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Differences in Nutrient Intake and Biochemical Nutrient Status Between Sarcopenic and Nonsarcopenic Older Adults—Results From the Maastricht Sarcopenia Study

Open AccessPublished:January 26, 2016DOI:https://doi.org/10.1016/j.jamda.2015.12.015

      Abstract

      Background

      There is growing evidence of a relationship between nutrients and muscle mass, strength, and physical performance. Although nutrition is seen as an important pillar of treating sarcopenia, data on the nutritional intake of sarcopenic older adults are limited.

      Objective

      To investigate potential nutritional gaps in the sarcopenic population, the present study compared nutrient intake and biochemical nutrient status between sarcopenic and nonsarcopenic older adults.

      Design

      The Maastricht Sarcopenia Study included 227 community-dwelling older adults (≥65 years) from Maastricht, 53 of whom were sarcopenic based on the European Working Group on Sarcopenia in Older People algorithm. Habitual dietary intake was assessed with a food frequency questionnaire and data on dietary supplement use were collected. In addition, serum 25-hydroxyvitamin D, magnesium and α-tocopherol/cholesterol, plasma homocysteine and red blood cell n-3, and n-6 fatty acids profiles were assessed. Nutrient intake and biochemical nutrient status of the sarcopenic groups were compared with those of the nonsarcopenic groups. The robustness of these results was tested with a multiple regression analysis, taking into account between-group differences in characteristics.

      Results

      Sarcopenic older adults had a 10%–18% lower intake of 5 nutrients (n-3 fatty acids, vitamin B6, folic acid, vitamin E, magnesium) compared with nonsarcopenic older adults (P < .05). When taking into account dietary supplement intake, a 19% difference remained for n-3 fatty acids intake (P = .005). For the 2 biochemical status markers, linoleic acid and homocysteine, a 7% and 27% difference was observed, respectively (P < .05). The higher homocysteine level confirmed the observed lower vitamin B intake in the sarcopenic group. Observed differences in eicosapentaenoic acid and 25-hydroxyvitamin D between the groups were related to differences in age and living situation.

      Conclusions

      Sarcopenic older adults differed in certain nutritional intakes and biochemical nutrient status compared with nonsarcopenic older adults. Dietary supplement intake reduced the gap for some of these nutrients. Targeted nutritional intervention may therefore improve the nutritional intake and biochemical status of sarcopenic older adults.

      Keywords

      The average age of the world's population is rapidly increasing. The United Nations estimates that from 2015 to 2050, the proportion of adults aged 65 years and older will increase from 8% to 16%.

      United Nations, Department of economic and Social Affairs. World Population Prospects, the 2015 Revision. Available at: http://esa.un.org/unpd/wpp/. Accessed January 13, 2016.

      With the increased life expectancy, the number of older adults who are care-dependent will also rise, with an expected 4-fold increase by 2050.

      World Health Organization. Aging and life course, Facts about ageing. Available at: http://www.who.int/ageing/about/facts/en/. Accessed January 13, 2016.

      This emphasizes the importance of promoting healthy aging, adding quality to the years lived, and prolonging independence and aging in place.
      One of the suggested causes of the loss of independence is sarcopenia.
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      The geriatric syndrome sarcopenia is defined by the European Working Group on Sarcopenia in Older People, as the loss of muscle mass, strength, and physical performance.
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      Based on this definition, up to 29% of community-dwelling older adults are sarcopenic.
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      Prevalence of and interventions for sarcopenia in ageing adults: A systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS).
      Multiple risk factors are identified for sarcopenia, including among others, physical inactivity, chronic diseases, malnutrition, and low protein intake.
      • Cruz-Jentoft A.J.
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      Understanding sarcopenia as a geriatric syndrome.
      Nutrition, and nutrition in combination with exercise, are seen as important pillars for the treatment and prevention of sarcopenia, and an optimal quantity and quality of dietary protein and adequate 25-hydroxyvitamin D levels are recommended by international societies.
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      In addition to protein and vitamin D, the B vitamins, antioxidants and omega 3 fatty acids have been found to be related to sarcopenia determinants (ie, muscle mass, strength, and physical performance).
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      Only a few studies have assessed the dietary intake of sarcopenic older adults. The Korea National Health and Nutrition Examination Survey (KNHANES) cohort observed a lower energy, protein, carbohydrate, and calcium intake among sarcopenic older adults.
      • Park S.
      • Ham J.O.
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      • Seo M.H.
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      • Park S.E.
      • et al.
      The association between daily calcium intake and sarcopenia in older, nonobese Korean adults: The fourth Korea National Health and Nutrition Examination Survey (KNHANES IV) 2009.
      Adhering to a Mediterranean diet was found to be inversely associated with sarcopenia in Iranian older adults.
      • Hashemi R.
      • Motlagh A.D.
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      The aim of the present study was to provide a comprehensive assessment of the nutrient intake and biochemical nutrient status of Dutch sarcopenic older adults, and to investigate if there are nutritional differences compared with nonsarcopenic older adults. Data from the Maastricht Sarcopenia Study (MaSS)
      • Mijnarends D.M.
      • Schols J.M.
      • Meijers J.M.
      • et al.
      Instruments to assess sarcopenia and physical frailty in older people living in a community (care) setting: Similarities and discrepancies.
      were used.

      Methods

      MaSS (clinicaltrials.gov #NCT01820988) is a cross-sectional study in which the characteristics, prevalence, and consequences of sarcopenia were assessed in community settings. For details on the study design and sarcopenia assessment see the original publication by Mijnarends et al.
      • Mijnarends D.M.
      • Schols J.M.
      • Meijers J.M.
      • et al.
      Instruments to assess sarcopenia and physical frailty in older people living in a community (care) setting: Similarities and discrepancies.
      In short, participants were recruited from May 2013 to March 2014 in Maastricht, The Netherlands. Older adults (aged ≥65 years) were eligible if they were living at home with or without professional home care, or living in an assisted or residential living facility and had an understanding of the Dutch language. In total 247 home visits were performed. Assessments took place during a 1- to 2-hour home visit, following standardized protocols. Older adults were excluded if they had a cognitive function (Mini-Mental State Examination (MMSE))
      • 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.
      score <24, or if the assessments could not be performed (ie, prosthesis, pacemaker, wheelchair bound or bedridden, severe active rheumatoid arthritis, acute angina pectoris, poststroke status with evident lingering symptoms, diseases of the nervous system, or dementia). Informed consent was obtained from all participants, and ethics approval was obtained from the Medical Ethics Committee of the Academic Hospital Maastricht and Maastricht University.

      Participant Characteristics

      During the home visit, the following participant characteristics were obtained via a questionnaire: sex, age, living situation, cognitive function (MMSE), ethnicity, smoking status, alcohol use, and comorbidities (Charlson Comorbidity Index
      • Charlson M.E.
      • Pompei P.
      • Ales K.L.
      • et al.
      A new method of classifying prognostic comorbidity in longitudinal studies: Development and validation.
      ). Body height and weight were assessed with a stadiometer (SECA 213, Seca, Hamburg, Germany) and scale (SECA 877), respectively. Body mass index (BMI) was calculated as weight in kg divided by height in m2. In addition, information was collected on physical activity with the Minnesota Leisure Time Physical Activity Questionnaire.
      • Conway J.M.
      • Irwin M.L.
      • Ainsworth B.E.
      Estimating energy expenditure from the Minnesota Leisure Time Physical Activity and Tecumseh Occupational Activity questionnaires—A doubly labeled water validation.
      • Richardson M.T.
      • Leon A.S.
      • Jacobs D.R.
      • et al.
      Comprehensive evaluation of the Minnesota Leisure Time Physical Activity Questionnaire.

