Fish consumption in multiple health outcomes: an umbrella review of meta-analyses of observational and clinical studies
Original Article

Fish consumption in multiple health outcomes: an umbrella review of meta-analyses of observational and clinical studies

Hailiang Zhao1,2#, Min Wang1#, Xiaojuan Peng1,3#, Lu Zhong1#, Xiongxiu Liu1, Ying Shi1, Yuting Li1, Yanfang Chen1, Shaohui Tang1

1Department of Gastroenterology, The First Affiliated Hospital, Jinan University, Guangzhou, China; 2Department of Gastroenterology, Affiliated Hospital of Youjiang Medical University for Nationalities, Baise, China; 3Department of Endocrinology, Liuzhou People’s Hospital, Liuzhou, China

Contributions: (I) Conception and design: S Tang, H Zhao; (II) Administrative support: H Zhao, M Wang, X Peng; (III) Provision of study materials or patients: S Tang, H Zhao, L Zhong, X Liu; (IV) Collection and assembly of data: M Wang, Y Shi, Y Li; (V) Data analysis and interpretation: S Tang, H Zhao, M Wang, Y Chen; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

#These authors contributed equally to this work.

Correspondence to: Shaohui Tang. Department of Gastroenterology, The First Affiliated Hospital, Jinan University, 613 W. Huangpu Avenue, Guangzhou 510630, China. Email: tangshaohui206@163.com.

Background: Omega-3 polyunsaturated fatty acids are known to be associated with numbers of health benefits, and which can be uptake from fish. The aim of this study was to evaluate the current evidence of associations between consumption of fish and diverse health outcomes. Here, we performed an umbrella review to summarize the breadth, strength, and validity of the evidence derived from meta-analyses and systematic reviews of fish consumption on all health outcomes.

Methods: The methodological quality of the included meta-analyses and the quality of the evidence were assessed by the Assessment of Multiple Systematic Reviews (AMSTAR) and the grading of recommendations, assessment, development, and evaluation (GRADE) tools, respectively. The umbrella review identified 91 meta-analyses with 66 unique health outcomes, of which 32 outcomes were beneficial, 34 showed nonsignificant associations and only one was harmful (myeloid leukemia).

Results: A total of 17 beneficial associations [all-cause mortality, prostate cancer mortality, cardiovascular disease (CVD) mortality, esophageal squamous cell carcinoma (ESCC), glioma, non-Hodgkin lymphoma (NHL), oral cancer, acute coronary syndrome (ACS), cerebrovascular disease, metabolic syndrome, age-related macular degeneration (AMD), inflammatory bowel disease (IBD), Crohn’s disease (CD), triglycerides, vitamin D, high-density lipoprotein (HDL)-cholesterol, and multiple sclerosis (MS)], and eight nonsignificant associations [colorectal cancer (CRC) mortality, esophageal adenocarcinoma (EAC), prostate cancer, renal cancer, ovarian cancer, hypertension, ulcerative colitis (UC), and rheumatoid arthritis (RA)] were evaluated as moderate/high quality of evidence. According to dose-response analyses, consumption of fish, especially fatty types, seems generally safe at one-two servings per week and could exert protective effects.

Conclusions: Fish consumption is often associated with a variety of health outcomes, both beneficial and harmless, but only about 34% of the associations were graded as based on a moderate/high quality of evidence, and additional multicenter high quality randomized controlled trials (RCTs) with a large sample size are needed to verify these findings in the future.

Keywords: Fish consumption; health; umbrella review; meta-analysis; systematic review

Submitted Dec 01, 2022. Accepted for publication Feb 07, 2023. Published online Feb 15, 2023.

doi: 10.21037/atm-22-6515

Highlight box

Key findings

• Our findings strongly support the important role for fish as part of a healthy diet, which was recommended by the dietary guidelines in various countries, such as the Australian Dietary Guidelines, Dietary Guidelines for Americans, and European Food Safety Authority (EFSA) Dietary Guidelines.

What is known and what is new?

• Recent epidemiological studies have investigated the relevance between the consumption of fish and a wide series of outcomes, including mortality, cancers, cardiovascular disease, metabolic, cognitive disorders, and other health-related outcomes;

• We performed an umbrella review to summarize the breadth, strength, and validity of the evidence derived from meta-analyses and systematic reviews of fish consumption on all health outcomes.

What is the implication, and what should change now?

• Additional multicenter, high quality RCTs with large sample sizes are needed to verify these findings in the future.

Introduction

Fish is a rich source of various nutrients, and one of the most commonly consumed sustenance worldwide (1). Per capita fish consumption is steadily increasing, especially in developed countries (2), and even small effects on individual health could be contributing to public health. The nutritional components of fish, especially n-3 polyunsaturated fatty acids (n-3 PUFA), such as eicosapentaenoic acid (EPA), docosapentaenoic acid (DPA), and docosahexaenoic acid (DHA), have been reported to have a protective effect against cardiovascular disease (CVD), cancers, and psychiatric illnesses, to exert immunomodulatory, anti-inflammatory, and anticancer effects, and to affect blood pressure, lipid metabolism, and glucose metabolism in previous experimental studies (3-10). In general, fish types can be divided into two categories; fatty fish and lean fish, among which fatty fish is more popular worldwide (11). Salmon, tuna, sardines, mackerel, and trout, are examples of fatty fish, in which a higher amount of n-3 PUFA is found, which is more beneficial than the saturated fat found in most meats and that in lean species of fish including cod (5,12).

Recently, epidemiological studies have investigated the relevance between fish consumption and a various of outcomes, including mortality, cancers, CVD, metabolic, cognitive disorders, and other health-related outcomes (13). However, there have been inconsistent conclusions about the overall effect of fish consumption on health problems, and its precise roles vary among different health outcomes (14). Although many of the reported associations could be causal, they could also be flawed due to residual confounding, reporting bias, or other biases, which frequently over-estimate the magnitudes of the observed effects (15,16). To the best of our knowledge, there are no existing umbrella reviews to comprehensively capture the breadth of health outcomes associated with fish consumption. Thus, we performed an umbrella review to summarize the broad, powerful, and efficient evidence derived from meta-analyses and systematic reviews of fish consumption on all health outcomes.

Methods

Literature search

Here, PubMed and Web of Science of Systematic Reviews were used for quantitative reviews of fish intake and health outcomes up to May 2021. The search terms were “fish” and “systematic review” OR “meta-analysis”. The references of eligible articles were conducted using manual screen. The search was performed by three independent researchers (M Wang, H Zhao, and X Peng) and consensus was used to resolve any differences in the literature search.

Eligibility criteria

The inclusion criterion was systematic review and meta-analysis of randomized controlled trials (RCTs) and observational studies considering fish intake as the exposure variable of interest and diverse health conditions. Articles with the following characteristics are excluded: (I) review articles without quantitative statistical analysis; (II) studies on genetic polymorphisms related to fish consumption; (III) RCTs including in vitro studies or animal trials; (IV) articles not published in English. As we were interested only in the relevance between total fish consumption and health outcomes, articles that evaluated the exposure to a fish ingredient, for example, fish oil or omega-3 fatty acids, were also excluded. If multiple health outcomes were presented in a single article, we included each of these separately. If a single meta-analysis divided into cohort study and case-control study without including the total estimated effect size for both, we lectured the results of cohort study as it was less influenced by recall and selection biases. If more than one published meta-analysis examined the same association, we assessed only the largest meta-analysis to avoid duplicate assessment of the same primary studies. In this umbrella review, we did not screen the individual component studies included in each meta-analysis.

