Abstract
Background
There is scarce epidemiological evidence regarding the relationships of the consumption of different types of vegetables or fruits with change in skeletal muscle strength. We prospectively examined the relationships among Japanese adults, using handgrip strength to assess skeletal muscle strength.
Methods
A 3-year study was carried out with 259 Japanese adults who were 22–68 years of age. The frequency of consumption of different types of vegetables or fruits were obtained using a validated self-administered dietary history questionnaire. Handgrip strength was measured with a handheld digital Smedley dynamometer.
Results
After adjustment for confounding factors, the mean change in handgrip strength in participants stratified according to the level of tomato and tomato product consumption at baseline were −3.2 (95% confidence interval [CI], −4.0 to −2.3) for <1 time/week, −2.7 (95% CI, −3.6 to −1.8) for 1 time/week, −1.6 (95% CI, −2.5 to −0.8) for 2–3 times/week, and −1.7 (95% CI, −2.8 to −0.7) for ≥4 times/week, (P for trend = 0.022). However, the significant relationships of consumption of other types of vegetables and different types of fruits with change in handgrip strength were not observed.
Conclusion
Higher consumption of tomato and tomato product at baseline was significantly associated with reduced decline in handgrip strength among Japanese adults over a 3-year follow-up period. This study suggests that consumption of tomato and tomato product could be protective against the decline in skeletal muscle strength associated with aging.
Key words: consumption of tomato and tomato product, handgrip strength, Japanese adults
INTRODUCTION
It is well known that aging leads to numerous anatomical and physiological degenerative changes, which can adversely affect physical function and skeletal muscle strength. Epidemiological studies have confirmed that lower skeletal muscle strength may predict all-cause mortality1 as well as several chronic diseases, including metabolic syndrome,2 type 2 diabetes mellitus,3 and cardiovascular disease.4 Thus, we considered that identification of easily modifiable determinants of decline in skeletal muscle strength is essential to the development of an effective preventive strategy.
Although the exact biological mechanisms involved in decline in skeletal muscle strength are not fully understood, enhanced oxidative stress may play an important role in individuals with lower skeletal muscle strength.5 In recent years, several studies have reported that dietary antioxidants, in particular, vitamin C, vitamin E, carotenoids, and lycopene, can help to protect against the decline in skeletal muscle strength with aging. Two cross-sectional studies showed that higher levels of dietary vitamin C6 and vitamin E7 were each independently associated with higher skeletal muscle strength in older women. In addition, a 6-year follow-up survey among older adults showed that those with lower plasma carotenoid levels are at a higher risk of declining skeletal muscle strength.8 However, lycopene has a stronger antioxidant ability to quench singlet oxygen and scavenge free radicals. Indeed, the antioxidant capacity of lycopene is 100 times that of vitamin E and 2 times that of other carotenes.9 Therefore, although lycopene may have a more favorable influence on the decline in skeletal muscle strength as compared to other antioxidants, the relationship between the consumption of dietary lycopene and decline in skeletal muscle strength has not been revealed.
Thus, we designed a 3-year longitudinal study to examine the relationship of the frequency of tomato and tomato product consumption, the richest dietary sources of lycopene, with change in handgrip strength among Japanese adults. To characterize the unique impact of consuming tomato and tomato product, fruit that are also rich in a large number of phytochemical antioxidants, we also examined the relationships of consumption of other types of vegetables and different types of fruits with change in handgrip strength.
METHODS
Study population
The Oroshisho study was carried out from 2008 to 2011 as continuous cross-sectional studies of 1,253 individuals working at the Sendai Oroshisho Center, which includes more than 120 small and medium size organizations in Sendai, Japan. A detailed study design has been previously published.10 Briefly, we recruited 1,253 individuals at baseline, who each received an annual health examination. Of these, 1,154 individuals agreed to participate and gave informed consent for analysis of their data. Of these, 617 individuals were excluded due to the following incomplete data at baseline (occupation, n = 6; drinking frequency, n = 73; metabolic syndrome, n = 5; adiponectin, n = 3; high-sensitivity C-reactive protein [hs-CRP], n = 1; physical activity [PA], n = 11; tomato and tomato product consumption, n = 1; handgrip strength, n = 517). We also excluded 278 individuals due to missing data on handgrip strength during the 3-year follow-up period. A total of 259 individuals (201 males and 58 females) were included in the study. Ethics approval was obtained from the Institutional Review Board of the Tohoku University Graduate School of Medicine.
