J Nutr Health Aging. 2018;22(6):700-709 © The Author(s) DIETARY PROTEIN INTAKE AND OVERALL DIET QUALITY ARE ASSOCIATED WITH HANDGRIP STRENGTH IN AFRICAN AMERICAN AND WHITE ADULTS 1 2 1 3 3 M. FANELLI KUCZMARSKI , R.T. POHLIG , E. STAVE SHUPE , A.B. ZONDERMAN , M.K. EVANS 1. University of Delaware, Department of Behavioral Health and Nutrition, 206C McDowell Hall, Newark, DE 19716, United States; 2. University of Delaware, College of Health Sciences, STAR, Newark, DE 19716, United States; 3. Laboratory of Epidemiology and Population Sciences, National Institute on Aging, NIH; 251 Bayview Blvd. Suite 100, Baltimore, MD 21224-6825, United States. Corresponding author: Marie Fanelli Kuczmarskia, University of Delaware, Department of Behavioral Health and Nutrition, 206C McDowell Hall, Newark, DE 19716, United States, , Ph: +1-302-831-8765; Fax: +1-302-831-4261, firstname.lastname@example.org Abstract: Objective: To determine the association of handgrip strength (HS) with protein intake, diet quality, and nutritional and cardiovascular biomarkers in African American and White adults. Design: Cross-sectional wave 3 (2009-2013) of the cohort Healthy Aging in Neighborhoods of Diversity across the Life Span (HANDLS) study. Participants: Socioeconomically diverse urban population of 2,468 persons aged 33 to 71 years. Measurements: Socio-demographic correlates, dietary intakes and biomarkers, HS, physical performance measures were collected. HS was measured using a dynamometer with the dominant hand. Functional measures included chair, tandem, and single leg stands. Two 24-hour recalls were collected using the US Department of Agriculture Automated Multiple Pass Method. The total protein intake and diet quality, evaluated by adherence to the DASH eating plan and Healthy Eating Index-2010, were calculated. Biomarkers included nutritional anemia, and serum levels of albumin, cholesterol, magnesium, and glucose. Results: The mean ±SE age of the sample was 52.3±0.2 years. Approximately 61% were African American and 57% were women. The mean ±SE HS of women was 29.1±0.2kg and for men was 45.9±0.4 kg. Protein, gm, per kg body weight for the women was 0.94±0.02 compared to 1.16 ±0.02 for men. After adjusting for socio-demographic factors, hypertension, and diabetes, HS/BMI ratio was significantly associated with protein intake per kg body weight (p<0.001) and diet quality, assessed by either the DASH adherence (p=0.009) or Health Eating Index-2010 (p=0.031) scores. For both men and women, participants in the upper tertile of HS maintained a single leg and tandem stances longer and completed 5 and 10 chair stands in shorter time compared to individuals in the lower HS tertile. Of the nutritional status indicators, the percent of men in the upper HS tertile with low serum magnesium and albumin, was significantly lower than those in the lower HS tertile [magnesium,7.4% vs 16.1%; albumin, 0.4% vs 4.5%]. The only difference observed for women was a lower percent of diabetes (14.4% for the upper HS tertile compared to 20.5% for the lower HS tertile. Conclusions: The findings confirm the role of protein and a healthful diet in the maintenance of muscle strength. In this community sample, HS was significantly associated with other physical performance measures but did not appear to be strongly associated with indicators of nutritional risk. These findings support the use of HS as a proxy for functional status and indicate the need for research to explore its role as a predictor of nutritional risk. Key words: Handgrip strength, protein, diet quality, African American, body mass index. Introduction performance (5). In northern European women, high adherence to a Mediterranean eating pattern was positively associated Universally, handgrip strength (HS), a muscle strength with indices of skeletal muscle mass and function (17). measurement (1), declines with age and predicts future Dietary protein intake is also associated with maintenance of disability and mortality (2-5). It is considered a reliable tool muscle mass and physical function with aging. Women who for assessing nutritional status across income groups in clinical participated in the OSTPRE- Fracture Prevention Study and practice (6, 7). HS is one of the six characteristics included in consumed high protein intakes (>1.2gm/kg) had less decline the recommendations to diagnose adult malnutrition (8). The in HS adjusted for body mass over 3 years and had better use of clinically relevant HS indices to identify older adults performance in HS/body mass, single leg stand, and chair who are at risk for functional impairment, weakness and low stand at baseline compared to women who consumed moderate muscle mass has also been recommended (1, 9). Evidence (0.81-1.19gm/kg) and low (<0.8gm/kg) intakes of protein exists that muscle strength per body mass index (BMI) would (18). Furthermore, McLean and colleagues found that higher be an appropriate relative strength index in clinical settings intakes of total and animal protein expressed as gram per (1, 10-12). However, research in community settings and the kg body weight were protective against loss of HS in men association of this index with protein intake and diet quality has and women aged 60 years and older from the Framingham not been fully investigated (13-16). Offspring Cohort, a primarily white, middle-class sample (16). Cross-sectional studies have documented that a healthful However, the relationship of dietary protein intake and diet diet is associated with better muscle strength and physical quality to muscle strength across races remains unclear. Published online February 22, 2018, http://dx.doi.org/10.1007/s12603-018-1006-8 Received August 14, 2017 