The Omega-3 Index Response to an 8 Week Randomized Intervention Containing Three Fatty Fish Meals Per Week Is Influenced by Adiposity in Overweight to Obese Women
Christine E Richardson, Sridevi Krishnan, Ira J Gray, Nancy L Keim, John W Newman, Christine E Richardson, Sridevi Krishnan, Ira J Gray, Nancy L Keim, John W Newman
Abstract
Background: The Dietary Guidelines for Americans (DGA) recommends consuming ~225 g/wk of a variety of seafood providing >1.75 g/wk of long-chain omega-3 fatty acids to reduce cardiovascular disease risk, however individual responses to treatment vary.
Objective: This study had three main objectives. First, to determine if a DGA-conforming diet (DGAD), in comparison to a typical American diet (TAD), can increase the omega-3 index (OM3I), i.e., the red blood cell mol% of eicosapentaenoic acid (EPA) + docosahexaenoic acid (DHA). Second, to identify factors explaining variability in the OM3I response to dietary treatment. Third to identify factors associated with the baseline OM3I.
Design: This is a secondary analysis of a randomized, double-blind 8 wk dietary intervention of overweight/obese women fed an 8d rotating TAD (n = 20) or DGAD (n = 22) registered at www.clinicaltrials.gov as NCT02298725. The DGAD-group consumed 240 g/wk of Atlantic farmed salmon and albacore tuna in three meals with an estimated EPA + DHA of 3.7 ± 0.6 g/wk. The TAD-group consumed ~160 g/wk of farmed white shrimp and a seafood salad containing imitation crab in three meal with an estimated EPA + DHA of 0.45 ± 0.05 g/wk. Habitual diet was determined at baseline, and body composition was determined at 0 and 8wks. Red blood cell fatty acids were measured at 0, 2 and 8 wk.
Results: At 8 wk, the TAD-group OM3I was unchanged (5.90 ± 1.35-5.80 ± 0.76%), while the DGAD-group OM3I increased (5.63 ± 1.27-7.33 ± 1.36%; p < 0.001). In the DGAD-group 9 of 22 participants achieved an OM3I >8%. Together, body composition and the baseline OM3I explained 83% of the response to treatment variability. Baseline OM3I (5.8 ± 1.3%; n = 42) was negatively correlated to the android fat mass (p = 0.0007) and positively correlated to the FFQ estimated habitual (EPA+DHA) when expressed as a ratio to total dietary fat (p = 0.006).
Conclusions: An 8 wk TAD did not change the OM3I of ~6%, while a DGAD with 240 g/wk of salmon and albacore tuna increased the OM3I. Body fat distribution and basal omega-3 status are primary factors influencing the OM3I response to dietary intake in overweight/obese women.
Keywords: Dietary Guidelines for Americans; dietary intervention; fish; omega-3 fatty acids; omega-3 index; omega-3 response; overweight women; typical American diet.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Copyright © 2022 Richardson, Krishnan, Gray, Keim and Newman.
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References
- Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, et al. . Heart disease and stroke statistics−2011 update: a report from the American Heart Association. Circulation. (2011) 123:e18–209. 10.1161/CIR.0b013e3182009701
- Khan SU, Lone AN, Khan MS, Virani SS, Blumenthal RS, Nasir K, et al. . Effect of omega-3 fatty acids on cardiovascular outcomes: a systematic review and meta-analysis. EClinicalMedicine. (2021) 38:100997. 10.1016/j.eclinm.2021.100997
- Caslake MJ, Miles EA, Kofler BM, Lietz G, Curtis P, Armah CK, et al. . Effect of sex and genotype on cardiovascular biomarker response to fish oils: the FINGEN study. Am J Clin Nutr. (2008) 88:618–29. 10.1093/ajcn/88.3.618
- Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA. (2006) 296:1885–99. 10.1001/jama.296.15.1885
- Bernasconi AA, Lavie CJ, Milani RV, Laukkanen JA. Omega-3 benefits remain strong post-STRENGTH. Mayo Clin Proc. (2021) 96:1371–2. 10.1016/j.mayocp.2021.03.004
- Rimm EB, Appel LJ, Chiuve SE, Djoussé L, Engler MB, Kris-Etherton PM, et al. . Seafood long-chain n-3 polyunsaturated fatty acids and cardiovascular disease: a science advisory from the American Heart Association. Circulation. (2018) 138:e35–47. 10.1161/CIR.0000000000000574
- Singer P, Richter V, Singer K, Lohlein I. Analyses and declarations of omega-3 fatty acids in canned seafood may help to quantify their dietary intake. Nutrients. (2021) 13:2970. 10.3390/nu13092970
