Med 2(51):51ec150.  https://doi.org/10.1126/scitranslmed.3001730 CrossRefGoogle Scholar
  19. Calder PC (2015) Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms and clinical relevance. Biochim Biophys Acta 1851(4):469–484.  https://doi.org/10.1016/j.bbalip.2014.08.010 CrossRefPubMedGoogle Scholar
  20. Cole GM, Lim GP, Yang F, Teter B, Begum A, Ma Q, Harris-White ME, Frautschy SA (2005) Prevention of Alzheimer’s disease: omega-3 fatty acid and phenolic anti-oxidant interventions. Neurobiol Aging 26(Suppl 1):133–136.  https://doi.org/10.1016/j.neurobiolaging.2005.09.005 CrossRefPubMedGoogle Scholar
  21. Cook CM, Larsen TS, Derrig LD, Kelly KM, Tande KS (2016) Wax ester rich oil from the marine crustacean, Calanus finmarchicus, is a bioavailable source of EPA and DHA for human consumption. Lipids 51(10):1137–1144.  https://doi.org/10.1007/s11745-016-4189-y CrossRefPubMedGoogle Scholar
  22. Cooper RE, Tye C, Kuntsi J, Vassos E, Asherson P (2016) The effect of omega-3 polyunsaturated fatty acid supplementation on emotional dysregulation, oppositional behaviour and conduct problems in ADHD: a systematic review and meta-analysis. J Affect Disord 190:474–482.  https://doi.org/10.1016/j.jad.2015.09.053 CrossRefPubMedGoogle Scholar
  23. Crandell JR (2016) Switching from EPA + DHA (omega-3-acid ethyl esters) to high-purity EPA (icosapent ethyl) in a statin-treated patient with persistent dyslipidemia and high cardiovascular risk: a case study. Clin Med Insights Cardiol 10:123–128.  https://doi.org/10.4137/CMC.S38123 CrossRefPubMedPubMedCentralGoogle Scholar
  24. de Araújo RF, Martins DB, Borba MA (2016) Oxidative stress and disease. In: Morales-Gonzalez JA, Morales-González A, Madrigal-Santillan EO (eds) A master regulator of oxidative stress: the transcription factor Nrf2. InTech, Rijeka, pp 185–199Google Scholar
  25. Dangour AD, Whitehouse PJ, Rafferty K, Mitchell SA, Smith L, Hawkesworth S, Vellas B (2010) B-vitamins and fatty acids in the prevention and treatment of Alzheimer’s disease and dementia: a systematic review. J Alzheimers Dis 22(1):205–224.  https://doi.org/10.3233/JAD-2010-090940 CrossRefPubMedGoogle Scholar
  26. D'Archivio M, Scazzocchio B, Vari R, Santangelo C, Giovannini C, Masella R (2018) Recent evidence on the role of dietary PUFAs in cancer development and prevention. Curr Med Chem 25(16):1818–1836.  https://doi.org/10.2174/0929867325666171204160231 CrossRefPubMedGoogle Scholar
  27. Das UN (2000) Beneficial effect(s) of n-3 fatty acids in cardiovascular diseases: but, why and how? Prostaglandins Leukot Essent Fat Acids 63(6):351–362.  https://doi.org/10.1054/plef.2000.0226 CrossRefGoogle Scholar
  28. Davinelli S, Nielsen ME, Scapagnini G (2018) Astaxanthin in skin health, repair, and disease: a comprehensive review. Nutrients 10(4).  https://doi.org/10.3390/nu10040522 CrossRefGoogle Scholar
  29. Echeverria F, Valenzuela R, Catalina Hernandez-Rodas M, Valenzuela A (2017) Docosahexaenoic acid (DHA), a fundamental fatty acid for the brain: new dietary sources. Prostaglandins Leukot Essent Fat Acids 124:1–10.  https://doi.org/10.1016/j.plefa.2017.08.001 CrossRefGoogle Scholar
  30. Eilertsen KE, Maehre HK, Jensen IJ, Devold H, Olsen JO, Lie RK, Brox J, Berg V, Elvevoll EO, Osterud B (2012) A wax ester and astaxanthin-rich extract from the marine copepod Calanus finmarchicus attenuates atherogenesis in female apolipoprotein E-deficient mice. J Nutr 142(3):508–512.  https://doi.org/10.3945/jn.111.145698 CrossRefPubMedGoogle Scholar