Accepted for publication November 8, 2017 700 J Nutr Health Aging Volume 22, Number 6, 2018 THE JOURNAL OF NUTRITION, HEALTH & AGING© Muscle strength may also play a role in cardiometabolic approximately 7-10 days later and consisted of the second disease, and HS has been proposed as a potential marker 24-hour dietary recall and dietary supplement questionnaire for detecting undiagnosed disease among adults at normal completed over the telephone. Study protocol was approved weight (19). Among healthy weight adults with no history by National Institute of Environmental Health Sciences IRB of cardiovascular disease examined in NHANES 2011-12, and the IRB at the University of Delaware. All HANDLS HS was lower in individuals with diagnosed and undiagnosed participants provided written informed consent following their hypertension and diabetes compared to individuals without access to a protocol booklet in layman’s terms and a video hypertension or diabetes (19). An inverse association between describing all procedures. They were compensated monetarily. dietary magnesium intake and cardiovascular risk and diabetes was also found in prospective cohort studies (20-22). The Sample role of magnesium in muscle function is widely recognized, In baseline HANDLS study a total of 3,720 AA and W emphasizing the importance of diet (23, 24). participants were examined. Of these participants, 2,468 were HS is dependent on many factors such as sex, age, and reexamined in Wave 3. Only 1,787 individuals [1,009 women, race (25-27). Men have higher HS than women of similar 776 men] completed HS measures. Of those with HS measures, ages (28-30). Peak HS occurs in young adulthood followed 1,714 persons [984 women, 730 men] completed two days of by accelerated decline beginning after 40 years (28, 31, 32). 24-hour dietary recalls. HS also differs among African Americans and Whites. HS of African American women is greater than that of White Physical Performance Measures women, regardless of income status (26). However, this finding HS was assessed by trained technicians using the Jamar was inconsistent for men (26). The usefulness of HS for Hydraulic Hand Dynamometer (Patterson Medical Holdings nutritional screening in a community setting with racially Inc., Bolingbrook, IL) (35). The participants were in a seated diverse populations of similar ages has not been extensively position with the elbow of the tested side resting on a table studied. at approximately 160°. The hand dynamometer registers the A comprehensive review of the literature did not reveal maximum kilograms of force per trial, where two trials were any studies which explored the association of HS/BMI performed for both the right and left hands with a 15-20 second ratio with protein intake and diet quality. Thus the primary rest between trials. If the participant reported surgery within the objective of this study was to determine the association of past three months or if they had pain and/or arthritis that would HS/BMI ratio with protein intake and diet quality adjusting impede their ability to successfully complete the handgrip for demographic and cardiovascular risk factors in a racially test, the test was not performed. The maximum force of the diverse urban population. The second objective was to explore dominate hand was used for this study. For those who reported the relationship of HS with selected nutritional status indicators that they were ambidextrous, the right-hand measure was used. and physical performance measures to evaluate the usefulness Physical performance was measured by a modified short in community-based assessments of nutritional risk. physical performance battery (SPPB) evaluation which included tests of standing balance tandem stand, chair stands, and single Methods leg stands (36). Only one full tandem leg stand for 30 seconds was performed, while the chair stands were increased from 5 Healthy Aging in Neighborhoods of Diversity across the to 10 repetitions. The single leg stand, the surrogate for the gait Life Span (HANDLS) Study Background test in the HANDLS study, was performed three times with The HANDLS study, a 20-year prospective study initiated in maximum time of 30 seconds per trial. 2004, has been described in detail elsewhere (33). Participants were drawn from 13 pre-determined Baltimore neighborhoods, Dietary Method yielding a representative factorial cross of four factors: age (30 The United States Department of Agriculture (USDA) to 64 years), sex (men and women), race [African Americans computerized Automated Multiple Pass Method was used to (AA) and Whites (W)], and income (self-reported household collect both 24-hour dietary recalls (37). An illustrated Food income <125% and ≥125% of the 2004 Health and Human Model Booklet, measuring cups, spoons, and ruler were used to Services poverty guidelines) (34), with approximately equal assist participants in estimating accurate quantities of foods and numbers of subjects per factorial cell. beverages consumed. Both recalls were administered by trained There were two interview sessions in the Wave 3 HANDLS interviewers. Dietary recalls were coded using Survey Net, study, 2009-2013. The first session was completed on the matching foods consumed with 8-digit codes in the Food and Mobile Research Vehicles (MRV) located in participants’ Nutrient Database for Dietary Studies version 5.0 (38). neighborhoods or homes. This session consisted of a medical history, physical performance assessments, physical Diet quality measures examination, cognitive evaluation, laboratory measures, and The score for Dietary Approaches to Stop Hypertension the first 24-hour dietary recall. The second session was done (DASH) diet