European Journal of Nutrition

, Volume 55, Issue 2, pp 699–711 | Cite as

Low-level mercury, omega-3 index and neurobehavioral outcomes in an adult US coastal population

  • Caterina Vacchi-Suzzi
  • Roxanne Karimi
  • Danielle Kruse
  • Susan M. Silbernagel
  • Keith E. Levine
  • Diane S. Rohlman
  • Jaymie R. Meliker
Original Contribution
  • 316 Downloads

Abstract

Background

Neurodevelopmental effects of omega-3 fatty acids and mercury from fish consumption have been characterized in children. In contrast, neurobehavioral outcomes associated with fish are not well studied in adults.

Objective

This study of avid seafood consumers on Long Island (NY, USA) sought to define associations between mercury, seafood consumption, omega-3 fatty acids and neurobehavioral outcomes.

Methods

A computer-based test system was used to assess neurobehavioral function. Blood total Hg (Hg) and omega-3 index were measured in 199 adult avid seafood eaters, who also completed the neurobehavioral assessment and an extensive food and fish frequency and demographic questionnaire.

Results

For most of the outcomes considered, neither Hg nor omega-3 index was associated with neurobehavioral outcomes after adjustment for key confounding variables. Fish consumption, however, was associated with decreased odds of both self-reported fatigue (OR 0.85; 95 % CI 0.72, 1.01) and a constellation of neurologic symptoms (OR 0.79; 95 % CI 0.66, 0.96).

Conclusions

Results from our study provide little evidence that omega-3 fatty acids or Hg is associated with cognitive function in adult avid seafood consumers. Larger studies are needed to confirm our finding of associations between fish consumption and decreased self-reported fatigue and neurologic impairment.

Keywords

Mercury Omega-3 n-3 fatty acids Methylmercury Neurological test Neurobehavioral test 

Notes

Acknowledgments

We wish to thank the participants and research support staff of the Long Island Seafood Study of avid seafood consumers, including the Clinical Research Core at Stony Brook Medical Center, Karen Warren, Anant Kharode, Nikita Timofeev, Jia Juan (Tommy) Chu, Rebecca Monastero, Paige de Rosa and Shivam Kothari. This work was supported by NY Sea Grant # R/SHH-17 and the Gelfond Fund for Mercury Research and Outreach (Stony Brook University, Stony Brook, NY). There was no input from the funding bodies on the content of this work.

Conflict of interest

Oregon Health and Science University (OHSU) and Dr. Rohlman have a significant financial interest in Northwest Education Training and Assessment [or NwETA], a company that may have a commercial interest in the results of this research and technology. This potential individual and institutional conflict of interest has been reviewed and managed by OHSU and the University of Iowa.

Supplementary material

394_2015_890_MOESM1_ESM.docx (35 kb)
Supplementary material 1 (DOCX 35 kb)