      Assessment of Sarcopenia

      Sarcopenia was assessed following the European Working Group on Sarcopenia in Older People algorithm,
      • Cruz-Jentoft A.J.
      • Baeyens J.P.
      • Bauer J.M.
      • et al.
      Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on sarcopenia in older people.
      including low muscle mass and poor grip strength and/or slow gait speed. In short, muscle mass was assessed after an overnight fast, by using bio-electrical impedance (Aker BIA 50 kHz; Akern Srl, Florence, Italy).
      • Kyle U.G.
      • Bosaeus I.
      • De Lorenzo A.D.
      • et al.
      Bioelectrical impedance analysis-part II: Utilization in clinical practice.
      Skeletal muscle mass (SMM) was calculated based on the Janssen equation.
      • Janssen I.
      • Heymsfield S.B.
      • Baumgartner R.N.
      • et al.
      Estimation of skeletal muscle mass by bioelectrical impedance analysis.
      Skeletal muscle index (SMI) was calculated as SMM divided by height in m2. Muscle mass was considered low if SMI ≤10.75 kg/m2 in men and ≤6.75 kg/m2 in women,
      • Janssen I.
      • Baumgartner R.N.
      • Ross R.
      • et al.
      Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women.
      thereby including both severe and moderate sarcopenia. Muscle strength was assessed with the Jamar hand-held dynamometer (Sammons Preston, Inc, Warrenville, IL). Three attempts were performed per hand, with alternating the left and right hand. The best attempt, the maximum grip strength, was used as the outcome measure. Muscle strength was defined as poor if <20 kg in women and <30 kg in men.
      • Lauretani F.
      • Russo C.R.
      • Bandinelli S.
      • et al.
      Age-associated changes in skeletal muscles and their effect on mobility: An operational diagnosis of sarcopenia.
      Gait speed was measured during a 4-meter walk test and considered slow if ≤0.8 m/s.
      • Cruz-Jentoft A.J.
      • Baeyens J.P.
      • Bauer J.M.
      • et al.
      Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on sarcopenia in older people.
      • Lauretani F.
      • Russo C.R.
      • Bandinelli S.
      • et al.
      Age-associated changes in skeletal muscles and their effect on mobility: An operational diagnosis of sarcopenia.
      • Guralnik J.M.
      • Simonsick E.M.
      • Ferrucci L.
      • et al.
      A short physical performance battery assessing lower extremity function: Association with self-reported disability and prediction of mortality and nursing home admission.

      Energy and Nutrient Intake and Malnutrition Assessment

      Habitual dietary intake was assessed with the food frequency questionnaire (FFQ) FQ29, which contains 67 questions and 104 items. The FQ29 was generated by the validated Dutch FFQ-TOOL.
      • Molag M.
      Towards Transparent Development of Food Frequency Questionnaires, Scientific Basis of the Dutch FFQ-TOOLTM: A Computer System to Generate, Apply and Process FFQs.
      The Dutch food composition table of 2010
      National Institute for Public Health and the Environment, Ministry of Health, Welfare and Sport (RIVM)
      Dutch Food Composition Dataset (NEVO), vn 2010/2.0.
      was used for calculating the nutrient intake per day. Portion sizes were based on standard weights.
      • Donders-Engelen M.
      • van der Heijden L.
      Maten, gewichten en codenummers 2003.
      The FQ29 assesses dietary intakes of energy, carbohydrates, protein, fat, total n-3 fatty acids [sum of α-linolenic acid (ALA, 18:3n-3), 18:4n-3, 20:3n-3, 20:4n-3, eicosapentaenoic acid (EPA, 20:5n-3), 22:3n-3, docosapentaenoic acid (DPA, 22:5n-3), and docosahexaenoic acid (DHA, 22:6n-3)], ALA, EPA, DHA, alcohol, calcium, magnesium, zinc, selenium, vitamins B6, B12, C, D, E, and folic acid equivalents. These nutrients were selected based on previous studies indicating associations between these nutrients and the determinants of sarcopenia.
      • Kuo H.K.
      • Liao K.C.
      • Leveille S.G.
      • et al.
      Relationship of homocysteine levels to quadriceps strength, gait speed, and late-life disability in older adults.
      • Visser M.
      • Deeg D.J.
      • Lips P.
      Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): The Longitudinal Aging Study Amsterdam.
      • Cesari M.
      • Pahor M.
      • Bartali B.
      • et al.
      Antioxidants and physical performance in elderly persons: The Invecchiare in Chianti (InCHIANTI) study.
      • Sharkey J.R.
      • Giuliani C.
      • Haines P.S.
      • et al.
      Summary measure of dietary musculoskeletal nutrient (calcium, vitamin D, magnesium, and phosphorus) intakes is associated with lower-extremity physical performance in homebound elderly men and women.
      • Lauretani F.
      • Semba R.D.
      • Bandinelli S.
      • et al.
      Association of low plasma selenium concentrations with poor muscle strength in older community-dwelling adults: The InCHIANTI study.
      • Abbatecola A.M.
      • Cherubini A.
      • Guralnik J.M.
      • et al.
      Plasma polyunsaturated fatty acids and age-related physical performance decline.
      • Houston D.K.
      • Nicklas B.J.
      • Ding J.
      • et al.
      Dietary protein intake is associated with lean mass change in older, community-dwelling adults: The Health, Aging, and Body Composition (Health ABC) study.
      In order to test the feasibility of the full set of MaSS assessments, a pilot study was performed in 8 older adults [assisted living (n = 4), residential living facility (n = 4)].
      • ter Borg S.
      • Mijnarends D.M.
      • Verlaan S.
      • et al.
      Pp032-Mon assessment of nutrient intake and status in sarcopenia—A pilot study.
      • Mijnarends D.
      • Meijers J.
      • Halfens R.
      • et al.
      Rationale and design of a cross-sectional study of the prevalence, characterization and health and economic consequences of sarcopenia in community-dwelling older people in The Netherlands [abstract].
      Based on this pilot study, it was decided to add an example page to the FFQ to increase the comprehensibility. Study participants were asked to fill in the paper version of the FFQ before the study visit. During the visit, the FFQ was checked for completeness, and additional information was added by the researchers if needed. Data were entered in the online FFQ-TOOL by 2 researchers, and a full data entry check was performed by a nutritionist. Dietary supplement intake was recorded separately, including details on supplement name, dose, and composition. From here on the term “dietary intake” will comprise the results from the FFQ, whereas “nutrient intake” includes the total intake: the sum of the dietary and supplement intake. The Mini Nutritional Assessment Short-Form (MNA-SF®)
      • Kaiser M.J.
      • Bauer J.M.
      • Ramsch C.
      • et al.
      Validation of the Mini Nutritional Assessment short-form (MNA-SF): A practical tool for identification of nutritional status.
      • Rubenstein L.Z.
      • Harker J.O.
      • Salva A.
      • et al.
      Screening for undernutrition in geriatric practice: Developing the short-form mini-nutritional assessment (MNA-SF).
      was used to determine the presence of malnutrition.