adherence was determined for each participant 701 J Nutr Health Aging Volume 22, Number 6, 2018 DIETARY PROTEIN INTAKE AND OVERALL DIET QUALITY using the formula reported by Mellen et al (39). These as MCV ≤ 95 µm3 accompanied by low ferritin levels (≤ 30 researchers identified DASH goals for eight target nutrients, ng/mL) or MCV ≤ 95 µm3 with normal ferritin levels (31-99 namely total fat, saturated fat, protein, fiber, cholesterol, ng/mL) and low transferrin saturation (FeSat)(<16%) (FeSat = calcium, magnesium, and potassium. Additionally, sodium serum iron/TIBC) (43). Criteria used to identify anemia due to was included as a target nutrient even though dietary sodium serum folate was <4 ng/mL and vitamin B12 was <200 pg/mL was held constant in the original DASH study. Micronutrient (44). goals were normalized to 1000 kcal. The total DASH score Several biomarkers were used to assess early signs of was generated by the sum of all nutrient targets met. If the malnutrition. Cholesterol levels <160 mg/dL (45), albumin participant achieved the DASH target for a nutrient a value <3.5 mg/dL, and magnesium <1.7 mg/dL (46) were used to of 1 was assigned, and if the intermediate target for a nutrient define inadequate levels of these biomarkers. was achieved a value of 0.5 was assigned. Zero was assigned Hypertension was defined as systolic blood pressure (SBP if neither target was met. Individuals meeting approximately ≥140 mm Hg), diastolic blood pressure (DBP) ≥90 mm Hg, half of the DASH targets (DASH score=4.5) were considered a history of blood pressure medication use, or a self-report of DASH adherent (39). diagnosed hypertension (45). SBP and DBP were assessed Food-based diet quality was also evaluated with the Health with the participant in a seated position following a 5-min Eating Index (HEI)-2010. The National Cancer Institute’s rest. One measure was obtained on each arm and then those Applied Research Web site provided the basic steps for measures were averaged. Prediabetes and diabetes mellitus calculating the HEI-2010 component and total scores and were defined as fasting glucose of 100-125 and ≥126 mg/dL statistical code for 24-hour recalls (40). A detailed description (47), respectively, a history of medication use, or a self-reported of the procedure used for this study is available on the diagnosis. HANDLS website (41). Component and total HEI-2010 scores were calculated for each recall day and were averaged to obtain Statistical Analysis the mean for both days combined. Means and standard errors for continuous variables and proportion of participants for relevant categorical variables Anthropometric, Clinic, and Blood Measures were calculated. Analysis of variance (ANOVA) was used to BMI (kg/m2) was calculated from measured weight and compare demographic and life-style factors, diet quality, HS height. Weight was obtained using a calibrated Med-weigh, and physical performance measures, across age categories (33- model 2500 digital scale, and height was measured with the 59 years, 60-71 years), and p-values were adjusted for multiple participant’s heels and back against a height meter supplied by comparisons of continuous variables using the Bonferroni Novel Products, Inc. test. For sample characteristics categorical data, χ2 tests were Fasting venous blood specimens were collected from used. Statistical significance was established at P<0.05. All participants during their MRV visit and analyzed at the Nichols statistical analyses were performed with IBM SPSS Statistics Institute of Quest Diagnostics, Inc. (Chantilly, VA, USA). for Windows v23. Fasting blood results utilized for the present study included Sex and race specific criteria for cut points were used to serum measures of albumin (g/L), magnesium (mg/dL), iron define the tertiles for HS. One- way ANOVA was used to (mcg/dL), folate (ng/mL), B12 (pg/mL), ferritin (ng/mL), total compare physical performance measures across tertiles. The iron binding capacity (TIBC)(mcg/dL), total cholesterol (mg/ number of people unable to perform each measure was also dL), and hemoglobin (g/dL) and glucose (mg/dL). Serum tallied. In addition, the HS cutpoints published by Alley et albumin, magnesium, iron, and total iron binding capacity and al (12) were used to determine the number of persons with glucose were measured by the standard clinical laboratory clinically relevant weakness. Weakness was associated with spectrophotometric assay. Serum ferritin was measured using mobility impairment, defined as gait speed less than 0.8m/s a standard chemiluminescence immunoassay. Serum folate (12). For comparisons of the proportion of the sample at and vitamin B12 were measured using enzyme immunoassay. nutritional risk, χ2 tests were used. Total serum cholesterol was assessed using a spectrophotometer Sequential multiple regression models were used to test if (Olympus 5400, Olympus, Melville, NY, USA). High- diet quality and protein intake per kg body weight predicted sensitivity CRP levels were assessed by the nephelometric HS/BMI ratio. In the first block were covariates and included method utilizing latex particles coated with CRP monoclonal age, sex, race, income, cigarette smoking status, diabetes, and antibodies. hypertension. The second block contained protein (g) per kg To diagnose nutritional anemia, participants were first body weight while the third block contained DASH diet score. categorized by presence of anemia defined by a hemoglobin The last block contained two-way interactions, specifically sex level less than 13 g/dL in men and less than 12 g/dL in x race, sex x income, and race x income. Blocks in sequential women (42). Then, among those with anemia, participants