Dietary frequency assessment
All study participants completed a brief self-administered dietary history questionnaire (BDHQ) that assessed intake of 75 principal food items, with specified consumption frequency to assess the usual consumption of tomato and tomato product (tomato; tomato ketchup; stewed tomato; or tomato stew), other types of vegetables (green-leaf vegetables; cabbage and Chinese cabbage; carrot and pumpkin; Japanese white radish [daikon] and turnips; and onion, burdock, and lotus root), different types of fruits (citrus fruit; strawberries, persimmon and kiwifruit; apple and banana), and other dietary components during the preceding month. Individuals answered these questions using seven possible responses as follows: 0, <1, 1, 2–3, 4–6, 7, or ≥14 times/week. Based on the distribution of frequency, the frequency of consumption of tomato and tomato product and other types of vegetables was divided into four categories: <1 time/week, 1 time/week, 2–3 times/week, and ≥4 times/week; the frequency of consumption of different types of fruits was divided into three categories: 0 times/week, <1 time/week and ≥1 time/week. To calculate the frequency of combined or separated vegetable and fruit consumption, the monthly consumption frequency of each item was calculated and summed to create a new frequency of combined or separated vegetable and fruit consumption, and then these consumptions was converted into the weekly consumption frequency. Based on the distribution of frequency, combined or separated vegetable and fruit consumption were re-categorized as <4 times/week; 4–6 times/week, and ≥7 times/week. Daily nutrient intake, including total energy, total protein, calcium, and vitamin D were calculated using an ad hoc computer program for the BDHQ, with reference to the 5th edition of the Standard Tables of Food Composition in Japan. The reproducibility and validity of the BDHQ have been described in detail elsewhere.11
Handgrip strength measurement
Handgrip strength was measured using a handheld digital Smedley dynamometer (TKK 5401; Takei Scientific Instruments Co., Ltd., Niigata, Japan). All individuals were told to adjust dynamometer width for optimal hand comfort, and to relax their arm in a standing and stationary position. Each individual made two attempts using each hand with a brief interval between trials. The highest of all four handgrip strength measures was used as a representative value of skeletal muscle strength. The change in handgrip strength was calculated as: handgrip strength at follow-up − handgrip strength at baseline.
Relevant covariant
Height and weight were measured using standard protocols. Body mass index (BMI) was calculated as weight (kg) divided by height squared (m2). Blood samples were drawn from the antecubital vein of seated subjects in the morning, following overnight fasting. Metabolic syndrome was defined according to the criteria of the American Heart Association Scientific Statement of 2009 for persons of Asian ethnicity (including Japanese).12 Serum adiponectin was measured using a specific sandwich enzyme-linked immunosorbent assay (Otsuka Pharmaceutical, Tokyo, Japan), and the intra- and inter-assay coefficients of variation were <10%. The concentration of serum hs-CRP was measured using N-latex CRP-2 (Siemens Healthcare Japan, Tokyo, Japan). Demographic variables and lifestyle factors were assessed using a self-administered questionnaire. Variables and factors assessed by the questionnaire included: sex (males or females), age (continuous variable), occupation (desk work or not), smoking status (never, former or current) and sleep duration (6–8 hr or not). Drinking frequency (7 times/week, 1–6 times/week or none) was also assessed using the BDHQ.11 Levels of PA were assessed using the International Physical Activity Questionnaire.13 The total weekly PA was calculated as follows: (daily hours of walking × days per week with walking × 3.3) + (daily hours of moderate intensity activity × days per week with moderate-intensity activity × 4.0) + (daily hours of vigorous activity × days per week with vigorous activity × 8.0). The total weekly PA was calculated as metabolic equivalents (METs·h/week).
Statistical analysis
All statistical analyses were performed with SPSS (version 20.0; SPSS, Chicago, IL, USA). For the baseline characteristics of subjects, continuous variables are expressed as means and 95% confidence intervals, and categorical variables are expressed as percentages. Continuous data with skewed distributions, as determined using the Kolmogorov-Smirnov test, were logarithmically transformed. Analysis of covariance (ANCOVA) and logistic regression analysis was used to compare the baseline characteristics of the categorized group, after adjustment for sex and age. The categories of frequency for consumption of tomato and tomato product were considered the independent variables, and baseline variables were considered dependent variables.
ANCOVA was also used to estimate the change in handgrip strength based on the categories of consumption of tomato and tomato product, and other types of vegetables and different types of fruits with adjustment for age (continuous variable) at baseline (model 1). Model 2 was further adjusted for demographic, lifestyle, and clinic variables, such as: sex (categorical variable: males or females), occupation (categorical variable: desk work or not), smoking status (categorical variable: never, former, or current), drinking frequency (categorical variable: 7 times/week, 1–6 times/week or none), PA (continuous variable), sleep duration (categorical variable: 6–8 hr or not), BMI (continuous variable), metabolic syndrome (categorical variable: yes or no), hs-CRP (continuous variable), serum adiponectin (continuous variable), and handgrip strength (continuous variable) at baseline. Model 3 was further adjusted for daily nutrient intake and different types of vegetables and fruits consumption, such as: total energy (continuous variable), total protein (continuous variable), calcium (continuous variable), vitamin D (continuous variable), and mutual other types of vegetables (continuous variable) or mutual other types of fruits consumption (continuous variable) at baseline.
We also explored in more detail whether or not combined or separated vegetable and fruit consumption have a protective effect on decline in handgrip strength. Thus, we used multivariate adjusted models to assess the relationships between combined or separated vegetable and fruit consumption, and change in handgrip strength. Two-sided P values <0.05 were considered significant.
RESULTS
The participants’ baseline characteristics, according to categories of consumption of tomato and tomato product are shown in Table 1. The higher frequency categories for consumption of tomato and tomato product contained a lower proportion of males (P for trend = 0.004), and higher average age than other frequency categories (P for trend = 0.005). Individuals with a higher frequency of consumption of tomato and tomato product also consumed more other types of vegetables (all P for trend <0.001), and citrus fruit (P for trend: 0.034), strawberries, persimmon and kiwifruit (P for trend: 0.008), apple and banana (P for trend: 0.026) and had higher consumption levels of total energy, total protein, calcium and vitamin D (all P for trend ≤0.005).
