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Breakfast Protein Quality and Muscle Strength in Japanese Older Adults: A Community-Based Longitudinal Study

  • Kaori Kinoshita
    Affiliations
    Department of Frailty Research, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
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  • Rei Otsuka
    Correspondence
    Address correspondence to Rei Otsuka, PhD, Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, 7-430 Morioka, Obu, Aichi 474-8511, Japan.
    Affiliations
    Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
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  • Yukiko Nishita
    Affiliations
    Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
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  • Chikako Tange
    Affiliations
    Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
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  • Makiko Tomida
    Affiliations
    Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
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  • Shu Zhang
    Affiliations
    Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
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  • Fujiko Ando
    Affiliations
    Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan

    Faculty of Health and Medical Sciences, Aichi Shukutoku University, Nagakute, Aichi, Japan
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  • Hiroshi Shimokata
    Affiliations
    Department of Epidemiology of Aging, Center for Gerontology and Social Science, Research Institute, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan

    Graduate School of Nutritional Sciences, Nagoya University of Arts and Sciences, Nissin, Aichi, Japan
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  • Hidenori Arai
    Affiliations
    National Center for Geriatrics and Gerontology, Obu, Aichi, Japan
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Open AccessPublished:January 07, 2022DOI:https://doi.org/10.1016/j.jamda.2021.11.037

      Abstract

      Objectives

      The amount of breakfast protein intake is important for maintaining muscle strength. However, the effect of breakfast protein quality (ie, bioavailability) remains unclear. We investigated the association between breakfast protein quality and the incidence of muscle weakness.

      Design

      Longitudinal study.

      Setting and Participants

      Healthy older adults age 60–83 years without stroke, arthritis, Parkinson disease, or muscle weakness at baseline (maximum follow-up period and participations were 9.2 years and 5 times, respectively).

      Methods

      Weakness was defined by the Asian Working Group for Sarcopenia 2019 criteria, using grip strength. Breakfast protein quality was evaluated using the protein digestibility–corrected amino acid score (PDCAAS), where higher scores represent higher quality, calculated from 3-day dietary records. Participants were classified according to sex-stratified tertiles of breakfast PDCAAS (ie, low to high groups). The association between PDCAAS and incident weakness was analyzed using the generalized estimating equation, after adjusting for sex, age, follow-up time, grip strength, body mass index, physical activity, cognition, education, smoking, economics, medical history, lunch and dinner PDCAASs, and energy and protein intake during 3 regular meals at baseline.

      Results

      Overall, 14.4% of the initial sample was excluded owing to a diagnosis of weakness-related diseases, and 58.3% (n = 701) had at least 1 follow-up measurement for inclusion in the analysis. The mean ± SD follow-up period was 6.9 ± 2.1 years; the cumulative number of participants was 3019, and 282 developed weakness. Using the low PDCAAS group as the reference, the adjusted odds ratios (95% CIs) for incident weakness in the middle and high PDCAAS groups were 0.71 (0.43–1.18) and 0.50 (0.29–0.86), respectively.

      Conclusions and Implications

      Higher breakfast protein quality was associated with a reduction in incident weakness in older adults, independent of protein intake. These findings may highlight the role of protein quality for muscle health in older adults.

      Keywords

      Maintaining functional ability is important for healthy aging; maintaining muscle strength is, therefore, essential. Grip strength is used worldwide as a measure of muscle strength.
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      and a decline in grip strength with age increases the risk of disability.
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      Daily dietary proteins supply amino acids required for muscle synthesis,
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      and their requirements are similar for all adults, regardless of age-related factors.
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      Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group.
      An epidemiologic study showed that high protein intake lowers the risk of death in older, but not young adults.
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      • et al.
      Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population.
      Given the health benefits, breakfast is important for longevity.
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      Meal Timing and Frequency: Implications for Cardiovascular Disease Prevention: A Scientific Statement From the American Heart Association.
      Infrequent breakfast consumption is associated with an increased risk of diabetes and cardiovascular disease (CVD).
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      • et al.
      Meal Timing and Frequency: Implications for Cardiovascular Disease Prevention: A Scientific Statement From the American Heart Association.
      As breakfast usually accounts for only 20%–25% of total daily intake,
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      it may be important to consume proteins with higher bioavailability (ie, higher quality proteins). However, the quality of protein varies depending on the food; while egg has a bioavailability of 118%, that of wheat is 42%.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      Maintaining muscle function is necessary for preventing adverse outcomes, including falls, disabilities, and death.
      • Cruz-Jentoft A.J.
      • Bahat G.
      • Bauer J.
      • et al.
      Sarcopenia: revised European consensus on definition and diagnosis.
      ,
      • Leong D.P.
      • Teo K.K.
      • Rangarajan S.
      • et al.
      Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study.
      ,
      • Ibrahim K.
      • May C.
      • Patel H.P.
      • et al.
      A feasibility study of implementing grip strength measurement into routine hospital practice (GRImP): study protocol.
      High protein intake at breakfast is associated with increased muscle synthesis and low frailty prevalence.
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      • Mettler J.A.
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      Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults.
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      Distribution but not amount of protein intake is associated with frailty: a cross-sectional investigation in the region of Nürnberg.
      • Yasuda J.
      • Tomita T.
      • Arimitsu T.
      • Fujita S.
      Evenly distributed protein intake over 3 meals augments resistance exercise-induced muscle hypertrophy in healthy young men.
      , The amount of protein intake at breakfast should be similar to that at lunch and dinner to promote optimal stimulation of muscle protein synthesis after all meals.
      • Bauer J.
      • Biolo G.
      • Cederholm T.
      • et al.
      Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group.
      ,
      • Breen L.
      • Phillips S.M.
      Skeletal muscle protein metabolism in the elderly: interventions to counteract the 'anabolic resistance' of ageing.
      A recent study suggests that higher protein intake at breakfast than at dinner is the most effective approach for promoting skeletal muscle synthesis
      • Aoyama S.
      • Kim H.K.
      • Hirooka R.
      • et al.
      Distribution of dietary protein intake in daily meals influences skeletal muscle hypertrophy via the muscle clock.
      ; however, protein intake reduces with aging.
      • Bauer J.
      • Biolo G.
      • Cederholm T.
      • et al.
      Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group.
      As bioavailability of dietary protein is based on protein quality,
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      ,
      World Health Organization
      Protein and amino acid requirements in human nutrition: report of a joint WHO/FAO/UNU expert consultation.
      ,
      Food and Agriculture Organization of the United Nations
      Dietary protein quality evaluation in human nutrition: report of an FAO expert consultation.
      considering quality is important for older people, especially at breakfast. We hypothesized that breakfast with a higher quality of protein could prevent muscle strength decline. To our knowledge, no study has investigated the association between breakfast protein quality and muscle strength in community-dwelling older adults. We, therefore, aimed to investigate the longitudinal association between breakfast protein quality and incidence of low grip strength among older people.