regression refer to predictors that are entered simultaneously. with nutritional anemia due to inadequate iron, folate, and/or Entering predictors in blocks allows for testing if the addition Vitamin B12 were identified. Nutritional anemia was defined of multiple predictors simultaneously significantly improves the 702 J Nutr Health Aging Volume 22, Number 6, 2018 THE JOURNAL OF NUTRITION, HEALTH & AGING© Table 1 Characteristics of Male Participants in Healthy Aging in Neighborhoods of Diversity across the Life Span (HANDLS) Study by Age within Race Categories Characteristic Males African American White n 33-59 yrs n 60 -71 yrs n 34-59 yrs n 60-71 yrs Demographics Age, yrs mean (SE) 377 48.6±0.4 110 64.2±0.3*** 230 49.3±0.4 68 64.2±0.3*** Low Income , % 377 45.9% 110 28.2%*** 230 28.3% 68 16.2%* Health Current smoker, % 296 61.1 83 47.0* 207 40.1 66 19.7** Body Mass Index, kg/m , mean (SE) 375 27.6±0.3 109 27.6±0.5 230 29.3±0.4 68 30.7±0.8 Glucose, mg/dL, mean (SE) 342 105.6±2.6 88 108.7±3.5 214 107.8±3.2 62 105.3±4.9 Prediabetes , %, 71 18.9 26 24.1 52 22.6 16 23.5 Diabetes , % 49 13.0 28 25.9*** 30 13.0 11 16.2 Hypertension , % 377 44.6 109 68.8*** 230 37.8 68 60.3*** Diet mean (SE) mean (SE) mean (SE) mean (SE) Protein/weight (g/kg/d) 350 1.21±0.04 102 1.10±0.06 208 1.17±0.04 68 0.98±0.06* DASH score 352 1.5±0.1 102 1.7±0.1 208 1.7±0.1 68 2.0±0.2 Healthy Eating Index-2010 score 352 45.3±0.5 102 47.0±1.2 208 44.6±0.8 68 47.8±1.5 Physical Performance Hand Grip Strength (kg) 371 47.8±0.5 108 41.9±1.0*** 229 46.3±0.7 68 40.7±1.0*** 5 Chair stands (sec) 377 15.7±0.2 110 18.5±0.4*** 230 16.3±0.3 68 16.9±0.6 10 Chair stands (sec) 373 31.7±0.4 108 36.3±0.8*** 230 32.5±0.5 65 34.4±1.1 Tandem (sec) 365 29.6±0.1 108 28.9±0.4* 223 29.5±0.2 61 28.9±0.5 Leg stand trial 1 (sec) 336 27.9±0.3 85 22.0±1.0*** 213 27.1±0.5 50 23.2±1.3*** Leg stand trial 2 (sec) 325 28.5±0.3 68 24.1±1.0*** 208 27.6±0.4 40 23.3±1.6*** Leg stand trial 3 (sec) 313 29.1±0.2 54 25.8±1.0*** 199 28.6±0.3 36 25.4±1.5*** Note: * P≤0.05, ** P≤0.01, ***P≤0.001; 1. Defined as < 125% of the 2004 United States Health and Human Services poverty guidelines ; 2. Defined as 100-125 mg/dL fasting glucose, taking medications, and self-report of diagnosed prediabetes; 3. Defined as ≥126 mg/dL fasting glucose, taking medications, and self-report of diagnosed diabetes; 4. Defined as systolic blood pressure ≥ 140mm Hg, diastolic blood pressure ≥90mm Hg, taking anti-hypertensive medications, and self-report of diagnosed hypertension; 5. DASH, Dietary Approaches to Stop Hypertension, eating plan with maximum score of 9; 6. Healthy Eating Index-2010, maximum score of 100 model. years compared to women less than 60 years (Tables 1 and 2). Separate regression analyses were also performed with HEI- BMI was not significantly different within either sex by 2010, the results were the same as those with DASH (data not race for age category (Tables 1 and 2). The percentage of the shown). population with incomes less than 125% of poverty guidelines was lower for both AA men and all women aged 60-71 years Results compared to their younger counterparts (Tables 1 and 2). The only significant differences in protein intake per kg body weight Sample Characteristics were found for W men, with the older age group consuming Approximately 23% of men and 24% of women were less protein per kg body weight compared to the younger age 60-71 years of age. The proportion of the population who group. With respect to diet quality, no differences were found currently smoked was significantly higher for the 33-59 years for men across age groups. For AA women, the mean DASH age category for all race-sex groups (Tables 1 and 2). Mean and HEI-2010 scores were higher for the older compared to glucose was similar across age for all race-sex groups (Tables 1 younger age group. For W women, HEI-2010 scores, but not and 2). Although the percent of individuals with prediabetes did DASH scores were higher for the older compared to younger not differ across age for either sex or race, diabetes was more age group. prevalent among AA men and women and W women 60-71 703 J Nutr Health Aging Volume 22, Number 6, 2018 DIETARY PROTEIN INTAKE AND OVERALL DIET QUALITY Table 2 Characteristics of Female Participants in Healthy Aging in Neighborhoods of Diversity across the Life Span (HANDLS) Study by Age within Race Categories Characteristic Females African American White n 33-59 yrs n 60-71 yrs n 33-59 yrs n ≥60-71 yrs Demographics Age, yrs mean (SE) 475 48.2±0.3 152 64.6±0.2*** 308 48.3±0.4 95 64.6±0.3*** Low Income , % 475 48.6 152 36.2** 308 31.8 95 18.9* Health Current smoker, % 376 46.8 109 35.8* 269 41.6 87 23** Body Mass Index, kg/m , mean (SE) 475 32.2±0.4 152 31.2±0.7 308 30.5±0.4 95 30.9±0.8 Glucose, mg/dL mean (SE) 437 98.6±1.4 140 103.2±2.2 289 97.3±1.6 86 101.3±2.5 Prediabetes , %, 70 14.7 23 15.1 54 17.5 23 24.2 Diabetes , % 78 16.4 49 32.2*** 24 7.8 18 18.9*** Hypertension , % 475 50.5 152 82.2*** 308 31.8 95 63.2*** Diet mean (SE) mean (SE) mean (SE) mean (SE) Protein/weight, (gm/kg/d) 455 0.95±0.03 150 0.90±0.05 290 0.95±0.03 88 0.94±0.05 DASH score 455 1.6±0.1 150 1.9±0.1** 291 2.1±0.1 88 2.4±0.2 Healthy Eating Index-2010 score 455 45.4±0.5 150 50.2±1.1*** 291 47.0±0.8 88 52.0±1.6** Physical Performance Hand Grip Strength (kg) 464 30.4±0.3 152 27.4±0.5*** 301 29.2±0.4 92 25.0±0.6*** 5 Chair stand (sec) 475 16.9±0.2 152 18.1±0.4** 308 16.7±0.2 95 18.61±0.6*** 10 Chair stand (sec) 472 34.0±0.5 147 35.3±0.8 304 33.4±0.5 95 35.8±1.1* Tandem (sec) 462 29.6±0.1 140 28.4±0.4*** 300 29.6±0.1 83 27.9±0.6*** Leg stand trial 1 (sec) 401 25.4±0.4 101 22.1±0.9*** 266 26.5±0.4 59 22.9±1.1*** Leg stand trial 2 (sec) 364 26.6±0.4 71 26.0±0.8 247 