Data extraction

Three authors (M Wang, H Zhao, and L Zhong) extracted data separately. From each eligible meta-analysis, the following information was extracted: (I) first author and publication year; (II) study design and outcomes; (III) total population and number of cases; (IV) type of exposure, measure of exposure, and effect sizes [risk ratio, odds ratio (OR), hazard ratio (HR), 95% confidence intervals (CIs), and continuous outcomes]. Finally, the type of effect model, publication bias by Egger’s test, and dose-response analyses were abstracted when possible. Discussion was used to resolve the discrepancies in the process of the extracted data.

Assessment of methodological quality

The evaluation of reporting and methodological quality of all included systematic reviews and meta-analyses were analyzed according to the 11 items of the Assessment of Multiple Systematic Reviews (AMSTAR) checklist (17). Each question could be answered with “yes”, “no”, “can’t answer”, and “not applicable”. A “yes” scored 1 point, whereas the other answers, including “no”, “can’t answer”, and “not applicable”, scored 0 points. An overall score of 3 points or less was defined as the cutoff value for low quality, 4–7 points as moderate quality, and 8 points or more as high quality.

Evaluation of the grading of evidence

The grading of recommendations, assessment, development, and evaluation (GRADE) tool was used to assess the quality of evidence for each outcome in each meta-analysis (18). Included observational studies that started with low deterministic evidence by default and were then downgraded or upgraded according to pre-specified criteria. The downgrade criteria included study boundedness [the weight of studies showed risk of bias by the Newcastle-Ottawa Scale (NOS)], inconformity (large amounts of agnogenic cross-study heterogeneity, I2 was equal or greater than 50% and P value was less than 0.10), indirectness (presence of factors relating to the exposures, population quantity, and denouements that limit pervasiveness), inexactitude [95% CIs were broad or decussated a minimally momentous discrepancy of 5% relative risk (RR): 0.95–1.05 for all denouements], and publication bias (prominent evidence of minitype-study effects). Upgrading criteria included a large size effect (RR >2 or RR <0.5 in defect of possible confounding factors), a dose-reactiongradient, and falloff by paradoxical confounding effects.

Statistical analysis

The estimated summary effect with its corresponding 95% CI was abstracted from each eligible meta-analysis. The Cochran’s Q test and the I2 statistic were performed to evaluate the heterogeneity between studies. Publication bias was calculated with Egger’s test, in which a P value less than 0.1 was considered significant. Dose-response analyses were not reanalyzed since we did not examine the primary articles.

Results

Characteristics of meta-analyses

The search strategy is shown in Figure 1. After following the selection process, 91 meta-analyses and systematic reviews of RCTs and observational studies with 66 unique health outcomes were identified, with most outcomes having more than one meta-analysis. The association between fish consumption and mortality is presented in Table 1 (19-27). Table 2 (14,22,27-45) presents the associations between consumption of fish and cancer outcomes (46-64), while those between fish consumption and CVD are presented Table 3 (13,65-77). Table 4 presents the associations between fish consumption and metabolic outcomes (78-87), and those between fish consumption and cognitive outcomes are presented in Table 5 (88-97). Table 6 presents the associations between fish consumption and allergic outcomes (98-100), and those between fish consumption and other outcomes are presented in Table 7 (101-106).

Figure 1 Flowchart of the selection process. From: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71. doi: 10.1136/bmj.n71. For more information, visit: http://www.prisma-statement.org/.

Table 1

Associations between fish consumption and mortality

Outcome Category Study No. of cases/total MA metric Estimates 95% CI No. of studies in MA Cohort Case control RCT Effects model I2 Egger test P value
Significant associations
   All-cause mortality Fish Schwingshackl 2017 157,688/NA RRa) 0.95 0.92–0.98 39 39 0 0 Random 51 NA
   All-cause mortality Fish Schwingshackl 2017 157,688/NA RRb2) 0.93 0.88–0.98 19 19 0 0 Random 53 NA
   Prostate cancer-specific mortality Fish Szymanski 2010 740/49,661 RRa) 0.37 0.18–0.74 4 4 0 0 Random 83 0.22
   CHD mortality Fish Zheng 2012 NA/315,812 RRb1) 0.84 0.75–0.95 16 16 0 0 Random 20.1 0.265
   CHD mortality Fish Zheng 2012 NA/315,812 RRd) 0.79 0.67–0.92 13 13 0 0 Random 56.7 0.018
   CVD mortality Fish Jayedi 2018 11,720/331,239 RRc) 0.96 0.94–0.98 8 8 0 0 Random 0 NA
   Mortality of total aortic diseases Fish Yamagishi 2019 NA HRc) 0.52 0.30–0.88 7 7 0 0 Random NA NA
   Aortic dissection mortality Fish Yamagishi 2019 NA HRc) 0.40 0.18–0.89 3 3 0 0 Random NA NA
Non-significant associations
   Total cancer mortality Fish Zhang 2018 NA RRa) 0.99 0.94–1.05 10 10 0 0 Random 39.3 >0.4
   Total cancer mortality Fish Zhang 2018 NA RRb2) 0.98 0.92–1.05 10 10 0 0 Random 21.3 NA
   CHD mortality Fish Zheng 2012 NA/315,812 RRe) 0.83 0.68–1.01 5 5 0 0 Random 0 NA
   CRC mortality Fish Geelen 2007 NA RRa) 1.02 0.90–1.16 4 4 0 0 Random 0 0.66
   Aortic aneurysm mortality Fish Yamagishi 2019 NA HRc) 0.84 0.23–1.11 5 5 0 0 Random NA NA

a), highest versus lowest/none; b1), one serving/week; b2), one serving/day; c), 1–2 servings/week; d), 2–4 servings/week; e), >5 servings/week. CHD, coronary heart disease; CI, confidence interval; CRC, colorectal cancer; CVD, cardiovascular disease; HR, hazard ratio; MA, meta-analysis; NA, not available; RCT, randomized controlled trial; RR, relative risk.

