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Cited by 203Nutritional Studies and DietMuscle metabolism and nutritionAgriculture Sustainability and Environmental Impact

Association of Animal and Plant Protein Intake With All-Cause and Cause-Specific Mortality in a Japanese Cohort

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Budhathoki, Sanjeev, Sawada, Norie, Iwasaki, Motoki, Yamaji, Taiki, Goto, Atsushi, Kotemori, Ayaka, Ishihara, Junko, Takachi, Ribeka +5 more·2019·JAMA Internal Medicine
DOI 10.1001/jamainternmed.2019.2806PMC PMC6714005
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Abstract

Importance: Epidemiological evidence regarding the long-term effects of higher dietary protein intake on mortality outcomes in the general population is not clear. Objective: To evaluate the associations between animal and plant protein intake and all-cause and cause-specific mortality. Design, Setting, and Participants: This prospective cohort study included 70 696 participants in the Japan Public Health Center-based Prospective Cohort who were aged 45 to 74 years and had no history of cancer, cerebrovascular disease, or ischemic heart disease at study baseline. Data were collected from January 1, 1995, through December 31, 1999, with follow-up completed December 31, 2016, during which 12 381 total deaths were documented. Dietary intake information was collected through a validated food frequency questionnaire and used to estimate protein intake in all participants. Participants were grouped into quintile categories based on their protein intake, expressed as a percentage of total energy. Data were analyzed from July 18, 2017, through April 10, 2019. Main Outcomes and Measures: Hazard ratios (HRs) and 95% CIs for all-cause and cause-specific mortality were estimated using Cox proportional hazards regression models with adjustment for potential confounding factors. Results: Among the 70 696 participants, 32 201 (45.5%) were men (mean [SD] age, 55.6 [7.6] years) and 38 495 (54.5%) were women (mean [SD] age, 55.8 [7.7] years). Intake of animal protein showed no clear association with total or cause-specific mortality. In contrast, intake of plant protein was associated with lower total mortality, with multivariable-adjusted HRs of 0.89 (95% CI, 0.83-0.95) for quintile 2; 0.88 (95% CI, 0.82-0.95) for quintile 3; 0.84 (95% CI, 0.77-0.92) for quintile 4; and 0.87 (95% CI, 0.78-0.96) for quintile 5, with quintile 1 as the reference category (P = .01 for trend). For cause-specific mortality, this association with plant protein intake was evident for cardiovascular disease (CVD)-related mortality (HRs, 0.84 [95% CI, 0.73-0.96] to 0.70 [95% CI, 0.59-0.83]; P = .002 for trend). Isocaloric substitution of 3% energy from plant protein for red meat protein was associated with lower total (HR, 0.66; 95% CI, 0.55-0.80), cancer-related (HR, 0.61; 95% CI, 0.45-0.82), and CVD-related (HR, 0.58; 95% CI, 0.39-0.86) mortality; substitution for processed meat protein was associated with lower total (HR, 0.54; 95% CI, 0.38-0.75) and cancer-related (HR, 0.50; 95% CI, 0.30-0.85) mortality. Conclusions and Relevance: In this large prospective study, higher plant protein intake was associated with lower total and CVD-related mortality. Although animal protein intake was not associated with mortality outcomes, replacement of red meat protein or processed meat protein with plant protein was associated with lower total, cancer-related, and CVD-related mortality.

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Crossref · 10.1001/jamainternmed.2019.2806

Cites

39 of 39 references verified0 citation errors · 0 not checkable

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Claims the paper makes

0 of 31 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    At 15 years, the estimated absolute risk reduction from replacing 3% of energy from red meat protein with plant protein was 1.92% for cancer-related mortality.

    “The estimated absolute risk reduction at 15 years for isocaloric substitution of 3% energy from plant protein for red meat protein was 3.60% (95% CI, 2.10%-4.86%)for total, 1.92% (95% CI, 0.87%-2.71%)for cancer-related, and 1.16% (95% CI, 0.39%-1.68%)for CVD-related mortality (eTable 4 in the Supplement).”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: The model treats protein intake as an isocaloric substitution, meaning its coefficient reflects replacing the same amount of energy from carbohydrates with protein.
  • Findingown data

    Plant protein intake was not associated with cancer mortality overall or by site.