27.3±0.4 46 24.7±1.2* Leg stand trial 3 (sec) 328 27.8±0.3 57 26.9±0.9 231 27.8±0.3 39 26.8±1.1 Note: * P≤0.05, ** P≤0.01, ***P≤0.001; 1. Defined as < 125% of the 2004 United States Health and Human Services poverty guidelines ; 2. Defined as 100-125 mg/dL fasting glucose, taking medications, and self-report of diagnosed prediabetes; 3. Defined as ≥126 mg/dL fasting glucose, taking medications, and self-report of diagnosed diabetes; 4. Defined as systolic blood pressure ≥ 140mm Hg, diastolic blood pressure ≥90mm Hg, taking anti-hypertensive medications, and self-report of diagnosed hypertension; 5. DASH, Dietary Approaches to Stop Hypertension, eating plan with maximum score of 9; 6. Healthy Eating Index-2010, maximum score of 100 Handgrip Strength and Physical Performance Measures (Table 1). Mean HS, and time to hold the single leg (first trial only) As presented in Tables 3 and 4, the upper tertile of HS was and tandem stands were significantly less, while time in associated with significantly better physical performance. Using seconds to complete 5 chair stands was significantly longer the total sample of men or women, the time to complete 5 or 10 for women aged 60-71 years compared to those women less chair stands was significantly less for those participants in the than 60 years (Table 2). The only significant difference in the upper tertile compared to the lower tertile of HS. With respect second and third trials of the single leg stand was found for W to the tandem stand and the first two single leg stands, persons women for the second trial. In addition, the time to complete in the upper tertile for HS held the stance for a significantly 10 chair stands was significantly longer for the older compared longer time than persons in the lower tertile for HS. With each to younger W women (Table 2). Comparable results were subsequent single leg stand the number of persons unable observed for men with these exceptions - time to complete 5 to complete the trial increased (Table 3 and 4). None of the or 10 chair stands did not differ for W men; time to complete 5 individuals in the upper HS tertile experienced weakness or or 10 chair stands was significantly longer for older AA men; intermediate mobility impairment. and significant differences were found for all trials of the single Unlike the findings for the W men who had no significant leg stand, with the older group holding the stance for less time difference in physical performance, the AA men in the upper 704 J Nutr Health Aging Volume 22, Number 6, 2018 THE JOURNAL OF NUTRITION, HEALTH & AGING© Table 3 Physical Performance and Nutritional Status Biomarkers categorized by Hand Grip Strength for Males 1 2 African American White Total Physical Performance Measures Lower tertile High tertile Lower tertile High tertile Lower tertile High tertile (n=168) (n=162) (n=99) (n=109) (n=267) (n=271) Chair stands 5 stands, Number completed, n 168 162 99 109 267 271 Time to complete 5 stands, mean (SE), sec 17.7±0.3 15.2±0.3*** 16.5±0.5 15.7±0.3 17.2±0.3 15.4±0.2*** 10 stands, Completed, n 165 161 97 109 262 270 Time to complete 10 stands, mean (SE), sec 34.5±0.7 30.9±0.6*** 33.5±0.8 31.5±0.6 34.1±0.5 31.1±0.4*** Tandem stands, n 161 158 90 108 251 266 Time to hold, mean (SE), sec 28.9±0.3 30.0±0.0*** 29.1±0.4 29.7±0.3 28.9±0.2 29.9±0.1*** Single leg stand First trial, Completed, n 130 153 78 104 208 257 First trial, mean (SE), sec 26.0±0.7 28.3±0.4** 25.8±0.9 27.0±0.7 25.9±0.5 27.8±0.4** Second trial, Completed, n 124 146 73 101 197 247 Second trial, mean (SE), sec 26.5±0.6 29.0±0.3*** 26.3±0.9 27.7±0.6 26.4±0.5 28.5±0.3*** Third trial, Completed, n 109 144 68 97 177 241 Third trial, mean (SE), sec 28.1±0.5 29.3±0.2* 28.1±0.7 28.2±0.6 28.1±0.4 28.8±0.3 Mobility Impairment Weak HS , n 10 0*** 7 0*** 17 0*** Intermediate HS , n 24 0*** 27 0*** 51 0*** Blood Biomarkers Nutritional anemia , % 6.0 4.3 5.1 0.9 5.6 3.0 <3.5 g/dL Serum albumin, % 6.0 0.6** 2.0 0.0 4.5 0.4** <1.7 mg/dL Serum magnesium, % 20.8 8.6** 8.1 5.5 16.1 7.4** <160 mg/dL Serum total cholesterol, % 35.1 30.2 29.3 29.4 33.0 29.9 Prediabetes , % 18.6 21.0 27.3 17.4 21.8 19.6 Diabetes , % 21.6 9.9* 15.2 10.1 19.2 10.0** Note: * P≤0.05, ** P≤0.01, ***P≤0.001; 1. Lower tertile defined as ≤42.00 kg and upper tertile as ≥51.00 kg; 2. Lower tertile defined as ≤40.32 kg and upper tertile as ≥49.00 kg; 3. 11 11 39 43 Weak HS defined as <26 kg ; 4. Intermediate HS defined as 26-32 Kg ; 5. Includes iron, folate and/or Vitamin B12 deficiencies ; 6. Defined as 100-125 mg/dL fasting glucose , taking medications, and self-report of diagnosed prediabetes; 7. Defined as ≥ 126 mg/dL fasting glucose , taking medications, and self-report of diagnosed diabetes; Chi-square test was used to test the differences of categorical variables across tertiles of HS strength; ANOVA was performed to test the differences of continuous variables across tertiles of HS strength. HS tertile had significantly better physical performance for in the lower compared to the upper HS tertile. Significant all measures compared to men in the lower tertile (Table 3). differences in these 3 biomarkers were also observed for Among women, both W and AA in upper HS tertile had better the AA but not the W men (Table 3). For the total sample physical performance with respect to 5 chair stands and the of women and W women, the presence of diabetes was tandem and first single leg stands compared to women in the significantly higher in the lower compared to the upper HS lower tertile (Table 4). tertile (Table 4). The AA appeared to be at greater nutrition risk compared Biomarkers of Nutrition Status to the W. For instance, approximately 20% of AA men and There were some significant