      Methods

       Study Design and Participants

      This study was derived from the National Institute for Longevity Sciences–Longitudinal Study of Aging (NILS-LSA), which was conducted using stratified random sampling by age and sex among community dwellers from Obu City and Higashiura Town in Aichi Prefecture, Japan.
      • Shimokata H.
      • Ando F.
      • Niino N.
      A new comprehensive study on aging—the National Institute for Longevity Sciences, Longitudinal Study of Aging (NILS-LSA).
      The NILS-LSA has been conducted every 2 years since 1997; participants were 40–79 years old at their first participation. Herein, the third survey of the NILS-LSA (between May 2002 and May 2004, n = 2378) was set as the baseline, because of the British bovine spongiform encephalopathy outbreak that occurred worldwide (including Japan) during the second NILS-LSA survey (between April 2000 and May 2002).
      • Matthews D.
      BSE: a global update.
      The bovine spongiform encephalopathy outbreak led to decreased meat consumption, the main source of amino acids.
      In this study, participants age ≥60 years were considered older adults. At baseline, there were 1202 participants age ≥60 years; 1006 participated in the follow-up survey (4th to 7th survey, up to July 2012) at least once. We excluded those with diseases influencing grip strength (ie, stroke, arthritis, and Parkinson disease, n = 173), without grip strength assessment (n = 9), with low grip strength (as defined later, n = 53), without dietary records (n = 35), who skipped at least 1 of the 3 regular meals (ie, 0 kcal/meal, n = 4), and who had missing covariate data (n = 31); data from 701 participants were finally analyzed (age range, 60-83 years; male, n = 375, 53.5%).
      This study was conducted according to the guidelines of the Declaration of Helsinki, and all procedures were approved by the relevant Ethics Committee of Human Research of the National Center for Geriatrics and Gerontology, Japan (No. 1377). Written informed consent was obtained from all the NILS-LSA participants.

       Muscle Strength Assessment

      To assess muscle strength, hand grip strength (kg) was measured using a handgrip dynamometer (Takei Scientific Instruments) at baseline, and during each follow-up survey.
      • Kozakai R.
      • Tsuzuku S.
      • Yabe K.
      • et al.
      Age-related changes in gait velocity and leg extension power in middle-aged and elderly people.
      Grip strength was measured twice for each hand in the standing position; the highest measurement was used for analysis. Low grip strength was defined based on the Asian Working Group for Sarcopenia 2019 criteria, as follows: <28 kg for male and <18 kg for female individuals.
      • Chen L.K.
      • Woo J.
      • Assantachai P.
      • et al.
      Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment.

       Dietary Breakfast Assessment

      Breakfast intake was assessed at baseline using a 3-day dietary record, including intake data from 2 weekdays and 1 weekend day; sheets for breakfast intake were separate sheets from those used for lunch and dinner. Participants weighed each food item using a kitchen scale before cooking (Sekisui Jushi) and photographed their meals using a disposable camera before and after eating (Fuji Film). Dietitians used these photographs to estimate complete food consumption for missing data from the dietary records and telephoned the participants to resolve any discrepancies or obtain further information. The average dietary intake for breakfast, lunch, and dinner over 3 days was calculated by the dietitians based on the Japanese Standard Tables of Food Composition.
      Ministry of Education, Culture, Sports, Science and Technology Japan
      Standard tables of food composition in Japan, v7.