References

  1. 1.
    American Heart Association (AMA) (2014) Fish and omega-3 fatty acids. http://www.heart.org/HEARTORG/GettingHealthy/NutritionCenter/HealthyDietGoals/Fish-and-Omega-3-Fatty-Acids_UCM_303248_Article.jsp. Accessed 12 Jan 2014
  2. 2.
    Sinn N, Milte CM, Street SJ, Buckley JD, Coates AM, Petkov J, Howe PR (2012) Effects of n-3 fatty acids, EPA v. DHA, on depressive symptoms, quality of life, memory and executive function in older adults with mild cognitive impairment: a 6-month randomised controlled trial. Br J Nutr 107(11):1682–1693. doi: 10.1017/s0007114511004788 CrossRefGoogle Scholar
  3. 3.
    Abu-Ouf NM, Jan MM (2014) The influence of fish oil on neurological development and function. Can J Neurol Sci 41(1):13–18CrossRefGoogle Scholar
  4. 4.
    Connor WE (2000) Importance of n-3 fatty acids in health and disease. Am J Clin Nutr 71(1 Suppl):171s–175sGoogle Scholar
  5. 5.
    Leckie RL, Manuck SB, Bhattacharjee N, Muldoon MF, Flory JM, Erickson KI (2014) Omega-3 fatty acids moderate effects of physical activity on cognitive function. Neuropsychologia 59:103–111. doi: 10.1016/j.neuropsychologia.2014.04.018 CrossRefGoogle Scholar
  6. 6.
    Strain JJ, Davidson PW, Bonham MP, Duffy EM, Stokes-Riner A, Thurston SW, Wallace JM, Robson PJ, Shamlaye CF, Georger LA, Sloane-Reeves J, Cernichiari E, Canfield RL, Cox C, Huang LS, Janciuras J, Myers GJ, Clarkson TW (2008) Associations of maternal long-chain polyunsaturated fatty acids, methyl mercury, and infant development in the Seychelles Child Development Nutrition Study. Neurotoxicology 29(5):776–782. doi: 10.1016/j.neuro.2008.06.002 CrossRefGoogle Scholar
  7. 7.
    Hooijmans CR, Pasker-de Jong PC, de Vries RB, Ritskes-Hoitinga M (2012) The effects of long-term omega-3 fatty acid supplementation on cognition and Alzheimer’s pathology in animal models of Alzheimer’s disease: a systematic review and meta-analysis. JAD 28(1):191–209. doi: 10.3233/jad-2011-111217 Google Scholar
  8. 8.
    Hashimoto M, Hossain S (2011) Neuroprotective and ameliorative actions of polyunsaturated fatty acids against neuronal diseases: beneficial effect of docosahexaenoic acid on cognitive decline in Alzheimer’s disease. J Pharmacol Sci 116(2):150–162CrossRefGoogle Scholar
  9. 9.
    Karagas MR, Choi AL, Oken E, Horvat M, Schoeny R, Kamai E, Cowell W, Grandjean P, Korrick S (2012) Evidence on the human health effects of low-level methylmercury exposure. Environ Health Perspect 120(6):799–806. doi: 10.1289/ehp.1104494 CrossRefGoogle Scholar
  10. 10.
    Cederholm T, Salem N Jr, Palmblad J (2013) Omega-3 fatty acids in the prevention of cognitive decline in humans. Adv Nutr (Bethesda, MD) 4(6):672–676. doi: 10.3945/an.113.004556 CrossRefGoogle Scholar
  11. 11.
    Mahaffey KR, Sunderland EM, Chan HM, Choi AL, Grandjean P, Marien K, Oken E, Sakamoto M, Schoeny R, Weihe P, Yan CH, Yasutake A (2011) Balancing the benefits of n-3 polyunsaturated fatty acids and the risks of methylmercury exposure from fish consumption. Nutr Rev 69(9):493–508. doi: 10.1111/j.1753-4887.2011.00415.x CrossRefGoogle Scholar
  12. 12.
    Stonehouse W (2014) Does consumption of LC omega-3 PUFA enhance cognitive performance in healthy school-aged children and throughout adulthood? Evidence from clinical trials. Nutrients 6(7):2730–2758. doi: 10.3390/nu6072730 CrossRefGoogle Scholar