Table 2

Associations between fish consumption and cancer outcomes

Outcome Category Study No. of cases/total MA metric Estimates 95% CI No. of studies in MA Cohort Case control Cross-sectional Effects model I2 Egger test P value
Significant associations
   Brain tumor Fish Lian 2017 NA RRa) 0.83 0.70–0.99 9 1 8 0 Random 37.5 0.02
   Brain tumor Fish Lian 2017 NA RRb) 0.95 0.91–0.98 9 1 8 0 Random 51.7 NA
   EC Fish Jiang 2016 NA RRa) 0.69 0.57–0.85 18 2 16 0 Random 63.6 NA
   ESCC Fish Han 2013 4,508/NA RRa) 0.81 0.66–0.99 17 3 14 0 Random 51.9 NA
   Glioma Fish Zhang 2019 NA RRa) 0.82 0.70–0.97 8 0 8 0 Random 43.6 0.088
   CRC Fish Wu 2012 NA RRa) 0.88 0.80–0.95 41 22 19 0 Random 56.8 0.45
   Liver cancer Fish Huang 2015 NA/3,624 RRa) 0.82 0.71–0.94 10 5 5 0 Random 12.8 0.07
   Liver cancer Fish Huang 2015 NA/3,624 RRc) 0.94 0.91–0.98 10 5 5 0 Random 0 NA
   Lung cancer Fish Song 2014 8,799/17,072 RRa) 0.79 0.69–0.92 20 3 17 0 Random 73 0.098
   Myeloid leukemia Fish Sergentanis 2019 416/NA RRa) 1.74 1.22–2.47 3 3 0 0 Random 0.8 NA
   NHL Fish Yang 2020 7,696/NA RRa) 0.80 0.68–0.94 9 2 7 0 Random 66.3 0.002
   Oral cancer Fish Hu 2019 5,211/7,005 ORa) 0.74 0.64–0.85 15 2 13 0 Random 25.2 0.487
Non-significant associations
   Colon cancer Fish Vieira 2017 10,512/NA RRb) 0.91 0.80–1.03 11 11 0 0 Random 0 NA
   Rectal cancer Fish Vieira 2017 3,944/NA RRb) 0.84 0.69–1.02 10 10 0 0 Random 15 NA
   EAC Fish Han 2013 1,610/NA RRa) 0.86 0.61–1.22 6 1 5 0 Random 58.4 NA
   Gastric cancer Fish Wu 2011 5,323/NA RRa) 0.87 0.71–1.07 17 2 15 0 Random 73.3 0.59
   Leukemia Fish Sergentanis 2019 2,536/NA RRa) 1.02 0.89–1.17 3 3 0 0 Random 0 NA
   CLL/SLL Fish Sergentanis 2019 1,370/NA RRa) 0.99 0.83–1.19 3 3 0 0 Random 0 NA
   MM Fish Sergentanis 2019 986/NA RRa) 0.94 0.67–1.33 3 3 0 0 Random 30.2 NA
   Prostate cancer Fish Szymanski2010 NA/445,820 RRa) 1.01 0.90–1.14 12 12 0 0 Random NA 0.84
   Thyroid cancer Fish Cho 2015 NA RRa) 1.01 0.83–1.23 16 0 16 0 Random 58 NA
   Renal cancer Fish Bai 2013 9,324/608,753 RRa) 0.99 0.92–1.07 15 3 12 0 Fixed 23.8 0.38
   Ovarian cancer Fish Jiang 2014 NA RRa) 1.04 0.89–1.22 5 5 0 0 Fixed 0 0.29
   Breast cancer Fish Wu 2016 20,810/914,451 RRa) 1.04 0.97–1.12 18 18 0 0 Random 47.9 0.613
   Breast cancer Fatty fish Wu 2016* NA RRa) 0.81 0.58–1.12 5 2 3 0 Random 87 NA
   Breast cancer Lean fish Wu 2016* NA RRa) 1.09 1.00–1.19 4 2 2 0 Random 0 NA
   Pancreatic cancer Fish Jiang 2019 4,994/1,794,601 RRa) 1.04 0.95–1.13 13 13 0 0 Random 0 0.77
   Endometrial cancer Fish Hou 2017 NA RRa) 1.04 0.84–1.30 12 4 8 0 Random 80.4 NA
   Endometrial cancer Fish Hou 2017 NA RRc) 1.00 0.94–1.07 10 2 8 0 Random 81.7 NA
   Bladder cancer Fish Li 2011 NA RRa) 0.86 0.61–1.12 14 5 9 0 Random 85.4 NA

a), highest versus lowest/none; b), one serving =100 g/day; c), one serving/week; *, Zhi-Hui Wu. CI, confidence interval; CLL/SLL, chronic lymphocytic leukemia/small lymphocytic lymphoma; CRC, colorectal cancer; EAC, esophageal adenocarcinoma; EC, endometrial cancer; ESCC, esophageal squamous cell carcinoma; MA, meta-analysis; MM, multiple myeloma; NA, not available; NHL, non-Hodgkin lymphoma; OR, odds ratio; RR, relative risk.

Table 3

Associations between fish consumption and cardiovascular disease

Outcome Category Study No. of cases/total MA metric Estimates 95% CI No. of studies in MA Cohort Case control RCT Effects model I2 Egger test P value
Significant associations
   Stroke Fish Zhao 2019 NA HRa) 0.90 0.85–0.96 33 33 0 0 Random 39.2 0.084
   Stroke Lean fish Qin 2018 NA RRa) 0.81 0.67–0.99 4 4 0 0 Random 0 0.324
   Hemorrhagic stroke Fish Zhao 2019 NA HRa) 0.88 0.80–0.96 13 13 0 0 Random 0 0.084
   ACS Fish Leung Yinko 2014 8,517/408,305 RRa) 0.78 0.70–0.88 19 11 8 0 Random 0 0.6
   MI Fish Jayedi 2019 NA/398,221 RRa) 0.73 0.59–0.87 11 11 0 0 Random 72 NA
   CHD Fish Bechthold 2019 NA RRb) 0.88 0.79–0.99 15 15 0 0 Random 40 NA
   HF Fish Bechthold 2019 7,945/NA RRa) 0.89 0.80–0.99 8 8 0 0 Random 18 NA
   HF Fish Bechthold 2019 NA RRb) 0.80 0.67–0.95 7 7 0 0 Random 20 NA
   Cerebrovascular disease Fish Chowdhury 2012 25,320/675,048 RRa) 0.88 0.84–0.93 21 21 0 0 Random 18.5 >0.05
   Cerebrovascular disease Fish Chowdhury 2012 24,612/650,210 RRd) 0.94 0.90–0.98 18 18 0 0 Random 22 >0.05
   Cerebrovascular disease Fish Chowdhury 2012 16,890/394,958 RRe) 0.88 0.81–0.96 8 8 0 0 Random 20 >0.05
   Cerebrovascular disease Fatty fish Chowdhury 2012 2,695/62,799 RRa) 0.84 0.72–0.98 4 4 0 0 Random 10.1 >0.05
   Triglycerides Fish Alhassan 2017 596/1,128 MD −0.11 mmol/L −0.18 to −0.04 14 0 0 14 Random 0 NA
   Triglycerides Fatty fish Alhassan 2017 438/831 MD −0.11 mmol/L −0.19 to −0.03 12 0 0 12 Random 7 NA
   HDL-cholesterol Fish Alhassan 2017 584/1,104 MD 0.06 mmol/L 0.02–0.11 13 0 0 13 Random 28 NA
   HDL-cholesterol Fatty fish Alhassan 2017 438/831 MD 0.08 mmol/L 0.04–0.13 12 0 0 12 Random 0 NA
Non-significant associations
   Stroke Fatty fish Qin 2018 NA RRa) 0.88 0.74–1.04 5 5 0 0 Random 26.2 0.891
   CHD Fish Bechthold 2019 16,732/NA RRa) 0.94 0.88–1.02 22 22 0 0 Random 52 NA
   Ischemic stroke Fish Zhao 2019 NA HRa) 0.96 0.89–1.03 15 15 0 0 Random 27.9 0.084
   Cerebrovascular disease Lean fish Chowdhury 2012 2,695/62,799 RRa) 1.03 0.90–1.19 4 4 0 0 Random 0 >0.05
   Triglycerides Lean fish Alhassan 2017 158/297 MD −0.09 mmol/L −0.26 to 0.04 2 0 0 2 Random 0 NA
   HDL-cholesterol Lean fish Alhassan 2017 146/273 MD −0.02 mmol/L −0.10 to 0.06 1 0 0 1 Random NA NA
   AF Fish Li 2017 NA RRa) 1.01 0.94–1.09 6 6 0 0 Random 0 NA
   AF Fish Li 2017 NA RRc) 0.99 0.96–1.02 6 6 0 0 Random 23 NA
   Hypertension Fish Schwingshackl 2017 NA/83,612 RRa) 1.01 0.92–1.10 8 8 0 0 Random 57 NA
   Hypertension Fish Schwingshackl 2017 NA RRb) 1.07 0.98–1.16 7 7 0 0 Random 74 NA
   VTE Fish Zhang 2020 NA RRa) 1.02 0.93–1.11 6 6 0 0 Random 33 0.176

