Serum α-Carotene, but Not Other Antioxidants, Is Positively Associated with Muscle Strength in Older Adults: NHANES 2001–2002
by
Renata R. Bruno
, 
Fernanda C. Rosa
,
Paula C. Nahas
,
Flávia M. S. de Branco
and
Erick P. de Oliveira
* Laboratory of Nutrition, Exercise and Health (LaNES), School of Medicine, Federal University of Uberlandia (UFU), Av. Para, 1.720 Bloco 2U-Sala 20, Campus Umuarama, Uberlandia 38400902, MG, Brazil
*
Author to whom correspondence should be addressed.
Antioxidants 2022, 11(12), 2386; https://doi.org/10.3390/antiox11122386
Submission received: 16 September 2022
/
Revised: 9 November 2022
/
Accepted: 24 November 2022
/
Published: 1 December 2022
(This article belongs to the Special Issue Redox Regulation of Skeletal Muscle Mass and Function in Health and Disease)
Abstract
:Aging is associated with an increased reactive oxygen species that can decrease muscle strength. Thus, antioxidant substances could be positively associated with muscle strength in older adults. To investigate the association between serum antioxidants and muscle strength in older adults. A cross-sectional study evaluating 1172 individuals (627 men and 545 women), aged 50 to 85 years from NHANES 2001–2002, was performed. Carotenoids (α-carotene, trans-β-carotene, cis-β-carotene, β-cryptoxanthin, lutein/zeaxanthin combination, trans-lycopene), vitamin E, and retinol were analyzed via the high-performance liquid chromatography method. Muscle strength was evaluated by the isokinetic knee extension test. Linear regression was performed to evaluate the association between tertiles of serum antioxidant levels and strength, adjusted for confounders (energy and protein intake, body mass index, sex, age, C-reactive protein, uric acid, race/ethnicity, marital status, annual household income, educational level, physical activity, smoking, hypertension, arthritis, and diabetes). Alpha-carotene levels (p-trend = 0.027) were positively associated with muscle strength. However, serum vitamin E, trans-β-carotene, cis-β-carotene, β-cryptoxanthin, carotenoids, and retinol levels were not associated with strength. Serum α-carotene, but not other antioxidants, was positively associated with muscle strength in older adults.
1. Introduction
Aging is associated with muscle strength loss [1], which increases the risk of mortality [2,3], is associated with an increased risk of falls [4] and fractures [5,6], as well as a lower ability to perform activities of daily living [7]. The decrease in strength is influenced by several factors, such as changes in eating patterns [8], anabolic resistance [9], comorbidities [10], reduced physical exercise practice, and increased oxidative stress [11,12,13].
Since increased oxidative stress seems to be one of the causes of muscle strength loss in older adults, substances with antioxidant properties could decrease the oxidative stress [14,15], maintaining the strength over time [16]. Carotenoids, vitamin E, and retinol are potent antioxidants that can decrease the oxidative stress, and thus can be positively associated with muscle strength [16,17,18,19,20,21,22]. Semba et al. [23] evaluated the association of plasma carotenoids and α-tocopherol with grip, hip and knee strength in older women. Higher levels of carotenoids and α-tocopherol were associated with higher muscle strength [23]. In a prospective cohort study, Sahni et al. [16] showed that the intake of total carotenoids, lycopene, and lutein + zeaxanthin was positively associated with handgrip strength. However, to date, the evidence is still limited regarding the association of serum antioxidants with muscle strength, as only a few studies have evaluated this topic [16,23]. In addition, the methodology of the studies is heterogeneous, since one study evaluated only women [23] and another study evaluated the consumption of antioxidants by conducting a food frequency questionnaire, and not by observing the concentrations of these antioxidants in the plasma [16]. Therefore, more studies evaluating the association between serum antioxidants and strength in older adults are needed. The aim of the present study was to assess the association between serum antioxidants and muscle strength in older adults from the National Health and Nutrition Examination Survey (NHANES) 2001–2002. We hypothesized that higher levels of serum carotenoids, vitamin E, and retinol would be associated with higher muscle strength.
2. Methods
2.1. Participants
This is a cross-sectional study conducted with NHANES data from 2001–2002. The NHANES is a survey developed by the National Center for Health Statistics (NCHS), comprising several assessments of health and the nutritional status of a representative sample of the non-institutionalized population of the United States. In NHANES 2001–2002, 11,039 individuals were evaluated; however, in the present study, individuals with missing data in the isokinetic strength test, serum vitamin A and carotenoids, dietary intake, and anthropometry, were excluded. In addition, participants with implausible peak force velocity (<55°/s or >65°/s) [24] and who did not perform at least 4 trials in the isokinetic strength test, were excluded from the study. Therefore, 1172 individuals (627 men and 545 women), aged between 50 and 85 years, were included in the present study (Figure 1). The age range was chosen due to the eligibility of the strength test and because it is an age range in which it is already possible to observe an important muscle strength loss [25]. Written consent, as well as approval from the Research Ethics Review Board of the NCHS (protocol n° 98-12 for the NHANES 2001 and 2002 cycle), were obtained from all NHANES participants.