  31. Ellulu MS, Patimah I, Khaza'ai H, Rahmat A, Abed Y (2017) Obesity and inflammation: the linking mechanism and the complications. Arch Med Sci 13(4):851–863.  https://doi.org/10.5114/aoms.2016.58928 CrossRefPubMedGoogle Scholar
  32. Ergas D, Eilat E, Mendlovic S, Sthoeger ZM (2002) N-3 fatty acids and the immune system in autoimmunity. Isr Med Assoc J 4(1):34–38PubMedGoogle Scholar
  33. Fabian CJ, Kimler BF, Hursting SD (2015) Omega-3 fatty acids for breast cancer prevention and survivorship. Breast Cancer Res 17:62.  https://doi.org/10.1186/s13058-015-0571-6 CrossRefPubMedPubMedCentralGoogle Scholar
  34. FAO/WHO (2003) Diet, nutrition, and the prevention of chronic diseases. WHO Technical Report Series 916. World Health Organisation, GenevaGoogle Scholar
  35. Feguri GR, Lima PRL, Franco AC, Cruz FRH, Borges DC, Toledo LR, Segri NJ, Aguilar-Nascimento JE (2019) Benefits of fasting abbreviation with carbohydrates and omega-3 infusion during CABG: a double-blind controlled randomized trial. Braz J Cardiovasc Surg 34(2):125–135.  https://doi.org/10.21470/1678-9741-2018-0336 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Fujisaka S, Usui I, Ikutani M, Aminuddin A, Takikawa A, Tsuneyama K, Mahmood A, Goda N, Nagai Y, Takatsu K, Tobe K (2013) Adipose tissue hypoxia induces inflammatory M1 polarity of macrophages in an HIF-1alpha-dependent and HIF-1alpha-independent manner in obese mice. Diabetologia 56(6):1403–1412.  https://doi.org/10.1007/s00125-013-2885-1 CrossRefPubMedGoogle Scholar
  37. Garcia-Esquinas E, Ortola R, Banegas JR, Lopez-Garcia E, Rodriguez-Artalejo F (2019) Dietary n-3 polyunsaturated fatty acids, fish intake and healthy ageing. Int J Epidemiol.  https://doi.org/10.1093/ije/dyz196 CrossRefGoogle Scholar
  38. Graeve M, Kattner G (1992) Species-specific differences in intact wax esters of Calanus hyperboreus and C. finmarchicus from Fram Strait—Greenland Sea. Mar Chem 39(4):269–281.  https://doi.org/10.1016/0304-4203(92)90013-Z CrossRefGoogle Scholar
  39. Grieve BD, Hare JA, Saba VS (2017) Projecting the effects of climate change on Calanus finmarchicus distribution within the U.S. Northeast Continental Shelf. Sci Rep 7(1):6264.  https://doi.org/10.1038/s41598-017-06524-1 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 21(5):210–216.  https://doi.org/10.1016/S0167-7799(03)00078-7 CrossRefPubMedGoogle Scholar
  41. Halvorsen B, Rustan AC, Christiansen EN (1995) Effect of long-chain mono-unsaturated and n-3 polyunsaturated fatty acids on postprandial blood and liver lipids in rats. Scand J Clin Lab Invest 55(6):469–475.  https://doi.org/10.1080/00365519509075384 CrossRefPubMedGoogle Scholar
  42. Hande LN, Thunhaug H, Enebakk T, Ludviksen J, Pettersen K, Hovland A, Lappegard KT (2019) Addition of marine omega-3 fatty acids to statins in familial hypercholesterolemia does not affect in vivo or in vitro endothelial function. J Clin Lipidol.  https://doi.org/10.1016/j.jacl.2019.08.004 CrossRefGoogle Scholar
  43. Hoper AC, Salma W, Khalid AM, Hafstad AD, Sollie SJ, Raa J, Larsen TS, Aasum E (2013) Oil from the marine zooplankton Calanus finmarchicus improves the cardiometabolic phenotype of diet-induced obese mice. Br J Nutr 110(12):2186–2193.  https://doi.org/10.1017/S0007114513001839 CrossRefPubMedGoogle Scholar
  44. Höper AC, Salma W, Sollie SJ, Hafstad AD, Lund J, Khalid AM, Raa J, Aasum E, Larsen TS (2014) Wax esters from the marine copepod Calanus finmarchicus reduce diet-induced obesity and obesity-related metabolic disorders in mice. J Nutr 144(2):164–169.  https://doi.org/10.3945/jn.113.182501 CrossRefPubMedGoogle Scholar