Table 1. Sex- and age-adjusted subject’s baseline characteristics according to frequency of consumption of tomatoes and tomato productsa.
| Participants (n = 259) | Categories of tomato and tomato product consumption | P for trendb | |||
| <1 time/week | 1 time/week | 2–3 times/week | ≥4 times/week | ||
| (n = 70) | (n = 62) | (n = 70) | (n = 57) | ||
| Mean intake, g/day | 3.6 | 11.3 | 27.5 | 64.6 | — |
| Grip strength (at baseline), kg | 40.9 (39.5, 42.3) | 42.5 (41.0, 44.0) | 40.3 (39.0, 41.7) | 40.2 (38.6, 41.8) | 0.220 |
| Grip strength (at follow-up), kg | 37.6 (36.2, 39.0) | 39.5 (38.1, 41.0) | 38.9 (37.5, 40.3) | 38.6 (37.0, 40.2) | 0.505 |
| Demographic characteristics | |||||
| Sex (males), % | 82.9 | 85.5 | 77.1 | 63.2 | 0.004 |
| Age, years | 43.6 (41.3, 46.0) | 44.3 (41.8, 46.8) | 45.1 (42.7, 47.4) | 48.8 (46.2, 51.5) | 0.005 |
| Occupation (desk work), % | 44.3 | 37.1 | 45.7 | 63.2 | 0.369 |
| Lifestyle characteristics | |||||
| Smoking status | |||||
| Current, % | 50.0 | 54.8 | 42.9 | 33.3 | 0.135 |
| Former, % | 7.1 | 19.4 | 17.1 | 14.0 | 0.135 |
| Drinking frequency | |||||
| 7 times/week, % | 28.6 | 32.3 | 34.3 | 22.8 | 0.734 |
| 1–6 times/week, % | 71.4 | 67.7 | 65.7 | 77.2 | 0.734 |
| PA, MET·h·week−1 | 51.0 (34.1, 68.0) | 34.0 (16.0, 52.0) | 33.4 (16.5, 50.3) | 33.0 (13.8, 52.1) | 0.190 |
| Sleep duration (6–8 hr), % | 57.1 | 38.7 | 57.1 | 63.2 | 0.210 |
| Clinic characteristics | |||||
| BMI, kg/m2 | 23.3 (22.5, 24.1) | 23.5 (22.7, 24.3) | 22.8 (22.0, 23.6) | 22.7 (21.8, 23.5) | 0.158 |
| Metabolic syndrome, % | 17.1 | 22.6 | 11.4 | 19.3 | 0.598 |
| Hs-CRP, mg/L | 0.7 (0.2, 1.3) | 1.0 (0.4, 1.6) | 1.3 (0.7, 1.9) | 0.6 (−0.1, 1.2) | 0.220 |
| Adiponectin, mg/L | 7.1 (6.3, 7.9) | 6.9 (6.0, 7.7) | 7.7 (6.9, 8.6) | 7.2 (6.3, 8.2) | 0.990 |
| Daily nutrient intake | |||||
| Total energy intake, kcal/day | 1707.3 (1562.1, 1852.5) | 1869.7 (1715.5, 2023.8) | 2001.9 (1857.6, 2146.2) | 2160.2 (1996.0, 2324.4) | <0.001 |
| Total protein intake, g/day | 55.9 (50.3, 61.5) | 59.8 (53.8, 65.8) | 69.3 (63.7, 74.9) | 73.1 (66.8, 79.5) | <0.001 |
| Calcium, mg/day | 374.8 (326.0, 423.6) | 424.0 (372.2, 475.9) | 522.6 (474.0, 571.1) | 557.1 (501.9, 612.4) | <0.001 |
| Vitamin D, µg/day | 9.6 (7.7, 11.4) | 9.9 (7.9, 11.9) | 13.7 (11.8, 15.6) | 12.9 (10.8, 15.0) | 0.005 |
| Other types of vegetables consumption | |||||
| Green-leaf vegetables, g/day | 18.5 (11.5, 25.5) | 28.4 (21.0, 35.9) | 36.3 (29.4, 43.2) | 54.2 (46.3, 62.1) | <0.001 |
| Cabbage and Chinese Cabbage, g/day | 21.7 (15.5, 27.8) | 27.5 (21.0, 34.0) | 33.0 (26.9, 39.1) | 46.8 (39.8, 53.7) | <0.001 |
| Carrot and pumpkin, g/day | 9.9 (6.4, 13.5) | 13.3 (9.5, 17.1) | 19.1 (15.6, 22.7) | 24.3 (20.3, 28.4) | <0.001 |
| Japanese white radish and Turnips, g/day | 15.5 (10.5, 20.4) | 15.0 (9.8, 20.2) | 20.9 (16.0, 25.8) | 32.1 (26.6, 37.7) | <0.001 |
| Onion, burdock, lotus root, g/day | 19.6 (14.2, 25.0) | 24.9 (19.2, 30.7) | 30.0 (24.6, 35.3) | 43.0 (36.8, 49.1) | <0.001 |
| Fruit consumption | |||||
| Citrus Fruit, g/day | 5.7 (0.7, 10.7) | 13.3 (8.0, 18.6) | 12.2 (7.2, 17.2) | 16.5 (10.9, 22.2) | 0.034 |
| Strawberries, persimmon and Kiwifruit, g/day | 3.2 (−0.6, 7.1) | 6.9 (2.8, 11.0) | 6.8 (3.0, 10.6) | 12.1 (7.8, 16.5) | 0.008 |
| Apple and banana, g/day | 17.0 (10.1, 23.9) | 22.5 (15.2, 29.9) | 25.9 (19.1, 32.8) | 39.3 (31.5, 47.1) | 0.026 |
BMI, body mass index; hs-CRP, hig-sensitivity C-reactive protein; MET, metabolic equivalent; PA, physical activity.
aContinuous variable without a normal distribution were log-transformed; Continuous variables are expressed as the estimated geometric means (95% confidence intervals) and categorical variables are expressed as percentages.
bLinear trends were assessed using ANCOVA for continuous variables and logistic regression analyses for categorical variables.
