Sarcopenia, which has been recently established as a muscle disease(Reference Cao and Morley1), is a condition of age-related loss of skeletal muscle mass, low muscle strength and/or low physical performance(Reference Chen, Woo and Assantachai2). For use in community-based health care and screening, the Asian Working Group for Sarcopenia 2019 consensus has introduced a concept of ‘possible sarcopenia’ defined as low muscle strength with or without low muscle mass(Reference Chen, Woo and Assantachai2). Low muscle strength was defined as handgrip strength <28 kg for Asian older men and <18 kg for Asian older women(Reference Chen, Woo and Assantachai2).
Since sarcopenia increases the risk of multiple chronic diseases, such as type 2 diabetes, CVD, non-alcoholic fatty liver disease and osteoporosis as well as impaired ability and frailty to perform daily activities(Reference Kunutsor, Isiozor and Khan3–Reference Malmstrom, Miller and Simonsick7), it is very important to manage muscle health with advancing age. Although having regular resistance training and higher dietary protein intake are major preventive factors for maintaining optimal muscle mass, strength and function(Reference Deutz, Bauer and Barazzoni8,Reference Jun, Cowan and Dwyer9) , emerging evidence suggests that adequate intakes of other nutrients, including dietary fibres, n-3 PUFA and micronutrients, play important roles in preventing muscle strength decline(Reference Kao, Yang and Chen10–Reference Ali, Corbi and Medoro13).
Nuts are rich in plant-based protein, dietary fibre, PUFA, MUFA, phytosterols and phytochemicals and are low in SFA and carbohydrates(Reference Bae, Kim and Choi14), and thus, they have been associated with numerous health outcomes including cardiometabolic diseases(Reference Balakrishna, Bjørnerud and Bemanian15). Given their nutrient profiles, nuts also have the potential to prevent muscle strength decline through an influence on various mechanisms influencing oxidative stress, inflammation and insulin resistance(Reference Alasalvar and Bolling16). However, little is known whether consumption of nuts exerts beneficial effects on muscle strength. Therefore, this study aimed to examine an association between nut consumption and low muscle strength among a representative sample of Korean adults.
Methods
Data source and subjects
The Korea National Health and Nutrition Examination Survey (KNHANES) is a cross-sectional survey of a nationally representative sample of the Korean population ≥1 year(Reference Kweon, Kim and Jang17,Reference Oh, Kim and Kweon18) . We used data from the KNHANES VII (2016–2018). Among 24 269 participants of the KNHANES VII, children <18 years (n 4880), those who did not complete a 24-h dietary recall (n 2535), those missing hand grip strength information (n 1455) and those with implausible energy intake (<500 kcal/d or >4000 kcal/d, n 555) were subsequently excluded. A final sample of 14 844 participants was stratified by sex and age to adjust for possible biological differences(Reference Dodds, Syddall and Cooper19): younger men aged 19–39 years (n 1620), younger women aged 19–39 years (n 2342), middle-aged men aged 40–64 years (n 2799), middle-aged women aged 40–64 years (n 4122), older men ≥65 years (n 1760) and older women ≥65 years (n 2201).
This study was conducted according to the guidelines laid down in the Declaration of Helsinki. The KNHANES data collection procedure was approved by the Institutional Review Board of the Korea Centers for Diseases Control and Prevention (IRB No. 2018-01-03-P-A), and written informed consent was obtained from all participants. Ethical review and approval were waived for the secondary analyses of the KNHANES data by the Institutional Review Board of the Seoul Women’s University (SWU IRB-2023A-02).
Dietary intake measures
Dietary intake data were collected by an in-person 24-h dietary recall by trained staff. Daily intakes of individual foods and nutrients and total energy were calculated using the KNHANES recipe and food composition databases.
We used a culinary definition of nuts including both tree nuts (hazelnuts, acorns, macadamia nuts, chestnuts, Brazil nuts, almonds, gingko nuts, pine nuts, cashew nuts, pecans, walnuts and pistachio nuts) and peanuts. Although peanuts are botanically categorised as legume, their nutrient profiles and culinary use are similar to tree nuts(Reference Ros and Mataix20–Reference Mattes, Kris-Etherton and Foster24). To assess if peanuts have distinct effects on muscle strength, we also reported the association of peanut consumption with low muscle strength separately. In addition, to examine whether nuts particularly rich in MUFA or PUFA (all but chestnut and gingko nut) exert distinguishable effects on muscle strength, we analysed the association of MUFA or PUFA rich nut consumption with low muscle health. Participants were categorised as participants into consumers and non-consumers.
