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2 REVIEW OF THE LITERATURE

2.5 ANIMAL PROTEIN SOURCES AND COGNITIVE PERFORMANCE

2.5.4 Fish and cognitive performance

intake and education, Requejo et al. (154) for MMSE score and age, and Lee et al. (149) for age. The majority of the studies in Table 18 were adjusted for at least one nutritional factor, which usually was total energy intake or sometimes BMI as a crude indicator of total energy intake. In addition, studies by Jiang et al. (190), Brouwer-Brolsma et al. (167), Qin et al. 2014 (197), and Samieri et al. (193) had more extensive dietary adjustments. As the adjustments are never complete and differences between the studies exists, it may explain some of the variation between the study results.

Of the 45 published studies (Table 18), two studies were systematic reviews or meta-analysis. The systematic review and meta-analysis by Zeng et al. (137) did not find an association between fish intake and cognitive performance, although the meta-analysis was only based on two studies.

In the meta-analysis by Samieri et al. (203), however, higher fish intake was associated with slower decline in certain cognitive domains in the pooled analysis. As far as is known, RCTs have not been published on this topic.

Twenty-one publications were prospective cohort studies (Table 18). Of those, 11 did not find an association between fish intake and cognitive outcomes. Nevertheless, eight studies found an association between higher fish intake and better cognitive performance and one an association between higher fish intake and worse cognitive performance. The latter was found between roasted or baked fish consumption and cognitive performance. In that same study, however, an association between total fish, fried fish, and barbequed or grilled fish and cognitive performance resulted in null findings (191). One of the prospective cohort studies found an association towards both directions: higher fresh fish intake was

associated with lower risk of cognitive impairment, whereas higher preserved fish intake was associated with increased risk of cognitive impairment (190).

Twenty studies used a cross-sectional design (Table 18). Of those, 14 studies did not find an association between fish intake and cognitive performance, five found an association between higher fish intake and better cognitive performance and one found an association between higher fish intake and lower performance in certain cognitive domains.

Two studies used case-control design, of which one ended up with an inverse association and the other with a null finding.

In conclusion, it seems that higher fish intake may not be associated with cognitive performance, or higher fish intake may be associated with better cognitive functioning. The high number of null findings may be explained by multiple reasons, such as the above-mentioned differences in study populations, cognitive assessments, or statistical analyses. It can also be explained by insufficient number of participants in the studies. This is supported by a meta-analysis by Samieri et al. (203): None of the original studies in the meta-analysis resulted in a statistically significant finding, but in the pooled analysis of five cohorts and 23 688 participants in total, higher fish intake was associated with slower decline in global cognition and episodic memory. Regardless, more studies with more uniform and more sensitive methods are needed to elucidate the association between fish consumption and cognitive performance.

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Table 18. Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Huang et al. 2021 (150) Cross-sectional study 4309 Chinese men and women, aged ≥55 y

Fish FFQ

MoCAHigher fish intake was associated with lower risk of MCI Nozaki et al. 2021 (134) Prospective cohort study, follow-up of 14 15 y 1127 Japanese men and women, aged 4564 y

Fish, n-3 PUFA rich fish FFQ

MMSE, Wechsler Memory Scale Revised logical memory I/II subtest, clock drawing test, Clinical Dementia Rating Scale

No association Zhang et al. 2021 (191) Prospective cohort study, follow-up of 10 15 y 503 UK women, aged 52 ± 9.4 y

Total fish, roasted/baked fish, fried fish, barbequed/grilled fish FFQ

Online reaction time ability tests Roasted/baked fish consumption was associated with slower simple reaction time Zhang et al. 2021 (157) Prospective cohort study, follow-up of 6 y 3029 Chinese men and women, aged ≥65 y

Fish FFQ

MMSE No association Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Zupo et al. 2021 (153) Cross-sectional study 584 Italian men and women, aged 6080 y

Fish, seafood/ shellfish FFQ

MMSE No association Fieldhouse et al. 2020 (199) Cross-sectional study 357 Dutch men and women, aged 65 ± 8.3 y

Fish FFQ

Visual Association Test, Rey Auditory Verbal Learning Task, animal naming, dot counting, fragmented letters, number location, TMT A, Stroop test, letter fluency

No association Jiang et al. 2020 (190) Prospective cohort study, follow-up of 20 y 16 948 Chinese men and women, aged 4574 y