differences in the percentage women in the lower HS tertile had low serum magnesium of people with blood markers suggesting inadequate nutritional concentrations compared to <10% of the W men and women. status between individuals in the lower compared to the upper Mean c-Reactive Protein (cRP) was also calculated for the tertile of HS. For the total sample of men, these biomarkers lower and upper tertiles for each sex-race group and no include low serum magnesium and albumin, and presence of significant differences were found (data not shown). diabetes (Table 3). As expected, the percentage was higher 705 J Nutr Health Aging Volume 22, Number 6, 2018 DIETARY PROTEIN INTAKE AND OVERALL DIET QUALITY Table 4 Physical Performance and Nutritional Status Biomarkers categorized by Low and Upper Tertiles of Hand Grip Strength for Females 1 2 African American White Total Physical Performance Measures Lower tertile Upper tertile Lower tertile Upper tertile Lower tertile Upper tertile (n=223) (n=239) (n=138) (n=136) (n=361) (n=375) Chair stands 5 stands, Number completed, n 223 239 138 136 361 375 Time to complete 5 stands, mean (SE), sec 18.1±0.4 16.6±0.3*** 18.2±0.5 16.5±0.4** 18.1±0.3 16.5±0.2*** 10 stands, Completed, n 217 237 138 135 355 372 Time to complete 10 stands, mean (SE), sec 35.2±0.7 33.9±0.7 35.4±0.9 33.0±0.7* 35.3±0.6 33.6±0.5* Tandem stands, n 206 234 125 133 331 367 Time to hold, mean (SE), sec 28.9±0.3 29.8±0.1*** 28.7±0.4 29.6±0.2* 28.9±0.2 29.8±0.1*** Single leg stand First trial, Completed, n 156 206 97 121 253 327 First trial, mean (SE), sec 23.9±0.6 26.0 ±0.5** 23.9 ±0.9 28.0±0.4*** 23.9±0.5 26.8±0.4*** Second trial, Completed, n 126 188 78 119 204 307 Second trial, mean (SE), sec 26.1±0.6 27.1±0.5 25.1±0.9 27.7±0.5** 25.7±0.5 27.3±0.3** Third trial, Completed, n 110 170 67 117 177 287 Third trial, mean (SE), sec 27.6±0.6 27.9±0.4 27.0±0.8 28.2±0.4 27.4±0.4 28.0±0.3 Mobility Impairment Weak HS , n 12 0*** 6 0*** 18 0*** Intermediate HS , n 45 0*** 41 0*** 86 0*** Blood Biomarkers Nutritional anemia , % 10.8 15.5 9.4 10.3 10.2 13.6 <3.5 g/dL Serum albumin, % 0.4 1.7 1.4 0.0 0.8 1.1 <1.7 mg/dL Serum magnesium, % 18.4 16.3 8.7 5.1 14.7 12.3 <160 mg/dL Serum total cholesterol, % 25.6 22.2 15.2 19.1 49.7 50.3 Prediabetes , % 14.8 11.7 19.6 19.1 16.6 14.4 Diabetes , % 25.6 19.7 12.3 5.1* 20.5 14.4* Note: * P≤0.05, ** P≤0.01, ***P≤0.001; 1. Lower tertile defined as ≤27.00kg and upper tertile as ≥32.00kg; 2.Lower tertile defined as ≤25.00kg and upper tertile as ≥31.00kg; 3. Weak 11 11 39 43 HS defined as <16 kg ; 4. Intermediate HS defined as 16-20 Kg ; 5. Includes iron, folate and/or Vitamin B12 deficiencies ; 6. Defined as 100-125 mg/dL fasting glucose , taking medications, and self-report of diagnosed prediabetes; 7. Defined as ≥ 126 mg/dL fasting glucose , taking medications, and self-report of diagnosed diabetes; Chi-square test was used to test the differences of categorical variables across tertiles of HS strength; ANOVA was performed to test the differences of continuous variables across tertiles of HS strength. Variables Associated with Handgrip Strength model was 0.566 (Table 5). As shown in Table 5, after adjusting for age, sex, race, income, smoking, diabetes, and hypertension, protein per kg Discussion body weight was positively associated (P < 0.001) with HS/ BMI ratio. Using the same model, overall diet quality, as With increasing longevity, the preservation of muscle measured by adherence to the DASH eating plan, was tested strength and quality are crucial for maintaining independence. and found to be positively associated (P < 0.009). Although The literature provides evidence that dietary protein intake, the change in R2 was low, it was significant with the addition as part of an overall healthful diet, and physical activity can of the dietary variables. Amongst the covariates, being male, a help protect against age-related muscle loss and functional nonsmoker, and not diabetic or hypertensive were associated decline (17, 18, 48-53). We are the first to report that relative with a higher HS/BMI ratio. Race and income were not HS, specifically HS/BMI ratio, was significantly associated associated with HS/BMI. Three interactions were tested (sex with higher intakes of protein per kg body weight intake and x race, sex x income, race x income), only the sex x race better compliance to the DASH eating plan, adjusting for interaction was significant (P = 0.002). The overall R2 of the demographic factors, diabetes, and hypertension. 706 J Nutr Health Aging Volume 22, Number 6, 2018 THE JOURNAL OF NUTRITION, HEALTH & AGING© dynamometer model (59), since statistically significant Table 5 differences in HS has been reported between the Jamar and Hand Grip Strength per Body Mass Index as predicted by Smedley dynamometers (60). Another possible explanation Protein Intake and Adherence to DASH Eating Pattern and is that the HANDLS study participants are weaker but lean Selected Sociodemographic Predictors: Regression model body measures would be needed to confirm this difference. HS measurements should be interpreted using ethnic/region Predictor Β (SE) P specific reference ranges since HS values can vary not only Block 1 Age, yrs -0.006 (0.001) <0.001 due to dynamometer models used but also the calibration of Sex (Female vs. Male) 0.595 (0.029) <0.001 these instruments, age categories, and differences in ethnicities, geographic regions, and physical activity levels (31, 32, 61). Race (W vs. AA ) 0.038 (0.026) 0.138 It is likely that the differences in HS also reflect variations in Income (≥125% vs. < 125%) -0.014 (0.020) 0.480 dietary patterns. Smoker (No vs. yes) 0.082 (0.020) <0.001 It is widely recognized that muscle