       Protein Quality Assessment—Calculation of the PDCAAS

      Dietary protein quality (ie, the nutritional value of the amino acids) was evaluated using the protein digestibility–corrected amino acid score (PDCAAS),
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      ,
      World Health Organization
      Protein and amino acid requirements in human nutrition: report of a joint WHO/FAO/UNU expert consultation.
      ,
      Food and Agriculture Organization of the United Nations
      Dietary protein quality evaluation in human nutrition: report of an FAO expert consultation.
      which is directly proportional to protein bioavailability and quality.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      The PDCAAS was calculated for each meal (ie, breakfast, lunch, and dinner) and total intake, based on the guidelines of the Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO)/United Nations University (UNU) expert consultation, as follows: PDCAAS = digestibility × amino acid score.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      To calculate the amino acid score, we referred to the 9 essential amino acid requirement patterns, as proposed by the FAO/WHO/UNU.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      ,
      World Health Organization
      Energy and protein requirements: report of a joint FAO/WHO/UNU expert consultation.
      The ratios of these 9 amino acids in the meal are calculated by comparing their requirement patterns; the lowest ratio is defined as the amino acid score.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      The formula is as follows: amino acid score (%) = amount of amino acid (mg) in 1 g protein/amount of amino acid (mg) in requirement pattern × 100.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      If the score exceeds 100%, the amino acid score is rounded down to 100%.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      As diets generally comprise various foods, the WHO/FAO/UNU report indicates the true protein digestibility of some mixed diets for calculating the PDCAAS; it was 96%, 88%, and 96% for the American, Filipino, and Chinese diets, respectively.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      ,
      World Health Organization
      Protein and amino acid requirements in human nutrition: report of a joint WHO/FAO/UNU expert consultation.
      However, the digestibility of the Japanese mixed diet has not been shown in the WHO/FAO/UNU report.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      ,
      World Health Organization
      Protein and amino acid requirements in human nutrition: report of a joint WHO/FAO/UNU expert consultation.
      We considered 90% digestibility for the present study, based on a previous Japanese study.
      • Kaneko K.
      • Ishikawa K.
      • Setoguchi K.
      • et al.
      Utilization and requirement of dietary protein taking into account the dermal and miscellaneous nitrogen losses in Japanese women.

       Other Measurements

      The body mass index (kg/m2) was calculated using anthropometric data. The trained staff measured height and weight. Daily total physical activity, measured in metabolic equivalent of tasks (MET-min/d), was assessed during interviews by the staff, using questionnaires regarding activity intensity and frequency over the year.
      • Iwai N.
      • Yoshiike N.
      • Saitoh S.
      • et al.
      Leisure-time physical activity and related lifestyle characteristics among middle-aged Japanese.
      Cognitive function was assessed by a trained psychologist or psychology graduate students, using the Japanese version of the Mini-Mental State Examination.
      • Mori E.
      • Mitani Y.
      • Yamadori A.
      Usefulness of a Japanese version of the Mini-Mental State Test in neurological patients.
      ,
      • Folstein M.F.
      • Folstein S.E.
      • McHugh P.R.
      “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician.
      Educational years, smoking status, household annual income, and medical history (ie, hypertension, dyslipidemia, diabetes mellitus, and ischemic heart disease) were assessed using self-reported questionnaires. The responses in self-reported questionnaires were confirmed by medical doctors and trained staff. These data were assessed at baseline and used as covariates.

       Statistical Analyses

      All statistical analyses were performed using the Statistical Analysis System v 9.3 (SAS Institute, Inc). A 2-sided P value of <.05 was considered statistically significant. Continuous variables are presented as means ± SD, and categorical variables are presented as numbers and percentages (%). To analyze the association between breakfast PDCAAS and incidence of low grip strength, we classified participants according to sex-stratified tertiles (T1 to T3) of breakfast PDCAAS. Groups T1, T2, and T3 were defined as the low-, middle-, and high-PDCAAS groups, respectively; the baseline characteristics of the participants in these groups were compared using the general linear model for continuous variables and the χ2 test for categorical variables. Food consumption (g/100 kcal) at breakfast was compared between the 3 PDCAAS groups using the general linear model.
      Association between PDCAAS and incident low grip strength was analyzed using the generalized estimating equation (GEE),
      • Liang K.-Y.
      • Zenger S.L.
      Longitudinal data analysis using generalized linear models.
      which assumes that data is missing completely at random, and can handle the unmeasured dependence of repeated observations within participants. It averages overall subject parameters, and provides a good estimate of within-subject covariance structure. It uses moment assumptions to iteratively select the optimal β to evaluate the relationship between explanatory variables and outcomes, instead of assumption of data generation from a certain distribution. In epidemiologic studies, repeated data is used as it controls for time-invariant unobservable differences between individuals; thus, the GEE is commonly used. Here, the GEE analysis was performed using the GENMOD procedure in SAS. The odds ratios (ORs) and 95% CIs of the middle and high PDCAAS groups for low grip strength were estimated using the GEE, considering the low PDCAAS group as reference. We adjusted for sex, age (year), follow-up time (year), and grip strength (kg) at baseline in model 1. In model 2, body mass index (kg/m2), total physical activity (MET-min/d), Mini-Mental State Examination (score), education (years), smoking status (current or not), household annual income (<3.50 million yen/year, 3.50–6.49 million yen/year, or ≥ 6.50 million yen/year), medical history (ie, hypertension, dyslipidemia, diabetes mellitus, and ischemic heart disease), and PDCAAS values for lunch and dinner (low to high at each meal) at baseline were added to model 1. In model 3, energy (kcal/meal) and protein (g/meal) intake at the 3 regular meals at baseline were added to model 2.
      Four types of supplemental analyses were performed. First, to investigate the effect of total daily intake, the GEE was used to evaluate the association between the PDCAAS for total daily intake and low grip strength. Second, to clarify the impact of the PDCAAS for breakfast in participants with insufficient protein intake, its association with low grip strength was evaluated using the GEE, after excluding participants with sufficient protein intake at breakfast (sufficiency was defined as ≥25 g/meal based on recommendations).
      • Bauer J.
      • Biolo G.
      • Cederholm T.
      • et al.
      Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group.
      Furthermore, to compare the incidence of low grip strength between individuals having high protein intake with low PDCAAS and low protein intake with high PDCAAS, participants were classified into 6 groups by combining median breakfast protein intake (ie, 20 g) and low-to-high PDCAAS. Using the high protein intake with low PDCAAS group as reference, the OR for the incidence of low grip strength was estimated. Third, to exclude selection bias, we compared characteristics between participants included and excluded. Fourth, to consider the effect of newly developed diseases that could influence grip strength during follow-up, we excluded participants who developed stroke, arthritis, and Parkinson disease during follow-up. The ORs and 95% CIs of the middle and high PDCAAS groups for low grip strength were estimated using the low PDCAAS group as the reference.