a), highest versus lowest/none; b), one serving =100 g/day; c), one serving/week; d), 2–4 versus ≤1 serving a week; e), ≥5 versus ≤1 serving a week. MA, meta-analysis; CI, confidence interval; RCT, randomized controlled trial; NA, not available; HR, hazard ratio; RR, relative risk; MD, mean difference; ACS, acute coronary syndrome; MI, myocardial infarction; CHD, coronary heart disease; HF, heart failure; HDL, high-density lipoprotein; AF, atrial fibrillation; VTE, venous thromboembolism.

Table 4

Associations between fish consumption and metabolic disease

Outcome Category Study No. of cases/total MA metric Estimates 95% CI No. of studies in MA Cohort Case control RCT Effects model I2 Egger test P value
Significant associations
   Metabolic Syndrome Fish Kim 2015 NA RRa) 0.71 0.58–0.87 2 2 0 0 fixed 60.7 NA
   Metabolic Syndrome Fish Kim 2015 NA RRc) 0.94 0.90–0.98 2 2 0 0 Fixed 66.3 NA
   T2DM Fatty fish Namazi 2019 NA RRa) 0.89 0.82–0.98 5 5 0 0 Random 0 0.42
   Vitamin D Fish Lehmann 2015 NA MDa) 4.4 nmol/L 1.7–7.1 9 0 0 9 Random 25 NA
   Vitamin D Fish Lehmann 2015 NA MDd) 3.8 nmol/L 0.6–6.9 10 0 0 10 Random 38 NA
   Vitamin D Fish Lehmann 2015 NA MDe) 8.3 nmol/L 2.1–14.5 4 0 0 4 Random 0 NA
   Vitamin D Fatty fish Lehmann 2015 NA MDa) 6.8 nmol/L 3.7–9.9 7 0 0 7 Random 0 NA
Non-significant associations
   T2DM Fish Schwingshackl 2017 NA/45,029 RRa) 1.04 0.95–1.13 16 16 0 0 Random 76 NA
   T2DM Fish Schwingshackl 2017 NA RRb) 1.09 0.93–1.28 15 15 0 0 Random 84 NA
   T2DM Lean fish Namazi 2019 NA RRa) 1.03 0.87–1.22 5 5 0 0 Random 51 0.36
   Vitamin D Lean fish Lehmann 2015 NA MDa) 1.9 nmol/L −2.3 to 6.0 7 0 0 7 Random 37 NA

a), highest versus lowest/none; b), one serving =100g/day; c), one serving/week; d), short-term studies (4–8 weeks); e), long-term studies (6 months or 23 weeks). CI, confidence interval; MA, meta-analysis; MD, mean difference; NA, not available; RCT, randomized controlled trial; RR, relative risk; T2DM, type 2 diabetes.

Table 5

Associations between fish consumption and cognitive disease

Outcome Category Study No. of cases/total MA metric Estimates 95% CI No. of studies in MA Cohort Case control Cross-sectional Effects model I2 Egger test P value
Significant associations
   Depression Fish Li 2016 NA/102,785 RRa) 0.83 0.74–0.93 26 10 0 16 Random 64.5 0.419
   Dementia Fish Bakre 2018 3,139/40,668 RRa) 0.80 0.74–0.87 8 6 2 0 Fixed 0 0.597
   AD Fish Zeng 2017 NA RRa) 0.80 0.65–0.97 7 7 0 0 Fixed 48.2 NA
   AD Fish Zeng 2017 NA RRb) 0.88 0.79–0.99 7 7 0 0 Random 55.3 NA
   MS Fish Rezaeizadeh 2022 2,370/7,170 RRa) 0.77 0.64–0.92 6 6 0 0 Random 54.7 0.051
Non-significant associations
   Mild cognitive impairment Fish Zeng 2017 NA RRa) 1.03 0.78–1.37 2 2 0 0 Fixed 0 NA

a), highest versus lowest/none; b), one serving/week. AD, Alzheimer’s disease; CI, confidence interval; MA, meta-analysis; MS, multiple sclerosis; NA, not available; RR, relative risk.

Table 6

Associations between fish consumption and allergic disease

Outcome Category Study No. of cases/total MA metric Estimates 95% CI No. of studies in MA Cohort Case control RCT Effects model I2 Egger test P value
Significant associations
   Current asthma Fish Papamichael2018 NA ORa) 0.75 0.60–0.95 3 3 0 0 Random 11.5 NA
   Current wheeze Fish Papamichael2018 NA ORb) 0.62 0.48–0.80 2 2 0 0 Random 0 NA
   Current asthma Fatty fish Papamichael2018 NA ORc) 0.35 0.18–0.67 2 2 0 0 Random 0 NA
   Eczema Fish Zhang 2017 NA/13,823 RRg) 0.61 0.47–0.80 4 4 0 0 Random 68 NA
   Allergic rhinitis Fish Zhang 2017 NA/9,987 RRg) 0.54 0.36–0.81 3 3 0 0 Random 74 NA
Non-significant associations
   Current wheeze Fish Papamichael2018 NA ORd) 0.81 0.64–1.02 9 9 0 0 Random 82.4 NA
   Asthma Fish Yang 2013 NA RRe) 0.90 0.69–1.18 2 2 0 0 Fixed 0 NA
   Sensitization Fish Zhang 2017 NA/3,099 RRf) 0.88 0.65–1.21 2 2 0 0 Random 33 NA
   Eczema Fish Zhang 2017 NA/15,945 RRf) 0.88 0.75–1.04 10 10 0 0 Random 53 NA
   Allergic rhinitis Fish Zhang 2017 NA/32,589 RRf) 0.95 0.62–1.45 3 3 0 0 Random 44 NA
   Wheeze Fish Zhang 2017 NA/42,096 RRf) 0.94 0.83–1.07 8 8 0 0 Random 26 NA
   Asthma Fish Zhang 2017 NA/37,295 RRf) 0.94 0.75–1.18 4 4 0 0 Random 52 NA
   Wheeze Fish Zhang 2017 NA/8,597 RRg) 0.94 0.77–1.14 2 2 0 0 Random 0 NA
   Asthma Fish Zhang 2017 NA/8,902 RRg) 0.84 0.69–1.02 3 3 0 0 Random 0 NA