      Biochemical Markers of Nutrient Status

      Blood samples were collected during the home visit, after an overnight fast. The following biochemical markers were assessed: 25-hydroxyvitamin D, magnesium, red blood cell (RBC) n-3, and n-6 fatty acid profile. The RBC fatty acid profiles were used to determine the percentage of total n-3, total n-6, EPA, DPA, DHA, linoleic acid (LA, 18:2n-6) and arachidonic acid (AA, 20:4n-6). The sum score of n-3 fatty acids was defined as the sum of ALA, 18:4n-3, 20:3n-3, EPA, 22:3n-3, DPA, and DHA. The sum score of n-6 fatty acids was defined as the sum of LA, 18:3n-6, 20:2n-6, 20:3n-6, AA, 22:4n-6, 22:5n-6, and 24:2n-6. As a marker for antioxidant status, α-tocopherol levels were assessed and corrected for cholesterol. Plasma homocysteine was measured as an indirect status marker for B vitamins B6, B12 and folate. Blood was collected in ethylenediaminetetraacetic acid-containing tubes for analysis of the lipid profile, in serum tubes for analysis of 25-hydroxyvitamin D, magnesium, α-tocopherol and cholesterol, and in Sarstedt tubes for the analysis of homocysteine. Blood samples were centrifuged directly following the home visits. RBCs were washed (0.9% NaCl). Aliquots were stored at −80°C until analysis. Serum 25-hydroxyvitamin D concentration was determined with the chemiluminescence IDS-iSYS 25-Hydroxy Vitamin Ds assay (Immunodiagnostic Systems Ltd, Boldon, England). Serum magnesium was determined photometrically with Magnesium Gen.2 (COBAS, Roche Diagnostics GmbH, Mannheim, Germany). Lipids were extracted from RBCs and were assessed qualitatively as percentage of the total lipid fraction, with gas chromatography (Shimadzu Benelux, 's-Hertogenbosch, The Netherlands). Serum α-tocopherol was assessed with ultra-fast liquid chromatography (Shimadzu Benelux). Cholesterol was assessed with the colorimetric method Cholesterol Gen.2 (COBAS, Roche Diagnostics GmbH). Plasma homocysteine, was analysed with a Quattro Premier tandem mass spectrometer (Waters Chromatography B.V., Etten-Leur, The Netherlands).

      Data Analyses

      For data interpretation, energy and nutrient intakes were compared with the nutritional reference values and data from existing cohorts. For a complete overview of the nutritional reference values used see Appendix Table A1. The nutritional reference values were selected based on the most recent recommendations in the following order: (1) the Dutch Health Council, (2) the Nordic Nutrition Recommendations; and (3) European Food Safety Authority, as advised by The Netherlands Nutrition Center Foundation.

      Brink EJ, Breedveld BC, Peters JAC. Recommendations for vitamins, minerals and trace elements. Factsheet. Available at: http://www.voedingscentrum.nl/Assets/Uploads/voedingscentrum/Documents/Professionals/Pers/Factsheets/English/Factsheet%20Recommendations%20for%20vitamins,%20minerals%20and%20trace%20elements.pdf. Accessed January 13, 2016.

      The acceptable macronutrient distribution range (AMDR) and the estimated average requirement (EAR) were used. If an EAR was not stated, the adequate intake was used. A MNA-SF® score of 0–7 was considered to represent malnutrition, 8–11 risk of malnutrition, and 12–14 no malnutrition.
      • Kaiser M.J.
      • Bauer J.M.
      • Ramsch C.
      • et al.
      Validation of the Mini Nutritional Assessment short-form (MNA-SF): A practical tool for identification of nutritional status.
      Serum magnesium levels were considered deficient if below 0.75 mmol/L.
      Biomarkers of Status Working Party
      Deliverable RA 1.2–4: Table of Biomakers of Status (Task 5).
      Serum α-tocopherol levels were considered low if the α-tocopherol-cholesterol ratio was below 2.25 μmol/mmol.
      World Health Organization and Food and Agriculture Organization of the United Nations
      Vitamin and Mineral Requirements in Human Nutrition.
      Serum 25-hydroxyvitamin D levels below 50 nmol/L were considered deficient.
      Health Council of The Netherlands
      Evaluation of the Dietary Reference Values for Vitamin D.
      Plasma homocysteine levels above 15 μmol/L were considered above the normal physiological range
      Biomarkers of Status Working Party
      Deliverable RA 1.2–4: Table of Biomakers of Status (Task 5).
      Health Council of the Netherlands
      Dietary Reference Intakes: Vitamin B6, Folic Acids, and Vitamin B12.
      and indicated low levels of vitamins B6, B12 and/or folate.
      Comparisons between groups were made using the 2 independent samples t-test. The Shapiro-Wilks test with alpha 0.01 was used to determine if the distribution of continuous variables deviated from the normal distribution in which case the nonparametric Wilcoxon rank sum test was used. For categorical variables, comparisons between groups were made using the χ2 test. Multiple regression analyses were used, taking possible covariates into account, thereby determining whether the nutrient intake and biochemical nutrient status differences between the groups were indeed related to sarcopenia and not to other participant characteristics. The following covariates were included for the evaluation of dietary and nutrient intake: age, sex, MNA-SF score and malnutrition category, living-situation, ethnicity, smoking status, alcohol drinking status and amount of alcohol consumed, MMSE, comorbidities, weight, height, BMI, physical activity, and energy intake. For the biochemical nutrient status, in addition, dietary supplement use was included as a covariate. The multiple regression analysis were performed by including all covariates in 1 model, followed by an analysis in which the covariates were tested one by one in separate models. Based on the results, subsequent subgroup analyses (for age categories and living situations) were performed by 1-way analysis of variance and Tukey all-pairs comparison. Results were considered statistically significant when the P value was <.05. Analyses were performed in SAS Enterprise Guide v 4.3 (SAS Institute Inc., Cary, NC).