      Results

      Table 1 shows the number of participants in each survey, from baseline to follow-up. The mean ± SD follow-up period and number of follow-up visits were 6.9 ± 2.1 years and 3.2 ± 1.1 times, respectively (Supplementary Table 1 shows a comparison of baseline characteristics between participants included in this study and those excluded). Table 2 shows the baseline characteristics of the low, middle, and high PDCAAS groups. Regarding nutritional intake at breakfast, although the protein/energy and fat/energy ratios significantly increased from the low to the high PDCAAS groups, the carbohydrate/energy ratio decreased significantly (P < .001, for both, group differences and trends). Figure 1 shows the food consumption at breakfast in the low to high PDCAAS groups. The consumption of cereal grains, sugars and sweeteners, and fats and oils was significantly higher in the low PDCAAS group; however, the consumption of beans and legumes, fish and seafood, eggs, and milk and dairy products was significantly lower in this group.
      Table 1Number of Participants at Each Survey from Baseline to Follow-Up
      Total n%Low Grip Strength
      Assessed using the AWGS 2019 criteria: grip strength <28 kg in male and <18 kg in female participants.
      n at Each Survey%
      Percentage for incidence of low grip strength in each survey.
      Third survey (baseline)70110000
      Fourth survey68497.6578.3
      Fifth survey61187.26310.3
      Sixth survey54377.58315.3
      Seventh survey48068.57916.5
      Cumulative number of participants3019-282-
      MeanSD
      Follow-up period (y)6.92.1
      Number of follow-ups (range: 1–4)3.21.1
      AWGS, Asian Working Group for Sarcopenia.
      Assessed using the AWGS 2019 criteria: grip strength <28 kg in male and <18 kg in female participants.
      Percentage for incidence of low grip strength in each survey.
      Table 2Baseline Characteristics of the Participants in Each Group According to Their Breakfast PDCAAS
      PDCAASP Value
      Low (n = 238)Middle (n = 234)High (n = 229)Diff.Trend
      Ranges
      Male28.2‒82.0382.13‒91.6091.69‒100.00
      Female12.76‒80.1780.21‒90.4460.90‒100.00
      Male, n (%)128 (53.8)125 (53.4)122 (53.3).994
      Age, y68.3 ± 5.968.5 ± 5.568.0 ± 5.7.708.596
      BMI, kg/m222.8 ± 2.722.9 ± 2.623.1 ± 2.8.566.311
      MMSE, range: 0–3027.9 ± 1.928.1 ± 1.628.0 ± 1.9.417.440
      Grip strength, kg
       Male38.0 ± 5.537.6 ± 5.638.8 ± 6.1.244.249
       Female23.8 ± 3.524.5 ± 3.723.7 ± 3.3.188.869
      Physical activity, MET-min/d1909.3 ± 231.11885.1 ± 149.01892.3 ± 162.4.345.322
      Education, y11.1 ± 2.611.2 ± 2.511.7 ± 2.7.044.019
      Hypertension, n (%)74 (31.1)89 (38.0)84 (36.7).246
      Dyslipidemia, n (%)43 (18.1)57 (24.4)49 (21.4).247
      Diabetes mellitus, n (%)20 (8.4)22 (9.4)27 (11.8).453
      Ischemic heart disease, n (%)22 (9.2)17 (7.3)20 (8.7).725
      Current smoker, n (%)36 (15.1)38 (16.2)25 (10.9).223
      Household annual income, n (%)
       <3.50 million yen
      3.50 million yen = 31804.6 US dollars at July 2021.
      82 (34.5)61 (26.1)74 (32.3).133
       3.50–6.49 million yen84 (35.3)98 (41.9)98 (42.8)
       ≥6.50 million yen72 (30.3)75 (32.1)57 (24.9)
      Nutritional intake
       Breakfast
      Energy, kcal/meal482.1 ± 151.4521.9 ± 121.9561.1 ± 144.1<.001<.001
      Protein, g/meal16.7 ± 6.420.6 ± 5.724.0 ± 7.0<.001<.001
      Protein/energy ratio, %13.7 ± 2.715.8 ± 2.617.1 ± 2.7<.001<.001
      Fat, g/meal12.2 ± 7.613.8 ± 6.216.1 ± 6.6<.001<.001
      Fat/energy ratio, %9.8 ± 4.510.5 ± 4.011.4 ± 3.4<.001<.001
      Carbohydrate, g/meal76.3 ± 24.778.5 ± 21.879.7 ± 23.0.287.120
      Carbohydrate/energy ratio, %64.1 ± 11.060.2 ± 9.656.9 ± 8.5<.001<.001
       Lunch
      Energy, kcal/meal602.8 ± 154.4573.1 ± 135.5589.9 ± 132.0.073.324
      Protein, g/meal22.6 ± 7.221.8 ± 6.623.0 ± 6.7.199.556
      Protein/energy ratio, %15.0 ± 2.915.3 ± 3.115.6 ± 3.2.088.028