  13. 13.
    Brenna JT, Carlson SE (2014) Docosahexaenoic acid and human brain development: evidence that a dietary supply is needed for optimal development. J Hum Evol. doi: 10.1016/j.jhevol.2014.02.017 Google Scholar
  14. 14.
    Boucher O, Burden MJ, Muckle G, Saint-Amour D, Ayotte P, Dewailly E, Nelson CA, Jacobson SW, Jacobson JL (2011) Neurophysiologic and neurobehavioral evidence of beneficial effects of prenatal omega-3 fatty acid intake on memory function at school age. Am J Clin Nutr 93(5):1025–1037. doi: 10.3945/ajcn.110.000323 CrossRefGoogle Scholar
  15. 15.
    Mahmoudi MJ, Hedayat M, Sharifi F, Mirarefin M, Nazari N, Mehrdad N, Ghaderpanahi M, Tajalizadekhoob Y, Badamchizade Z, Larijani B, Alatab S, Alizadeh M, Arzaghi SM, Najafi B, Fakhrzadeh H (2014) Effect of low dose omega-3 poly unsaturated fatty acids on cognitive status among older people: a double-blind randomized placebo-controlled study. J Diabetes Metab Disord 13(1):34. doi: 10.1186/2251-6581-13-34 CrossRefGoogle Scholar
  16. 16.
    Hibbeln JR, Gow RV (2014) The potential for military diets to reduce depression, suicide, and impulsive aggression: a review of current evidence for omega-3 and omega-6 fatty acids. Mil Med 179(11 Suppl):117–128. doi: 10.7205/milmed-d-14-00153 CrossRefGoogle Scholar
  17. 17.
    Muldoon MF, Ryan CM, Sheu L, Yao JK, Conklin SM, Manuck SB (2010) Serum phospholipid docosahexaenonic acid is associated with cognitive functioning during middle adulthood. J Nutr 140(4):848–853. doi: 10.3945/jn.109.119578 CrossRefGoogle Scholar
  18. 18.
    Danthiir V, Hosking D, Burns NR, Wilson C, Nettelbeck T, Calvaresi E, Clifton P, Wittert GA (2014) Cognitive performance in older adults is inversely associated with fish consumption but not erythrocyte membrane n-3 fatty acids. J Nutr 144(3):311–320. doi: 10.3945/jn.113.175695 CrossRefGoogle Scholar
  19. 19.
    van Gelder BM, Tijhuis M, Kalmijn S, Kromhout D (2007) Fish consumption, n-3 fatty acids, and subsequent 5-y cognitive decline in elderly men: the Zutphen Elderly Study. Am J Clin Nutr 85(4):1142–1147Google Scholar
  20. 20.
    Hashimoto M, Maekawa M, Katakura M, Hamazaki K, Matsuoka Y (2014) Possibility of polyunsaturated fatty acids for the prevention and treatment of neuropsychiatric illnesses. J Pharmacol Sci 124(3):294–300CrossRefGoogle Scholar
  21. 21.
    von Schacky C, Harris WS (2007) Cardiovascular risk and the omega-3 index. J Cardiovasc Med (Hagerstown, MD) 8(Suppl 1):S46–S49. doi: 10.2459/01.jcm.0000289273.87803.87 CrossRefGoogle Scholar
  22. 22.
    Johnston DT, Deuster PA, Harris WS, Macrae H, Dretsch MN (2013) Red blood cell omega-3 fatty acid levels and neurocognitive performance in deployed U.S. Servicemembers. Nutr Neurosci 16(1):30–38. doi: 10.1179/1476830512y.0000000025 CrossRefGoogle Scholar
  23. 23.
    Rice KM, Walker EM Jr, Wu M, Gillette C, Blough ER (2014) Environmental mercury and its toxic effects. J Prev Med Public Health 47(2):74–83. doi: 10.3961/jpmph.2014.47.2.74 CrossRefGoogle Scholar
  24. 24.