- Keenan AH, Pedersen TL, Fillaus K, Larson MK, Shearer GC, Newman JW. Basal omega-3 fatty acid status affects fatty acid and oxylipin responses to high-dose n3-HUFA in healthy volunteers. J Lipid Res. (2012) 53:1662–9. 10.1194/jlr.P025577
- Flock MR, Skulas-Ray AC, Harris WS, Etherton TD, Fleming JA, Kris-Etherton PM. Determinants of erythrocyte omega-3 fatty acid content in response to fish oil supplementation: a dose-response randomized controlled trial. J Am Heart Assoc. (2013) 2:e000513. 10.1161/JAHA.113.000513
- Sarter B, Kelsey KS, Schwartz TA, Harris WS. Blood docosahexaenoic acid and eicosapentaenoic acid in vegans: associations with age and gender and effects of an algal-derived omega-3 fatty acid supplement. Clin Nutr. (2015) 34:212–8. 10.1016/j.clnu.2014.03.003
- Minihane AM. Impact of Genotype on EPA and DHA status and responsiveness to increased intakes. Nutrients. (2016) 8:123. 10.3390/nu8030123
- Harris WS, Del Gobbo L, Tintle NL. The Omega-3 Index and relative risk for coronary heart disease mortality: estimation from 10 cohort studies. Atherosclerosis. (2017) 262:51–4. 10.1016/j.atherosclerosis.2017.05.007
- Walker RE, Jackson KH, Tintle NL, Shearer GC, Bernasconi A, Masson S, et al. . Predicting the effects of supplemental EPA and DHA on the omega-3 index. Am J Clin Nutr. (2019) 110:1034–40. 10.1093/ajcn/nqz161
- Zhang Z, Fulgoni VL, Kris-Etherton PM, Mitmesser SH. Dietary intakes of EPA and DHA omega-3 fatty acids among us childbearing-age and pregnant women: an analysis of NHANES 2001-2014. Nutrients. (2018) 10:416. 10.3390/nu10040416
- Dougherty RM, Galli C, Ferro-Luzzi A, Iacono JM. Lipid and phospholipid fatty acid composition of plasma, red blood cells, and platelets and how they are affected by dietary lipids: a study of normal subjects from Italy, Finland, and the USA. Am J Clin Nutr. (1987) 45:443–55. 10.1093/ajcn/45.2.443
- Franco RS. Measurement of red cell lifespan and aging. Transfus Med Hemother. (2012) 39:302–7. 10.1159/000342232
- Harris WS, Von Schacky C. The Omega-3 Index: a new risk factor for death from coronary heart disease? Prev Med. (2004) 39:212–20. 10.1016/j.ypmed.2004.02.030
- Grenon SM, Conte MS, Nosova E, Alley H, Chong K, Harris WS, et al. . Association between n-3 polyunsaturated fatty acid content of red blood cells and inflammatory biomarkers in patients with peripheral artery disease. J Vasc Surg. (2013) 58:1283–90. 10.1016/j.jvs.2013.05.024
- Mcburney MI, Tintle NL, Harris WS. Omega-3 index is directly associated with a healthy red blood cell distribution width. Prostaglandins Leukot Essent Fatty Acids. (2021) 176:102376. 10.1101/2021.10.22.21264652
- Von Schacky C. Omega-3 index and cardiovascular health. Nutrients. (2014) 6:799–814. 10.3390/nu6020799
- Krishnan S, Adams SH, Allen LH, Laugero KD, Newman JW, Stephensen CB, et al. . A randomized controlled-feeding trial based on the Dietary Guidelines for Americans on cardiometabolic health indexes. Am J Clin Nutr. (2018) 108:266–78. 10.1093/ajcn/nqy113
- Krishnan S, Lee F, Burnett DJ, Kan A, Bonnel EL, Allen LH, et al. . Challenges in designing and delivering diets and assessing adherence: a randomized controlled trial evaluating the 2010 dietary guidelines for Americans. Curr Dev Nutr. (2020) 4:nzaa022. 10.1093/cdn/nzaa022
- Grapov D, Adams SH, Pedersen TL, Garvey WT, Newman JW. Type 2 diabetes associated changes in the plasma non-esterified fatty acids, oxylipins and endocannabinoids. PLoS ONE. (2012) 7:e48852. 10.1371/journal.pone.0048852
- Tepaamorndech S, Kirschke CP, Pedersen TL, Keyes WR, Newman JW, Huang L. Zinc transporter 7 deficiency affects lipid synthesis in adipocytes by inhibiting insulin-dependent Akt activation and glucose uptake. FEBS J. (2016) 283:378–94. 10.1111/febs.13582
- Lemaitre RN, King IB, Sotoodehnia N, Rea TD, Raghunathan TE, Rice KM, et al. . Red blood cell membrane alpha-linolenic acid and the risk of sudden cardiac arrest. Metabolism. (2009) 58:534–40. 10.1016/j.metabol.2008.11.013
- Vannice G, Rasmussen H. Position of the academy of nutrition and dietetics: dietary fatty acids for healthy adults. J Acad Nutr Diet. (2014) 114:136–53. 10.1016/j.jand.2013.11.001
- Gonzalez-Acevedo O, Hernandez-Sierra JF, Salazar-Martinez A, Mandeville PB, Valadez-Castillo FJ, De La Cruz-Mendoza E, et al. . [Effect of Omega 3 fatty acids on body female obese composition]. Arch Latinoam Nutr. (2013) 63:224–31.