Table 2 shows the relationships of the frequency of consumption of tomato and tomato product and other types of vegetables at baseline with change in handgrip strength over the 3-year follow-up period. Higher frequency of consumption of tomato and tomato product was associated with reduced decline in handgrip strength after adjustment for all covariates. In model 3, the mean change in handgrip strength among the categories of tomato and tomato product consumption were −3.2 (95% CI, −4.0 to −2.3) for <1 time/week, −2.7 (95% CI, −3.6 to −1.8) for 1 time/week, −1.6 (95% CI, −2.5 to −0.8) for 2–3 times/week, and −1.7 (95% CI, −2.8 to −0.7) for ≥4 times/week (P for trend = 0.022). We also conducted a stratified gender-specific analysis, which confirmed that consumption of tomato and tomato product was associated negatively with the change in handgrip strength among males (P for trend = 0.028); for females, there was not a negative relationship between consumption of tomato and tomato product and change in handgrip strength (P for trend = 0.102) (eTable 1). There were no significant relationships between the consumption of other types of vegetables and changes in handgrip strength.
Table 2. Multivariable-adjusted relationships of consumption of different types of vegetables with change in handgrip strength during the 3-year follow-up period.
| n = 259 | Number of participants | Mean intake, g/day | Model 1a | Model 2b | Model 3c |
| Categories of tomato and tomato product consumption | |||||
| <1 time/week | 70 | 3.6 | −3.3 (−4.2, −2.5) | −3.2 (−4.0, −2.4) | −3.2 (−4.0, −2.3) |
| 1 time/week | 62 | 11.3 | −3.0 (−4.0, −2.1) | −2.7 (−3.5, −1.8) | −2.7 (−3.6, −1.8) |
| 2–3 times/week | 70 | 27.5 | −1.5 (−2.4, −0.6) | −1.6 (−2.4, −0.8) | −1.6 (−2.5, −0.8) |
| ≥4 times/week | 57 | 64.6 | −1.4 (−2.3, −0.4) | −1.8 (−2.8, −0.9) | −1.7 (−2.8, −0.7) |
| P for trendd | — | — | <0.001 | 0.012 | 0.022 |
| Categories of green-leaf vegetables consumption | |||||
| <1 time/week | 59 | 4.1 | −3.7 (−4.6, −2.7) | −3.3 (−4.2, −2.4) | −3.1 (−4.1, −2.1) |
| 1 time/week | 54 | 13.0 | −2.3 (−3.3, −1.3) | −2.5 (−3.4, −1.6) | −2.4 (−3.4, −1.4) |
| 2–3 times/week | 82 | 32.1 | −1.4 (−2.2, −0.5) | −1.5 (−2.2, −0.7) | −1.6 (−2.3, −0.8) |
| ≥4 times/week | 64 | 79.9 | −2.3 (−3.2, −1.4) | −2.4 (−3.2, −1.5) | −2.5 (−3.5, −1.4) |
| P for trendd | — | — | 0.019 | 0.051 | 0.305 |
| Categories of cabbage and Chinese cabbage consumption | |||||
| <1 time/week | 39 | 5.0 | −3.0 (−4.2, −1.8) | −2.6 (−3.7, −1.5) | −2.1 (−3.3, −0.9) |
| 1 time/week | 63 | 12.7 | −1.9 (−2.8, −1.0) | −2.1 (−2.9, −1.2) | −1.9 (−2.8, −1.0) |
| 2–3 times/week | 109 | 32.7 | −2.4 (−3.2, −1.7) | −2.4 (−3.1, −1.7) | −2.4 (−3.0, −1.7) |
| ≥4 times/week | 48 | 75.8 | −2.1 (−3.2, −1.0) | −2.3 (−3.3, −1.3) | −2.9 (−4.2, −1.7) |
| P for trendd | — | — | 0.408 | 0.804 | 0.342 |
| Categories of carrot and pumpkin consumption | |||||
| <1 time/week | 66 | 2.5 | −3.2 (−4.1, −2.3) | −2.9 (−3.8, −2.1) | −2.8 (−3.8, −1.9) |
| 1 time/week | 55 | 7.4 | −2.2 (−3.2, −1.2) | −2.4 (−3.3, −1.4) | −2.4 (−3.3, −1.4) |
| 2–3 times/week | 95 | 18.2 | −1.9 (−2.7, −1.2) | −1.9 (−2.6, −1.2) | −1.9 (−2.6, −1.2) |
| ≥4 times/week | 43 | 45.1 | −2.0 (−3.1, −0.9) | −2.1 (−3.2, −1.1) | −2.4 (−3.8, −0.9) |
| P for trendd | — | — | 0.091 | 0.189 | 0.554 |
| Categories of Japanese white radish (daikon) and turnips consumption | |||||
| <1 time/week | 76 | 3.4 | −2.2 (−3.1, −1.3) | −2.3 (−3.1, −1.5) | −2.0 (−2.9, −1.1) |
| 1 time/week | 75 | 11.0 | −2.1 (−3.0, −1.3) | −2.3 (−3.1, −1.5) | −2.2 (−3.0, −1.4) |
| 2–3 times/week | 78 | 27.8 | −2.7 (−3.5, −1.8) | −2.4 (−3.2, −1.6) | −2.5 (−3.3, −1.7) |
| ≥4 times/week | 30 | 68.4 | −2.2 (−3.6, −0.8) | −2.2 (−3.5, −0.9) | −3.0 (−4.6, −1.3) |
| P for trendd | — | — | 0.824 | 0.956 | 0.330 |
| Categories of onion, burdock, lotus root consumption | |||||
| <1 time/week | 39 | 3.7 | −2.3 (−3.5, −1.1) | −2.3 (−3.4, −1.2) | −2.0 (−3.2, −0.8) |
| 1 time/week | 67 | 11.1 | −2.4 (−3.3, −1.5) | −2.6 (−3.4, −1.7) | −2.4 (−3.3, −1.5) |
| 2–3 times/week | 91 | 27.9 | −2.5 (−3.3, −1.7) | −2.3 (−3.0, −1.5) | −2.2 (−2.9, −1.4) |
| ≥4 times/week | 62 | 65.1 | −2.0 (−2.9, −1.0) | −2.1 (−3.0, −1.2) | −2.7 (−3.7, −1.6) |
| P for trendd | — | — | 0.701 | 0.696 | 0.503 |
aModel 1: Adjusted for age (continuous variable) at baseline.