    “but not with cancer mortality (overall or site-specific) (Table 2 and eTable 1 in the Supplement).”
    Quote in the paperSubstantial claim
  • Findingown data

    At 15 years, the estimated absolute risk reduction from replacing 3% of energy from red meat protein with plant protein was 1.16% for CVD-related mortality.

    “The estimated absolute risk reduction at 15 years for isocaloric substitution of 3% energy from plant protein for red meat protein was 3.60% (95% CI, 2.10%-4.86%)for total, 1.92% (95% CI, 0.87%-2.71%)for cancer-related, and 1.16% (95% CI, 0.39%-1.68%)for CVD-related mortality (eTable 4 in the Supplement).”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: The model treats protein intake as an isocaloric substitution, meaning its coefficient reflects replacing the same amount of energy from carbohydrates with protein.
  • Findingown data

    Replacing processed meat protein with fish protein was linked to lower all-cause mortality (HR 0.61; 95% CI 0.44-0.84).

    “Among animal proteins, substitution of fish protein for red meat was associated with lower total (HR, 0.75; 95% CI, 0.65-0.87),cancerrelated (HR, 0.67; 95% CI, 0.53-0.85),and CVD-related (HR, 0.67; 95% CI, 0.50-0.91)mortality; and substitution of fish protein for processed meat was associated with lower total (HR, 0.61; 95% CI, 0.44-0.84)and cancer-related (HR, 0.55; 95% CI, 0.34-0.91)mortality (”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: The model treats protein intake as an isocaloric substitution, meaning its coefficient reflects replacing the same amount of energy from carbohydrates with protein.
  • Findingown data

    Plant protein intake was associated with lower cerebrovascular disease mortality (quintile 5 HR 0.72; 95% CI 0.51-1.00).

    “Among cause-specific mortality, this inverse association with plant protein intake was evident for CVD mortality (HR for quintile 5, 0.73; 95% CI, 0.59-0.91)and its subdivisions of heart disease (HR for quintile 5, 0.72; 95% CI, 0.54-0.97)and cerebrovascular disease mortality (HR for quintile 5, 0.72; 95% CI, 0.51-1.00),but not with cancer mortality (overall or site-specific) (Table 2 and eTable 1”
    Quote in the paperSubstantial claim
  • May combine two claims. 10
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 21

  • May combine two claims. The quote only partly states this claim.

    Findingown data

    The analysis included 70,696 Japanese adults aged 45-74 years who were free of cancer, cerebrovascular disease, and ischemic heart disease at baseline; 12,381 deaths occurred over a mean 18-year follow-up.

    “This prospective cohort study included 70 696 participants in the Japan Public Health Center-based Prospective Cohort who were aged 45 to 74 years and had no history of cancer, cerebrovascular disease, or ischemic heart disease at study baseline.”
    • Also stated in: § Results · plain
      “During a mean follow-up of 18 years, we documented 12 381 deaths due to all causes, including 5055 due to cancer, 3025 due to CVD, 1528 due to heart disease, and 1198 due to cerebrovascular disease.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Animal protein intake was not clearly associated with total or cause-specific mortality in this Japanese cohort.

    “Intake of animal protein showed no clear association with total or cause-specific mortality.”
    • Also stated in: § Results · plain
      “Higher total and animal protein intake was not associated with risk of overall mortality or cause-specific mortality (Table 2).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Total protein intake was not associated with overall or cause-specific mortality in this cohort.

    “Higher total and animal protein intake was not associated with risk of overall mortality or cause-specific mortality (Table 2).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Plant protein intake was linked to lower all-cause and cardiovascular disease mortality.

    “We found that plant protein intake was associated with lower risk of all-cause and CVD-related mortality.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The difference may also be explained by the main animal protein source: red and processed meat in the US study versus fish in our study.

    “The discrepancy might also be attributable to a difference in the main dietary source of animal protein, which was red and processed meat in the US study vs fish intake in the present study.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Interpretationown data

    Very low plant protein intake or deprivation might also increase mortality risk.