Fish/shellfish, fresh fish/shellfish, preserved fish/shellfish FFQ

MMSE Higher fresh fish intake associated with lower risk of cognitive impairment. Higher preserved fish intake associated with higher risk of cognitive impairment Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Qiu et al. 2020 (201) Prospective cohort study, follow-up of 12 y 3859 Chinese men and women, aged 62108 y Fish Survey of health-related behavior, inc. fish intake

MMSE Fish intake was associated with better cognitive function in cognitively stable group Xu et al. 2020 (148) Cross-sectional study 1262 Chinese men and women, aged ≥65 y

Fish/shellfish FFQ

MMSE No association An et al. 2019 (158) Prospective cohort study, follow-up of 14 y 4749 Chinese men and women, aged ≥80 y

Fish FFQ

MMSE No association Chuang et al. 2019 (114) Cross-sectional study 1436 Taiwanese men and women, aged ≥65 y

Fish, deep sea fish, shellfish, seafood FFQ

MMSE No association Mao et al. 2019 (204) Prospective cohort study, follow-up of 25 y 3231 US men and women, aged 1830 y

Non-fried seafood 30-d diet history questionnaire Rey Auditory Verbal Learning Test, Digit Symbol Substitution Test, Stroop test Higher non-fried seafood intake was associated with better cognitive performance Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Brouwer- Brolsma et al. 2018 (167) Cross-sectional study 1607 Dutch men and women, aged 2070 y

Fish and seafood FFQ

Letter Fluency Test, Symbol Digit Modalities Test, Story Recall Test

No association Fischer et al. 2018 (128) Prospective cohort study, follow-up of 10 y 2622 German men and women, aged ≥75 y

Fresh fish FFQ

World List Immediate and Delayed Recall and Recognition

No association Kim et al. 2018 (159) Cross-sectional study 276 Korean men and women, aged ≥50 y

Fish FFQ

MMSE No association Nooyens et al. 2018 (195) Prospective cohort study, follow-up of 5 y 2612 men and women, aged 4370 y

Total fish, lean or moderately fatty fish, shellfish, fatty fish FFQ Verbal Learning Test, Stroop Colour- Word Test, Word Fluency test, Letter Digit Substitution Test

Low fatty fish consumption was associated with slower memory decline compared to non-users Samieri et al. 2018 (203) Meta-analysis 23 688 participants from 5 cohorts

Fish FFQ

Global cognition score, episodic memory score Higher fish intake was associated with slower decline in global cognition and episodic memory Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Zhu et al. 2018 (188) Prospective cohort study, follow-up of 14 y 30484 Chinese men and women, aged 4074 y

Fish FFQ

Evaluation of functional statusHigher fish intake was associated with lower risk of memory and decision-making problems Anastasiou et al. 2017 (120)

Cross-sectional study 1865 Greek men and women, aged 73 ± 6 y

Fish FFQ

e.g., MMSE, TMT, Clock Drawing Test, Motor Programming, Complex Figure Test, Anomalous Sentence Repetition, verbal tests, orientation tests

No association Araki et al. 2017 (160) Prospective cohort study, follow-up of 6 y 237 Japanese men and women, aged 65 y

Fish FFQ

MMSE No association Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings van de Rest et al. 2016 (200)

Prospective cohort study, follow-up of 4.9 y 915 US men and women, aged 81.4 ± 7.2 y

Seafood FFQ

19 cognitive tests assessing episodic memory, semantic memory, working memory, perceptual speed, and visuospatial ability

Seafood intake was associated with slower decline in semantic memory and perceptual speed Zeng et al. 2017 (137) Systematic review and meta-analysis 2 studies for the meta- analysis

Fish No association Del Brutto et al. 2016 (205) Cross-sectional study 307 Ecuadorian men and women, aged ≥60 y

Oily fish Survey

MoCAHigher oily fish intake was associated with better cognitive performance Dong et al. 2016 (161) Cross-sectional study 894 Chinese men and women, aged ≥50 y

Fish FFQ

MoCANo association França et al. 2016 (194) Cross-sectional study 1197 Brazilian men and women, aged ≥60 y

Fish FFQ

MMSE No association Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Trichopoulou et al. 2015 (170) Prospective cohort study, follow-up of 7 y 401 Greek men and women, aged ≥60 y

Fish FFQ

MMSE No association Zhao et al. 2015 (147) Case-control study 404 Chinese men and women, aged ≥60 y

Marine products FFQ

MoCAHigher intake of marine products was associated with lower risk of MCI Bajerska et al. 2014 (176) Cross-sectional study 87 Polish men and women, aged ≥60 y

Fish FFQ

e.g., MMSE, TMT, Stroop test, memory tests, Spatial Span test, Rapid Visual Information Processing test, Paired Associates Learning test