bModel 2: Adjusted for the variables in model 1 and sex (categorical variable), occupation (categorical variable: desk work or not), smoking status (categorical variable: never, former, or current), drinking frequency (categorical variable: 7 times/week, 1–6 times/week and none), PA (continuous variable), sleep duration (categorical variable: 6–8 hours or not), BMI (continuous variable), metabolic syndrome (categorical variable: yes or no), hs-CRP (continuous variable), adiponectin (continuous variable), and handgrip strength at baseline.
cModel 3: Adjusted for the variables in model 2 and total energy (continuous variable), total protein (continuous variable), calcium (continuous variable), vitamin D (continuous variable) and mutual other types of vegetables (continuous variable) and fruit consumption (continuous variable: citrus fruit; strawberries, persimmon and kiwifruit; apple and banana) at baseline.
dLinear trends were assessed using ANCOVA.
We also investigated the relationships of different types of fruits consumption and pooled vegetable and fruit consumption with change in handgrip strength. However, the relationships of different types of fruits and pooled vegetable and fruit consumption with reduced decline in handgrip strength were not significant (Table 3 and Figure 1).
Table 3. Multivariable-adjusted relationships of consumption of different types of fruits with change in handgrip strength during the 3-year follow-up period.
| n = 259 | Number of participants | Mean intake, g/day | Model 1a | Model 2b | Model 3c |
| Categories of citrus fruit consumption | |||||
| 0 times/week | 112 | 0.0 | −2.2 (−2.9, −1.5) | −2.1 (−2.8, −1.5) | −2.0 (−2.7, −1.3) |
| <1 time/week | 71 | 6.7 | −2.8 (−3.7, −1.9) | −2.6 (−3.4, −1.7) | −2.7 (−3.5, −1.9) |
| ≥1 time/week | 76 | 33.5 | −2.0 (−2.9, −1.2) | −2.4 (−3.2, −1.6) | −2.4 (−3.3, −1.6) |
| P for trendd | — | — | 0.699 | 0.619 | 0.486 |
| Categories of strawberries, persimmon and kiwifruit consumption | |||||
| 0 times/week | 146 | 0.0 | −2.4 (−3.0, −1.8) | −2.4 (−2.9, −1.8) | −2.3 (−2.9, −1.7) |
| <1 time/week | 62 | 6.7 | −2.3 (−3.3, −1.4) | −2.4 (−3.3, −1.5) | −2.5 (−3.3, −1.6) |
| ≥1 time/week | 51 | 27.5 | −2.1 (−3.1, −1.0) | −2.1 (−3.1, −1.1) | −2.2 (−3.2, −1.2) |
| P for trendd | — | — | 0.583 | 0.613 | 0.855 |
| Categories of apple and banana consumption | |||||
| 0 times/week | 25 | 0.0 | −2.3 (−3.8, −0.8) | −1.9 (−3.3, −0.5) | −1.7 (−3.1, −0.2) |
| <1 time/week | 78 | 6.6 | −2.7 (−3.6, −1.9) | −2.6 (−3.4, −1.9) | −2.5 (−3.3, −1.7) |
| ≥1 time/week | 156 | 39.3 | −2.1 (−2.7, −1.5) | −2.2 (−2.8, −1.7) | −2.3 (−2.9, −1.8) |
| P for trendd | — | — | 0.832 | 0.651 | 0.417 |
aModel 1: Adjusted for age (continuous variable) at baseline.
bModel 2: Adjusted for the variables in model 1 and sex (categorical variable), occupation (categorical variable: desk work or not), smoking status (categorical variable: never, former, or current), drinking frequency (categorical variable: 7 times/week, 1–6 times/week and none), PA (continuous variable), sleep duration (categorical variable: 6–8 hours or not), BMI (continuous variable), metabolic syndrome (categorical variable: yes or no), hs-CRP (continuous variable), adiponectin (continuous variable), and handgrip strength at baseline.
cModel 3: Adjusted for the variables in model 2 and total energy (continuous variable), total protein (continuous variable), calcium (continuous variable), vitamin D (continuous variable) and mutual other types of fruits (continuous variable) and vegetable consumption (continuous variable: tomato and tomato product; green-leaf vegetables; cabbage and Chinese cabbage; carrot and pumpkin; Japanese white radish [daikon] and turnips; onion, burdock, lotus root) at baseline.
dLinear trends were assessed using ANCOVA.