    Ekino S, Susa M, Ninomiya T, Imamura K, Kitamura T (2007) Minamata disease revisited: an update on the acute and chronic manifestations of methyl mercury poisoning. J Neurol Sci 262(1–2):131–144. doi: 10.1016/j.jns.2007.06.036 CrossRefGoogle Scholar
  25. 25.
    Castoldi AF, Coccini T, Ceccatelli S, Manzo L (2001) Neurotoxicity and molecular effects of methylmercury. Brain Res Bull 55(2):197–203CrossRefGoogle Scholar
  26. 26.
    Harada M (1995) Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol 25(1):1–24. doi: 10.3109/10408449509089885 CrossRefGoogle Scholar
  27. 27.
    Bakir F, Damluji SF, Amin-Zaki L, Murtadha M, Khalidi A, Al-Rawi NY, Tikriti S, Dahahir HI, Clarkson TW, Smith JC, Doherty RA (1973) Methylmercury poisoning in Iraq. Science 181(4096):230–241CrossRefGoogle Scholar
  28. 28.
    Counter SA, Buchanan LH (2004) Mercury exposure in children: a review. Toxicol Appl Pharmacol 198(2):209–230. doi: 10.1016/j.taap.2003.11.032 CrossRefGoogle Scholar
  29. 29.
    Grandjean P, Weihe P, White RF, Debes F, Araki S, Yokoyama K, Murata K, Sorensen N, Dahl R, Jorgensen PJ (1997) Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol Teratol 19(6):417–428CrossRefGoogle Scholar
  30. 30.
    Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182CrossRefGoogle Scholar
  31. 31.
    Kim RB, Kim BG, Kim YM, Hong YS, You CH, Kim DS (2013) Association between low-level mercury exposure and neurobehavioral functions in Korean adults living in a coastal city. Environ Health Toxicol 28:e2013015. doi: 10.5620/eht.2013.28.e2013015 CrossRefGoogle Scholar
  32. 32.
    Weil M, Bressler J, Parsons P, Bolla K, Glass T, Schwartz B (2005) Blood mercury levels and neurobehavioral function. JAMA 293(15):1875–1882. doi: 10.1001/jama.293.15.1875 CrossRefGoogle Scholar
  33. 33.
    Carta P, Flore C, Alinovi R, Ibba A, Tocco MG, Aru G, Carta R, Girei E, Mutti A, Lucchini R, Randaccio FS (2003) Sub-clinical neurobehavioral abnormalities associated with low level of mercury exposure through fish consumption. Neurotoxicology 24(4–5):617–623. doi: 10.1016/s0161-813x(03)00080-9 CrossRefGoogle Scholar
  34. 34.
    Masley SC, Masley LV, Gualtieri CT (2012) Effect of mercury levels and seafood intake on cognitive function in middle-aged adults. Integr Med 11(3):32–39Google Scholar
  35. 35.
    Yokoo EM, Valente JG, Grattan L, Schmidt SL, Platt I, Silbergeld EK (2003) Low level methylmercury exposure affects neuropsychological function in adults. Environ Health Glob Access Sci Source 2(1):8. doi: 10.1186/1476-069x-2-8 Google Scholar
  36. 36.
    Dolbec J, Mergler D, Sousa Passos CJ, Sousa de Morais S, Lebel J (2000) Methylmercury exposure affects motor performance of a riverine population of the Tapajos river, Brazilian Amazon. Int Arch Occup Environ Health 73(3):195–203CrossRefGoogle Scholar
  37. 37.
    Lebel J, Mergler D, Branches F, Lucotte M, Amorim M, Larribe F, Dolbec J (1998) Neurotoxic effects of low-level methylmercury contamination in the Amazonian Basin. Environ Res 79(1):20–32. doi: 10.1006/enrs.1998.3846 CrossRefGoogle Scholar
  38. 38.
    Choi AL, Mogensen UB, Bjerve KS, Debes F, Weihe P, Grandjean P, Budtz-Jorgensen E (2014) Negative confounding by essential fatty acids in methylmercury neurotoxicity associations. Neurotoxicol Teratol 42:85–92. doi: 10.1016/j.ntt.2014.02.003 CrossRefGoogle Scholar