strength declines (31, 32) Diabetes(No, Pre, vs Yes) -0.099 (0.013) <0.001 while BMI increases with age (62). As anticipated the mean Hypertension (No vs Yes) -0.101 (0.020) <0.001 HS of the HANDLS study participants at Wave 3 was less than their reported values in the baseline phase of the study Block 2 Protein per kg body weight 0.148 (0.016) <0.001 3 (26). Evidence exists that HS is positively associated with Block 3 DASH adherence 0.105 (0.041) 0.009 BMI, however this association may be less pronounced in obese Block 4 Sex x race 0.117 (0.038) 0.002 individuals compared to individuals of other BMI categories R P (31, 61). The mean BMI of the HANDLS study participants Model Fit Block 1 0.535 <0.001 indicates that overweightness and obesity are prevalent in this population. Some researchers have reported that HS/BMI ratio ΔR2 with Block 2 0.025 <0.001 is the best predictor of mobility impairment for women (12). ΔR2 with Block 3 0.002 <0.001 Among the HANDLS study sample, weakness was present ΔR2 with Block 4 0.003 0.006 in approximately 27% of persons within the lower HS tertile. Final Model 0.566 0.002 Obesity combined with muscle weakness has been associated 1. AA= African American, W=White; 2. Income defined as <125% or ≥125% 2004 with a 3.9 fold greater risk of developing mobility limitation United States Health and Human Services poverty guidelines ; 3. DASH, Dietary (63). Approaches to Stop Hypertension score In this urban population, HS was significantly associated with other physical performance measures similar to findings Adherence to Mediterranean diet or DASH eating patterns, of Stevens and colleagues (64). However, HS did not appear to which are rich in antioxidant nutrients, such as magnesium be strongly associated with indicators of nutritional risk. These and vitamins C and E, can lower inflammatory markers. findings differ from those reported in clinical settings where Chronic low-grade inflammation and oxidative stress can HS can be a sensitive method for the diagnosis of malnutrition trigger catabolism and increase protein turnover in skeletal (3, 65). Yet they are consistent with the results of Springstroh muscle, reducing strength (54-56), as well as increase formation and colleagues who found that HS was weakly associated of reactive oxygen species resulting in an overload of the with nutritional risk in community-dwelling older adults (66). antioxidant defense system (57). Adherence to the DASH While low hemoglobin has been reported to contribute to eating pattern was significantly associated with relative low HS independent of inflammatory markers and age (67), HS in this study. However, the association of adherence to in our sample there were no differences in the percent of the Mediterranean diet with HS was only found significant in population with nutritional anemia when comparing the lower unadjusted analyses by Kelaiditi and colleagues (17). The to upper HS tertile. A single measure of HS may be appropriate researchers explained this lack of association by the fact that for nutrition screening while HS variation over time may be age was a strong determinant of HS in their cross-sectional better for nutritional status assessment in community-dwelling studies (17). However, the differences might reflect the use of populations. Regardless, early identification of older adults at relative HS rather than absolute HS. malnutrition risk is beneficial for the initiation of nutritional Similar to the findings of other researchers, the mean HS of interventions (68). the HANDLS study population was less for Whites compared The association of HS with nutritional biomarkers to AA (26) and for women compared to men (31, 58). The appeared to be stronger for men than women but the findings mean and median HS of the HANDLS study participants were were inconsistent across the sexes by race. For example, considerably lower than the mean and median HS reported low levels of serum albumin and magnesium, as well as for the National Health and Nutrition Examination Survey, presence of diabetes, were significantly more prevalent for 2011-12, which represents a national US sample (30). These men in the lower, compared to the upper HS tertile, while reference values were categorized by age and sex for all races. only the presence of diabetes was significant for women. The difference may be partially attributed to the different 707 J Nutr Health Aging Volume 22, Number 6, 2018 DIETARY PROTEIN INTAKE AND OVERALL DIET QUALITY 5. Granic A, Jagger C, Davies K, Adamson A, Kirkwood T, Hill TR, et al. Effect of The observation that lower HS was associated with greater Dietary Patterns on Muscle Strength and Physical Performance in the Very Old: prevalence of diabetes is consistent with the results of Mainous Findings from the Newcastle 85 Study. PloS one. 2016;11(3):e0149699. 6. Flood A, Chung A, Parker H, Kearns V, O’Sullivan TA. The use of hand and colleagues (19). grip strength as a predictor of nutrition status in hospital patients. Clin Nutr. As with any study there are strengths and limitations. The 2014;Feb;33(1):106-14. strengths of the study include the use of two 24-hour recalls 7. Hasheminejad N, Namdari M, Mahmoodi MR, Bahrampour A, Azmandian J. Association of handgrip strength with malnutrition-inflammation score as for the evaluation of adherence to the DASH eating pattern, an assessment of nutritional status in hemodialysis patients. Iran J Kidney Dis. inclusion of a racially diverse independent population younger 2016;10(1). 