Handgrip strength measures
Handgrip strength was measured in an upright position with the elbow fully extended using the Digital Grip Strength Dynamometer (T.K.K.5401). We used the maximum value of three trials of the dominant hand, expressed in kg. Participants self-determined their eligibility based on a priori criteria (e.g. no acute injury or operation and no amputation or paralysis) from 2016. Low muscle strength was defined as hand grip strength <28 kg for men and <18 kg for women based on the Asian Working Group for Sarcopenia 2019 consensus(Reference Chen, Woo and Assantachai2).
Covariate measures
Information on demographic and socio-economic factors, lifestyle factors and medical history was collected during an in-person health interview using a structured questionnaire. Household income was categorised into quartiles: low (Q1), middle-low (Q2), middle-high (Q3) and high (Q4). Current alcohol consumer was defined as those who drank more than once a month during the year before the interview. Current smoker was defined as those who smoked >100 cigarettes in their lifetime and were still smoking. Regular resistance exercise was defined as performing strength exercise (e.g. push-ups, sit-ups, deadlifts and chin-ups) more than twice a week. Medical history was operationalised as any history of type 2 diabetes, stroke, arthritis, osteoporosis, cancer, kidney disease, myocardial infarction or angina, which may affect dietary intake and muscle health.
Body weight and height were measured during the health examination. BMI was calculated as weight in kg divided by the square of height in metre.
Statistical analyses
All statistical analyses were conducted using the SAS software (Version 9.4, SAS Institute) adjusting for survey design effects. A two-sided P-value < 0·05 was considered statistically significant with the exact P-values presented to enhance interpretation.
General characteristics were described by nut consumption using the means or percentages ± standard errors. Differences in general characteristics between nut consumers and non-consumers were determined using the Rao–Scott χ 2 tests for categorical variables and t-tests for continuous variables. The associations between nut consumption and low muscle strength were analysed using multivariate logistic regression models with the non-consumer group set as the reference group. Unadjusted model estimated crude OR and 95 % CI. Model 1 was adjusted for age, BMI and total energy intake. Model 2 was additionally adjusted for household income, current alcohol consumption, current smoking, regular resistant exercise and medical history. Model 3 added protein intake, an established preventive factor for low muscle mass(Reference Paddon-Jones, Short and Campbell25).
Results
One in four (24·5 %) Korean adults were consuming nuts: 16·8 % in younger men 19–39 years, 19·8 % in younger women 19–39 years, 26·6 % in middle-aged men 40–64 years, 31·4 % in middle-aged women 40–64 years, 26·2 % in older men ≥65 years and 23·3 % in older women ≥65 years (Fig. 1). The most frequently consumed type was peanut.
Fig. 1. Proportion of nut consumers by age and sex. Nut includes tree nuts (hazelnuts, acorns, macadamia nuts, chestnuts, Brazil nuts, almonds, gingko nuts, pine nuts, cashew nuts, pecans, walnuts and pistachio nuts) and peanuts. Nuts high in MUFA or PUFA include all but chestnuts and gingko nuts.
General characteristics of nut consumers and non-consumers are presented by sex and age in online Supplementary Table 1–3. Among younger men and women 19–39 years, nut consumers were older, were more likely to have a higher household income and had a higher protein intake. Among younger men, nut consumers were less likely to be current smokers and had a lower BMI. Among younger women, nut consumers were less likely to be current alcohol consumers and more likely to do regular resistance exercise. No differences in maximal handgrip strength were observed between consumers and non-consumers. Daily mean intakes of nuts among consumers were 8·7 and 9·5 g for younger men and women, respectively (online Supplementary Table 1).
Among middle-aged men and women 40–64 years, nut consumers were older, were more likely to have a higher household income and do regular resistance exercise, less likely to be current smokers and had higher intakes of energy and protein. Among middle-aged women, nut consumers less likely to be current alcohol consumers and had a lower BMI. No statistical differences in maximal handgrip strength were noted between consumers and non-consumers. Daily mean intakes of nuts among consumers were 14·6 and 14·4 g for middle-aged men and women, respectively (online Supplementary Table 2).