  39. 39.
    Lynch ML, Huang LS, Cox C, Strain JJ, Myers GJ, Bonham MP, Shamlaye CF, Stokes-Riner A, Wallace JM, Duffy EM, Clarkson TW, Davidson PW (2011) Varying coefficient function models to explore interactions between maternal nutritional status and prenatal methylmercury toxicity in the Seychelles Child Development Nutrition Study. Environ Res 111(1):75–80. doi: 10.1016/j.envres.2010.09.005 CrossRefGoogle Scholar
  40. 40.
    Rohlman DS, Gimenes LS, Eckerman DA, Kang SK, Farahat FM, Anger WK (2003) Development of the Behavioral Assessment and Research System (BARS) to detect and characterize neurotoxicity in humans. Neurotoxicology 24(4–5):523–531CrossRefGoogle Scholar
  41. 41.
    Block G, Hartman AM, Naughton D (1990) A reduced dietary questionnaire: development and validation. Epidemiology (Cambridge, MA) 1(1):58–64CrossRefGoogle Scholar
  42. 42.
    Karimi R, Silbernagel S, Fisher NS, Meliker JR (2014) Elevated blood Hg at recommended seafood consumption rates in adult seafood consumers. Int J Hyg Environ Health. doi: 10.1016/j.ijheh.2014.03.007 Google Scholar
  43. 43.
    Karimi R, Fisher NS, Meliker JR (2014) Mercury–nutrient signatures in seafood and in the blood of avid seafood consumers. Sci Total Environ 496:636–643. doi: 10.1016/j.scitotenv.2014.04.049 CrossRefGoogle Scholar
  44. 44.
    Karimi R, Silbernagel S, Fisher NS, Meliker JR (2014) Elevated blood Hg at recommended seafood consumption rates in adult seafood consumers. Int J Hyg Environ Health 217(7):758–764. doi: 10.1016/j.ijheh.2014.03.007 CrossRefGoogle Scholar
  45. 45.
    Smiciklas-Wright H, Mitchell DC, Mickle SJ, Cook AJ, Goldman JD, United States Department of Agriculture, Agricultural Research Service (2002) Foods commonly eaten in the United States, quantities consumed per eating occasion and in a day in 1994–96Google Scholar
  46. 46.
    Food and Drug Administration (FDA) (2004) What you need to know about mercury in fish and shellfish. http://www.fda.gov/food/resourcesforyou/consumers/ucm110591.htm. Accessed 26 March 2015
  47. 47.
    Rodriguez-Barranco M, Lacasana M, Gil F, Lorca A, Alguacil J, Rohlman DS, Gonzalez-Alzaga B, Molina-Villalba I, Mendoza R, Aguilar-Garduno C (2014) Cadmium exposure and neuropsychological development in school children in southwestern Spain. Environ Res 134c:66–73. doi: 10.1016/j.envres.2014.06.026 CrossRefGoogle Scholar
  48. 48.
    Echeverria D, Woods JS, Heyer NJ, Martin MD, Rohlman DS, Farin FM, Li T (2010) The association between serotonin transporter gene promotor polymorphism (5-HTTLPR) and elemental mercury exposure on mood and behavior in humans. J Toxicol Environ Health Part A 73(15):1003–1020. doi: 10.1080/15287390903566591 CrossRefGoogle Scholar
  49. 49.
    Rohlman DS, Arcury TA, Quandt SA, Lasarev M, Rothlein J, Travers R, Tamulinas A, Scherer J, Early J, Marin A, Phillips J, McCauley L (2005) Neurobehavioral performance in preschool children from agricultural and non-agricultural communities in Oregon and North Carolina. Neurotoxicology 26(4):589–598. doi: 10.1016/j.neuro.2004.12.002 CrossRefGoogle Scholar
  50. 50.