Figure 1. Pooled analysis of relationships of vegetable and fruit consumption with change in handgrip strength among Japanese adults (2008–2011). Means for change in handgrip strength are presented for total vegetable and fruit, vegetable, fruit consumption. The multivariate model that was adjusted for covariates as in Table 2 excluded total vegetable and fruit, vegetable, and fruit consumption.
DISCUSSION
This 3-year longitudinal study examined the relationships of the frequency of consumption of different types of vegetables or fruits with change in handgrip strength over time among Japanese adults. These results showed a significant relationship of higher baseline frequency of consumption of tomato and tomato product, but not other types of vegetables and different types of fruits, with reduced decline in handgrip strength, after adjustment for confounding factors. Our findings suggested that consumption of tomato and tomato product could be protective against the decline in skeletal muscle strength associated with aging among Japanese adults.
Results from this longitudinal study support the hypothesis that higher consumption of tomato and tomato product, but not other types of vegetables, could slow the decline in skeletal muscle strength associated with aging. The present findings here are consistent with those of several previous studies. For instance, Kim et al14 investigated the relationship of vegetable and fruit consumption with sarcopenia in older adults through a cross-sectional study and found that higher consumption of vegetable and fruit was associated with a lower risk of sarcopenia. Additionally, an interventional study showed that increased consumption of vegetable and fruit may modestly increase handgrip strength in older adults.15
Regarding potential mechanisms underlying the relationship of the frequency of consumption of tomato and tomato product with decline in handgrip strength, antioxidants present in tomato may mediate this effect. Skeletal muscles are one of the largest oxygenated tissues, and muscle fibers continuously generate reactive oxygen species with aging.16 Oxidative damage is increased when the production of reactive oxygen species increases and/or the antioxidant status decreases. Moreover, according to the cellular constituents affected by the oxidative stress, lipid peroxidation,17 protein oxidation,18 and DNA damage19 will result in abnormalities of cellular structures, leading to cell death. Such cellular decline is believed to be responsible for the degeneration of skeletal muscle strength.16 Tomato and tomato product account for more than 85% of all the dietary sources of lycopene, a powerful antioxidant.20 Lycopene is a lipid-soluble carotenoid that can interact with the lipid membrane bilayer. It has the ability to scavenge free radicals and quench singlet oxygen21; dietary antioxidants are efficient in preventing oxidative damage to lipoproteins.22 Antioxidant supplements are reported to reduce oxidative DNA damage21 and to improve protein synthesis.23 Therefore, dietary lycopene may help delay the decline in skeletal muscle strength.
The present study also revealed that a higher frequency of consumption of tomato and tomato product was associated with higher levels of consumption of trace elements, including vitamin D and calcium. A randomized controlled trial has shown that vitamin D and calcium supplementation was associated with an increase in skeletal muscle strength in older populations.24 Vitamin D and calcium intake may enhance nerve conduction and transmission at the neuromuscular junction and, in turn, enhance contraction of skeletal muscles.25 However, additional adjustment for dietary intake of vitamin D and calcium in our analysis did not alter our findings.
Alternatively, cooking methods could also explain our findings that higher consumption of tomato and tomato product, but not other types of vegetables, was significantly associated with reduced decline in handgrip strength. In Japan, tomato is most often consumed raw, while other types of vegetables are frequently consumed after cooking. A biochemical study showed that the cooking method not only affects the nutritional composition of food but also the level of available bioactive compounds.26 Experimental studies have provided evidence that cooking has a significant destructive effect on the antioxidant activity in food products,27,28 and antioxidants are leached from food to the cooking water29 or oil.30 Indeed, Danesi et al proposed that, at least for antioxidant activity, raw and fresh vegetable have superior nutritional value compared to cooked vegetable.27 Thus, further studies are needed to examine the influence of cooking methods of vegetable on the change in handgrip strength over time.
Although fruit also rich in a large number of phytochemical antioxidants, such as carotenoids and vitamin C, we did not find the significant relationships between the consumption of different types of fruits or total fruit and change in handgrip strength. It is possible that, in our population, fruit consumption was at an insufficient level to show no relationship with handgrip strength (the median consumption of total fruit was 2 times/week). In a mean 2.5-year follow-up study, fruit consumption was not associated with improvement of skeletal muscle strength among community-dwelling older adults, even in populations with an average consumption of 3 portions of fruit/day.31
We also conducted analysis regarding the relationships of pooled frequency of vegetable and fruit or vegetable consumption with change in handgrip strength. However, the current study did not show any significant relationships in multivariate analysis. It is possible that the participants in our study who ate tomato and tomato product more frequently could have consumed fewer other types of vegetables or fruits. Further study is needed to clarify the relationships of pooled frequency of vegetable and fruit or vegetable consumption with change in handgrip strength.