2.2. Muscle Strength
The peak isokinetic knee extensor strength was evaluated using six measurements from the right quadriceps, performed at a speed of 60° per second and using the Kinetic Communicator isokinetic dynamometer (Kin Com MP, Chattecx Corp., Chattanooga, TN, USA). The first three trials were used for learning the movement and warming up; therefore, the participants were instructed not to apply maximum strength. In the last three trials, they were encouraged to perform with maximum effort for the muscle strength assessment. Participants who had extreme peak-force velocity values (<55°/s or >65°/s) [24] were excluded, and for individuals who completed 4–6 trials, the highest value was used.
2.3. Serum Antioxidants
Vitamin E, retinol, α-carotene, trans-β-carotene, cis-β-carotene, β-cryptoxanthin, lutein/zeaxanthin combination, and trans-lycopene were the antioxidants evaluated in the blood. The sum of α-carotene, trans-β-carotene, cis-β-carotene, β-cryptoxanthin, lutein/zeaxanthin combination, and trans-lycopene were considered for total carotenoids. The high-performance liquid chromatography method, with photodiode array detection, was used for the assessment of serum antioxidants. In order to obtain more reliable results, a fasting sample was obtained and the exposure of the serum to sunlight or other sources of full spectrum radiation was avoided [26]. Serum antioxidant data were expressed in µmol/L, with the exception of retinol, which was expressed in µg/dL.
2.4. Anthropometry
The Lohman protocol [27] was used for the analysis of body weight and height, and the body mass index (BMI) was calculated by body weight divided by height squared.
2.5. Dietary Intake
For the dietary intake assessment, a 24-h food recall was performed. In NHANES 2001, dietary intake was evaluated through the 4-step multiple pass (quick unstructured listing of consumed foods; recall of forgotten foods; investigation of the time or the occasion of each meal; search for more detailed information) [28], while in NHANES 2002, the evaluation was performed using the automated 5-step multiple-pass method of the US Department of Agriculture (USDA) [28,29]. In NHANES 2001–2002, the USDA food and nutrient database was used to process a dietary intake analysis. We evaluated the intake of total energy (kcal/day), carbohydrate (g/day), protein (g/day and g/kg), lipids (g/day), saturated fat (g/day), monounsaturated fat (g/day), polyunsaturated fat (g/day), fiber (g/day), alcohol (g/day), total omega-3 (g/day), vitamin A (mcg/day), vitamin E (mg/day), retinol (mcg/day), lycopene (mcg/day), combined lutein/zeaxanthin (mcg/day), β-cryptoxanthin (mcg/day), β-carotene (mcg/day), and α-carotene (mcg/day).
2.6. Covariates of Interest
Since some factors can confound the association between serum antioxidants and muscle strength, some variables were considered as possible confounders in this association. In relation to demographic parameters, age (years), race/ethnicity (non-Hispanic white, non-Hispanic black, Mexican American, other Hispanic, other races), sex (men or women), marital status (single/divorced/widowed/never married or married/living as married), annual household income (0 to $19,999, from $20,000 to 54,999, or above $55,000), and educational level (under/high school graduate and some college or over), were included. Habits and health conditions were self-reported by the participants and included: hypertension (yes or no), diabetes (yes, no, or pre-diabetes), smoking (yes or no), and arthritis (yes or no). In addition, physical activity was analyzed according to intensity, divided into moderate (yes or no) and vigorous (yes or no), and strength exercise (yes or no). Regarding biochemical parameters, uric acid (mg/dL) and C-reactive protein (CRP) (mg/dL) were considered confounders. In the dietary intake, energy (kcal/day) and protein (g/day) intakes were included. BMI was considered a confounder of anthropometric data.
2.7. Statistical Analysis
Sociodemographic, health conditions and habits, anthropometry, muscle strength, serum antioxidants, and biochemical and dietary intake characteristics were described for the total sample and according to sex. Mean and standard deviation were used to describe continuous variables, whereas percentage and confidence interval were used for categorical variables. In addition, a missing category was created to categorize participants who had missing data in some variables (marital status, annual family income, education, moderate and vigorous physical activity, strength physical activity, smoking, hypertension, menopause). Linear regression was used to estimate the coefficients and 95% confidence intervals (95% CI) for peak strength (muscle strength), by tertile of serum antioxidants. Analyses were performed without adjustments (Model 1) and with adjustments for confounders (co-variates of interest). A statistical analysis was performed using the Stata 14.0 software (StataCorp, College Station, TX, USA) and p < 0.05 was considered statistically significant.