Among older men and women ≥65 years, nut consumers were younger, were more likely to have a higher household income, do regular resistance exercise, had higher intakes of total energy and protein and had a higher maximal handgrip strength. No significant differences were observed for current alcohol consumption, medical history (any history of type 2 diabetes, stroke, arthritis, osteoporosis, cancer, kidney disease, myocardial infarction or angina) or BMI (both men and women) or current smoking (women). Nut consumers were less likely be currently smoking than non-consumers only among older men. Daily mean intakes of nuts among consumers were 16·8 and 20·1 g for older men and women, respectively (online Supplementary Table 3).
The associations between nut consumption and low muscle strength differed by age (Table 1). Among younger or middle-aged men and women, there was no significant association between nut consumption and low muscle strength. However, among older men and women, nut consumption was associated with a substantially lower risk of low muscle strength. In the multivariate model 3 that included a range of demographic, socio-economic, lifestyle and dietary factors, older male nut consumers had 45 % reduced risk (OR 0·55; 95 % CI (0·38, 0·79)) and older female nut consumers had 31 % reduced risk (OR 0·69; 95 % CI (0·51, 0·93)) compared with non-consumers. Similar patterns were observed for peanuts alone (Table 2) and for nuts high in MUFA or PUFA (all but chestnut and gingko nut) (Table 3) with the exception that the higher consumption of nuts high in MUFA or PUFA was associated with the higher risk of low muscle strength among younger women 19–39 years.
Table 1. Association between nut consumption and low muscle strength by age and sex (Numbers; odds ratios and 95 % confidence intervals)
* Model 1: adjusted for age, BMI and total energy intake.
† Model 2: adjusted for all covariates included in model 1 plus household income, alcohol consumption, smoking, resistance exercise and medical history.
‡ Model 3: adjusted for all covariates included in model 2 plus protein intake.
§ Unweighted n.
Nut includes tree nuts (hazelnuts, acorns, macadamia nuts, chestnuts, Brazil nuts, almonds, gingko nuts, pine nuts, cashew nuts, pecans, walnuts and pistachio nuts) and peanuts.
Table 2. Association between peanut consumption and low muscle strength by age and sex (Numbers; odds ratios and 95 % confidence intervals)
* Model 1: adjusted for age, BMI and total energy intake.
† Model 2: adjusted for all covariates included in model 1 plus household income, alcohol consumption, smoking, resistance exercise and medical history.
‡ Model 3: adjusted for all covariates included in model 2 plus protein intake.
§ Unweighted n.
Table 3. Association between nuts high in MUFA or PUFA consumption and low muscle strength by age and sex (Numbers; odds ratios and 95 % confidence intervals)
* Model 1: adjusted for age, BMI and total energy intake.
† Model 2: adjusted for all covariates included in model 1 plus household income, alcohol consumption, smoking, resistance exercise and medical history.
‡ Model 3: adjusted for all covariates included in model 2 plus protein intake.
§ Unweighted n.
Nuts high in MUFA or PUFA include all but chestnuts and gingko nuts.
Discussion
Nuts are known as a healthy food group for cardiometabolic health(Reference Balakrishna, Bjørnerud and Bemanian15), but it is not clear if the beneficial effect of nuts extends to muscle health despite close relationship between metabolic health and muscle health(Reference Kalyani, Corriere and Ferrucci26). Therefore, this study investigated the cross-sectional association between nut consumption and low muscle strength among Korean adults by sex and age.
Our analysis of the KNHANES VII (2016–2018) data found that one in four Korean adults were consuming nuts with less than 20 % of younger adults consuming nuts. Among nut consumers, the daily mean intake amounts of nuts among consumers increased by age, but the average nut intakes ranged from 8·7 g (younger men 19–39 years) to 20·1 g (older women ≥65 years). Although the amount of nut consumption is far below than the recommended amounts from multiple dietary guidelines (approximately 30 g/d)(Reference Sievenpiper, Chan and Dworatzek27,Reference Nishi, Viguiliouk and Blanco Mejia28) , older men and women ≥65 years who consumed nuts had substantially lower risks of low muscle strength, after adjusting for confounding factors, compared with those who did not consume nuts. Null or rather disadvantageous associations of nut consumption with low muscle strength among younger adults observed in this study call for further studies using longitudinal data to examine how those associations change across life course or future studies using different cut-offs for low muscle strength because the current cut-offs were derived from older adult data(Reference Chen, Woo and Assantachai2).