We also considered potential confounding factors, including age, BMI, occupation, smoking status, drinking frequency, PA, sleep duration, metabolic syndrome, hs-CRP, adiponectin, consumption of total energy, total protein and handgrip strength at baseline. However, the relationship remained significant, even after adjustment for these confounding factors. Our results suggest that consumption of tomato and tomato product is independently associated with the decline in handgrip strength observed in aging.
There are limitations in the present study. First, due to our observational design, it is difficult to draw a causal relationship. Future studies should focus on confirming causality using interventional or experimental methods. Second, our regional results may not be representative of other populations. Further studies with larger sample sizes are essential to confirm these findings. Third, although the validated BDHQ was used to survey dietary information, there is still some subjectivity in self-reporting. Fourth, the present study did not measure muscle fiber size or muscle mass, both of which are predictive factors for skeletal muscle strength. Therefore, further studies are warranted to assess these two indicators. Fifth, the relatively large number of participants who were not recruited and those who did not return for follow-up might have biased the results; we examined whether there are differences in independent variables between participants and nonparticipants, but there were no significant relationships among them (eTable 2).
In conclusion, this study found that increased frequency of consumption of tomato and tomato product was associated with reduced decline in handgrip strength among Japanese adults, even after consideration of potential confounders. Therefore, this study suggests that consumption of tomato and tomato product may be protective against the decline in skeletal muscle strength associated with aging.
ACKNOWLEDGMENTS
The authors thank the study participants who agreed to participate and gave informed consent for analysis of their data. We also would like to thank our staff from the Sendai Oroshisho Center for their dedicated work. This study was supported by a Grant-in-Aid under the Knowledge Cluster Initiative from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and partially supported by the Center of Innovation Program from Japan Science and Technology Agency.
Conflicts of interest: None declared.
APPENDIX A. SUPPLEMENTARY DATA
The following is the supplementary data related to this article:
eTable 1. Multivariable-adjusted sex-specific relationships of consumption of tomato and tomato product and other types of vegetables with change in handgrip strength during the 3-year follow-up period
eTable 2. Subject’s baseline characteristics according to handgrip strength with missing values and without missing values at baseline and follow-up period
REFERENCES
- 1.Stenholm S, Mehta NK, Elo IT, Heliövaara M, Koskinen S, Aromaa A. Obesity and muscle strength as long-term determinants of all-cause mortality—a 33-year follow-up of the Mini-Finland Health Examination Survey. Int J Obes (Lond). 2014;38:1126–1132. 10.1038/ijo.2013.214 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Kawamoto R, Ninomiya D, Kasai Y, et al. Handgrip strength is associated with metabolic syndrome among middle-aged and elderly community-dwelling persons. Clin Exp Hypertens. 2016;38:245–251. 10.3109/10641963.2015.1081232 [DOI] [PubMed] [Google Scholar]
- 3.Van der Kooi AL, Snijder MB, Peters RJ, van Valkengoed IG. The association of handgrip strength and type 2 diabetes mellitus in six ethnic groups: an analysis of the HELIUS study. PLoS One. 2015;10:e0137739. 10.1371/journal.pone.0137739 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Andersen K, Rasmussen F, Held C, Neovius M, Tynelius P, Sundström J. Exercise capacity and muscle strength and risk of vascular disease and arrhythmia in 1.1 million young Swedish men: cohort study. BMJ. 2015;351:h4543. 10.1136/bmj.h4543 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Mecocci P, Fanó G, Fulle S, et al. Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. Free Radic Biol Med. 1999;26:303–308. 10.1016/S0891-5849(98)00208-1 [DOI] [PubMed] [Google Scholar]
- 6.Cesari M, Pahor M, Bartali B, et al. Antioxidants and physical performance in elderly persons: the Invecchiare in Chianti (InCHIANTI) study. Am J Clin Nutr. 2004;79:289–294. 10.1093/ajcn/79.2.289 [DOI] [PubMed] [Google Scholar]
- 7.Semba RD, Blaum C, Guralnik JM, Moncrief DT, Ricks MO, Fried LP. Carotenoid and vitamin E status are associated with indicators of sarcopenia among older women living in the community. Aging Clin Exp Res. 2003;15:482–487. 10.1007/BF03327377 [DOI] [PubMed] [Google Scholar]
- 8.Lauretani F, Semba RD, Bandinelli S, et al. Low plasma carotenoids and skeletal muscle strength decline over 6 years. J Gerontol A Biol Sci Med Sci. 2008;63:376–383. 10.1093/gerona/63.4.376 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Zhao X, Wei C, Zhong J, Li J. Physiological functions and extraction technology of Lycopene-a natural antioxidant. Bulg Chem Commun. 2016;48:153–158. [Google Scholar]
- 10.Guo H, Niu K, Monma H, et al. Association of Japanese dietary pattern with serum adiponectin concentration in Japanese adult men. Nutr Metab Cardiovasc Dis. 2012;22:277–284. 10.1016/j.numecd.2010.06.006 [DOI] [PubMed] [Google Scholar]
- 11.Sasaki S. Serum biomarker-based validation of a brief-type self-administered diet history questionnaire for Japanese subjects. The Study Group of Ministry of Health, Labor and Welfare of Japan, Tanaka H, chairman, A research for assessment of nutrition and dietary habit in “Kenko Nippon 21”. 2005;10–42.