  45. Horrocks LA, Yeo YK (1999) Health benefits of docosahexaenoic acid (DHA). Pharmacol Res 40(3):211–225.  https://doi.org/10.1006/phrs.1999.0495 CrossRefPubMedGoogle Scholar
  46. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444(7121):860–867.  https://doi.org/10.1038/nature05485 CrossRefPubMedGoogle Scholar
  47. Hruby A, Hu FB (2015) The epidemiology of obesity: a big picture. Pharmacoeconomics 33(7):673–689.  https://doi.org/10.1007/s40273-014-0243-x CrossRefPubMedPubMedCentralGoogle Scholar
  48. Im DS (2018) FFA4 (GPR120) as a fatty acid sensor involved in appetite control, insulin sensitivity and inflammation regulation. Mol Asp Med 64:92–108.  https://doi.org/10.1016/j.mam.2017.09.001 CrossRefGoogle Scholar
  49. Jansen KM, Larsen TS (2017) Dietary and pharmacological anti-obesogenic treatments improve myocardial metabolism in diet-induced obese mice. Paper presented at the 12th Conference on Mitochondrial Physiology and MitoEAGLE WG and MC Meeting, Hradec KraloveGoogle Scholar
  50. Jansen KM, Moreno S, Garcia-Roves PM, Larsen TS (2019) Dietary calanus oil recovers metabolic flexibility and rescues postischemic cardiac function in obese female mice. Am J Physiol Heart Circ Physiol 317(2):H290–H299.  https://doi.org/10.1152/ajpheart.00191.2019 CrossRefPubMedGoogle Scholar
  51. Jiao J, Li Q, Chu J, Zeng W, Yang M, Zhu S (2014) Effect of n-3 PUFA supplementation on cognitive function throughout the life span from infancy to old age: a systematic review and meta-analysis of randomized controlled trials. Am J Clin Nutr 100(6):1422–1436.  https://doi.org/10.3945/ajcn.114.095315 CrossRefPubMedGoogle Scholar
  52. Johnsen SH, Jacobsen BK, Brækkan SK, Hansen JB, Mathiesen EB (2018) Fish consumption, fish oil supplements and risk of atherosclerosis in the Tromsø study. Nutr J 17(1):56–59.  https://doi.org/10.1186/s12937-018-0364-8 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Karakula-Juchnowicz H, Rog J, Juchnowicz D, Morylowska-Topolska J (2017) GPR120: mechanism of action, role and potential for medical applications. Postepy Hig Med Dosw (Online) 71(0):942–953.  https://doi.org/10.5604/01.3001.0010.5809 CrossRefGoogle Scholar
  54. Kvile KO, Langangen O, Prokopchuk I, Stenseth NC, Stige LC (2016) Disentangling the mechanisms behind climate effects on zooplankton. Proc Natl Acad Sci U S A 113(7):1841–1846.  https://doi.org/10.1073/pnas.1525130113 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kidd PM (2007) Omega-3 DHA and EPA for cognition, behavior, and mood: clinical findings and structural-functional synergies with cell membrane phospholipids. Altern Med Rev 12(3):207-227Google Scholar
  56. Lee RF, Nevenzel JC, Paffenhofer GA (1970) Wax esters in marine copepods. Science 167(3924):1510–1511.  https://doi.org/10.1126/science.167.3924.1510 CrossRefPubMedGoogle Scholar
  57. Lee KR, Kim KH, Kim JB, Hong SB, Jeon I, Kim HU, Lee MH, Kim JK (2019) High accumulation of gamma-linolenic acid and stearidonic acid in transgenic Perilla (Perilla frutescens var. frutescens) seeds. BMC Plant Biol 19(1):120.  https://doi.org/10.1186/s12870-019-1713-2 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Li F, Liu X, Zhang D (2016) Fish consumption and risk of depression: a meta-analysis. J Epidemiol Community Health 70(3):299–304.  https://doi.org/10.1136/jech-2015-206278 CrossRefPubMedGoogle Scholar
  59. Linder M, Belhaj N, Sautot P, Tehrany EA (2010) From krill to whale: an overview of marine fatty acids and lipid composition. OCL 17(4):194–204CrossRefGoogle Scholar