a), children (0–4 years old) for ‘all fish’ intake versus ‘no fish’; b), children (0–4.5 years old) for ‘all fish’ intake versus ‘no fish’; c), ‘fatty fish’ intake versus ‘no fatty fish’ in children (8–14 years); d), children (0–13 years old) for ‘all fish’ intake versus ‘no fish’; e), highest versus lowest in adults; f), maternal fish intake during pregnancy; g), fish intake in infancy. CI, confidence interval; MA, meta-analysis; NA, not available; OR, odds ratio; RCT, randomized controlled trial; RR, relative risk.

Table 7

Associations between fish consumption and AMD, IBD, skeletal, and arthritis disease

Outcome Category Study No. of cases/total MA metric Estimates 95% CI No. of studies in MA Cohort Case control RCT Effects model I2 Egger test P value
Significant associations
   AMD Fish Dinu 2019 NA/237,464 RRa) 0.82 0.75–0.90 8 8 0 0 Random 33 NA
   IBD Fish Mozaffari 2020 823/41,601 ESa) 0.68 0.46–1.00 6 1 5 0 Random 76.4 NA
   CD Fish Mozaffari 2020 NA ESa) 0.54 0.31–0.96 5 1 4 0 Random NA NA
   Hip fracture Fish Sadeghi 2019 NA ESa) 0.88 0.79–0.98 6 4 2 0 Fixed 57.9 >0.44
Non-significant associations
   UC Fish Mozaffari 2020 NA ESa) 0.82 0.56–1.22 3 2 1 0 Fixed 30.6 NA
   RA Fish Di Giuseppe 2014 3,346/174,702 RRa) 0.96 0.91–1.01 7 3 4 0 Random 0 0.27

a), highest versus lowest/none. AMD, age-related macular degeneration; CD, Crohn’s disease; CI, confidence interval; ES, estimated size; IBD, inflammatory bowel disease; MA, meta-analysis; NA, not available; RA, rheumatoid arthritis; RCT, randomized controlled trial; RR, relative risk; UC, ulcerative colitis.

Quality assessment of meta-analyses

The AMSTAR rating for all studies was determined to be high for approximate 70% or moderate for approximate 30%. The most common reasons for quality downgrades were lack of a registration scheme, unsatisfactory reporting/assessment of the risk of bias in pilot studies, and inappropriate metanalytic methodology.

Mortality

High consumption of fish decreased the risk of all-cause death rate (RR: 0.95; 95% CI: 0.92, 0.98) and prostate cancer death (RR: 0.37; 95% CI: 0.18, 0.74) (21,22). Moreover, compared with the minimum intake of fish (less than one serving per month or one to three servings per month) (one serving =100 g), either low (one serving/week) (RR: 0.84; 95% CI: 0.75, 0.95) or moderate intake of fish (two to four servings per week) (RR: 0.79; 95% CI: 0.67, 0.92), but not high fish consumption (more than five servings per week) (RR: 0.83; 95% CI: 0.68, 1.01), had a significantly beneficial effect on the prevention of coronary heart disease (CHD) mortality (23). An increment intake of fish was also inversely associated with a decreased risk of aortic diseases mortality (including aortic dissection mortality), and the largest benefit was at 1–2 servings a week (RR: 0.52; 95% CI: 0.30, 0.88) (24). Dose-response analysis showed a one serving per day increment in fish consumption was associated with a decreased risk of all-cause mortality (RR: 0.93; 95% CI: 0.88, 0.98) (21). Consistently, the intake of one serving of fish per week was associated with a decreased risk of CVD mortality (RR: 0.96; 95% CI: 0.94, 0.98) and CHD mortality (RR: 0.94; 95% CI: 0.90, 0.98) (23,25). However, no associations were found between fish consumption and total cancer mortality (RR: 0.99; 95% CI: 0.94, 1.05), aortic aneurysm mortality (HR, 0.84; 95% CI: 0.23, 1.11), as well as colorectal cancer (CRC) mortality (RR: 1.02; 95% CI: 0.90, 1.16) (24,26,27).

Cancer outcomes

High intake of fish was associated with a reduced risk of oral cancer (OR, 0.74; 95% CI: 0.64, 0.85), brain cancer (RR: 0.83; 95% CI: 0.70, 0.99), hepatocellular carcinoma (HCC) (RR: 0.82; 95% CI: 0.71, 0.94), CRC (RR: 0.88; 95% CI: 0.80, 0.95), lung cancer (RR: 0.79; 95% CI: 0.69, 0.92), esophageal cancer (EC) (RR: 0.69; 95% CI: 0.57, 0.85) and its subtype esophageal squamous cell carcinoma (ESCC) (RR: 0.81; 95% CI: 0.66, 0.99), non-Hodgkin lymphoma (NHL) (RR: 0.80; 95% CI: 0.68, 0.94), and glioma (RR: 0.82; 95% CI: 0.70, 0.97) (28,30,32,38,39,42,43,45). Conversely, a positive association between fish intake and myeloid leukemia risk (RR: 1.74; 95% CI: 1.22, 2.47) was observed in high-compared with low-intake categories (44). The subgroup analysis by sex showed a protective effect of fish consumption on lung cancer was present only in females (39), and when the subgroup analysis was conducted by geographic location, a protective effect was only observed in HCC and lung cancer for Asian populations, as well as oral cancer and ESCC for European populations (28,32,39,43).