      Results

      In total, 227 participants had complete data sets and were included in the analysis. For the flow diagram on participant selection see Figure 1. Participants without FFQ data (n = 1) or when no blood sample was available (n = 1) were excluded from the intake and biochemical status analysis, respectively. Population characteristics and differences between the sarcopenic and nonsarcopenic groups are shown in Table 1. Fifty-three participants (23%) were identified as being sarcopenic. The median age of the MaSS participants was 74 years, with the sarcopenic group being significantly older than the nonsarcopenic participants (81 vs 72 years of age, respectively, P < .001). Of the MaSS population, 9% was at risk of malnutrition and 1% was malnourished, with no significant difference in the MNA-SF categories between the sarcopenic and nonsarcopenic (P = .194). Although the MNA-SF® score was significantly different between the 2 groups (P = .039), both groups had a median score at the upper limit of 14. The sarcopenic older adults lived more frequently in a care providing setting (P < .01), had a higher number of comorbidities (P < .001), and a lower MMSE score (P = .003). Median MMSE score was however near the maximum of 30 in both the sarcopenic and nonsarcopenic group. Body height (P = .007), weight (P = .002), and BMI (P = .048), were lower in the sarcopenic older adults compared with the nonsarcopenic older adults. The difference between the groups in sarcopenia status was confirmed by significantly lower SMM (P = .003), SMI (P = .020), handgrip strength (P < .001), gait speed (P < .001), and physical activity (P < .001) in the sarcopenic group.
      Figure thumbnail gr1
      Fig. 1Flow diagram of the inclusion of MaSS participants, adapted from Mijnarends et al.
      • Mijnarends D.M.
      • Schols J.M.
      • Meijers J.M.
      • et al.
      Instruments to assess sarcopenia and physical frailty in older people living in a community (care) setting: Similarities and discrepancies.
      Table 1Characteristics of the MaSS Participants
      Total (n = 227)Nonsarcopenic (n = 174)Sarcopenic (n = 53)P Value
      Sex, n (%)
       Male110 (49%)85 (49%)25 (47%).830
      χ2 test.
       Female117 (52%)89 (51%)28 (53%)
      Age, years74 (69–79)72 (68–76)81 (77–86)<.001
      Nonparametric Wilcoxon rank sum test.
      MNA-SF® categories, n (%)
       Nonmalnourished204 (90%)157 (90%)47 (89%).194
      χ2 test.
       At risk20 (9%)16 (9%)4 (8%)
       Malnourished3 (1%)1 (1%)2 (4%)
      MNA-SF® score14 (13–14)14 (13–14)14 (12–14).039
      Nonparametric Wilcoxon rank sum test.
      Living situation, n (%)
       Independent living157 (69%)138 (79%)19 (36%)<.001
      χ2 test.
       Home care/assisted living41 (18%)24 (14%)17 (32%)
       Residential home29 (13%)12 (7%)17 (32%)
      Ethnicity, n (%)
       Caucasian221 (97%)171 (98%)50 (94%).118
      χ2 test.
       Asian6 (3%)3 (2%)3 (6%)
      Smoking status, n (%)
       No79 (35%)60 (35%)19 (36%).983
      χ2 test.
       Formerly126 (56%)97 (56%)29 (55%)
       Yes22 (10%)17 (10%)5 (9%)
      Consume alcohol, n (%)
       No26 (12%)19 (11%)7 (13%).657
      χ2 test.
       Yes200 (89%)154 (89%)46 (87%)
      Taking nutritional supplements, n (%)
       No136 (60%)101 (58%)35 (66%).299
      χ2 test.
       Yes91 (40%)73 (42%)18 (34%)
      MMSE score29 (28–30)29 (28–30)28 (28–29).003
      Nonparametric Wilcoxon rank sum test.
      Number of comorbidities2.0 (1.0–3.0)1.0 (1.0–3.0)3.0 (1.0–4.0)<.001
      Nonparametric Wilcoxon rank sum test.
      Body composition
       Weight, kg76.0 (67.7–83.2)77.0 (69.1–83.7)71.5 (59.3–79.5).002
      Nonparametric Wilcoxon rank sum test.
       Height, m1.67 (0.09)1.68 (0.09)1.64 (0.09).007
      2 independent samples t-test.
       BMI, kg/m226.6 (24.6–29.4)26.8 (24.7–29.6)26.1 (23.5–28.2).048
      Nonparametric Wilcoxon rank sum test.
       SMM, kg23.5 (17.1–28.4)24.0 (17.7–28.8)22.7 (15.2–26.3).003
      Nonparametric Wilcoxon rank sum test.
       SMI, kg/m28.3 (6.7–9.5)8.4 (6.9–9.5)7.9 (6.1–9.4).020
      Nonparametric Wilcoxon rank sum test.
      Physical function
       Hand grip strength, kg26.4 (9.7)28.7 (9.2)18.8 (7.1)<.001
      2 independent samples t-test.
       Gait speed, m/s1.01 (0.27)1.08 (0.24)0.76 (0.23)<.001
      2 independent samples t-test.
       Physical activity, kcal/week1893 (636–3431)2230 (1074–3646)765 (246–2083)<.001
      Nonparametric Wilcoxon rank sum test.
      SD, standard deviation.
      Data are presented as n (%), mean (SD) or median (Q1-Q3).
      χ2 test.
      Nonparametric Wilcoxon rank sum test.
      2 independent samples t-test.