  60. Lo Van A, Sakayori N, Hachem M, Belkouch M, Picq M, Lagarde M, Osumi N, Bernoud-Hubac N (2016) Mechanisms of DHA transport to the brain and potential therapy to neurodegenerative diseases. Biochimie 130:163–167.  https://doi.org/10.1016/j.biochi.2016.07.011 CrossRefPubMedGoogle Scholar
  61. Lohmeier TE (2012) Angiotensin II infusion model of hypertension: is there an important sympathetic component? Hypertension 59(3):539–541.  https://doi.org/10.1161/HYPERTENSIONAHA.111.188714 CrossRefPubMedGoogle Scholar
  62. Lovren F, Teoh H, Verma S (2015) Obesity and atherosclerosis: mechanistic insights. Can J Cardiol 31(2):177–183.  https://doi.org/10.1016/j.cjca.2014.11.031 CrossRefPubMedGoogle Scholar
  63. Marion-Letellier R, Savoye G, Ghosh S (2015) Polyunsaturated fatty acids and inflammation. IUBMB Life 67(9):659–667.  https://doi.org/10.1002/iub.1428 CrossRefPubMedGoogle Scholar
  64. Mazereeuw G, Lanctot KL, Chau SA, Swardfager W, Herrmann N (2012) Effects of omega-3 fatty acids on cognitive performance: a meta-analysis. Neurobiol Aging 33(7):1482 e17–1482 e29.  https://doi.org/10.1016/j.neurobiolaging.2011.12.014 CrossRefGoogle Scholar
  65. Minihane AM, Vinoy S, Russell WR, Baka A, Roche HM, Tuohy KM, Teeling JL, Blaak EE, Fenech M, Vauzour D, McArdle HJ, Kremer BH, Sterkman L, Vafeiadou K, Benedetti MM, Williams CM, Calder PC (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114(7):999–1012.  https://doi.org/10.1017/S0007114515002093 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Moniri NH (2016) Free-fatty acid receptor-4 (GPR120): cellular and molecular function and its role in metabolic disorders. Biochem Pharmacol 110-111:1–15.  https://doi.org/10.1016/j.bcp.2016.01.021 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Mozaffarian D, Rimm EB (2006) Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA 296(15):1885–1899.  https://doi.org/10.1001/jama.296.15.1885 CrossRefPubMedGoogle Scholar
  68. Nabavi SF, Bilotto S, Russo GL, Orhan IE, Habtemariam S, Daglia M, Devi KP, Loizzo MR, Tundis R, Nabavi SM (2015) Omega-3 polyunsaturated fatty acids and cancer: lessons learned from clinical trials. Cancer Metastasis Rev 34(3):359–380.  https://doi.org/10.1007/s10555-015-9572-2 CrossRefPubMedGoogle Scholar
  69. Nakamura MT, Yudell BE, Loor JJ (2014) Regulation of energy metabolism by long-chain fatty acids. Prog Lipid Res 53:124–144.  https://doi.org/10.1016/j.plipres.2013.12.001 CrossRefPubMedGoogle Scholar
  70. Noverr MC, Erb-Downward JR, Huffnagle GB (2003) Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin Microbiol Rev 16(3):517–533.  https://doi.org/10.1128/cmr.16.3.517-533.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  71. O’Connell TD, Block RC, Huang SP, Shearer GC (2017) Omega-3-polyunsaturated fatty acids for heart failure: effects of dose on efficacy and novel signaling through free fatty acid receptor 4. J Mol Cell Cardiol 103:74–92.  https://doi.org/10.1016/j.yjmcc.2016.12.003 CrossRefPubMedGoogle Scholar
  72. Parker HM, Cohn JS, O'Connor HT, Garg ML, Caterson ID, George J, Johnson NA (2019) Effect of fish oil supplementation on hepatic and visceral fat in overweight men: a randomized controlled trial. Nutrients 11(2).  https://doi.org/10.3390/nu11020475 CrossRefGoogle Scholar
  73. Patra S, Nithya S, Srinithya B, Meenakshi SM (2015) Review of medicinal plants for anti-obesity activity. Transl Biomed 6:3.  https://doi.org/10.21767/2172-0479.100021 CrossRefGoogle Scholar
  74. Pedersen AM (2016) Calanus® oil. Utilization, composition and digestion. Doctoral thesis. Arctic University of Norway, TromsøGoogle Scholar