According to dose-response analyses, fish intake of one serving per week was associated with a decreased risk of brain cancer (RR: 0.95; 95% CI: 0.91, 0.98) and HCC (RR: 0.94; 95% CI: 0.91, 0.98) (29,32). There was no relevance between a high intake of fish with the risk of prostate cancer (RR: 1.01; 95% CI: 0.90, 1.14), renal cancer (RR: 0.99; 95% CI: 0.92, 1.07), ovarian cancer (RR: 1.04; 95% CI: 0.89, 1.22), gastric cancer (RR: 0.87; 95% CI: 0.71, 1.07), thyroid cancer (RR: 1.01; 95% CI: 0.83, 1.23), bladder cancer (RR: 0.86; 95% CI: 0.61, 1.12), breast cancer (RR: 1.04; 95% CI: 0.97, 1.12), endometrial cancer (RR: 1.04; 95% CI: 0.84, 1.30), pancreatic cancer (RR: 1.04; 95% CI: 0.95, 1.13), colon cancer (RR: 0.91; 95% CI: 0.80, 1.03), rectal cancer (RR: 0.84; 95% CI: 0.69, 1.02), esophageal adenocarcinoma (EAC) (RR: 0.86; 95% CI: 0.61, 1.22), leukemia (RR: 1.02; 95% CI: 0.89, 1.17), chronic lymphocytic leukemia/small lymphocytic lymphoma (CLL/SLL) (RR: 0.99; 95% CI: 0.83, 1.19), and multiple myeloma (MM) (RR: 0.94; 95% CI: 0.67, 1.33) (22,36,38,43,44,47,48,51,53,55,56,62,63). However, for endometrial cancer, although the null association was observed for every one additional serving/week of fish intake, an inverse association was detected in studies conducted in Europe (RR: 0.90; 95% CI: 0.84, 0.97) and studies adjusted for smoking (RR: 0.95; 95% CI: 0.91, 1.00), and a significant positive association was detected in studies conducted in Asia (RR: 1.15; 95% CI: 1.10, 1.21) (62). In addition, studies conducted in Europe (RR: 0.71; 95% CI: 0.61, 0.82) and Australia (RR: 0.76; 95% CI: 0.63, 0.92) have shown that fish consumption is associated with a significantly reduced risk of ovarian cancer, and studies adjusted for the use of oral contraceptives (RR: 0.79; 95% CI: 0.63, 0.99) and parity (RR: 0.79; 95% CI: 0.63, 0.99) (48). In addition, a slightly increased risk of thyroid cancer was observed among those consuming high amounts of fish in iodine nondeficient areas (RR: 1.18; 95% CI: 1.03, 1.35) (53).

Cardiovascular outcomes and ischemic diseases

Fish consumption was associated with a decreased risk of acute coronary syndrome (ACS) (RR: 0.78; 95% CI: 0.70, 0.88), cerebrovascular disease (RR: 0.88; 95% CI: 0.84, 0.93), heart failure (HF) (RR: 0.89; 95% CI: 0.80, 0.99), myocardial infarction (MI) (RR: 0.73; 95% CI: 0.59, 0.87), and stroke (HR, 0.90; 95% CI: 0.85, 0.96), multiple sclerosis (MS) (OR: 0.77; 95% CI: 0.64, 0.92), especially hemorrhagic stroke (HR, 0.88; 95% CI: 0.80, 0.96) (65-69). Considering the different types of fish, the consumption of fatty fish (RR: 0.84; 95% CI: 0.72, 0.98) could decrease the risk of cerebrovascular disease, while no significant association was found for lean fish (RR: 1.03; 95% CI: 0.90, 1.19) (66). In contrast, the reduction of stroke risk was associated with the consumption of lean fish (RR: 0.81; 95% CI: 0.67, 0.99), but not fatty fish (RR: 0.88; 95% CI: 0.74, 1.04) (13).

According to dose-response analyses, an increment of two servings per week of fish consumption could decrease the risk of cerebrovascular disease by 4% (RR: 0.96; 95% CI: 0.93, 0.99) (66). A linear dose-responses analyses showed the risk of stroke decreased by 2–12% with increased fish consumption up to one-seven servings/week (69). Also, an increase of one serving of fish per day could decrease the risk of HF (RR: 0.80; 95% CI: 0.67, 0.95) by 20%, and an increase of one serving per week was associated with a 4% decreased risk of MI (RR: 0.96; 95% CI: 0.94, 0.99) in Asia (RR: 0.94; 95% CI: 0.91, 0.97) and a 5% reduced risk of ACS (RR: 0.95; 95% CI: 0.92, 0.97), respectively (65,67,68).

There was a small association between consumption of fish and CHD risk comparing the highest categories and the lowest categories, a small association was seen between fish intake and risk of CHD (RR: 0.94; 95% CI: 0.88, 1.02), atrial fibrillation (AF) (RR: 1.01; 95% CI: 0.94, 1.09) and venous thromboembolism (VTE) (RR: 1.02; 95% CI: 0.93, 1.11), but neither association reached significance (70,73,77). In addition, dose-responses analyses showed the intake of one serving of fish per day was associated with a 12% (RR: 0.88; 95% CI: 0.79, 0.99) decreased risk of CHD, particularly for females (RR: 0.64; 95% CI: 0.50, 0.81) (70).

In addition, a meta-analysis of 14 RCTs showed consumption of fish, especially fatty fish, was associated with a moderately significant reduction in plasma triglycerides levels [mean difference (MD): −0.11 mmol/L; 95% CI: −0.18, 0.04] and an increase in high-density lipoprotein (HDL) levels (MD: 0.06 mmol/L; 95% CI: 0.02, 0.11) (74). Highest compared with the lowest category (RR: 1.01; 95% CI: 0.92, 1.10) and dose-responses analyses (RR: 1.07; 95% CI: 0.98, 1.16) of fish intake were not statistically significantly associated with the risk of hypertension, respectively (75).

Metabolic outcomes

The consumption of fish increased serum 25-hydroxyvitamin D [25(OH)D] concentrations by a weighted MD of 4.4 nmol/L (MD: 4.4 nmol/L; 95% CI: 1.7, 7.1), and long-term (~6 months) (MD: 8.3 nmol/L; 95% CI: 2.1, 14.5) consumption showed a higher MD than short-term (4–8 weeks) (MD: 3.8 nmol/L; 95% CI: 0.6, 6.9). Considering the type of the fish, the consumption of fatty fish resulted in a MD of 6.8 nmol/L (MD: 6.8 nmol/L; 95% CI: 3.7, 9.9), whereas for lean fish the MD was 1.9 nmol/L (MD: 1.9 nmol/L; 95% CI: −2.3, 6.0) (78). Moreover, consumption of fish was associated with a reduced risk of metabolic syndrome (MetS) (RR: 0.71; 95% CI: 0.58, 0.87), and an increase of one serving/week fish intake could reduce the risk by 6% (RR: 0.94; 95% CI: 0.90, 0.98) (79). In addition, total fish (RR: 1.04; 95% CI: 0.95, 1.13) and lean fish consumption (RR: 1.03; 95% CI: 0.87, 1.22) were not significantly related to the risk of type 2 diabetes mellitus (T2DM), while fatty fish consumption (RR: 0.89; 95% CI: 0.82, 0.98) was inversely associated with the risk of T2DM (80,82).

Cognitive outcomes

Highest compared with the lowest category of fish intake was associated with a decreased risk of developing depression (RR: 0.83; 95% CI: 0.74, 0.93) in Europe (RR: 0.72; 95% CI: 0.63, 0.82) (88). Analyses of high versus low consumption of fish indicated dementia risk was reduced by 20% (RR: 0.80; 95% CI: 0.74, 0.87) regardless of income level, and dose-response models showed fish consumption could decrease the risk of dementia by 16%, 22%, and 23% for low level consumers (consumed fish once weekly) (RR: 0.84; 95% CI: 0.72, 0.98), middle level consumers (≥ twice weekly) (RR: 0.78; 95% CI: 0.68, 0.90), and high level consumers (≥ once daily) (RR: 0.77; 95% CI: 0.61, 0.98), respectively (94). For Alzheimer’s disease (AD), an inverse association was observed for the highest compared with the lowest fish intake category (RR: 0.80; 95% CI: 0.65, 0.97), and for each additional one serving per week (RR: 0.88; 95% CI: 0.79, 0.99) (95). However, increasing fish intake had no obvious effect on the risk of mild cognitive impairment (MCI) (RR: 1.03; 95% CI: 0.78, 1.37) (96). Fish consumption was also associated with a decreased risk of MS (OR, 0.77; 95% CI: 0.64, 0.92) (97).