      Fat, g/meal14.9 ± 5.913.8 ± 6.215.1 ± 6.3.041.712
      Fat/energy ratio, %9.8 ± 2.89.4 ± 3.310.2 ± 3.3.050.252
      Carbohydrate, g/meal91.6 ± 24.787.4 ± 21.587.5 ± 21.4.075.056
      Carbohydrate/energy ratio, %61.1 ± 7.361.5 ± 8.559.7 ± 8.6.040.066
       Dinner
      Energy, kcal/meal746.9 ± 211.8738.8 ± 186.9739.7 ± 195.4.887.693
      Protein, g/meal32.1 ± 9.932.6 ± 9.232.9 ± 9.4.645.351
      Protein/energy ratio, %17.4 ± 3.717.9 ± 3.618.0 ± 3.1.158.073
      Fat, g/meal19.5 ± 8.019.5 ± 7.319.7 ± 7.5.943.761
      Fat/energy ratio, %10.3 ± 2.910.6 ± 3.010.6 ± 2.8.520.304
      Carbohydrate, g/meal96.6 ± 25.892.9 ± 24.592.2 ± 23.4.116.053
      Carbohydrate/energy ratio, %53.0 ± 9.751.1 ± 9.651.1 ± 10.2.042.027
      PDCAAS
       Lunch74.7 ± 16.075.5 ± 15.776.8 ± 14.4.315.132
       Dinner82.6 ± 11.383.7 ± 11.384.9 ± 10.4.084.026
      BMI, body mass index; MMSE, Mini‒Mental State Examination; MET, metabolic equivalents.
      Data are presented as means ± SD or n (%). P values were obtained using the χ2 test for categorical variables and the general linear model for continuous variables.
      3.50 million yen = 31804.6 US dollars at July 2021.
      Figure thumbnail gr1
      Fig. 1Food consumption at breakfast for the groups stratified according to breakfast PDCAAS. The graphs illustrate the mean and standard error of food consumption (g/100 kcal) at breakfast in the low, middle, and high PDCAAS groups. The differences and trends of the groups were analyzed using the general linear model. ∗∗P <.001 for both difference and trend, ∗P <.05 for both difference and trend. Abbreviation: PDCAAS, protein digestibility‒corrected amino acid score.
      Table 3 shows the multivariable-adjusted association between breakfast PDCAAS and low grip strength over 8 years. In all models, the adjusted OR for low grip strength was significantly lower in the high than in the low PDCAAS group. This association remained when participants with newly developed stroke, arthritis, and Parkinson disease during follow-up were further excluded (Supplementary Table 2). On supplemental analysis, there was no significant association between the PDCAAS for lunch, dinner, and total daily intake, and low grip strength (Supplementary Table 3). In addition, the analyses aimed at clarifying the impact of the PDCAAS in participants with an insufficient protein intake; when 166 participants with sufficient protein intake at breakfast were excluded, the adjusted OR (95% CI) of the high PDCAAS group for low grip strength was 0.36 (0.19–0.70). On considering the group with high protein intake and low PDCAAS as the reference while comparing incidence of low grip strength, the OR (95% CI) of the group with low protein and high PDCAAS was estimated at 0.35 (0.14–0.91).
      Table 3Multivariable-Adjusted Association between Breakfast PDCAAS and Low Grip Strength over 8 Years
      PDCAASModel 1Model 2Model 3
      OR95% CIP ValueOR95% CIP ValueOR95% CIP Value
      LowRefRefRef
      Middle0.710.45–1.12.1430.740.46–1.19.2130.710.43–1.18.182
      High0.570.35–0.93.0260.560.34–0.94.0280.500.29–0.86.012
      BMI, body mass index; MET, metabolic equivalents; MMSE, Mini-Mental State Examination; Ref, reference.
      ORs and 95% CIs were estimated using the generalized estimating equations.
      Model 1: adjusted for sex, age (y), follow-up period (y), and grip strength (kg) at baseline.
      Model 2: adjusted for BMI (kg/m2), total physical activity (MET-min/d), MMSE (score), education (y), smoking status (current or not), household annual income (<3.50 million yen/3.50–6.49 million yen/≥6.50 million yen), history of hypertension, dyslipidemia, diabetes mellitus, and ischemic heart disease, and PDCAAS for lunch and dinner (low/middle/high, respectively) in addition to the variables in model 1.
      Model 3: adjusted for energy (kcal/meal) and protein (g/meal) intake at 3 regular meals in addition to the variables in model 2.