    Rohlman DS, Ismail AA, Abdel-Rasoul G, Lasarev M, Hendy O, Olson JR (2014) Characterizing exposures and neurobehavioral performance in Egyptian adolescent pesticide applicators. Metab Brain Dis 29(3):845–855. doi: 10.1007/s11011-014-9565-9 CrossRefGoogle Scholar
  51. 51.
    Echeverria D, Heyer NJ, Martin MD, Naleway CA, Woods JS, Bittner AC Jr (1995) Behavioral effects of low-level exposure to elemental Hg among dentists. Neurotoxicol Teratol 17(2):161–168CrossRefGoogle Scholar
  52. 52.
    Echeverria D, Woods JS, Heyer NJ, Rohlman D, Farin FM, Li T, Garabedian CE (2006) The association between a genetic polymorphism of coproporphyrinogen oxidase, dental mercury exposure and neurobehavioral response in humans. Neurotoxicol Teratol 28(1):39–48. doi: 10.1016/j.ntt.2005.10.006 CrossRefGoogle Scholar
  53. 53.
    Echeverria D, Woods JS, Heyer NJ, Rohlman DS, Farin FM, Bittner AC Jr, Li T, Garabedian C (2005) Chronic low-level mercury exposure, BDNF polymorphism, and associations with cognitive and motor function. Neurotoxicol Teratol 27(6):781–796. doi: 10.1016/j.ntt.2005.08.001 CrossRefGoogle Scholar
  54. 54.
    Heyer NJ, Bittner AC, Echeverria D, Woods JS (2007) Reply to the Letter to the Editor: Response to comment on: “A cascade analysis of the interaction of mercury and coproporphyrinogen oxidase (CPOX) polymorphism on the heme biosynthetic pathway and porphyrin production” by Heyer et al. [Toxicol. Lett. 1612006 159–166]. Toxicol Lett 169(1):93–94. doi: 10.1016/j.toxlet.2006.11.011 CrossRefGoogle Scholar
  55. 55.
    Heyer NJ, Bittner AC Jr, Echeverria D, Woods JS (2006) A cascade analysis of the interaction of mercury and coproporphyrinogen oxidase (CPOX) polymorphism on the heme biosynthetic pathway and porphyrin production. Toxicol Lett 161(2):159–166. doi: 10.1016/j.toxlet.2005.09.005 CrossRefGoogle Scholar
  56. 56.
    Heyer NJ, Echeverria D, Bittner AC Jr, Farin FM, Garabedian CC, Woods JS (2004) Chronic low-level mercury exposure, BDNF polymorphism, and associations with self-reported symptoms and mood. Toxicol Sci 81(2):354–363. doi: 10.1093/toxsci/kfh220 CrossRefGoogle Scholar
  57. 57.
    Heyer NJ, Echeverria D, Farin FM, Woods JS (2008) The association between serotonin transporter gene promoter polymorphism (5-HTTLPR), self-reported symptoms, and dental mercury exposure. J Toxicol Environ Health Part A 71(19):1318–1326. doi: 10.1080/15287390802240850 CrossRefGoogle Scholar
  58. 58.
    Heyer NJ, Echeverria D, Martin MD, Farin FM, Woods JS (2009) Catechol O-methyltransferase (COMT) VAL158MET functional polymorphism, dental mercury exposure, and self-reported symptoms and mood. J Toxicol Environ Health Part A 72(9):599–609. doi: 10.1080/15287390802706405 CrossRefGoogle Scholar
  59. 59.
    Ngim CH, Foo SC, Boey KW, Jeyaratnam J (1992) Chronic neurobehavioural effects of elemental mercury in dentists. Br J Ind Med 49(11):782–790Google Scholar
  60. 60.
    de Jager CA, Dye L, de Bruin EA, Butler L, Fletcher J, Lamport DJ, Latulippe ME, Spencer JP, Wesnes K (2014) Criteria for validation and selection of cognitive tests for investigating the effects of foods and nutrients. Nutr Rev 72(3):162–179. doi: 10.1111/nure.12094 CrossRefGoogle Scholar
  61. 61.
    Rohlman DS, Lucchini R, Anger WK, Bellinger DC, van Thriel C (2008) Neurobehavioral testing in human risk assessment. Neurotoxicology 29(3):556–567. doi: 10.1016/j.neuro.2008.04.003 CrossRefGoogle Scholar