    “Interestingly, the greatest change in HRs in our study was between the first and second quintiles, which might suggest the possibility that very low intake or deprivation of plant protein might also be a risk for increased mortality.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Plant protein intake, but not animal protein intake, has been linked to favorable changes in blood pressure, waist circumference, and weight.

    “Indeed, intake of plant protein, but not animal protein, has been associated with favorable changes in blood pressure level, waist circumference, and weight.[25][26][27][28]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25][26][27][28]

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In postmenopausal women in Iowa, a higher intake of vegetable protein was linked to a 30% lower risk of death from coronary heart disease compared with a lower intake.

    “In a study of postmenopausal women in Iowa, 16 higher vegetable protein intake was associated with 30% lower risk of coronary heart disease mortality compared with lower vegetable protein intake.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [16] source

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  • Classified as probably not a substantial claim.

    Premisecitation

    In the US study, higher animal protein intake was positively associated with cardiovascular disease mortality.

    “This lack of association with animal protein does not accord with the above-mentioned US study, 17 wherein higher animal protein intake was positively associated with CVD-related mortality.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [17] source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In that same pooled analysis, each 3% increase in energy from plant protein was linked to a 12% lower risk of death from cardiovascular disease.

    “More recently, in a combined analysis of the Nurses' Health Study and the Health Professionals Follow-up Study, Song et al 17 revealed a similar inverse association with plant protein intake, wherein a 3% increase in energy from plant protein was associated with 10% lower risk of overall mortality and 12% lower risk of cardiovascular mortality.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Song et al 17

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The study had a large sample size.

    “Strengths of this study include its population-based design, prospective collection of lifestyle data, use of validated food frequency questionnaires, large sample size, and long followup.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Short-term trials showed that high-protein diets led to more weight loss, more fat mass loss, and better lean mass preservation than normal-protein diets.

    “In short-term trials, consumption of high-protein diets have been shown to produce greater weight loss, loss of fat mass, and preservation of lean mass compared with the consumption of normal-protein diets.5,6”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [5] source

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  • May combine two claims.

    Premisecitation

    Two other US studies failed to confirm a positive overall mortality link with animal protein, but they did find lower CVD mortality risk with more plant protein.

    “Two other US studies 16,17 did not replicate this positive association of overall mortality with animal protein but did report a reduced risk of CVD-related mortality associated with higher plant protein.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [16] source

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    • cites [17] source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Another study found that replacing meat protein with nonmeat protein was favorably linked to fasting insulin levels and insulin resistance.

    “A recent systematic review 27 found that consumption of plant protein (soy protein with isoflavones) was more strongly linked to lower levels of total and low-density lipoprotein cholesterol than the consumption of animal protein, whereas another study 31 found that substitution of nonmeat protein for meat protein was favorably associated with fasting insulin levels and insulin resistance.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [31] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    A NHANES analysis found that greater protein intake was tied to a significantly higher risk of death from all causes.

    “An analysis using the US National Health and Nutrition Examination Survey (NHANES) reported a significant increase in the risk of death due to all causes associated with higher protein intake.15”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [15] source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Lifestyle data were collected prospectively.

    “Strengths of this study include its population-based design, prospective collection of lifestyle data, use of validated food frequency questionnaires, large sample size, and long followup.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Other evidence suggests that higher plant protein intake is linked to a null or lower risk of type 2 diabetes, while higher animal protein intake is linked to increased risk.

    “Other evidence suggests a null or even lower risk of type 2 diabetes associated with higher intake of plant protein vs increased risk associated with animal protein.32,33”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [32] source

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    • cites [33] source

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  • May combine two claims.

    Study design and conductcitation

    Dietary protein intake was estimated using a validated food frequency questionnaire, with reported validity and reproducibility correlation coefficients.