      Discussion

      The importance of breakfast has been acknowledged for decades.
      • Kaplan G.A.
      • Seeman T.E.
      • Cohen R.D.
      • et al.
      Mortality among the elderly in the Alameda County Study: behavioral and demographic risk factors.
      The contribution of this study is that it demonstrates the importance of protein intake in muscle health; protein appears to be a key element of the contribution of breakfast toward muscular health and function, which is increasingly being recognized as an important component of healthy aging. To our knowledge, this is the first longitudinal epidemiologic study to investigate the association between the PDCAAS (ie, protein quality) for breakfast and incidence of low grip strength in community-dwelling older adults. The results of this study showed that the OR of the high-PDCAAS group for incidence of low grip strength was 50% lower than that of the low-PDCAAS group, after adjusting for covariates including baseline grip strength, energy and protein intake at 3 regular meals, and the PDCAAS for lunch and dinner. There was no significant association between grip strength and the PDCAAS for the total daily intake, lunch, or dinner. These findings suggest that a diet containing good quality, (ie, more bioavailable, protein at breakfast is important for maintaining muscle strength in older adults).
      Breakfast has an important role in preventing CVD and diabetes, which lead to muscle weakness or inhibition of skeletal muscle synthesis. Infrequent breakfast consumption is associated with elevated hemoglobin A1c, higher fasting plasma glucose, all-day postprandial hyperglycemia, increased serum cholesterol, and higher risks of developing type 2 diabetes mellitus and CVD.
      • Reutrakul S.
      • Hood M.M.
      • Crowley S.J.
      • et al.
      The relationship between breakfast skipping, chronotype, and glycemic control in type 2 diabetes.
      • Kollannoor-Samuel G.
      • Chhabra J.
      • Fernandez M.L.
      • et al.
      Determinants of fasting plasma glucose and glycosylated hemoglobin among low income Latinos with poorly controlled type 2 diabetes.
      • Bi H.
      • Gan Y.
      • Yang C.
      • et al.
      Breakfast skipping and the risk of type 2 diabetes: a meta-analysis of observational studies.
      • Farshchi H.R.
      • Taylor M.A.
      • Macdonald I.A.
      Deleterious effects of omitting breakfast on insulin sensitivity and fasting lipid profiles in healthy lean women.
      • Kubota Y.
      • Iso H.
      • Sawada N.
      • Tsugane S.
      Association of breakfast intake with incident stroke and coronary heart disease: the Japan public health center-based study.
      A high protein breakfast induces good muscle synthesis.
      • Mamerow M.M.
      • Mettler J.A.
      • English K.L.
      • et al.
      Dietary protein distribution positively influences 24-h muscle protein synthesis in healthy adults.
      ,
      • Yasuda J.
      • Tomita T.
      • Arimitsu T.
      • Fujita S.
      Evenly distributed protein intake over 3 meals augments resistance exercise-induced muscle hypertrophy in healthy young men.
      ,
      • Aoyama S.
      • Kim H.K.
      • Hirooka R.
      • et al.
      Distribution of dietary protein intake in daily meals influences skeletal muscle hypertrophy via the muscle clock.
      Thus, breakfast may have great value in healthy aging. Although it is recommended that older people consume more protein than younger adults,
      • Bauer J.
      • Biolo G.
      • Cederholm T.
      • et al.
      Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group.
      their dietary intake generally reduces as they age.
      • Bauer J.
      • Biolo G.
      • Cederholm T.
      • et al.
      Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group.
      ,
      • Morley J.E.
      Decreased food intake with aging.
      ,
      Ministry of Health, Labour and Welfare, Japan
      National Health and Nutrition Survey Report.
      Grain-derived protein makes a relatively large contribution to the total daily protein intake of the Japanese people. As grain protein is limited by lysine, it has a low PDCAAS.
      Food and Agriculture Organization of the United Nations
      Protein quality evaluation: report of the joint FAO/WHO expert consultation.
      Depending on the combination of foods in the diet, as in the case of a grain-based meal, there is a difference between the calculated total protein amount and the available protein (ie, the PDCAAS). Therefore, a diet with a high PDCAAS may be more important when dietary intake is low. Sex-stratified analysis showed significant association between high PDCAAS and the incidence of low grip strength only in female individuals (data not shown). This suggested sex-related differences; however, the power of analysis may have been small due to the small number of participants. This result may be attributed to lower protein intake in female individuals. In additional analyses that investigated the impact of the PDCAAS in participants with a low protein intake, the OR of the high PDCAAS group for low grip strength was lower than that before the exclusion of participants with sufficient protein intake at breakfast. In addition, individuals with low protein intake and high PDCAAS showed a negative association with the incidence of low grip strength, compared with those with high protein intake and low PDCAAS. This suggested the importance of protein quality over the amount of protein intake at breakfast. Food intake in older adults changes because of physical conditions or social problems/norms/trends, resulting in an unbalanced diet.
      • Iwasaki M.
      • Yoshihara A.
      • Ogawa H.
      • et al.
      Longitudinal association of dentition status with dietary intake in Japanese adults aged 75 to 80 years.
      • Fukutake M.
      • Ikebe K.
      • Okubo H.
      • et al.
      Relationship between oral stereognostic ability and dietary intake in older Japanese adults with complete dentures.
      • Nakamura H.
      • Nakamura M.
      • Okada E.
      • et al.
      Association of food access and neighbor relationships with diet and underweight among community-dwelling older Japanese.
      Accordingly, older people may easily have an unbalanced diet, such as a grain-based diet containing poor quality protein. Therefore, more focus should be directed to the protein quality of meals, especially breakfast, for healthy aging.
      This study had several limitations. First, we only assessed the PDCAAS at baseline. Dietary intake changes with time, because it is influenced by aging, which is associated with reduced chewing function, decreased economic status, and limited food access
      • Morley J.E.
      Undernutrition in older adults.
      ; thus, PDCAAS may also change with aging. However, these factors could not be considered, and we may have underestimated the PDCAAS. In addition, physical activity and cognitive function were also adjusted only at baseline; these functional changes may affect grip strength. Second, we assessed nutritional intake using a 3-day dietary record, which might not have reflected habitual intake. However, general nutritional assessments, such as the food frequency questionnaire, are unable to assess breakfast, lunch, and dinner separately. Therefore, dietary records are the best for assessing dietary intake at each meal. Epidemiologic data were used in this study, and the effect of breakfast protein intake could not be completely separated from that of total protein intake; the effect of breakfast protein quality on muscle strength therefore needs to be investigated in future intervention studies. Third, although the average grip strength in male and female individuals was close to the national average,
      Agency Sports Agency
      Results of physical fitness and athletic ability survey 2020.
      the enrolled participants in this study were healthier than those excluded. Although only Japanese individuals were included as participants, dietary habits may differ across races and regions; further studies including different countries, races, and regions are therefore needed.