      Dietary and Nutrient Intake

      The dietary and nutrient intakes of the total MaSS population and the sarcopenic and nonsarcopenic groups are shown in Table 2. Sarcopenic and nonsarcopenic group comparisons were made for both dietary intake and nutrient intake. Overall, dietary supplement use seemed less in the sarcopenic older adults compared with the nonsarcopenic older adults (34% vs 42%, respectively), although this difference was not statistically significant. When considering dietary intake only, significant lower intakes were found between sarcopenic and nonsarcopenic groups for protein (g/d), n-3 fatty acids, ALA, vitamin B6, folic acid equivalents, vitamin E, magnesium, and selenium. Vitamin D intake was lower in the sarcopenic group, although not significant (P = .053). Differences in n-3 fatty acids, vitamin B6, folic acid equivalents, vitamin E, and magnesium were robust, taking the covariates into account, with a 10%–18% lower intake in the sarcopenic group compared with the nonsarcopenic group. Correcting for the covariates, however, decreased the significance of the differences in protein (g/d), ALA, and selenium intake to the level that the difference was no longer statistically significant. When taking dietary supplement intake into account, similar nutrients were identified to differ between the groups (protein (g/d), n-3 fatty acids, ALA, folic acid, magnesium). Differences in vitamin B6, vitamin E, and selenium were, however, no longer significant. Differences in n-3 fatty acids remained robust with a 10% and 19% (n-3 fatty acids expressed as En% and g/d, respectively) difference between the 2 groups, whereas the differences in protein (g/d), ALA, folic acid equivalents, and magnesium intake were no longer significant, based on the analysis taking the covariates into account. Examples of possible confounding factors were energy intake and weight (Table 2).
      Table 2Total Daily Nutrient Intake, Including Dietary and Supplement Intake of the Total MaSS Population, and for the Sarcopenic and Nonsarcopenic Participants Separately
      Supplement Users
      Number of subjects consuming micronutrients via a dietary supplement.
      Dietary IntakeTotal Energy and Nutrient Intake
      Total nutrient intake includes both dietary and supplement nutrient intake.
      Total n = 226Nonsarcopenic n = 173Sarcopenic n = 53P Value
      Comparison sarcopenic vs nonsarcopenic (2 independent samples t-test).
      Nonsarcopenic n = 167
      Number of participants for EPA and DHA (nonsarcopenic: n = 166, sarcopenic: n = 53) and alcohol (nonsarcopenic: n = 173. sarcopenic: n = 53).
      Sarcopenic n = 53
      Number of participants for EPA and DHA (nonsarcopenic: n = 166, sarcopenic: n = 53) and alcohol (nonsarcopenic: n = 173. sarcopenic: n = 53).
      P Value
      Comparison sarcopenic vs nonsarcopenic (2 independent samples t-test).
      Energy, MJ7.6 (2.2)7.7 (2.2)7.2 (2.2).1337.8 (2.2)7.2 (2.2).119
      Energy, kcal1818 (526)1847 (525)1723 (521).1331853 (527)1724 (521).119
      Carbohydrate, g184 (57)187 (56)176 (61).246188 (56)177 (61).221
      Carbohydrate, En%41 (6)41 (6)41 (7).69141 (6)41 (7).696
      Protein, g73 (21)74 (20)68 (22).048
      Significant covariates: MNA-SF®, ethnicity, alcohol consumption, MMSE score, comorbidities, weight, height, BMI, physical activity, energy intake.
      74 (20)68 (22).048
      Significant covariates: MNA-SF®, ethnicity, smoking, alcohol consumption, MMSE score, comorbidities, weight, height, BMI, physical activity, energy intake.
      Protein, g/kg bw0.98 (0.31)0.98 (0.29)0.98 (0.36).9150.97 (0.27)0.98 (0.36).835
      Protein, En%16 (3)16 (3)16 (3).18616 (3)16 (3).226
      Fat, g72 (27)74 (28)68 (25).22274 (28)68 (25).214
      Fat, En%35 (5)35 (5)36 (6).90935 (5)36 (6).861
      Alcohol, g13 (16)13 (16)13 (16).81813 (16)13 (16).818
      Alcohol, En%4.9 (5.9)4.9 (5.7)5.1 (6.6).7655 (6)5 (7).839
      n-3 fatty acids, g52.0 (0.8)2.0 (0.8)1.7 (0.7).0072.1 (0.8)1.7 (0.7).005
      n-3 fatty acids, En%1.0 (0.3)1.0 (0.2)0.9 (0.3).0261.0 (0.3)0.9 (0.3).022
       ALA, 18:3n-3, g11.67 (0.69)1.73 (0.71)1.47 (0.59).019
      Significant covariates: weight and height, physical activity, energy intake.
      1.73 (0.72)1.47 (0.59).018
      Significant covariates: weight and height, physical activity, energy intake.
       EPA, 20:5n-3, g140.08 (0.07)0.09 (0.08)0.07 (0.06).0760.10 (0.11)0.08 (0.07).089
       DHA, 22:6n-3, g130.11 (0.11)0.12 (0.12)0.09 (0.09).1010.14 (0.14)0.10 (0.09).064
      Vitamin B6, mg541.6 (0.5)1.7 (0.5)1.4 (0.5).0052.9 (8.0)2.4 (3.8).679
      Vitamin B12, μg545.0 (2.8)5.2 (3.0)4.4 (2.1).07910.7 (45.8)6.9 (13.9).550
      Folic acid equivalents, μg46305 (112)319 (110)260 (104)<.001375 (167)312 (160).016
      Significant covariates: physical activity, energy intake.
      Vitamin C, mg59116 (59)119 (58)104 (61).103179 (191)178 (227).966
      Vitamin D, μg523.6 (1.5)3.7 (1.6)3.3 (1.3).0535.2 (3.6)4.5 (3.0).197
      Vitamin E, mg5313 (5)13 (5)11 (4).00518 (19)19 (30).689
      Calcium, mg46869 (395)874 (406)852 (358).726903 (402)894 (383).884
      Magnesium, mg52308 (93)317 (92)279 (92).009350 (125)305 (132).024
      Significant covariates: age, living situation, height, physical activity, energy intake.
      Selenium, μg4943 (13)44 (13)40 (13).020
      Significant covariates: MMSE score, weight, height, physical activity, energy intake.
      56 (29)54 (32).632
      Zinc, mg5110 (3)10 (3)9 (3).09412 (5)11 (6).576
      ‖, ¶, #, ∗∗, ††, ‡‡, §§ No longer statistically significant following the multiple regression analysis.
      Data are presented as mean (SD).
      Total nutrient intake includes both dietary and supplement nutrient intake.
      Number of subjects consuming micronutrients via a dietary supplement.
      Comparison sarcopenic vs nonsarcopenic (2 independent samples t-test).
      § Number of participants for EPA and DHA (nonsarcopenic: n = 166, sarcopenic: n = 53) and alcohol (nonsarcopenic: n = 173. sarcopenic: n = 53).
      Significant covariates: MNA-SF®, ethnicity, alcohol consumption, MMSE score, comorbidities, weight, height, BMI, physical activity, energy intake.
      Significant covariates: MNA-SF®, ethnicity, smoking, alcohol consumption, MMSE score, comorbidities, weight, height, BMI, physical activity, energy intake.
      # Significant covariates: weight and height, physical activity, energy intake.
      ∗∗ Significant covariates: weight and height, physical activity, energy intake.
      †† Significant covariates: physical activity, energy intake.
      ‡‡ Significant covariates: age, living situation, height, physical activity, energy intake.
      §§ Significant covariates: MMSE score, weight, height, physical activity, energy intake.
      Compared with the nutritional reference values (Appendix Table A1), most mean nutrient intakes of the total MaSS population were above the reference values. The mean energy intake of men and the carbohydrate intakes of men and women were, however, below the reference values. Although the mean protein intake was within the AMDR of 15–20 En%, 25% of the sarcopenic group and 12% of the nonsarcopenic group were below the EAR of 0.66 g/kg bw/d. Compared with the AMDR derived reference value, 74% and 81% were below 1.2 g/kg bw/d for sarcopenic and nonsarcopenic, respectively. The mean intakes of EPA, DHA, and of selenium were below the adequate intakes. Vitamin D intake was considerably lower than the EAR, with 100% in the sarcopenic groups and 99% in the nonsarcopenic group below 20 μg/d.