3. Results
3.1. Individual’s Characteristics
The total sample characteristics and results separated by sex are shown in Table 1. Assessing the total sample, the average age was 61.4 ± 9.3 years, the individuals were predominantly men, non-Hispanic white, married/living as married, had an annual household income above US $20,000, and a high education level. Most performed moderate exercise and did not have a diagnosis of diabetes, hypertension or arthritis. In general, men and women presented similar characteristics to those reported for the total sample.
Compared with men, women were older, had lower weight, height, and peak strength; however, they presented a higher prevalence of hypertension and arthritis. Regarding the blood parameters evaluated, women showed higher levels of vitamin E (µmol/L), α-carotene (µmol/L), trans-β-carotene (µmol/L), cis-β-carotene (µmol/L), β-cryptoxanthin (µmol/L), carotenoids (µmol/L), and C-reactive protein (mg/dl), while men had higher values of retinol (µg/dL) and uric acid (mg/dL). Regarding dietary data, women had a lower consumption of energy (kcal) and nutrients.
3.2. Peak Force and Tertiles of Plasma Antioxidants
Table 2 shows the linear regression between tertiles of serum antioxidants and muscle strength. In the unadjusted analyses, muscle strength was negatively associated with α-carotene, trans-β-carotene, cis-β-carotene, β-cryptoxanthin and vitamin E; meanwhile, trans lycopene was positively associated with muscle strength (Model 1). However, after adjustments for confounders, only α-carotene was positively associated with muscle strength (Model 2).
4. Discussions
The main result of the present study was that serum α-carotene levels, but not other antioxidants, were positively associated with muscle strength in older adults. This result suggests that the type of antioxidant seems to be important for its association with muscle strength.
The aging process leads to strength loss and one of the possible causes is the increased oxidative stress [17,18,19,20,21]. Thus, antioxidants can minimize the increase of oxidative stress in older adults and can be positively associated with muscle strength. The explanation as to why only serum α-carotene (but not all the other antioxidants) was associated with strength in the present study is not fully clear, but can be related to the antioxidant action promoted by α-carotene. Although α-carotene is chemically similar to β-carotene, some studies suggest that α-carotene may have a greater potential antioxidant effect [30,31]. For example, an in vivo study showed that α-carotene seems to inhibit the proliferation of the human neuroblastoma cells about 10 times more than β-carotene [30]. In addition, the consumption of foods with high α-carotene content, such as dark green and yellow–orange vegetables, was more strongly associated with a decreased risk of lung cancer than compared with the consumption of all other types of vegetables [32]. Lastly, serum α-carotene levels are inversely associated with the risk of death from several causes [33]. Collectively, α-carotene seems to have more important antioxidant properties when compared with other types of carotenoids, such as β-carotene. The main food predictors of α-carotene are carrots and other root vegetables [34,35], bananas, oranges, and tangerines [34,36], but α-carotene is also correlated with the total consumption of fruits and vegetables [35]. Therefore, it is possible to suggest that an increased consumption of fruits and vegetables (mainly the α-carotene food sources) may be a protective factor for muscle strength in older adults. However, longitudinal studies or randomized clinical trials should be performed to confirm this hypothesis.
In the present study, vitamin E, trans-β-carotene, cis-β-carotene, β-cryptoxanthin, carotenoids, and retinol were not associated with muscle strength, but this is not a consensus in the literature. Semba et al. [23] carried out a study with 669 older women aged between 70 and 79 years. An independent association was observed between the levels of carotenoids and α-tocopherol in the blood, and handgrip, knee, and hip extension strength. Sahni et al. [16] performed a prospective cohort study that associated the antioxidant intake (evaluated by Food Frequency Questionnaire, not serum levels) with handgrip strength. Total carotenoids, lycopene, and lutein + zeaxanthin were positively associated with strength [16]. In addition, Cesari et al. [37] observed a positive association between dietary β-carotene and knee extension strength in older adults from Italy. Differences in study design, populations, confounders added as adjustments, and forms to assess the consumption of antioxidants (diet vs. serum), may explain the controversial results between these studies [16,23,37] and ours. Nevertheless, collectively, we and others [16,23,37] show that antioxidant intake seems to be important for muscle strength, which reinforces that older adults should consume adequate servings of fruits and vegetables.
Our study has limitations. First, it is not possible to establish causality, since this is cross-sectional study. Second, as this is an observational study, confounding factors can influence the results; however, we adjusted the regression analyses for several important confounders. Third, oxidative stress biomarkers were not evaluated, which could aid an understanding of the results. However, the strengths of this study are the method we used to assess muscle strength (isokinetic dynamometer), and the method of measuring antioxidants in the blood (high-performance liquid chromatography method). Finally, the results found can be extrapolated to the population of the United States, since this is a representative sample.