      Conclusions and Implications

      Higher breakfast protein quality reduced the incidence of low muscle strength in community-dwelling older adults, independent of protein intake, suggesting that a diet with high amounts of bioavailable protein at breakfast is important for maintaining muscle strength in older people. Our findings may provide valuable insights on nutritional approaches for maintaining muscle strength and, therefore, quality of life in the older population.

      Acknowledgments

      We appreciate the cooperation and contributions of all participants and staff of the NILS-LSA. We thank Editage (www.editage.com) for English language editing. This study was supported in part by the Food Science Institute Foundation and Research Funding for Longevity Sciences from the National Center for Geriatrics and Gerontology , Japan (grant number 19-10 , 21-18 ). The sponsor had no role in the preparation of this article, including the design, methods, subject recruitment, data collection, and analysis.

      Supplementary Data

      Supplementary Table 1Comparison of Baseline Characteristics between Participants Included in this Study and Those Excluded
      ParticipantsP Value
      IncludedExcluded
      nn
      Male, n (%)701375 (53.5)501232 (46.3).014
      Age, y70168.3 ± 5.750172.3 ± 6.0<.001
      BMI, kg/m270122.9 ± 2.750123.0 ± 3.3.759
      MMSE, range: 0–3070128.0 ± 1.848627.2 ± 2.2<.001
      Grip strength, kg
       Male37538.1 ± 5.722434.0 ± 6.7<.001
       Female32624.0 ± 3.526021.2 ± 4.6<.001
      Physical activity, MET-min/d7011895.7 ± 184.85001864.6 ± 170.7.003
      Education, y70111.3 ± 2.649510.4 ± 2.5<.001
      Hypertension, n (%)701247 (35.2)494218 (44.1).002
      Dyslipidemia, n (%)701149 (21.3)491126 (25.7).076
      Diabetes mellitus, n (%)70169 (9.8)49567 (13.5).048
      Ischemic heart disease, n (%)70159 (8.4)49157 (11.6).067
      Current smoker, n (%)70199 (14.1)49566 (13.3).697
      Household annual income, n (%)701453
       ˂3.50 million yen
      3.50 million yen = 31,804.6 US dollars in July 2021.
      217 (31.0)193 (42.6)<.001
       3.50–6.49 million yen280 (39.9)154 (34.0)
       ≥6.50 million yen204 (29.1)106 (23.4)
      Nutritional intake
       Breakfast701427
      Energy, kcal/meal521.2 ± 143.2502.5 ± 146.7.036
      Protein, g/meal20.4 ± 7.019.6 ± 7.3.062
      Protein/energy ratio, %15.5 ± 3.015.5 ± 3.2.952
      Fat, g/meal14.0 ± 7.012.6 ± 6.5.001
      Fat/energy ratio, %10.6 ± 4.19.9 ± 3.9.007
      Carbohydrate, g/meal78.1 ± 23.277.3 ± 24.4.570
      Carbohydrate/energy ratio, %60.4 ± 10.261.8 ± 10.0.025
       Lunch701427
      Energy, kcal/meal588.7 ± 141.5534.6 ± 153.0<.001
      Protein, g/meal22.5 ± 6.820.3 ± 6.8<.001
      Protein/energy ratio, %15.3 ± 3.115.3 ± 3.3.961
      Fat, g/meal14.6 ± 6.213.3 ± 6.4.001
      Fat/energy ratio, %9.8 ± 3.29.8 ± 3.3.883
      Carbohydrate, g/meal88.8 ± 22.781.3 ± 25.1<.001
      Carbohydrate/energy ratio, %60.8 ± 8.261.1 ± 8.5.498
       Dinner701427
      Energy, kcal/meal741.8 ± 198.2687.0 ± 196.3<.001
      Protein, g/meal32.5 ± 9.529.6 ± 9.3<.001
      Protein/energy ratio, %17.8 ± 3.517.4 ± 3.6.157
      Fat, g/meal19.6 ± 7.617.9 ± 7.5.001
      Fat/energy ratio, %10.5 ± 2.910.4 ± 3.1.469
      Carbohydrate, g/meal93.9 ± 24.691.4 ± 26.0.101
      Carbohydrate/energy ratio, %51.7 ± 9.954.1 ± 10.0<.001
      PDCAAS701427
       Breakfast83.4 ± 13.681.4 ± 15.4.024