- 12.Alberti KG, Eckel RH, Grundy SM, et al. ; International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity . Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; American heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation. 2009;120:1640–1645. 10.1161/CIRCULATIONAHA.109.192644 [DOI] [PubMed] [Google Scholar]
- 13.Craig CL, Marshall AL, Sjöström M, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc. 2003;35:1381–1395. 10.1249/01.MSS.0000078924.61453.FB [DOI] [PubMed] [Google Scholar]
- 14.Kim J, Lee Y, Kye S, Chung YS, Kim KM. Association of vegetables and fruits consumption with sarcopenia in older adults: the Fourth Korea National Health and Nutrition Examination Survey. Age Ageing. 2015;44:96–102. 10.1093/ageing/afu028 [DOI] [PubMed] [Google Scholar]
- 15.Neville CE, Young IS, Gilchrist SE, et al. Effect of increased fruit and vegetable consumption on physical function and muscle strength in older adults. Age (Omaha). 2013;35:2409–2422. 10.1007/s11357-013-9530-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Cerullo F, Gambassi G, Cesari M. Rationale for antioxidant supplementation in sarcopenia. J Aging Res. 2012;2012:316943. 10.1155/2012/316943 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Schafer FQ, Buettner GR. Acidic pH amplifies iron-mediated lipid peroxidation in cells. Free Radic Biol Med. 2000;28:1175–1181. 10.1016/S0891-5849(00)00319-1 [DOI] [PubMed] [Google Scholar]
- 18.Dean RT, Hunt JV, Grant AJ, Yamamoto Y, Niki E. Free radical damage to proteins: the influence of the relative localization of radical generation, antioxidants, and target proteins. Free Radic Biol Med. 1991;11:161–168. 10.1016/0891-5849(91)90167-2 [DOI] [PubMed] [Google Scholar]
- 19.Valko M, Izakovic M, Mazur M, Rhodes CJ, Telser J. Role of oxygen radicals in DNA damage and cancer incidence. Mol Cell Biochem. 2004;266:37–56. 10.1023/B:MCBI.0000049134.69131.89 [DOI] [PubMed] [Google Scholar]
- 20.Rao AV, Rao LG. Carotenoids and human health. Pharmacol Res. 2007;55:207–216. 10.1016/j.phrs.2007.01.012 [DOI] [PubMed] [Google Scholar]
- 21.Ryan MJ, Dudash HJ, Docherty M, et al. Vitamin E and C supplementation reduces oxidative stress, improves antioxidant enzymes and positive muscle work in chronically loaded muscles of aged rats. Exp Gerontol. 2010;45:882–895. 10.1016/j.exger.2010.08.002 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Haegele AD, Briggs SP, Thompson HJ. Antioxidant status and dietary lipid unsaturation modulate oxidative DNA damage. Free Radic Biol Med. 1994;16:111–115. 10.1016/0891-5849(94)90247-X [DOI] [PubMed] [Google Scholar]
- 23.Marzani B, Balage M, Vénien A, et al. Antioxidant supplementation restores defective leucine stimulation of protein synthesis in skeletal muscle from old rats. J Nutr. 2008;138:2205–2211. 10.3945/jn.108.094029 [DOI] [PubMed] [Google Scholar]
- 24.Moreira-Pfrimer LD, Pedrosa MA, Teixeira L, Lazaretti-Castro M. Treatment of vitamin D deficiency increases lower limb muscle strength in institutionalized older people independently of regular physical activity: a randomized double-blind controlled trial. Ann Nutr Metab. 2009;54:291–300. 10.1159/000235874 [DOI] [PubMed] [Google Scholar]
- 25.Gupta R, Sharma U, Gupta N, et al. Effect of cholecalciferol and calcium supplementation on muscle strength and energy metabolism in vitamin D-deficient Asian Indians: a randomized, controlled trial. Clin Endocrinol (Oxf). 2010;73:445–451. [DOI] [PubMed] [Google Scholar]
- 26.Kao FJ, Chiu YS, Chiang WD. Effect of water cooking on antioxidant capacity of carotenoid-rich vegetables in Taiwan. J Food Drug Anal. 2014;22:202–209. 10.1016/j.jfda.2013.09.010 [DOI] [Google Scholar]
- 27.Danesi F, Bordoni A. Effect of home freezing and Italian style of cooking on antioxidant activity of edible vegetables. J Food Sci. 2008;73:H109–H112. 10.1111/j.1750-3841.2008.00826.x [DOI] [PubMed] [Google Scholar]
- 28.Xu F, Zheng Y, Yang Z, Cao S, Shao X, Wang H. Domestic cooking methods affect the nutritional quality of red cabbage. Food Chem. 2014;161:162–167. 10.1016/j.foodchem.2014.04.025 [DOI] [PubMed] [Google Scholar]
- 29.Wachtel-Galor S, Wong KW, Benzie IF. The effect of cooking on Brassica vegetables. Food Chem. 2008;110:706–710. 10.1016/j.foodchem.2008.02.056 [DOI] [Google Scholar]
- 30.Kao FJ, Chiu YS, Tsou MJ, Chiang WD. Effects of Chinese domestic cooking methods on the carotenoid composition of vegetables in Taiwan. LWT-Food Sci Technol. 2012;46:485–492. 10.1016/j.lwt.2011.11.019 [DOI] [Google Scholar]
- 31.García-Esquinas E, Rahi B, Peres K, et al. Consumption of fruit and vegetables and risk of frailty: a dose-response analysis of 3 prospective cohorts of community-dwelling older adults. Am J Clin Nutr. 2016;104:132–142. 10.3945/ajcn.115.125781 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.