5. Conclusions
We conclude that α-carotene, but not other antioxidants, is positively associated with muscle strength in older adults. Future randomized clinical trials should evaluate the effect of the increased intake of α-carotene food sources on muscle strength in older adults.
Author Contributions
R.R.B. and F.C.R. wrote the manuscript and participated in the interpretation of data; P.C.N. and F.M.S.d.B. participated in the analysis, data interpretation, data set configuration, organization of the statistical analysis, and contributed to the manuscript review. E.P.d.O. wrote the manuscript, participated in data interpretation, and reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.
Funding
No sources of funding were used to assist in the article preparation. R.R.B. would like to thank “the National Development Council Scientific and Technological” (CNPq, Brazil, 2020–2021) for the financial support. We are thankful to “Pró-Reitoria de Pesquisa e Pós-graduação” (PROPP) of the Federal University of Uberlandia for covering the costs to publish in open access.
Institutional Review Board Statement
The study was conducted in accordance with the Declaration of Helsinki, and approved by the Research Ethics Review Board of the NCHS (protocol n° 98-12 for the NHANES 2001 and 2002 cycle).
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement
Data can be found in “https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/default.aspx?BeginYear=2001”.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Zammit, A.R.; Robitaille, A.; Piccinin, A.M.; Muniz-Terrera, G.; Hofer, S.M. Associations Between Aging-Related Changes in Grip Strength and Cognitive Function in Older Adults: A Systematic Review. J. Gerontol. Ser. A 2018, 74, 519–527. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, R.; Xia, J.; Zhang, X.; Gathirua-Mwangi, W.G.; Guo, J.; Li, Y.; Mckenzie, S.; Song, Y. Associations of Muscle Mass and Strength with All-Cause Mortality among US Older Adults. Med. Sci. Sports Exerc. 2018, 50, 458–467. [Google Scholar] [CrossRef]
- Loprinzi, P.D. Lower extremity muscular strength, sedentary behavior, and mortality. Age 2016, 38, 32. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, C.K.; Lyass, A.; Larson, M.G.; Massaro, J.M.; Wang, N.; D’Agostino, R.B.; Murabito, J.M. Biomarkers of oxidative stress are associated with frailty: The Framingham Offspring Study. Age 2016, 38, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fielding, R.A.; Vellas, B.; Evans, W.J.; Bhasin, S.; Morley, J.E.; Newman, A.B.; Zamboni, M. Sarcopenia: An undiagnosed condition in older adults. Current consensus definition: Prevalence, etiology, and consequences. International working group on sarcopenia. J. Am. Med. Dir. Assoc. 2011, 12, 249–256. [Google Scholar] [CrossRef] [Green Version]
- Uusi-Rasi, K.; Karinkanta, S.; Tokola, K.; Kannus, P.; Sievänen, H. Bone Mass and Strength and Fall-Related Fractures in Older Age. J. Osteoporos. 2019, 2019, 5134690. [Google Scholar] [CrossRef]
- Reid, K.F.; Naumova, E.; Carabello, R.J.; Phillips, E.M.; Fielding, R.A. Lower extremity muscle mass predicts functional performance in mobility-limited elders. J. Nutr. Health Aging 2008, 12, 493–498. [Google Scholar] [CrossRef]
- Granic, A.; Sayer, A.A.; Robinson, S.M. Dietary patterns, skeletal muscle health, and sarcopenia in older adults. Nutrients 2019, 11, 745. [Google Scholar] [CrossRef] [Green Version]
- Cuthbertson, D.; Smith, K.; Babraj, J.; Leese, G.; Waddell, T.; Atherton, P.; Rennie, M.J. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 2005, 19, 422–424. [Google Scholar] [CrossRef] [Green Version]