  75. Pedersen AM (2019) The new lipids from the Arctic. PUblisher https://wwwcalanusno/research-and-development/calanus-oil/the-new-lipids-from-the-arctic Accessed October 7 2019
  76. Pedersen AM, Vang B, Olsen RL (2014) Oil from Calanus finmarchicus—composition and possible use: a review. J Aquat Food Prod Technol 23(6):633–646.  https://doi.org/10.1080/10498850.2012.741662 CrossRefGoogle Scholar
  77. Pham-Huy LA, He H, Pham-Huy C (2008) Free radicals, antioxidants in disease and health. Int J Biomed Sci 4(2):89–96PubMedPubMedCentralGoogle Scholar
  78. Place AR (1992) Comparative aspects of lipid digestion and absorption: physiological correlates of wax ester digestion. Am J Phys 263(3 Pt 2):R464–R471.  https://doi.org/10.1152/ajpregu.1992.263.3.R464 CrossRefGoogle Scholar
  79. Raphael W, Sordillo LM (2013) Dietary polyunsaturated fatty acids and inflammation: the role of phospholipid biosynthesis. Int J Mol Sci 14(10):21167–21188.  https://doi.org/10.3390/ijms141021167 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Rashed AA, Nawi MD, Sulaiman K (2016) Assessment of essential oil as a potential anti-obesity agent: a narrative review. J Essent Oil Res 29(1):1–10.  https://doi.org/10.1080/10412905.2016.1213668 CrossRefGoogle Scholar
  81. Rechenberg K, Humphries D (2013) Nutritional interventions in depression and perinatal depression. Yale J Biol Med 86(2):127–137PubMedPubMedCentralGoogle Scholar
  82. Rehman K, Akash MS (2016) Mechanisms of inflammatory responses and development of insulin resistance: how are they interlinked? J Biomed Sci 23(1):87.  https://doi.org/10.1186/s12929-016-0303-y CrossRefPubMedPubMedCentralGoogle Scholar
  83. Salma W, Franekova V, Lund T, Hoper A, Ludvigsen S, Lund J, Aasum E, Ytrehus K, Belke DD, Larsen TS (2016) Dietary Calanus oil antagonizes angiotensin II-induced hypertension and tissue wasting in diet-induced obese mice. Prostaglandins Leukot Essent Fat Acids 108:13–21.  https://doi.org/10.1016/j.plefa.2016.03.006 CrossRefGoogle Scholar
  84. Salvayre R, Negre-Salvayre A, Camare C (2016) Oxidative theory of atherosclerosis and antioxidants. Biochimie 125:281–296.  https://doi.org/10.1016/j.biochi.2015.12.014 CrossRefPubMedGoogle Scholar
  85. Sears B (2009) Anti-inflammatory diets for obesity and diabetes. J Am Coll Nutr 28(Suppl):482S–491S.  https://doi.org/10.1080/07315724.2009.10718115 CrossRefPubMedGoogle Scholar
  86. Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8(5):349–361.  https://doi.org/10.1038/nri2294 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Shanaida MI (2019) Carboxilic acids of Nigella sativa and N. damascenа seeds (in Ukrainian). Ukr Biopharmaceut J (3):71–76.  https://doi.org/10.24959/ubphj.19.229 CrossRefGoogle Scholar
  88. Shen S, Unger JM, Crew KD, Till C, Greenlee H, Gralow J, Dakhil SR, Minasian LM, Wade JL 3rd, Fisch MJ, Henry NL, Hershman DL (2018) Omega-3 fatty acid use for obese breast cancer patients with aromatase inhibitor-related arthralgia (SWOG S0927). Breast Cancer Res Treat 172(3):603–610.  https://doi.org/10.1007/s10549-018-4946-0 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Simopoulos AP (2002) The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 56(8):365–379CrossRefGoogle Scholar
  90. Simopoulos AP (2006) Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biomed Pharmacother 60(9):502–507.  https://doi.org/10.1016/j.biopha.2006.07.080 CrossRefPubMedGoogle Scholar
  91. Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med (Maywood) 233(6):674–688.  https://doi.org/10.3181/0711-MR-311 CrossRefGoogle Scholar