Our findings about beneficial effects of nuts on low muscle strength among older adults were consistent with the findings from a prospective study in Spain on a dose–response association of nut consumption with a lower risk of impaired agility and mobility in men and a lower risk of impaired overall physical function in women(Reference Arias-Fernández, Machado-Fragua and Graciani29). Other studies that examined nuts as a component of dietary quality indices also suggested that nuts within a diet are associated with a reduced risk of falling(Reference Ballesteros, Struijk and Rodríguez-Artalejo30) and lower odds of sarcopenia(Reference Hashemi, Motlagh and Heshmat31) and low gait speed(Reference Schacht, Lind and Mertz32), although it is difficult to disentangle the effect of nuts from those of other food components.
To rule out the possibility that the observed beneficial associations between nuts and low muscle strength are driven by protein intake, a well-established preventive dietary factor for low muscle strength(Reference Paddon-Jones, Short and Campbell25), we included total protein intake variable in the multivariate logistic regression model (i.e., model 3). The adjustment for protein intake led to considerable attenuation in older women as expected, but not in men, and the associations between nuts and low muscle strength were still significant in both older women and men. These results suggest that nut consumption has unique benefits beyond total protein intake, which may be partially attributable to protein quality, dietary fibre, MUFA and PUFA, minerals and phytochemicals contributed by nuts(Reference Alasalvar and Bolling16).
In particular, nuts are very good sources of MUFA and PUFA, contributing about 16 % of MUFA and 17 % of PUFA but only 8 % of SFA among nut-consuming older adults. Higher intakes of MUFA and PUFA were associated with a lower risk of muscle weakness operationalised as lowest quintile of handgrip strength, whereas higher intake of SFA intake was associated with an increased risk of lower-extremity functional impairment among older adults(Reference Arias-Fernández, Struijk and Rodríguez-Artalejo33). Several fish oil or n-3 supplementation trials supported beneficial effect of PUFA on muscle mass and function among older adults(Reference Smith, Julliand and Reeds34–Reference Krzymińska-Siemaszko, Czepulis and Lewandowicz36). MUFA is known to improve metabolic fitness(Reference Jones, Jew and AbuMweis37,Reference Esposito, Kastorini and Panagiotakos38) by increasing fatty acid oxidation and decreasing inflammation in both skeletal muscle and adipose tissue(Reference Lim, Gerhart-Hines and Dominy39–Reference Shin and Ajuwon41). The high ratio of MUFA or PUFA to SFA in nuts might help to prevent sarcopenia partially through anti-inflammatory pathways considering that the decline of muscle strength and function can be caused by adipose inflammation(Reference Li, Yu and Shyh-Chang42) and through stimulation of anabolic signalling in myocytes(Reference Tachtsis, Camera and Lacham-Kaplan43).
The major strengths of this study include the use of a large nationally representative data collected using validated methods, but several limitations should be considered when interpreting the results. First, there remains a possibility of residual confounding and reverse causation coming from the cross-sectional nature of the KNHANES. Second, the KNHANES VII did not include measurements of muscle mass and physical performance, so we could not formally diagnose sarcopenia. However, handgrip strength is a practical indicator of whole muscle strength and physical function(Reference Tatangelo, Muollo and Ghiotto44), and we were able to define low muscle strength based on handgrip strength cut-offs recommended by the Asian Working Group for Sarcopenia 2019 consensus(Reference Chen, Woo and Assantachai2). Nonetheless, the applicability of these cut-offs derived from older adult data is yet to be confirmed. Indeed, the prevalence of low muscle strength was less than 3 % among younger and middle-aged men and less than 10 % among younger and middle-aged women, which may be one of the reasons for null associations among younger and middle-aged adults. Lastly, nut intake measured via single 24-h recall may not fully reflect usual nut intake.
In summary, this study observed an inverse association between nut consumption and low muscle strength among Korean older adults. Our findings suggest that consuming nuts may be beneficial in lowering the risk of low muscle strength among older adults, although longitudinal and intervention studies are warranted to confirm the true effect of nuts on muscle strength as well as to reveal underlying biological mechanisms.
Acknowledgements
We thank all research staff who contributed to the KNHANES data collection. This work was supported by a research grant from Seoul Women’s University (2021-0089).
Conceptualisation: S. S.; investigation: S. J. and S. S.; writing – original draft: S. J. and S. S.; writing – review and editing: S. J. and S. S.; funding acquisition: S. S.; supervision: S. S.
There are no conflicts of interest.
Supplementary material
For supplementary material referred to in this article, please visit https://doi.org/10.1017/S0007114523002386