- Volaklis, K.; Halle, M.; Thorand, B.; Peters, A.; Ladwig, K.; Schulz, H.; Koenig, W.; Meisinger, C. Handgrip strength is inversely and independently associated with multimorbidity among older women: Results from the KORA—Age study. Eur. J. Intern. Med. 2016, 31, 35–40. [Google Scholar] [CrossRef]
- Langhammer, B.; Bergland, A.; Rydwik, E. The Importance of Physical Activity Exercise among Older People. BioMed. Res. Int. 2018, 2018, 7856823. [Google Scholar] [CrossRef] [PubMed]
- Gregorio, L.; Brindisi, J.; Kleppinger, A.; Sullivan, R.; Mangano, K.; Bihuniak, J.D.; Kenny, A.M.; Kerstetter, J.E.; Insogna, K. Adequate dietary protein is associated with better physical performance among post-menopausal women 60–90 years. J. Nutr. Health Aging 2013, 18, 155–160. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Montero-Fernández, N.; Serra-Rexach, J.A. Role of exercise on sarcopenia in the elderly. Eur. J. Phys. Rehabil. Med. 2013, 49, 131–143. [Google Scholar] [PubMed]
- Fulle, S.; Protasi, F.; Di Tano, G.; Pietrangelo, T.; Beltramin, A.; Boncompagni, S.; Vecchiet, L.; Fanò, G. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp. Gerontol. 2003, 39, 17–24. [Google Scholar] [CrossRef] [PubMed]
- Baumann, C.W.; Kwak, D.; Liu, H.M.; Thompson, L.V. Age-induced oxidative stress: How does it influence skeletal muscle quantity and quality? J. Appl. Physiol. 2016, 121, 1047–1052. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sahni, S.; Dufour, A.B.; Fielding, R.A.; Newman, A.B.; Kiel, D.P.; Hannan, M.T.; Jacques, P.F. Total carotenoid intake is associated with reduced loss of grip strength and gait speed over time in adults: The Framingham Offspring Study. Am. J. Clin. Nutr. 2021, 113, 437–445. [Google Scholar] [CrossRef]
- Morley, J.E.; Mooradian, A.D.; Silver, A.J.; Heber, D.; Alfin-Slater, R.B. Nutrition in the elderly. Ann. Intern. Med. 1988, 109, 890–904. [Google Scholar] [CrossRef]
- Barrera-Mendoza, C.C.; Ayala-Mata, F.; Cortés-Rojo, C.; García-Pérez, M.E.; Rodríguez-Orozco, A.R. Antioxidant vitamins in asthma. Rev. Alerg. México 2018, 65, 61–77. [Google Scholar] [CrossRef] [Green Version]
- Harman, D. Aging: A Theory Based on Free Radical and Radiation Chemistry. J. Gerontol. 1956, 11, 298–300. [Google Scholar] [CrossRef] [Green Version]
- Jama, J.W.; Launer, L.J.; Witteman, J.C.M.; Den Breeijen, J.H.; Breteler, M.M.B.; Grobbee, D.E.; Hofman, A. Dietary antioxidants and cognitive function in a population-based sample of older persons: The Rotterdam Study. Am. J. Epidemiol. 1996, 144, 275–280. [Google Scholar] [CrossRef]
- Mecocci, P.; Polidori, M.C.; Troiano, L.; Cherubini, A.; Cecchetti, R.; Pini, G.; Senin, U. Plasma antioxidants and longevity: A study on healthy centenarians. Free. Radic. Biol. Med. 2000, 28, 1243–1248. [Google Scholar] [CrossRef] [PubMed]
- Nahas, P.C.; Rossato, L.T.; de Branco, F.M.; Azeredo, C.M.; Rinaldi, A.E.M.; de Oliveira, E.P. Serum uric acid is positively associated with muscle strength in older men and women: Findings from NHANES 1999–2002. Clin. Nutr. 2021, 40, 4386–4393. [Google Scholar] [CrossRef] [PubMed]
- Semba, R.D.; Blaum, C.; Guralnik, J.M.; Moncrief, D.T.; Ricks, M.O.; Fried, L.P. 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. [Google Scholar] [CrossRef] [PubMed]
- Rossato, L.T.; de Branco, F.M.; Azeredo, C.M.; Rinaldi, A.E.M.; de Oliveira, E.P. Association between omega-3 fatty acids intake and muscle strength in older adults: A study from National Health and Nutrition Examination Survey (NHANES) 1999–2002. Clin. Nutr. 2020, 39, 3434–3441. [Google Scholar] [CrossRef]
- Dodds, R.M.; Syddall, H.E.; Cooper, R.; Benzeval, M.; Deary, I.J.; Dennison, E.M.; Sayer, A.A. Grip strength across the life course: Normative data from twelve British studies. PLoS ONE 2014, 9, e113637. [Google Scholar] [CrossRef] [Green Version]