Allergic outcomes

Comparing the highest group of fish consumption with the lowest group, no significant association was found between fish and asthma among adults (98). Additionally, maternal fish intake during pregnancy did not affect any atopic outcome in children and adults, whereas total fish or fatty fish consumption during the infancy period seemed to have a protective impact on asthma, wheeze, eczema, and allergic rhinitis in children, especially up to 4.5 years old or 8–14 years old, respectively (99,100).

Other outcomes

There was no dose-response association between fish consumption and risk of rheumatoid arthritis (RA) (RR: 0.96; 95% CI: 0.91, 1.01) (101). Fish consumption was inversely associated with risk of hip fracture [estimated size (ES), 0.88; 95% CI: 0.79, 0.98] (102), while it conferred a beneficial effect on the development of age-related macular degeneration (AMD) (RR: 0.82; 95% CI: 0.75, 0.90), regardless of whether early (RR: 0.84; 95% CI: 0.73, 0.97) or late AMD (RR: 0.79; 95% CI: 0.70, 0.90) (103). In addition, using a random-effects model, a marginally negative association was observed between fish consumption and inflammatory bowel disease (IBD) (ES, 0.68; 95% CI: 0.46, 1.00), while a strong inverse association regarding Crohn’s disease (CD) (ES, 0.54; 95% CI: 0.31, 0.96) was detected in studies conducted in Asian countries (ES, 0.54; 95% CI: 0.37, 0.78) and in studies adjusted for BMI and smoking (ES, 0.35; 95% CI: 0.19, 0.66) (106).

Heterogeneity

Approximately, 44% of the meta-analyses had low heterogeneity, with I2<25%; 8% had very high heterogeneity, with I2>75%; and 42% had moderate-to-high heterogeneity, with I2 ranging from 25–75%. The individual studies in each meta-analysis differed for a number of factors, including geography and ethnicity, treatment differences, methods used to determine fish consumption, measurements of fish consumption, duration of follow-up, and evaluation of outcomes. The remaining 6% of the included meta-analyses did not disclose the heterogeneity of the studies that included specific comparisons, nor were they re-analyzed using randomized or fixed models.

Publication bias

Egger’s regression test was performed in the present umbrella review. P value for publication bias were reported in 36 included meta-analyses, three of which reported statistical evidence of publication bias. These included CHD mortality (P=0.018), NHL (P=0.002), and brain tumor (P=0.02) (23,29,45). While not report significant publication bias was reported in the remaining meta-analyses, in all probability that unmeasured publication bias exists in numerous of the conclusive evaluations we have rendered and not assessed.

Strength of epidemiologic evidence

A total of 15 inverse associations (including all-cause mortality, prostate cancer mortality, CVD mortality, ESCC, glioma, oral cancer, NHL, ACS, cerebrovascular disease, triglycerides, MetS, AMD, IBD, CD, and MS), two positive associations (vitamin D and HDL-cholesterol), and nine nonsignificant associations [comprising CRC mortality, EAC, prostate cancer, renal cancer, ovarian cancer, hypertension, VTE, ulcerative colitis (UC), and RA] showed moderate/high epidemiologic evidence.

In total, 15 additional inverse associations (mortality of total aortic diseases, aortic dissection mortality, brain cancer, EC, CRC, liver cancer, lung cancer, stroke, hemorrhagic stroke, MI, HF, depression, dementia, AD, and hip fracture) and one positive association (myeloid leukemia) showed statistically significant risk estimates, and their credibility was weak.

The other 24 outcomes (such as total cancer mortality, aortic aneurysm mortality, CHD mortality, colon cancer, rectal cancer, gastric cancer, leukemia, CLL/SLL, MM, thyroid cancer, breast cancer, pancreatic cancer, endometrial cancer, bladder cancer, ischemic stroke, CHD, AF, T2DM, asthma, sensitization, eczema, allergic rhinitis, wheeze, and MCI) did not show significant associations, and the quality of evidence was low or very low.

Discussion

Main findings

This umbrella review of meta-analyses of RCTs and observational studies provides a comprehensive overview and critical assessment of the consumption of fish associated with human health. A total of 64 outcomes, including mortality, cancer, CVD, metabolic, cognitive, allergy, and other outcomes, have been studied. The methodologic quality varied considerably across the published meta-analyses. The quality of evidence was graded as moderate or high for all-cause mortality, prostate cancer mortality, CVD mortality, ESCC, oral cancer, ACS, cerebrovascular disease, triglycerides, MetS, AMD, IBD, and CD, for which fish consumption reduced their risks; for vitamin D and HDL-cholesterol, whose levels were raised by fish consumption; and for CRC mortality, EAC, prostate cancer, renal cancer, ovarian cancer, hypertension, UC, and RA, whose risks were not related to fish consumption. For the other outcomes, the quality of evidence was low or very low, which might be explained by the high proportion of meta-analyses that included fewer than five studies or had high heterogeneity.

Outcome interpretation

Fish consumption and mortality outcomes

The results showed a higher intake of fish was associated with a decreased risk of all-cause mortality, prostate cancer mortality, and CVD mortality but no association between fish consumption and CRC mortality was found, for which we found moderate quality of evidence (21,22,25,27). Our results support the recommendation made by the recent 2015–2020 Dietary Guidelines for Americans to consume more than 227 g fish per week (107). It is worth noting that subgroup analysis by geographic location showed a significant association of fish consumption with all-cause mortality for studies conducted in Asia, but not in Europe (21). The different results appeared possibly due to the different dietary pattern of fish consumption in Asian and Western populations, of which the former have a higher intake, which may impact the significance of the results (25).

Although intake of fish had a protective effect on the risk of CHD mortality (low and moderate fish consumption, not high fish consumption), total aortic disease and its subtype aortic dissection mortality, total cancer mortality, and aortic aneurysm mortality, the quality of evidence was only low and further investigation is needed (23,24,26).

Fish consumption and cancer outcomes

Our findings confirm Australian Dietary Guidelines recommendations for a higher intake of fish, and we observed a moderate quality of evidence for an inverse association with oral cancer, glioma, NHL, and ESCC, and a nonsignificant association with prostate cancer, renal cancer, ovarian cancer, and EAC (22,28,30,43,45,47,48,108).

The World Cancer Research Fund and American Institute for Cancer Research (WCRF/AICR) recommend a higher intake of fish, for which we also found an inverse association with the risk of brain cancer, EC, CRC, liver cancer, and lung cancer, but the quality of evidence was low (29,32,38,39,42,109). We also found low quality of evidence for a positive association of fish intake with the risk of myeloid leukemia, and a null association with the risk of colon cancer, rectal cancer, gastric cancer, leukemia, CLL/SLL, MM, thyroid cancer, breast cancer, pancreatic cancer, endometrial cancer, and bladder cancer (36,44,51,53,55,56,62,63). It may be that heavy metals, which are frequently linked to the increased intake of fish, lead to the increased risk of myeloid leukemia in the highest fish consumption levels (44,110,111). These results indicate that more studies are needed. Additionally, a previous meta-analysis indicated an increase of one serving/week of salted fish intake, but not fresh fish, was significantly associated with an increased risk of gastric cancer (50). This may be because highly salted or smoked fish products can contain chemical carcinogens (112).