  62. 62.
    ATSDR (Agency for Toxic Substances & Disease registry) (1999) Toxicological profile for mercury. http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=115&tid=24
  63. 63.
    Smith JC, Farris FF (1996) Methyl mercury pharmacokinetics in man: a reevaluation. Toxicol Appl Pharmacol 137(2):245–252. doi: 10.1006/taap.1996.0078 CrossRefGoogle Scholar
  64. 64.
    Carrier G, Bouchard M, Brunet RC, Caza M (2001) A toxicokinetic model for predicting the tissue distribution and elimination of organic and inorganic mercury following exposure to methyl mercury in animals and humans. II. Application and validation of the model in humans. Toxicol Appl Pharmacol 171(1):50–60. doi: 10.1006/taap.2000.9113 CrossRefGoogle Scholar
  65. 65.
    Berglund M, Lind B, Bjornberg K, Palm B, Einarsson O, Vahter M (2005) Inter-individual variations of human mercury exposure biomarkers: a cross-sectional assessment. Environ Health 4(1):20CrossRefGoogle Scholar
  66. 66.
    Kingman A, Albertini T, Brown LJ (1998) Mercury concentrations in urine and whole blood associated with amalgam exposure in a US military population. J Dent Res 77(3):461–471CrossRefGoogle Scholar
  67. 67.
    Harris WS (2007) Omega-3 fatty acids and cardiovascular disease: a case for omega-3 index as a new risk factor. Pharmacol Res 55(3):217–223. doi: 10.1016/j.phrs.2007.01.013 CrossRefGoogle Scholar
  68. 68.
    Strain JJ, Davidson PW, Thurston SW, Harrington D, Mulhern MS, McAfee AJ, van Wijngaarden E, Shamlaye CF, Henderson J, Watson GE, Zareba G, Cory-Slechta DA, Lynch M, Wallace JM, McSorley EM, Bonham MP, Stokes-Riner A, Sloane-Reeves J, Janciuras J, Wong R, Clarkson TW, Myers GJ (2012) Maternal PUFA status but not prenatal methylmercury exposure is associated with children’s language functions at age five years in the Seychelles. J Nutr 142(11):1943–1949. doi: 10.3945/jn.112.163493 CrossRefGoogle Scholar
  69. 69.
    Phelps RW, Clarkson TW, Kershaw TG, Wheatley B (1980) Interrelationships of blood and hair mercury concentrations in a North American population exposed to methylmercury. Arch Environ Health 35(3):161–168CrossRefGoogle Scholar
  70. 70.
    Yurko-Mauro K, McCarthy D, Rom D, Nelson EB, Ryan AS, Blackwell A, Salem N Jr, Stedman M (2010) Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline. Alzheimer’s Dement J Alzheimer’s Assoc 6(6):456–464. doi: 10.1016/j.jalz.2010.01.013 CrossRefGoogle Scholar
  71. 71.
    Kalmijn S, van Boxtel MP, Ocke M, Verschuren WM, Kromhout D, Launer LJ (2004) Dietary intake of fatty acids and fish in relation to cognitive performance at middle age. Neurology 62(2):275–280CrossRefGoogle Scholar
  72. 72.
    Rice DC (2008) Overview of modifiers of methylmercury neurotoxicity: chemicals, nutrients, and the social environment. Neurotoxicology 29(5):761–766. doi: 10.1016/j.neuro.2008.07.004 CrossRefGoogle Scholar
  73. 73.
    Sydenham E, Dangour AD, Lim WS (2012) Omega 3 fatty acid for the prevention of cognitive decline and dementia. Cochrane Database Syst Rev 6:Cd005379. doi: 10.1002/14651858.CD005379.pub3 Google Scholar
  74. 74.