- Vargas, S.; Romance, R.; Petro, J.L.; Bonilla, D.A.; Galancho, I.; Espinar, S.; Kreider, R.B.; Benítez-Porres, J. Efficacy of ketogenic diet on body composition during resistance training in trained men: A randomized controlled trial. J. Int. Soc. Sports Nutr. 2018, 15, 31. [Google Scholar] [CrossRef] [Green Version]
- Lohman, T.G.; Roche, A.F.; Martorell, R. Anthropometric Standardization Reference Manual; Human Kinetics Books: Champaign, IL, USA, 1988. [Google Scholar]
- Papanikolaou, Y.; Brooks, J.; Reider, C.; Fulgoni, V.L. US adults are not meeting recommended levels for fish and omega-3 fatty acid intake: Results of an analysis using observational data from NHANES 2003–2008. Nutr. J. 2014, 13, 31. [Google Scholar] [CrossRef] [Green Version]
- Conway, J.M.; A Ingwersen, L.; Vinyard, B.T.; Moshfegh, A.J. Effectiveness of the US Department of Agriculture 5-step multiple-pass method in assessing food intake in obese and nonobese women. Am. J. Clin. Nutr. 2003, 77, 1171–1178. [Google Scholar] [CrossRef] [Green Version]
- Murakoshi, M.; Takayasu, J.; Kimura, O.; Kohmura, E.; Nishino, H.; Iwashima, A.; Iwasaki, R. Inhibitory effects of α-carotene on proliferation of the human neuroblastoma cell line GOTO. JNCI: J. Natl. Cancer Inst. 1989, 81, 1649–1652. [Google Scholar] [CrossRef]
- Murakoshi, M.; Nishino, H.; Satomi, Y.; Takayasu, J.; Hasegawa, T.; Tokuda, H.; Iwasaki, R. Potent preventive action of α-carotene against carcinogenesis: Spontaneous liver carcinogenesis and promoting stage of lung and skin carcinogenesis in mice are suppressed more effectively by α-carotene than by β-carotene. Cancer Res. 1992, 52, 6583–6587. [Google Scholar]
- Ziegler, R.G.; Colavito, E.A.; Hartge, P.; McAdams, M.J.; Schoenberg, J.B.; Mason, T.J.; Fraumeni Jr, J.F. Importance of α-carotene, β-carotene, and other phytochemicals in the etiology of lung cancer. JNCI J. Natl. Cancer Inst. 1996, 88, 612–615. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Ford, E.S.; Zhao, G.; Balluz, L.S.; Giles, W.H.; Liu, S. Serum α-carotene concentrations and risk of death among US adults: The Third National Health and Nutrition Examination Survey Follow-up Study. Arch. Intern. Med. 2011, 171, 507–515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hendrickson, S.J.; Willett, W.C.; Rosner, B.A.; Eliassen, A.H. Food Predictors of Plasma Carotenoids. Nutrients 2013, 5, 4051–4066. [Google Scholar] [CrossRef] [PubMed]
- Al-Delaimy, W.K.; Ferrari, P.; Slimani, N.; Pala, V.; Johansson, I.; Nilsson, S.; Riboli, E. Plasma carotenoids as biomarkers of intake of fruits and vegetables: Individual-level correlations in the European Prospective Investigation into Cancer and Nutrition (EPIC). Eur. J. Clin. Nutr. 2005, 59, 1387–1396. [Google Scholar] [CrossRef]
- Olmedilla-Alonso, B.; Rodríguez-Rodríguez, E.; Beltrán-de-Miguel, B.; Estévez-Santiago, R. Dietary β-cryptoxanthin and α-carotene have greater apparent bioavailability than β-carotene in subjects from countries with different dietary patterns. Nutrients 2020, 12, 2639. [Google Scholar] [CrossRef]
- Cesari, M.; Pahor, M.; Bartali, B.; Cherubini, A.; Penninx, B.W.J.H.; Williams, G.R.; Atkinson, H.; Martin, A.; Guralnik, J.M.; Ferrucci, L. Antioxidants and physical performance in elderly persons: The Invecchiare in Chianti (InCHIANTI) study. Am. J. Clin. Nutr. 2004, 79, 289–294. [Google Scholar] [CrossRef]
Figure 1.
Flowchart of the sample selection from NHANES 2001–2002.
Table 1.
Sociodemographic, anthropometric and body composition characteristics of the individuals in the total sample and according to sex. NHANES, 2001–2002.
Table 1.
Sociodemographic, anthropometric and body composition characteristics of the individuals in the total sample and according to sex. NHANES, 2001–2002.