    “The dietary intake information estimated from the food frequency questionnaire was previously compared with dietary intake estimates from 14-or 28-day dietary records (validity) and with intake estimates computed from subsequent questionnaires administered 1 year apart (reproducibility) in a cohort subsample.”
    • Also stated in: § Participants · plain
      “Spearman correlation coefficients were 0.31 in men and 0.33 in women for validity and 0.57 in men and 0.54 in women for reproducibility.19,20”
    • Also stated in: § Participants · plain
      “Spearman correlation coefficients for validity for animal protein and plant protein were 0.21 and 0.59, respectively, in men and 0.26 and 0.49, respectively, in women.21 Corresponding values for reproducibility were 0.49 for animal protein and 0.60 for plant protein in men and 0.48 for animal protein and 0.58 for plant protein in women.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [19] source

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  • Classified as probably not a substantial claim.

    Premisecitation

    Prior ecological research found a positive link between total animal protein consumption and death from cardiovascular disease and cancer.

    “Earlier ecologic studies 13,14 reported a positive correlation between overall animal protein intake and mortality due to cardiovascular disease (CVD) and cancer.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [13] source

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    • cites [14] source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The study had a population-based design.

    “Strengths of this study include its population-based design, prospective collection of lifestyle data, use of validated food frequency questionnaires, large sample size, and long followup.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Multiple imputation for missing covariates produced hazard ratios similar to complete-case analysis.

    “Repetition of the above analysis by includ- ing observations with missing information for covariates using multiple imputation produced similar HRs to that of com- plete case analysis (eTable 2 in the Supplement).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    High-protein diets have also been associated with better cardiovascular risk profiles, such as blood pressure, blood lipids, and glucose regulation.

    “High-protein diets are also linked to improvements in cardiovascular risk factors, including blood pressure, blood lipid and lipoprotein profiles, and glycemic regulation.9,10”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [9] source

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    • cites [10] source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The study had long follow-up.

    “Strengths of this study include its population-based design, prospective collection of lifestyle data, use of validated food frequency questionnaires, large sample size, and long followup.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The study used validated food frequency questionnaires.

    “Strengths of this study include its population-based design, prospective collection of lifestyle data, use of validated food frequency questionnaires, large sample size, and long followup.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A recent systematic review found that plant protein (soy protein with isoflavones) was more strongly linked to lower total and low-density lipoprotein cholesterol than animal protein.

    “A recent systematic review 27 found that consumption of plant protein (soy protein with isoflavones) was more strongly linked to lower levels of total and low-density lipoprotein cholesterol than the consumption of animal protein, whereas another study 31 found that substitution of nonmeat protein for meat protein was favorably associated with fasting insulin levels and insulin resistance.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [27]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In a pooled analysis of the Nurses' Health Study and the Health Professionals Follow-up Study, each 3% increase in energy from plant protein was linked to a 10% lower risk of death from any cause.

    “More recently, in a combined analysis of the Nurses' Health Study and the Health Professionals Follow-up Study, Song et al 17 revealed a similar inverse association with plant protein intake, wherein a 3% increase in energy from plant protein was associated with 10% lower risk of overall mortality and 12% lower risk of cardiovascular mortality.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Song et al 17

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Animal and plant proteins differ in amino acid composition, and choosing one protein source over another also changes intake of other macronutrients, micronutrients, and polyphenols, which could produce different health effects.

    “Furthermore, among protein sources, proteins originating from animal and plant sources have different amino acid combinations, 11 and the choices of dietary protein source also necessarily influence other macronutrients, micronutrients, and polyphenols in the diet, 12 potentially leading to differential health effects.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [11] source

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    • cites [12] source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The validity correlation coefficient for protein intake was moderate to low.

    “The correlation coefficient for validity for protein intake was moderate to low.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Although participants with a history of chronic disease were excluded, subclinical disease might have changed dietary habits.

    “Although we excluded participants with a history of chronic diseases, the presence of subclinical diseases might have led to changes in dietary habits.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationnone given

    Plant protein intake may reflect healthy eating behavior.

    “Plant protein intake may represent a healthy eating behavior; although adjustment for several lifestyle factors showed little difference in the overall results, the possibility of residual confounding in the association between plant protein and mortality remains.”
    Quote in the paperNot a substantial claim
30 of 30

  • The authors state this as an assumption.