  92. Smith DJ, Sarris J, Dowling N, O’Connor M, Ng CH (2018) Adjunctive low-dose docosahexaenoic acid (DHA) for major depression: an open-label pilot trial. Nutr Neurosci 21(3):224–228.  https://doi.org/10.1080/1028415X.2017.1283128 CrossRefPubMedGoogle Scholar
  93. Song M, Ou FS, Zemla TJ, Hull MA, Shi Q, Limburg PJ, Alberts SR, Sinicrope FA, Giovannucci EL, Van Blarigan EL, Meyerhardt JA, Chan AT (2019) Marine omega-3 fatty acid intake and survival of stage III colon cancer according to tumor molecular markers in NCCTG phase III trial N0147 (Alliance). Int J Cancer 145(2):380–389.  https://doi.org/10.1002/ijc.32113 CrossRefPubMedGoogle Scholar
  94. Spahis S, Alvarez F, Ahmed N, Dubois J, Jalbout R, Paganelli M, Grzywacz K, Delvin E, Peretti N, Levy E (2018) Non-alcoholic fatty liver disease severity and metabolic complications in obese children: impact of omega-3 fatty acids. J Nutr Biochem 58:28–36.  https://doi.org/10.1016/j.jnutbio.2018.03.025 CrossRefPubMedGoogle Scholar
  95. Sung J, Jeon H, Kim IH, Jeong HS, Lee J (2017) Anti-inflammatory effects of stearidonic acid mediated by suppression of NF-kappaB and MAP-kinase pathways in macrophages. Lipids 52(9):781–787.  https://doi.org/10.1007/s11745-017-4278-6 CrossRefPubMedGoogle Scholar
  96. Tande KS, Vo TD, Lynch BS (2016) Clinical safety evaluation of marine oil derived from Calanus finmarchicus. Regul Toxicol Pharmacol 80:25–31.  https://doi.org/10.1016/j.yrtph.2016.05.030 CrossRefPubMedGoogle Scholar
  97. Turchini GM (2013) Fish oils, misconceptions and the environment. Am J Public Health 103(11):e4.  https://doi.org/10.2105/AJPH.2013.301510 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Turchini GM, Ng WK, Tocher DR (2010) Fish oil replacement and alternative lipid sources in aquaculture feeds. CRC Press, Boca RatonCrossRefGoogle Scholar
  99. van der Burg KP, Cribb L, Firth J, Karmacoska D, Mischoulon D, Byrne GJ, Bousman C, Stough C, Murphy J, Oliver G, Berk M, Ng CH, Sarris J (2019) EPA and DHA as markers of nutraceutical treatment response in major depressive disorder. Eur J Nutr:1–9.  https://doi.org/10.1007/s00394-019-02090-6
  100. Valenzuela A, Valenzuela R (2013) Omega-3 docosahexaenoic acid (DHA) and mood disorders: why and how to provide supplementation? In: Kocabaşoğlu N (ed) Mood disorders. InTech, Rijeka, pp 241–261Google Scholar
  101. Van Dinh K, Olsen MW, Altin D, Vismann B, Nielsen TG (2019) Impact of temperature and pyrene exposure on the functional response of males and females of the copepod Calanus finmarchicus. Environ Sci Pollut Res Int 26:29327–29333.  https://doi.org/10.1007/s11356-019-06078-x CrossRefPubMedGoogle Scholar
  102. Vang B, Pedersen AM, Olsen RL (2013) Oil extraction from the copepod Calanus finmarchicus using proteolytic enzymes. J Aquat Food Prod Technol 22(6):619–628.  https://doi.org/10.1080/10498850.2012.686008 CrossRefGoogle Scholar
  103. Venegas-Caleron M, Sayanova O, Napier JA (2010) An alternative to fish oils: metabolic engineering of oil-seed crops to produce omega-3 long chain polyunsaturated fatty acids. Prog Lipid Res 49(2):108–119.  https://doi.org/10.1016/j.plipres.2009.10.001 CrossRefPubMedGoogle Scholar
  104. Vinding RK, Stokholm J, Sevelsted A, Sejersen T, Chawes BL, Bonnelykke K, Thorsen J, Howe LD, Krakauer M, Bisgaard H (2018) Effect of fish oil supplementation in pregnancy on bone, lean, and fat mass at six years: randomised clinical trial. BMJ 362:k3312.  https://doi.org/10.1136/bmj.k3312 CrossRefPubMedPubMedCentralGoogle Scholar