8. White JV, Guenter P, Jensen G, Malone A, Schofield M, Group AMW, et al. than 60 years of age, and confirmation of the regression Consensus statement of the Academy of Nutrition and Dietetics/American Society for findings using two diet quality indices. Limitations include Parenteral and Enteral Nutrition: characteristics recommended for the identification and documentation of adult malnutrition (undernutrition). J Acad Nutr Diet. the lack of persons over 71 years of age, of dual-energy X-ray 2012;112(5):730-8. absorptiometry data and physical activity measures, and the 9. Dong H, Marcusson J, Wressle E, Unosson M. Obese very old women have low small number of nutritional biomarkers. relative handgrip strength, poor physical function, and difficulties in daily living. J Nutr Health Aging. 2015;19(1):20-5. In conclusion, the findings support the recognized 10. Barbat-Artigas S, Rolland Y, Cesari M, Abellan van Kan G, Vellas B, Aubertin- association between protein intake, healthful diet and HS. Leheudre M. Clinical relevance of different muscle strength indexes and functional impairment in women aged 75 years and older. J Gerontol A Biol Sci Med Sci. There is evidence that higher levels of muscle strength in older 2013;68(7):811-9. adults are seen with protein intakes ≥ 1.2g/kg body weight / 11. Choquette S, Bouchard D, Doyon C, Sénéchal M, Brochu M, Dionne IJ. Relative strength as a determinant of mobility in elders 67–84 years of age. A nuage study: day (51, 69). To achieve this level, protein enrichment with Nutrition as a determinant of successful aging. J Nutr Health Aging. 2010;1-6. familiar foods can be an effective strategy (70). The dietary 12. Alley DE, Shardell MD, Peters KW, McLean RR, Dam TT, Kenny AM, et al. Grip protein content for an optimal diet is currently under review strength cutpoints for the identification of clinically relevant weakness. J Gerontol A Biol Sci Med Sci. May; 2014;69(5):559-66. with a focus on not only the total amount but also the amino 13. Farsijani S, Payette H, Morais JA, Shatenstein B, Gaudreau P, Chevalier S. Even acid content, quality, digestibility and daily protein distribution mealtime distribution of protein intake is associated with greater muscle strength, but not with 3-y physical function decline, in free-living older adults: the Quebec (71, 72). The results also support the use of HS as a proxy longitudinal study on Nutrition as a Determinant of Successful Aging (NuAge study). for functional status when assessing nutritional status risk Am J Clin Nutr.2017;Jul;106(1):113-24. 14. Yokoyama Y, Nishi M, Murayama H, Amano H, Taniguchi Y, Nofuji Y, et al. in community settings. However, HS was not consistently Dietary variety and decline in lean mass and physical performance in community- associated with nutritional status indicators used in this study. dwelling older Japanese: A 4-year follow-up study. J Nutr Health Aging. Given the ease and inexpensive costs of obtaining HS, there is a 2017;21(1):11-6. 15. Bjorkman MP, Suominen MH, Pitkälä KH, Finne-Soveri HU, Tilvis RS. Porvoo need for research to further explore its role with other markers sarcopenia and nutrition trial: effects of protein supplementation on functional of nutritional risk in noninstitutionalized populations. performance in home-dwelling sarcopenic older people-study protocol for a randomized controlled trial. Trials. 2013;14(1):387. 16. McLean RR, Mangano KM, Hannan MT, Kiel DP, Sahni S. Dietary protein intake Ethical Standards Disclosure: This study was conducted according to the guidelines is protective against loss of grip strength among older adults in the Framingham laid down in the Declaration of Helsinki and the study protocol was approved by Offspring Cohort. J Gerontol A Biol Sci Med Sci. 2016;71(3):356-61. Institutional Review Boards at National Institute of Environmental Health Science and the 17. Kelaiditi E, Jennings A, Steves C, Skinner J, Cassidy A, MacGregor A, et al. University of Delaware. Written informed consent was obtained from all subjects. Measurements of skeletal muscle mass and power are positively related to a Mediterranean dietary pattern in women. Osteoporosis Int. 2016;27(11):3251-60. Statement of Potential Conflict of Interest: No potential conflict of interest was 18. Isanejad M, Mursu J, Sirola J, Kröger H, Rikkonen T, Tuppurainen M, et al. Dietary reported by the authors. protein intake is associated with better physical function and muscle strength among elderly women. Br J Nutr. 2016;115(07):1281-91. Financial disclosure: All authors have no financial disclosures. 19. Mainous AG, Tanner RJ, Anton SD, Jo A. Grip strength as a marker of hypertension and diabetes in healthy weight adults. Am J Prev Med. 2015;49(6):850-8. Acknowledgements: This work is supported by the Intramural Research Program, 20. Del Gobbo LC, Imamura F, Wu JH, de Oliveira Otto MC, Chiuve SE, Mozaffarian D. National Institute on Aging, National Institutes of Health, grant Z01-AG000194. Circulating and dietary magnesium and risk of cardiovascular disease: a systematic review and meta-analysis of prospective studies. Am J Clin Nutr. 2013;Jul;98(1):160- Open Access: This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), 21. Joosten MM, Gansevoort RT, Mukamal KJ, van der Harst P, Geleijnse JM, Feskens which permits use, duplication, adaptation, distribution and reproduction in any medium EJ, et al. Urinary and plasma magnesium and risk of ischemic heart disease. Am J or format, as long as you give appropriate credit to the original author(s) and the source, Clin Nutr. Jun;97(6):1299-306. provide a link to the Creative Commons license and indicate if changes were made. 22. Volpe SL. (2013) Magnesium in disease prevention and overall health. Adv Nutr. 2013;May 1;4(3):378S-83S. 23. Welch AA, Kelaiditi E, Jennings A, Steves CJ, Spector TD, MacGregor A. 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