| Variables | Total | Men | Women | p-Value |
|---|---|---|---|---|
| Age, years | 61.4 (9.3) | 60.8 (9.0) | 62.0 (9.6) | 0.013 |
| Non-Hispanic white, % | 83.7 (77.6–88.3) | 84.9 (77.3–90.3) | 82.3 (77.0–86.6) | 0.171 |
| Sex, % | ||||
| Men | 51.4 (49.4–53.3) | |||
| Women | 48.6 (46.6–50.6) | |||
| Marital status, % | 0.930 | |||
| Single/divorced/widowed/never married | 26.1 (22.2–30.4) | 15.9 (11.8–21.0) | 36.9 (31.6–42.4) | |
| Married/living as married | 73.6 (69.3–77.6) | 83.7 (78.5–87.8) | 63.0 (57.5–68.3) | |
| Missing | 0.3 (0.04–1.5) | 0.4 (0.04–3.2) | 0.1 (0.01–0.7) | |
| Annual family income, % | 0.165 | |||
| $0–19.999 | 17.8 (14.6–21.4) | 14.3 (10.9–18.5) | 21.4 (17.4–26.1) | |
| $20.000–54.999 | 40.1 (35.3–45.1) | 40.2 (33.0–47.8) | 40.0 (36.5–43.7) | |
| $55.000–74.999 | 40.0 (33.4–47.1) | 44 (35.9–52.4) | 35.9 (30.1–42.1) | |
| Missing | 2.1 (1.2–3.4) | 1.5 (0.8–2.7) | 2.7 (1.4–4.7) | |
| Educational level, % | 0.287 | |||
| High school graduate or under | 41.7 (37.2–46.2) | 39.7 (33.2–46.5) | 43.7 (38.9–48.7) | |
| Some college or above | 58.3 (53.7–62.7) | 60.3 (53.5–66.7) | 56.2 (51.2–70.0) | |
| Health conditions and habits, % | ||||
| Hypertension | 37.7 (33.3–42.2) | 32.7 (27.8–38.1) | 42.9 (36.9–49.0) | 0.032 |
| Missing | 0.1 (0.02–0.43) | 0.2 (0.04–0.8) | ||
| Diabetes | 0.173 | |||
| Pre-diabetes | 2.4 (1.2–4.7) | 2.6 (1.05–6.5) | 2.1 (0.9–4.6) | |
| Yes | 9.0 (7.4–11.0) | 10.7 (8.1–14.0) | 7.3 (5.4–9.8) | |
| No | 88.6 (85.5–91.1) | 86.6 (81.5–90.5) | 90.6 (87.8–92.8) | |
| Smoking | 0.640 | |||
| Yes | 17.3 (14.6–20.4) | 18.1 (14.4–22.4) | 16.5 (13.4–20.2) | |
| No | 82.5 (79.6–85.2) | 81.8 (77.5–85.3) | 83.4 (79.7–86.5) | |
| Missing | 0.2 (0.03–0.45) | 0.1 (0.02–0.8) | 0.1 (0.01–0.7) | |
| Arthritis | 0.002 | |||
| Yes | 35.7 (31.1–40.7) | 30.9 (25.7–36.7) | 40.8 (35.5–46.4) | |
| No | 64.2 (59.3–68.9) | 69.1 (63.3–74.3) | 59.1 (53.6–64.5) | |
| Physical activity % | 0.775 | |||
| Moderate physical activity | ||||
| Yes | 51.4 (45.8–56.9) | 50.9 (44.7–57.1) | 51.8 (42.9–60.6) | |
| No | 48.6 (43.0–54.2) | 49.1 (42.8–55.3) | 48.1 (39.2–57.1) | |
| Vigorous physical activity | ||||
| Yes | 28.9 (23.9–34.4) | 32.1 (25.3–39.9) | 25.4 (20.3–31.2) | |
| No | 71.1 (65.5–76.1) | 67.8 (60.1–74.7) | 74.5 (68.6–79.6) | |
| Resistance physical activity | ||||
| Yes | 24.1 (19.2–29.7) | 23.4 (17.2–30.9) | 24.8 (19.0–31.7) | |
| No | 75.8 (70.2–80.7) | 76.6 (69.1–82.7) | 75.1 (68.2–80.9) | |
| Missing | 0.1 (0.06–0.1) | 0.1 (0.01–0.7) | ||
| Anthropometrics | ||||
| Weight, kg | 80.4 (18.1) | 87.2 (16.0) | 73.1 (17.4) | <0.001 |
| Height, m | 1.68 (0.10) | 1.75 (0.07) | 1.61 (0.06) | <0.001 |
| Body mass index, kg/m2 | 28.2 (5.5) | 28.25 (4.6) | 28.1 (6.4) | 0.813 |
| Strength | ||||
| Peak force, N | 384 (123,7) | 457 (111) | 307 (82.4) | <0.001 |
| Time to peak force, s | 1.03 (0.48) | 0.99 (0.39) | 1.06 (0.56) | 0.067 |
| Peak force velocity, degree/s | 60.7 (0.62) | 60.7 (0.67) | 60.6 (0.57) | 0.121 |
| Biochemical parameters | ||||
| Vitamin E (µmol/L) | 37.6 (15.7) | 36.1 (15.1) | 39.2 (16.2) | 0.013 |
| α-carotene (µmol/L) | 0.09 (0.13) | 0.08 (0.10) | 0.11 (0.16) | 0.008 |