      Biochemical Markers of Nutrient Status

      Biochemical nutrient levels of the MaSS population and sarcopenic and nonsarcopenic groups are shown in Table 3. The sarcopenic group had significant, 7%–20% lower levels of EPA, LA, and 25-hydroxyvitamin D, compared with the nonsarcopenic group. Homocysteine levels were significantly higher in the sarcopenic group, with a 27% higher level than the nonsarcopenic group. Age was identified as a covariate for both EPA (P = .048) and 25-hydroxyvitamin D (P ≤ .001). Correcting for this covariate decreased the significance of the group differences in EPA and 25-hydroxyvitamin D levels to the level that the difference was no longer statistically significant (P = .108, P = .367, respectively). In addition, living situation was identified as a covariate for EPA (P = .002) and 25-hydroxyvitamin D (P < .001). As with age, correcting for living situation decreased the significance of the differences in EPA and 25-hydroxyvitamin D to the levels that the differences were no longer statistically significant (P = .247, P = .426, respectively). The observed differences in EPA and 25-hydroxyvitamin D between the groups were, therefore, related to differences in age and living situation. To illustrate, a significant difference was observed for EPA status between the age categories (P = .024, based on overall test) and living situations (P < .001, based on overall test) (Figure 2). The same was observed for 25-hydroxyvitamin D status for both the age categories (P < .001) and living situations (P < .001) (Figure 3). Lower levels of both EPA and 25-hydroxyvitamin D were present in those aged 86–95 years compared with those aged 65–75 years (P = .023, P < .001, respectively). Those living in residential care had lower levels of EPA and 25-hydroxyvitamin D compared with those living independently (P < .001, P < .001, respectively, for overall test).
      Table 3Biochemical Nutrient Status of the Total MaSS Population and for the Sarcopenic and Nonsarcopenic Participants Separately
      Total n = 226
      Number of participants for n-3 fatty acids, EPA, DPA, DHA, n-6 fatty acids, LA, AA, homocysteine, α-tocopherol/cholesterol: total n = 225, nonsarcopenic n = 173, sarcopenic n = 52.
      Nonsarcopenic n = 173
      Number of participants for n-3 fatty acids, EPA, DPA, DHA, n-6 fatty acids, LA, AA, homocysteine, α-tocopherol/cholesterol: total n = 225, nonsarcopenic n = 173, sarcopenic n = 52.
      Sarcopenic n = 53
      Number of participants for n-3 fatty acids, EPA, DPA, DHA, n-6 fatty acids, LA, AA, homocysteine, α-tocopherol/cholesterol: total n = 225, nonsarcopenic n = 173, sarcopenic n = 52.
      P Value
      Comparison sarcopenic vs nonsarcopenic (2 independent samples t-test).
      25-hydroxyvitamin D, nmol/l66.8 (31.0)70.1 (30.3)56.2 (31.3).004
      No longer statistically significant following the multiple regression analysis, significant covariates are age and living situation.
      Magnesium, mmol/l0.87 (0.08)0.87 (0.08)0.87 (0.08).941
      n-3 fatty acids, %7.10 (1.15)7.14 (1.19)6.98 (1.03).390
       EPA, 20:5n-3, %0.91 (0.36)0.94 (0.38)0.79 (0.27).007
      No longer statistically significant following the multiple regression analysis, significant covariates are age and living situation.
       DPA, 22:5n-3, %2.13 (0.25)2.13 (0.25)2.12 (0.27).860
       DHA, 22:6n-3, %3.80 (0.81)3.80 (0.83)3.81 (0.74).964
      n-6 fatty acids, %28.0 (1.7)28.0 (1.7)27.9 (1.6).583
       LA, 18:2n-6, %10.4 (1.6)10.6 (1.6)9.9 (1.6).016
       AA, 20:4n-6, %12.7 (1.3)12.6 (1.3)12.9 (1.5).196
      Homocysteine, μmol/l12.8 (5.4)12.1 (4.2)15.2 (7.9)<.001
      α-tocopherol/cholesterol, μmol/mmol6.87 (1.15)6.86 (1.18)6.92 (1.06).730
      Data are presented as mean (SD).
      Number of participants for n-3 fatty acids, EPA, DPA, DHA, n-6 fatty acids, LA, AA, homocysteine, α-tocopherol/cholesterol: total n = 225, nonsarcopenic n = 173, sarcopenic n = 52.
      Comparison sarcopenic vs nonsarcopenic (2 independent samples t-test).
      No longer statistically significant following the multiple regression analysis, significant covariates are age and living situation.
      Figure thumbnail gr2
      Fig. 2(A) Box plot representing the RBC EPA level (%) of the total MaSS population, per age category. The boxes represent the interquartile range (IQR), with the median indicated as a bar within the box. The whiskers represent 1.5 times the IQR, outliers are indicated as circles, and extreme outliers with a star. Different letters indicate significant differences in group mean EPA levels (P < .05, 1-way analysis of variance (ANOVA) with Tukey all-pairs comparison). (B) Box plot representing the RBC EPA level (%) of the total MaSS population, per living situation. The boxes represent the IQR, with the median indicated as a bar within the box. The whiskers represent 1.5 times the IQR, outliers are indicated as circles and extreme outliers with a star. Different letters indicate significant differences in group mean EPA levels (P < .01, 1-way ANOVA with Tukey all-pairs comparison).
      Figure thumbnail gr3
      Fig. 3(A) Box plot representing the 25-hydroxyvitamin D levels of the total MaSS population, per age category. The boxes represent the IQR, with the median indicated as a bar within the box. The whiskers represent 1.5 times the IQR, outliers are indicated as circles, and extreme outliers with a star. Different letters indicate significant differences in group mean 25-hydroxyvitamin D levels (P < .01, 1-way ANOVA with Tukey all-pairs comparison). (B) Box plot representing the 25-hydroxyvitamin D levels of the total MaSS population, per living situation. The boxes represent the IQR, with the median indicated as a bar within the box. The whiskers represent 1.5 times the IQR, outliers are indicated as circles and extreme outliers with a star. Different letters indicate significant differences in group mean 25-hydroxyvitamin D levels (P < .01, 1-way ANOVA with Tukey all-pairs comparison).
      Although the mean 25-hydroxyvitamin D status of the MaSS participants was above the reference value, 51% of the sarcopenic group and 25% of the nonsarcopenic group had a status below 50 nmol/L. The sarcopenic older adults had a mean homocysteine level slightly above the cut-off value of 15 μmol/L. In the sarcopenic group 33% was above 15 μmol/L compared with 16% in the nonsarcopenic group. No major deficiencies were observed for magnesium and α-tocopherol.