Fish intake was associated with better cognitive performance Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Danthiir et al. 2014 (196) Cross-sectional study 390 Australian men and women, aged 6591 y Total fish, oily fish, white fish FFQ

Tests of reasoning, working/short-term memory, retrieval fluency, perceptual speed, reaction time, speed of memory-scanning and reasoning, inhibition, psychomotor speed

Higher total fish, oily fish or white fish intake was associated with worse cognitive performance in some cognitive domains Kesse-Guyot et al. 2014 (202)

Prospective cohort study, follow-up of 13 y 2430 French men and women, aged 65.6 ± 4.5 y at the end of follow-up Fish or seafood Questionnaire Forward and backward digit span test, TMT, cued recall test, verbal fluency tasks

No association Qin et al. 2014 (197) Prospective cohort study, follow-up of 5.3 y 1566 Chinese men and women, aged ≥55 y

Fish and shellfish (fresh and preserved), fresh fish 3-d 24-h dietary recall Immediate and delayed recall, counting backward from 20, serial 7 subtraction, orientation Higher fish intake was associated with lower rate of cognitive decline among≥65 y participants Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Crichton et al. 2013 (177) Cross-sectional study 1183 Australian men and women, aged 4065

Fish FFQ

Cognitive failures questionnaire, Memory Functioning Questionnaire

No association Katsiardanis et al. 2013 (183)

Cross-sectional study 557 Greek men and women, aged ≥65 y Fish and shellfish FFQ

MMSE No association Kim et al. 2013 (198) Prospective cohort study, follow-up of 5.6 y 5988 US women, aged ≥45 y

Total seafood, tuna and other dark-meat fish, light-meat fish, shellfish FFQ Telephone Interview for Cognitive Status, MMSE, immediate and delayed recall tests, category fluency

Higher tuna and dark-meat fish intake were associated with lower verbal memory decline Samieri et al. 2013 (193) Prospective cohort study, follow-up of over 4 y 6174 US women, aged ≥65 y

Fish, shrimp FFQ

Telephone Interview for Cognitive Status, immediate and delayed recall tests, category fluency

No association Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Titova et al. 2013 (174) Prospective cohort study, follow-up of 5 y 194 Swedish men and women, aged 70 y

Fish 7-d food diary

Seven-minute screeningNo association Wengreen et al. 2013 (175) Prospective cohort study, follow-up of 11 y 3580 US men and women, aged ≥65 y

Fish FFQ

MMSE No association Chen et al. 2012 (155) Population-based, prospective nested case-control study 5691 Chinese men and women, aged ≥65 y

Fish FFQ

MMSE No association Aparicio Vizuete et al. 2010 (146)

Cross-sectional study 178 Spanish men and women, aged ≥65 y Fish 7-d food record, weighing Short Portable Mental Status Questionnaire

Fish intake was associated with better cognitive performance Wang et al. 2010 (156) Cross-sectional study 364 Chinese men and women, aged ≥90 y

Fish and shrimp FFQ

MMSE No association Table 18 continues

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Table 18. (continued) Summary of the studies on the associations of fish with cognitive performance. ReferenceStudy design Study populationExposure Exposure assessment Outcome assessment Main findings Vercambre et al. 2009 (152) Prospective cohort study, follow-up of 13 y 4758 French women, aged 65.5 ± 1.8 y

Fish Diet history questionnaire

Instrumental activities of daily living, observed cognitive deterioration

Lower fish intake was associated with cognitive decline Rahman et al. 2007 (179) Cross-sectional study 1056 US men and women, aged 5594 y

Fish FFQ

Mental Status QuestionnaireNo association Almeida et al. 2006 (184) Prospective cohort study, follow-up of 4.8 y 601 Australian men, aged ≥65 y

Fish Self-report questionnaire

MMSE, Geriatric Depression ScaleNo association Requejo et al. 2003 (154) Cross-sectional study 168 Spanish men and women, aged ≥65 y

Fish 7-d food record, weighing

MMSE Higher fish intake was associated with better cognitive performance Lee et al. 2001 (149) Cross-sectional study 449 Korean men and women, aged ≥60 y

Seafood 24-h dietary recall

MMSE No association FFQ, food frequency questionnaire; MCI, mild cognitive impairment; MoCA, Montreal Cognitive Assessment; MMSE, Mini Mental State Examination; PUFA, polyunsaturated fatty acid; TMT A; Trail Making Test, Part A; UK, the United Kingdom; US, the United States

2.6 APOE, DIETARY CHOLESTEROL AND CHOLINE INTAKE AND