    The model treats protein intake as an isocaloric substitution, meaning its coefficient reflects replacing the same amount of energy from carbohydrates with protein.

    “The latter model assumes isocaloric substitution interpretation, wherein the coefficient for protein represents the substitution effect of an equal amount of energy from protein for carbohydrates.22,23”

  • The paper relies on this without support.

    Before this study, there were no published reports from an Asian population on this topic.

    “Moreover, no reports on this issue have yet appeared from an Asian population, despite the differences in dietary habits between Asian and western populations.”

  • The paper relies on this without support.

    It was unclear how long-term adherence to a high-protein diet affects health and mortality.

    “Despite these benefits, the health effects of adherence to high dietary protein intake on long-term health and mortality remain to be clarified.”

  • The paper relies on this without support.

    Eating more protein inevitably means eating less of other foods, typically carbohydrates, and cutting back on high-fiber carbohydrate foods could be harmful.

    “Importantly, high consumption of dietary protein is unavoidably linked to a decrease in other foods, usually carbohydrates, and a decrease in carbohydrate foods with high fiber and other micronutrients may have a negative effect.”

  • The paper relies on this without support.

    Japanese diets include more fish and soy than Western diets, so the mix of animal and plant protein sources may differ between the two.

    “The higher fish and soy product consumption in Japan than in western populations suggests that their sources of animal and plant proteins may differ.”
5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The Japan Public Health Center-Based Prospective Cohort Study found reduced overall and cancer- or cardiovascular disease-related mortality with a 3% energy substitution of plant protein for red meat protein.

    “whereas reduced risk of mortality overall and mortality related to cancer or CVD was associated with a 3% energy substitution of plant protein for red meat protein in the Japan Public Health Center-Based Prospective Cohort Study of 70 696 participants.13”

    From Association Between Plant and Animal Protein Intake and Overall and Cause-Specific Mortality (2020) · cites this paper as [13]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Conclusion overstates the cardiovascular finding for processed meat

    Minor

    The conclusion says replacing processed meat protein with plant protein was associated with lower CVD-related mortality. The results instead state that the cardiovascular estimate for that substitution was not significant.

1 of 1

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Authors
Budhathoki, S., Sawada, N., Iwasaki, M., Yamaji, T., Goto, A., Kotemori, A., Ishihara, J., Takachi, R., Charvat, H., Mizoue, T., Iso, H., Tsugane, S., & for the Japan Public Health Center–based Prospective Study Group
Affiliations
  • National Cancer Centre Japan (JP)
  • Azabu University (JP)
  • Nara Women's University (JP)
  • National Center for Global Health and Medicine (JP)
  • The University of Osaka (JP)
Corresponding author
Sawada, Norie
ORCID
Venue
JAMA Internal Medicine
Publisher
American Medical Association (AMA)
Published
2019-11-01
Volume
179
Issue
11
Pages
1509
ISSN
2168-6106 (ISSN-L)
DOI
10.1001/jamainternmed.2019.2806
PMC
PMC6714005
OpenAlex
W2970943766
Cited by
203
References
39
Citations by year
2026: 22 · 2025: 34 · 2024: 30 · 2023: 25 · 2022: 33 · 2021: 29 · 2020: 26 · 2019: 4
FWCI
21.05
Type
journal article
Language
en
Open access
Locations
  • JAMA Internal Medicine (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
  • Physical Sciences › Environmental Science › Ecology › Agriculture Sustainability and Environmental Impact
Keywords
plant protein intake, animal protein intake, dietary protein, all-cause mortality, cause-specific mortality, cancer mortality, cardiovascular mortality, middle-aged and older adults, dietary intake, mortality risk factors, cancer risk factors, cardiovascular risk factors, lifestyle risk factors, alcohol consumption, physical activity, body mass index
MeSH terms
Adult, Aged, Cardiovascular Diseases, Cause of Death, Diet, Feeding Behavior, Female, Follow-Up Studies, Humans, Japan, Male, Meat, Middle Aged, Neoplasms, Plant Proteins, Prospective Studies, Risk Factors, Time Factors, Survival Rate, Risk Assessment

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