      Discussion

      Our results indicate that sarcopenic older adults had a lower intake of 5 nutrients (n-3 fatty acids, vitamin B6, folic acid, vitamin E, and magnesium) compared with nonsarcopenic older adults. When considering dietary supplement intake, 1 nutrient (n-3 fatty acids) was lower in the sarcopenic older adults. The supplement intake, therefore, seems to decrease the intake gap between the sarcopenic and nonsarcopenic older adults. In addition, 2 biochemical markers (LA and homocysteine) differed between the 2 groups, with lower LA and higher homocysteine levels in the sarcopenic older adults. The higher homocysteine level confirmed the observed lower vitamin B intake in the sarcopenic group.
      Scientific literature and sarcopenia guidelines indicate that dietary protein is an important pillar of sarcopenia treatment, as older adults have an increased need for dietary protein to stimulate their muscle protein synthesis.
      • 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.
      • Argiles J.M.
      • Evans W.J.
      • et al.
      Nutritional recommendations for the management of sarcopenia.
      In the present study, a significant difference in protein intake (in g/d) was found between sarcopenic and nonsarcopenic older adults. The multiple regression analysis indicated that the difference in protein intake is related to the difference in, amongst others, energy intake and MNA-SF® score. A low energy intake can increase the risk of a low protein intake, and adequate daily protein intake is, therefore, important to monitor. The relative measure of protein intake adjusted for bodyweight (in g/kg bw/d) might be less appropriate for detecting differences between sarcopenic and nonsarcopenic older adults, when groups differ in bodyweight and SMI, as was the case in this study.
      N-3 fatty acids are mentioned as part of an integrated management of sarcopenia, combined with physical activity, protein, and vitamin D.
      • Boirie Y.
      • Morio B.
      • Caumon E.
      • et al.
      Nutrition and protein energy homeostasis in elderly.
      We observed a significant difference in RBC EPA levels between the sarcopenic and nonsarcopenic groups. The analysis taking into account possible covariates and the subgroup analysis, however, indicate that this difference was related to a difference in age and living situation, rather than primarily because of the presence of sarcopenia. This decrease in RBC EPA levels with age was also observed in another study, with decreasing levels after the age of 70.
      • Harris W.S.
      • Pottala J.V.
      • Varvel S.A.
      • et al.
      Erythrocyte omega-3 fatty acids increase and linoleic acid decreases with age: Observations from 160,000 patients.
      Overall, the RBC n-3 and n-6 fatty acids profile in the MaSS population were comparable to a previous study in French community-dwelling older adults.
      • Berr C.
      • Akbaraly T.
      • Arnaud J.
      • et al.
      Increased selenium intake in elderly high fish consumers may account for health benefits previously ascribed to omega-3 fatty acids.
      We observed a lower intake of vitamin B6 and folic acid and higher homocysteine level in the sarcopenic older adults compared with the nonsarcopenic group. Vitamins B6, B12, and folate are cofactors of homocysteine metabolism and deficiencies of these vitamins can result in elevated homocysteine levels.
      • Rosenberg I.H.
      • Miller J.W.
      Nutritional factors in physical and cognitive functions of elderly people.
      It has been hypothesized that these higher homocysteine levels may increase oxidative stress and muscle protein degradation and negatively impact muscle strength and physical functioning in older adults.
      • Kuo H.K.
      • Liao K.C.
      • Leveille S.G.
      • et al.
      Relationship of homocysteine levels to quadriceps strength, gait speed, and late-life disability in older adults.
      • Kado D.M.
      • Bucur A.
      • Selhub J.
      • et al.
      Homocysteine levels and decline in physical function: MacArthur studies of successful aging.
      Although the dietary vitamin D intake was not significantly different between the groups (P = .053), we did observe a significantly lower 25-hydroxyvitamin D level in the sarcopenic group. This might indicate that our sarcopenic and nonsarcopenic groups differed in their sun exposure. The sarcopenic older adults in our study received home care more frequently than the nonsarcopenic older adults. This may indicate a higher level of dependence, less time spend outdoors, and, thus, less sun exposure. The multiple regression analysis correcting for possible covariates and subsequent subgroup analysis demonstrated that the difference in 25-hydroxyvitamin D was related to age and living situation. This may indicate that these factors play a role in the observed group difference, rather than primarily the presence of sarcopenia. The discrepancy between the low (<20 μg) vitamin D intake and the mean adequate (>50 nmol/L) 25-hydroxyvitamin D levels illustrates the importance of biomarker assessments when interpreting vitamin D data. Comparable results were found in the B-Vitamins for Prevention of Osteoporotic Fractures Study,
      • Brouwer-Brolsma E.M.
      • Vaes A.M.
      • van der Zwaluw N.L.
      • et al.
      Relative importance of summer sun exposure, vitamin D intake, and genes to vitamin D status in Dutch older adults: The B-PROOF study.
      in which a total (including supplements) vitamin D intake of 5.2 μg/d was found for those with a 25-hydroxyvitamin level of >50 nmol/L. In addition the authors of the B-PROOF also observed a decrease in 25-hydroxyvitamin D with age, which is in line with our multiple regression and subgroup analyses. Overall, only 24% of the MaSS population took dietary supplements containing vitamin D, in contrast to the Dutch national recommendation that advices vitamin D supplements for older adults.
      Health Council of The Netherlands
      Evaluation of the dietary reference values for vitamin D. Publication no. 2012/15.
      Both the sarcopenic and nonsarcopenic group had average 25-hydroxyvitamin D levels above 50 nmol/L, however, 51% of the sarcopenic group and 25% of the nonsarcopenic group had a deficient status.
      Health Council of The Netherlands
      Evaluation of the dietary reference values for vitamin D. Publication no. 2012/15.
      Part of the overall MaSS participants are, therefore, at risk of loss of muscle mass, as the Longitudinal Aging Study Amsterdam cohort
      • Visser M.
      • Deeg D.J.
      • Lips P.
      Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): The Longitudinal Aging Study Amsterdam.
      indicates that older adults with serum levels below 25 nmol and between 25 and 50 nmol/L are at an increased risk of loss of appendicular skeletal muscle mass compared with those with levels equal or above 50 nmol/L.
      The sarcopenic participants differed in their vitamin E intake compared with the nonsarcopenic group, however, no significant difference was observed in the α-tocopherol to total cholesterol ratio. Although a linear relationship has been reported for intake and plasma levels, the strength of this relationship varies among studies,

      Harvey LJ, Collings R, Casgrain A. Best practice guidelines: Biomarkers of status/exposure. Available at: http://www.eurreca.org/everyone/8566/7/0/32. Accessed April 8, 2015.

      which may explain the observed discrepancy in our results. We also observed a lower selenium intake among the sarcopenic older adults. Vitamin E and selenium might act as antioxidants, addressing oxidative damage. Oxidative damage has been proposed as one of the contributors to sarcopenia, through DNA, lipid and protein damage, and subsequent muscle atrophy.
      • Mecocci P.
      • Fano G.
      • Fulle S.
      • et al.
      Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle.
      • Khor S.C.
      • Abdul Karim N.
      • Ngah W.Z.
      • et al.
      Vitamin E in sarcopenia: Current evidences on its role in prevention and treatment.
      Magnesium intake differed significantly between the sarcopenic group compared with the nonsarcopenic group, however, this was not reflected in a difference in serum magnesium levels. Serum magnesium levels are a useful marker for major deficiencies but may not be sensitive to small differences in magnesium intake. Magnesium levels are kept constant
      • Barbagallo M.
      • Belvedere M.
      • Dominguez L.J.
      Magnesium homeostasis and aging.
      and are strictly regulated by urinary excretion, bone stores, and gastrointestinal tract,

      Harvey LJ, Collings R, Casgrain A. Best practice guidelines: Biomarkers of status/exposure. Available at: http://www.eurreca.org/everyone/8566/7/0/32. Accessed April 8, 2015.