Fish consumption and cardiovascular outcomes

Recommendations for improving the cardiovascular health of all Americans with a dietary pattern including consumption of fish at least one to two servings per week, are included in the guidelines of the American Heart Association (AHA) Goals and Metrics Committee of the Strategic Planning Task Force issued 2020 Impact Goals (113). This information accords with our results which show a higher intake of fish was associated with a decreased level or risk of ACS, cerebrovascular disease and triglycerides, and an increased level of HDL-cholesterol, for which we found high quality of evidence (65,66,74). Particularly, fatty fish, but not lean fish could play an important role in the prevention of cerebrovascular diseases (66). In addition, we found moderate quality evidence that consumption of fish was not significantly associated with the risk of hypertension and VTE (75,77).

Our results also confirmed the inverse association of fish consumption with the risk of stroke, hemorrhagic stroke, MI, and HF, and a null association with ischemic stroke, CHD, and AF, but the quality of evidence for these associations was low, indicating further investigation is needed (67-70,73). Interestingly, lean fish, but not fatty fish, could confer a decreased risk of stroke, which was somewhat opposite to the general knowledge that fatty fish is “better” than lean fish (13). Nevertheless, a Norwegian diet study gives a possible explanation that lean fish contains more iodine, selenium, and less energy than fatty fish, which are beneficial to health (114). Generally, both fatty fish and lean fish are good for cardiovascular and cerebrovascular health, and frequent consumption of fatty fish is better than lean fish.

Fish consumption and other outcomes

In this umbrella review, we found high quality evidence that consumption of fish was associated with an increased level of vitamin D, while it was not significantly associated with the risk of RA (78,101). A randomized intervention trial came to similar conclusions concerning the beneficial association between fish intake and the level of vitamin D (115). In particular, long-term fish consumption or consumption of fatty fish resulted in higher serum 25(OH)D concentrations than short-term or lean fish, respectively (78). Moreover, our findings showed that higher consumption of fish was associated with a decreased risk of MetS, AMD, IBD, and CD but no association between fish consumption and UC was found, for which we found a moderate quality of evidence (79,103,106).

Although we also observed a reduced risk of MS, depression, dementia, AD, and hip fracture, and a null association of T2DM and MCI with consumption of fish, respectively, the quality of evidence for these associations was low and further investigation is needed (80,88,94,95,97,102).

Possible mechanisms

Although the precise mechanisms by which fish consumption beneficially affects health are not well-established, fish is a rich source of n-3 PUFA, vitamins, essential amino acids, and trace elements, which exert chemopreventive activity, anti-carcinogenic, anti-inflammatory, and synergistic antioxidant properties, which may at least partly explain its protective effects (116-119). For example, fish is a good source of trace elements, especially selenium, which may have synergistic antioxidant effects against all-cause mortality (21). In addition, n-3 PUFA, which has antiarrhythmic properties and reduces serum triacylglycerol (TAG) and platelet aggregation, has been observed to play an important role in the protective effect of fish on CHD risk (120,121). Also, it has been shown that higher consumption of n-3 PUFA may be associated with lower risk of cancer, partially due to its favorable effects of chemopreventive activity, including inhibition of eicosanoid biosynthesis derived from arachidonic acid, promotion of vasodilation, attenuation of inflammation, inhibition of mutations, and enhancement of cell apoptosis (122-124). Fish is also a good source of vitamin D, which has been linked to inverse T2DM risk (125). Considering the synergic effect of many components in fish, such as n-3 PUFA, trace elements, amino acid, and vitamins, comprehensive analysis of the potential mechanism behind the association between fish consumption and health is necessary.

Strengths and limitations

There are also some restrictions that should be considered. Firstly, this umbrella reviewer relied on existing systematic reviews and meta-analyses. As a consequence, the quality of the included articles might impact the quality of systematic reviews and meta-analyses directly. Secondly, although a large number of studies were included in the present meta-analysis, potential publication bias should also be considered. Thirdly, reporting bias might cause a form of reverse causation, and fourthly, a number of health-related outcomes were inappropriately covered, and this gap has been emphasized. Fifthly, due to the lack of a dose-response meta-analysis, we did not examine the original article and therefore did not conduct a re-analysis, and finally, we did not go back to original publications and re-calculate meta-analyses and we do not have information about confounding. The outcomes such as total cancer mortality, aortic aneurysm mortality, CHD mortality, colon cancer, rectal cancer, gastric cancer, leukemia, CLL/SLL, MM, thyroid cancer, breast cancer, pancreatic cancer, endometrial cancer, bladder cancer, ischemic stroke, CHD, AF, T2DM, asthma, sensitization, eczema, allergic rhinitis, wheeze, and MCI did not show significant associations, and the quality of evidence was low or very low. Further research is required.

Conclusions

Taken together, in this umbrella review, the relevance between fish consumption and multiple health outcomes has been examined in several meta-analyses. Evidence indicates fish consumption often has beneficial or harmless associations with various health outcomes. Although the methodological quality of the included meta-analyses was mostly high, the quality of evidence was moderate/high only for 15 inverse associations (all-cause mortality, prostate cancer mortality, CVD mortality, glioma, NHL, ESCC, oral cancer, ACS, cerebrovascular disease, MetS, AMD, IBD, CD, triglycerides, and MS), two positive associations (vitamin D and HDL-cholesterol), and eight nonsignificant associations (CRC mortality, EAC, prostate cancer, renal cancer, ovarian cancer, hypertension, UC, and RA). According to dose-response analyses, consumption of fish, especially fatty types, seems generally safe at one to two servings per week and could exert obvious protective effects. Our findings strongly support the important role of fish as part of a healthy diet, which was recommended by the dietary guidelines in various countries, such as Australian Dietary Guidelines, Dietary Guidelines for Americans, and European Food Safety Authority (EFSA) Dietary Guidelines (108,126,127). Additional multicenter high quality RCTs with a large sample size are needed to verify these findings in the future.

Acknowledgments

Funding: This work was supported by the Health Commission Funding Project of Hunan Province (No. B2019145), Science and Technology Funding Project of Chenzhou City (No. zdyf201848), and Science and Technology Funding Project of Hunan Province (No. 2017SK4010). The content of the paper is solely the responsibility of the authors and does not necessarily represent the official views of the funders.

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://atm.amegroups.com/article/view/10.21037/atm-22-6515/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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(English Language Editor: B. Draper)

Cite this article as: Zhao H, Wang M, Peng X, Zhong L, Liu X, Shi Y, Li Y, Chen Y, Tang S. Fish consumption in multiple health outcomes: an umbrella review of meta-analyses of observational and clinical studies. Ann Transl Med 2023;11(3):152. doi: 10.21037/atm-22-6515

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