- Kang SM, Yoon JW, Ahn HY, Kim SY, Lee KH, Shin H, et al. . Android fat depot is more closely associated with metabolic syndrome than abdominal visceral fat in elderly people. PLoS ONE. (2011) 6:e27694. 10.1371/journal.pone.0027694
- Bouchi R, Fukuda T, Takeuchi T, Nakano Y, Murakami M, Minami I, et al. . Gender difference in the impact of gynoid and android fat masses on the progression of hepatic steatosis in Japanese patients with type 2 diabetes. BMC Obes. (2017) 4:27. 10.1186/s40608-017-0163-3
- Alferink LJM, Trajanoska K, Erler NS, Schoufour JD, De Knegt RJ, Ikram MA, et al. . Nonalcoholic fatty liver disease in the rotterdam study: about muscle mass, sarcopenia, fat mass, and fat distribution. J Bone Miner Res. (2019) 34:1254–63. 10.1002/jbmr.3713
- Sari CI, Eikelis N, Head GA, Schlaich M, Meikle P, Lambert G, et al. . Android Fat deposition and its association with cardiovascular risk factors in overweight young males. Front Physiol. (2019) 10:1162. 10.3389/fphys.2019.01162
- Block RC, Harris WS, Pottala JV. Determinants of blood cell omega-3 fatty acid content. Open Biomark J. (2008) 1:1–6. 10.2174/1875318300801010001
- Garneau V, Rudkowska I, Paradis AM, Godin G, Julien P, Perusse L, et al. . Omega-3 fatty acids status in human subjects estimated using a food frequency questionnaire and plasma phospholipids levels. Nutr J. (2012) 11:46. 10.1186/1475-2891-11-46
- Zhang AC, Downie LE. Preliminary validation of a food frequency questionnaire to assess long-chain omega-3 fatty acid intake in eye care practice. Nutrients. (2019) 11:E817. 10.3390/nu11040817
- Ritz PP, Rogers MB, Zabinsky JS, Hedrick VE, Rockwell JA, Rimer EG, et al. . Dietary and biological assessment of the omega-3 status of collegiate athletes: a cross-sectional analysis. PLoS ONE. (2020) 15:e0228834. 10.1371/journal.pone.0228834
- Li YH, Sun TY, Wu YY, Li CF, Ling CY, Zeng FF, et al. . Higher erythrocyte n-3 polyunsaturated fatty acid were associated with a better profile of DXA-derived body fat and fat distribution in adults. Int J Obes. (2020) 44:1884–92. 10.1038/s41366-020-0569-8
- Muka T, Blekkenhorst LC, Lewis JR, Prince RL, Erler NS, Hofman A, et al. . Dietary fat composition, total body fat and regional body fat distribution in two Caucasian populations of middle-aged and older adult women. Clin Nutr. (2017) 36:1411–9. 10.1016/j.clnu.2016.09.018
- Richardson CE, Krishnan S, Gray IJ, Keim NL, Newman JW. An 8 week randomized DGA-based diet intervention improves the omega-3 index of healthy subjects. medRxiv. (2021). 10.1101/2021.09.22.21263899
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