      which may explain why the difference in magnesium intake was not reflected by a difference in the serum magnesium levels between the 2 groups.
      Energy intake did not differ significantly between the sarcopenic and nonsarcopenic groups in the present study, but was identified as a covariate for some of the observed nutrient intake differences. This indicates that there could be a difference in diet quality between sarcopenic and nonsarcopenic older adults in the MaSS population, rather than an overall lower food intake. Among Iranian older adults, adherence to the Mediterranean diet was associated with a lower odds of sarcopenia,
      • Hashemi R.
      • Motlagh A.D.
      • Heshmat R.
      • et al.
      Diet and its relationship to sarcopenia in community dwelling Iranian elderly: A cross-sectional study.
      which illustrated the importance of diet quality. Understanding the food pattern and food choices of sarcopenic older adults would, therefore, be of added value. Although we did not observe significant differences in energy intake between the 2 groups, it is important to monitor energy intake as anorexia is associated with sarcopenia,
      • Landi F.
      • Liperoti R.
      • Russo A.
      • et al.
      Association of anorexia with sarcopenia in a community-dwelling elderly population: Results from the ilSIRENTE study.
      and low energy intakes are frequently reported among community-dwelling older adults.
      • ter Borg S.
      • Verlaan S.
      • Mijnarends D.M.
      • et al.
      Macronutrient intake and inadequacies of community-dwelling older adults, a systematic review.
      Compared with the nutritional reference values, a low energy intake in the MaSS men was observed. We, however, do not expect that the overall MaSS population was suffering from an energy deficit. Both groups had a maximum MNA-SF® score of 14 with 1% of the total population being malnourished and 9% at risk of malnutrition. The mean BMI of the MaSS population was 27 kg/m2. The nutritional reference value based on a physical activity level of 1.6, which represents a light active lifestyle, may have overestimated their actual energy need.
      The nutrient intake of the MaSS population is comparable to that of the Dutch National Food Survey (DNFCS)
      • Ocke M.C.
      • Buursma-Rethans E.J.M.
      • de Boer E.J.
      • et al.
      Diet of Community-Dwelling Older Adults: Dutch National Food Consumption Survey Older Adults 2010–2012.
      and recent systematic literature reviews
      • ter Borg S.
      • Verlaan S.
      • Mijnarends D.M.
      • et al.
      Macronutrient intake and inadequacies of community-dwelling older adults, a systematic review.
      • ter Borg S.
      • Verlaan S.
      • Hemsworth J.
      • et al.
      Micronutrient intakes and potential inadequacies of community-dwelling older adults: A systematic review.
      (Appendix Table A1). Only 1 cohort study (KNHANES)
      • Park S.
      • Ham J.O.
      • Lee B.K.
      A positive association of vitamin D deficiency and sarcopenia in 50 year old women, but not men.
      • Seo M.H.
      • Kim M.K.
      • Park S.E.
      • et al.
      The association between daily calcium intake and sarcopenia in older, nonobese Korean adults: The fourth Korea National Health and Nutrition Examination Survey (KNHANES IV) 2009.
      previously investigated the difference in nutrient intake (ie, energy, protein, carbohydrate, vitamin D, and calcium) between, Korean, sarcopenic, and nonsarcopenic older adults. The KNHANES found differences in energy, carbohydrate, and calcium intakes between sarcopenic and nonsarcopenic older adults. Although we observed slightly lower carbohydrate intakes in the sarcopenic group, the difference between the 2 groups was not significant. We also did not observe significant differences for calcium intake. Calcium intake in the MaSS population was considerably higher compared with the KNHANES cohort (901 mg vs 410 mg, respectively), indicating that the MaSS older adults had adequate access to calcium-rich foods. Differences in sarcopenia definition (appendicular skeletal muscle mass to body weight ratio of at least 2 standard deviations below the mean for young adults), methodology, and participant characteristics may explain the different findings in the Korean and the MaSS cohorts.
      Several strengths and limitations need to be mentioned. One of the strengths of the present study is the comprehensive assessment of dietary and supplement intake and biomarker nutrient status, as well as sarcopenia determinants. It, therefore, provides a more complete overview than most other publications that focus on 1 single nutrient and a specific muscle parameter. The MaSS population was recruited in Maastricht and is a representative sample (based on age, sex, cognition, BMI, smoking) of healthy Dutch community-dwelling older adults compared with the DNFCS.
      • Ocke M.C.
      • Buursma-Rethans E.J.M.
      • de Boer E.J.
      • et al.
      Diet of Community-Dwelling Older Adults: Dutch National Food Consumption Survey Older Adults 2010–2012.
      The analysis of dietary supplement intake is of added value, as for certain nutrients the supplements contributed to up to one-third of their total nutrient intake and may have affected their nutritional status and subsequently their health (eg, sarcopenia). In addition, the inclusion of biochemical nutrient markers and covariates with the multiple regression analysis has strengthened the conclusion of the present study.
      There are also several limitations that should be considered when interpreting the results of the present study. An FFQ was used to assess the habitual nutrient intake. Although it is a valid method to assess habitual intake, an older adult population may have difficulties with recalling all foods and community-dwelling older adults are known to underreport their energy intakes by 10%-15%.
      • Ocke M.C.
      • Buursma-Rethans E.J.M.
      • de Boer E.J.
      • et al.
      Diet of Community-Dwelling Older Adults: Dutch National Food Consumption Survey Older Adults 2010–2012.
      • de Vries J.H.
      • de Groot L.C.
      • van Staveren W.A.
      Dietary assessment in elderly people: Experiences gained from studies in the Netherlands.
      Our results on dietary intake are, however, in line with the DNFCS,
      • Ocke M.C.
      • Buursma-Rethans E.J.M.
      • de Boer E.J.
      • et al.
      Diet of Community-Dwelling Older Adults: Dutch National Food Consumption Survey Older Adults 2010–2012.
      which used two 24-hour dietary recalls to assess intake. The observed differences in intake may be related to differences in underreporting between sarcopenic and nonsarcopenic older adults. We, however, do not have grounds to believe that those suffering from sarcopenia differ in their reporting from nonsarcopenic older adults. As we use the FFQ, we might have underestimated the variance in dietary intake of our MaSS population. In addition, we were not able to assess the prevalence of underreporters. Including supplement intake increased the nutrient intake variation, which may have influenced our ability to detect significant differences between the groups. The statistical method used to correct for possible confounding factors assumed a linear relationship between the dependent variable and the possible confounding factor. The validity of these models may depend on whether this assumption was justified. As the present study had a cross-sectional design, no conclusions can be made on a causal relationship between the observed nutrient differences and sarcopenia. Longitudinal studies may provide further insight whether the observed differences in nutrient intake can lead to changes in (the determinants of) sarcopenia.

      Conclusions

      Sarcopenic older adults had a 10%–18% lower intake of 5 nutrients (n-3 fatty acids, vitamin B6, folic acid, vitamin E, and magnesium) compared with nonsarcopenic older adults. For the 2 biochemical status markers, LA and homocysteine, a 7% and 27% difference was observed, respectively. Dietary supplement intake seems to reduce the gap for some of these nutrients. Targeted nutritional intervention may, therefore, improve the nutrient intake and biochemical nutrient status of sarcopenic older adults.

      Acknowledgments

      We would like to thank Elles Lenaerts (School CAPHRI, Maastricht University) for her strong commitment and help with the data collection. Furthermore, we would like to thank the MaSS participants for their interest and participation in our study. We are grateful for the support of the municipalities of Maastricht for their assistance in the participant recruitment. We would like to thank Sophie Swinkels and Evian Fernandez Garcia (Nutricia Research, Utrecht) for their advice and assistance with the data analysis. In addition, we thank Loe Donselaar (Central diagnostic laboratory, Maastricht UMC+), Jörgen Bierau (Clinical Genetics, Maastricht UMC+), and Gerrit Witte (Nutricia Research, Utrecht) for the biochemical nutrient analyses.

      Supplementary Data

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      Linked Article

      • Letter to the Editor on the Maastricht Sarcopenia Study
        Journal of the American Medical Directors AssociationVol. 17Issue 6
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          We read the recent article published in your journal and written by Ter Borg et al1 with great interest. The study is well designed and its findings are important and remarkable. Ter Borg et al1 found in this cross-sectional study that daily intake of some nutrients, such as omega 3 fatty acids, vitamin B6, folic acid, vitamin E, and magnesium level, is lower in sarcopenic patients than in nonsarcopenic individuals and these nutrients might be related to sarcopenia. Studies on this subject are lacking in the literature, and in light of the findings of the recent study, further studies should be designed.
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