       Lunch75.6 ± 15.475.1 ± 17.1.573
       Dinner83.7 ± 11.182.9 ± 11.5.259
      BMI, body mass index; MMSE, Mini-Mental State Examination; MET, metabolic equivalents.
      Analyses were performed using the χ2 test for proportion variables and t-test for continuous variables.
      Data are presented as means ± SD or n (%).
      P values were obtained using the χ2 test for categorical variables and the t‒test for continuous variables.
      3.50 million yen = 31,804.6 US dollars in July 2021.
      Supplementary Table 2Multivariable-Adjusted Association of Breakfast PDCAAS for Risk of Low Grip Strength over 8 Years, when Participants with Newly Developed Stroke, Arthritis, and Parkinson Disease during Follow-Up were Further Excluded (n = 452)
      Model 1Model 2Model 3
      OR95 % CIP ValueOR95 % CIP ValueOR95 % CIP Value
      LowRefRefRef
      Middle0.710.44–1.16.1710.740.44–1.24.2590.700.40–1.22.208
      High0.580.35–0.96.0340.570.34–0.97.0380.500.28–0.88.017
      BMI, body mass index; MET, metabolic equivalents; MMSE, Mini-Mental State Examination. Ref, reference.
      ORs and 95% CIs were estimated using the generalized estimating equations.
      Model 1: adjusted for sex, age (y), follow-up period (y), and grip strength (kg) at baseline.
      Model 2: adjusted for BMI (kg/m2), total physical activity (MET-min/d), MMSE (score), education (y), smoking status (current or not), household annual income (<3.50 million yen/3.50–6.49 million yen/≥6.50 million yen), history of hypertension, dyslipidemia, diabetes mellitus, and ischemic heart disease, and PDCAAS for lunch and dinner (low/middle/high, respectively) in addition to the variables in model 1.
      Model 3: adjusted for energy (kcal/meal) and protein (g/meal) intake at 3 regular meals in addition to the variables in model 2.
      Supplementary Table 3Multivariable-Adjusted Association of the PDCAAS for Lunch, Dinner, and Total Daily Intake with Low Grip Strength over 8 Years
      Model 1Model 2Model 3
      OR95 % CIP ValueOR95 % CIP ValueOR95 % CIP Value
      Lunch PDCAAS
       LowRefRefRef
       Middle0.960.60–1.64.8800.940.58–1.62.8000.920.56–1.53.756
       High0.830.50–1.36.4570.820.49–1.38.4480.810.48–1.35.419
      Dinner PDCAAS
       LowRefRefRef
       Middle1.010.62–1.66.9621.040.61–1.70.8911.070.64–1.79.788
       High0.850.53–1.38.5100.860.53–1.37.5270.890.54–1.47.654
      Daily total PDCAAS
       LowRefRefRef
       Middle0.700.41–1.12.1590.720.42–1.15.1870.730.44–1.21.221
       High0.700.45–1.11.1220.670.42–1.08.0990.680.42–1.11.121
      BMI, body mass index; MET, metabolic equivalents; MMSE, Mini-Mental State Examination; Ref, reference.
      ORs and 95% CIs were estimated using the generalized estimating equations.
      Model 1: adjusted for sex, age (y), follow‒up period (y), and grip strength (kg) at baseline.
      Model 2: adjusted for BMI (kg/m2), total physical activity (MET‒min/d), MMSE (score), education (y), smoking status (current or not), household annual income (<3.50 million yen/3.50–6.49 million yen/≥6.50 million yen), history of hypertension, dyslipidemia, diabetes mellitus, and ischemic heart disease, and PDCAAS of other meals (low/middle/high, respectively) in addition to the variables in model 1.
      Model 3: adjusted for energy (kcal/meal) and protein (g/meal) intake at 3 regular meals in addition to the variables in model 2.

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