  105. Walker CG, Jebb SA, Calder PC (2013) Stearidonic acid as a supplemental source of omega-3 polyunsaturated fatty acids to enhance status for improved human health. Nutrition 29(2):363–369.  https://doi.org/10.1016/j.nut.2012.06.003 CrossRefPubMedGoogle Scholar
  106. Wang C, Chung M, Lichtenstein A, Balk E, Kupelnick B, DeVine D, Lawrence A, Lau J (2004) Effects of omega-3 fatty acids on cardiovascular disease. Evid Rep Technol Assess (Summ) (94):1–8Google Scholar
  107. Wang Y, Beydoun MA, Liang L, Caballero B, Kumanyika SK (2008) Will all Americans become overweight or obese? Estimating the progression and cost of the US obesity epidemic. Obesity (Silver Spring) 16(10):2323–2330.  https://doi.org/10.1038/oby.2008.351 CrossRefGoogle Scholar
  108. Wang JF, Zhang HM, Li YY, Xia S, Wei Y, Yang L, Wang D, Ye JJ, Li HX, Yuan J, Pan RR (2019) A combination of omega-3 and plant sterols regulate glucose and lipid metabolism in individuals with impaired glucose regulation: a randomized and controlled clinical trial. Lipids Health Dis 18(1):106.  https://doi.org/10.1186/s12944-019-1048-x CrossRefPubMedPubMedCentralGoogle Scholar
  109. Weylandt KH, Serini S, Chen YQ, Su HM, Lim K, Cittadini A, Calviello G (2015) Omega-3 polyunsaturated fatty acids: the way forward in times of mixed evidence. Biomed Res Int 2015:143109.  https://doi.org/10.1155/2015/143109 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Yang ZH, Emma-Okon B, Remaley AT (2016) Dietary marine-derived long-chain monounsaturated fatty acids and cardiovascular disease risk: a mini review. Lipids Health Dis 15(1):201.  https://doi.org/10.1186/s12944-016-0366-5 CrossRefPubMedPubMedCentralGoogle Scholar
  111. Yang B, Shi MQ, Li ZH, Shi L, Wang AM, Guo XJ, Li D (2019) Effects of n-3 fatty acid supplements on cardiometabolic profiles in hypertensive patients with abdominal obesity in Inner Mongolia: a randomized controlled trial. Food Funct 10(3):1661–1670.  https://doi.org/10.1039/c8fo01707g CrossRefPubMedGoogle Scholar
  112. Yurko-Mauro K, Alexander DD, Van Elswyk ME (2015) Docosahexaenoic acid and adult memory: a systematic review and meta-analysis. PLoS One 10(3):e0120391.  https://doi.org/10.1371/journal.pone.0120391 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Zehr KR, Walker MK (2018) Omega-3 polyunsaturated fatty acids improve endothelial function in humans at risk for atherosclerosis: a review. Prostaglandins Other Lipid Mediat 134:131–140.  https://doi.org/10.1016/j.prostaglandins.2017.07.005 CrossRefPubMedGoogle Scholar
  114. Zuluaga M, Gueguen V, Letourneur D, Pavon-Djavid G (2018) Astaxanthin-antioxidant impact on excessive reactive oxygen species generation induced by ischemia and reperfusion injury. Chem Biol Interact 279:145–158.  https://doi.org/10.1016/j.cbi.2017.11.012 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Société Francophone de Nutrithérapie et de Nutrigénétique AppliquéeVilleurbanneFrance
  2. 2.Birla Institute of Technology and Science-PilaniHyderabadIndia
  3. 3.Department of Pharmacognosy and Medical BotanyI. Horbachevsky Ternopil National Medical UniversityTernopilUkraine
  4. 4.Danylo Halytsky Lviv National Medical UniversityLvivUkraine
  5. 5.CONEM Ukraine Life Science Research Group, Department of Pharmacognosy and BotanyDanylo Halytsky Lviv National Medical UniversityLvivUkraine
  6. 6.Department of Pharmacology, Faculty of MedicineOvidius UniversityConstantaRomania
  7. 7.Department of Neurosciences, Biomedicine and Movement SciencesUniversity of VeronaVeronaItaly
  8. 8.CONEM Scientific SecretaryVeronaItaly
  9. 9.Council for Nutritional and Environmental Medicine (CONEM)Mo i RanaNorway

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