    Clarkson TW, Strain JJ (2003) Nutritional factors may modify the toxic action of methyl mercury in fish-eating populations. J Nutr 133(5 Suppl 1):1539s–1543sGoogle Scholar
  75. 75.
    Morris M, Evans DA, Tangney CC, Bienias JL, Wilson RS (2005) Fish consumption and cognitive decline with age in a large community study. Arch Neurol 62(12):1849–1853. doi: 10.1001/archneur.62.12.noc50161 CrossRefGoogle Scholar
  76. 76.
    Dangour AD, Allen E, Elbourne D, Fletcher A, Richards M, Uauy R (2009) Fish consumption and cognitive function among older people in the UK: baseline data from the OPAL study. J Nutr Health Aging 13(3):198–202. doi: 10.1007/s12603-009-0057-2 CrossRefGoogle Scholar
  77. 77.
    Beck AT, Steer RA, Carbin MG (1988) Psychometric properties of the beck depression inventory: twenty-five years of evaluation. Clin Psychol Rev 8(1):77–100. doi: 10.1016/0272-7358(88)90050-5 CrossRefGoogle Scholar
  78. 78.
    Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389CrossRefGoogle Scholar
  79. 79.
    Serra-Majem L, Nissensohn M, Overby NC, Fekete K (2012) Dietary methods and biomarkers of omega 3 fatty acids: a systematic review. Br J Nutr 107(Suppl 2):S64–S76. doi: 10.1017/s000711451200147x CrossRefGoogle Scholar
  80. 80.
    Block RC, Harris WS, Pottala JV (2008) Determinants of blood cell omega-3 fatty acid content. Open Biomark J 1:1–6. doi: 10.2174/1875318300801010001 CrossRefGoogle Scholar
  81. 81.
    Blasbalg TL, Hibbeln JR, Ramsden CE, Majchrzak SF, Rawlings RR (2011) Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr 93(5):950–962. doi: 10.3945/ajcn.110.006643 CrossRefGoogle Scholar
  82. 82.
    U.S. Environmental Protection Agency (EPA) (2013) Trends in blood mercury concentrations and fish consumption among U.S. women of childbearing age NHANES, 1999–2010. http://water.epa.gov/scitech/swguidance/fishshellfish/fishadvisories/upload/Trends-in-Blood-Mercury-Concentrations-and-Fish-Consumption-Among-U-S-Women-of-Childbearing-Age-NHANES-1999-2010.pdf. Accessed 26 March 2015
  83. 83.
    Laclaustra M, Stranges S, Navas-Acien A, Ordovas JM, Guallar E (2010) Serum selenium and serum lipids in US adults: National Health and Nutrition Examination Survey (NHANES) 2003–2004. Atherosclerosis 210(2):643–648. doi: 10.1016/j.atherosclerosis.2010.01.005 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Caterina Vacchi-Suzzi
    • 1
  • Roxanne Karimi
    • 2
  • Danielle Kruse
    • 7
  • Susan M. Silbernagel
    • 6
  • Keith E. Levine
    • 3
  • Diane S. Rohlman
    • 4
    • 5
  • Jaymie R. Meliker
    • 1
  1. 1.Program in Public Health, Department of Preventive MedicineStony Brook UniversityStony BrookUSA
  2. 2.School of Marine and Atmospheric SciencesStony Brook UniversityStony BrookUSA
  3. 3.Trace Inorganics Department, Technologies for Industry and the EnvironmentRTI InternationalResearch Triangle ParkUSA
  4. 4.Occupational and Environmental HealthUniversity of IowaIowa CityUSA
  5. 5.Oregon Institute for Occupational Health SciencesOregon Health and Science UniversityPortlandUSA
  6. 6.Division of Allergy and Infectious Diseases, Department of MedicineUniversity of WashingtonSeattleUSA
  7. 7.School of MedicineStony Brook UniversityStony BrookUSA

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