| Trans-β-carotene (µmol/L) | 0.44 (0.43) | 0.37 (0.36) | 0.52 (0.48) | <0.001 |
| Cis-β-carotene (µmol/L) | 0.02 (0.02) | 0.02 (0.02) | 0.03 (0.03) | <0.001 |
| β-cryptoxanthin (µmol/L) | 0.18 (0.13) | 0.16 (0.12) | 0.19 (0.14) | 0.017 |
| Combined Lutein/zeaxanthin (µmol/L) | 0.31 (0.17) | 0.30 (0.16) | 0.32 (0.18) | 0.163 |
| Trans-lycopene (µmol/L) | 0.41 (0.21) | 0.42 (0.22) | 0.41 (0.20) | 0.834 |
| Carotenoids (µmol/L) | 1.46 (0.79) | 1.35 (0.70) | 1.58 (0.87) | 0.002 |
| Retinol (µg/dL) | 67.1 (1.02) | 69.2 (1.04) | 64.9 (1.20) | <0.001 |
| C-reactive protein (mg/dL) | 0.41 (0.03) | 0.35 (0.03) | 0.48 (0.04) | <0.001 |
| Uric acid (mg/dL) | 5.58 (1.41) | 6.10 (1.29) | 5.03 (1.31) | <0.001 |
| Dietary intake | ||||
| Energy, kcal | 1997 (960) | 2313 (1112) | 1662 (609) | <0.001 |
| Carbohydrate, g | 245 (126) | 278 (149) | 210 (82.1) | <0.001 |
| Protein, g | 75.7 (39.4) | 87.0 (44.8) | 63.7 (28.1) | <0.001 |
| Protein, g/kg | 0.97 (0.49) | 1.01 (0.51) | 0.92 (0.47) | 0.006 |
| Lipids, g | 77.5 (47,9) | 90.4 (56.6) | 63.9 (31.6) | <0.001 |
| Saturated fat, g | 24.1 (16.2) | 28.4 (19.1) | 19.5 (10.8) | <0.001 |
| Monounsaturated fat, g | 27.7 (18.7) | 32.7 (22.1) | 22.5 (12.3) | <0.001 |
| Polyunsaturated fat, g | 16.4 (12.1) | 18.5 (14.2) | 14.2 (8.9) | <0.001 |
| Total omega-3, g | 1.80 (1.50) | 2.04 (1.71) | 1.55 (1.18) | 0.001 |
| ALA, g | 1.50 (1.21) | 1.68 (1.33) | 1.32 (1.03) | 0.001 |
| EPA, g | 0.05 (0.19) | 0.06 (0.21) | 0.04 (0.16) | 0.198 |
| DHA, g | 0.09 (0.30) | 0.11 (0.36) | 0.07 (0.22) | 0.119 |
| Fiber, g | 16.2 (10.4) | 17.5 (12.0) | 14.8 (8.1) | 0.010 |
| Alcohol, g | 8.68 (24.1) | 12.4 (29.0) | 4.72 (16.8) | <0.001 |
| Vitamin A, RAE (mcg) | 629 (719) | 670 (886) | 586 (480) | 0.086 |
| Vitamin E, as α-tocopherol (mg) | 7.07 (5.75) | 7.85 (6.64) | 6.25 (4.51) | 0.002 |
| Retinol (mcg) | 416 (586) | 467 (757) | 361 (307) | 0.002 |
| Lycopene (mcg) | 5520 (10271) | 6108 (11183) | 4899 (9179) | 0.029 |
| Lutein + zeaxanthin (mcg) | 1717 (3118) | 1760 (3285) | 1672 (2934) | 0.705 |
| β-cryptoxanthin (mcg) | 146 (229) | 157 (253) | 134 (201) | 0.128 |
| β-carotene (mcg) | 2271 (4185) | 2125 (4391) | 2425 (3954) | 0.322 |
| α-carotene (mcg) | 412 (1480) | 428 (1766) | 395 (1100) | 0.738 |
Data are described as mean (standard deviation) or percentage (confidence interval). Notes: DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid, ALA: alpha linolenic acid, RAE, retinol activity equivalents.
Table 2.
Linear regression between tertiles of serum antioxidants and muscle strength. NHANES, 2001–2002.
Table 2.
Linear regression between tertiles of serum antioxidants and muscle strength. NHANES, 2001–2002.
| Model 1 β (95% CI) | Model 2 β (95% CI) | |||||||
|---|---|---|---|---|---|---|---|---|
| T1 | T2 | T3 | p-Trend | T1 | T2 | T3 | p-Trend | |
| α-carotene (µmol/L) | Ref | 2.37 (−17.7; 22.5) | −18.0 (−32.1; −3.90) | 0.016 | Ref | 15.1 (2.24; 28.0) | 16.0 (1.89; 30.1) | 0.027 |
| Trans-β-carotene (µmol/L) | Ref | 1.24 (−15.5; 18.0) | −42.6 (−64.8; −20.4) | 0.001 | Ref | 11.1 (−2.83; 25.1) | 9.13 (−9.41; 27.7) | 0.316 |
| Cis-β-carotene (µmol/L) | Ref | −17.6 (−30.8; −4.42) | −50.2 (−68.7; −31.6) | <0.001 | Ref | 4.70 (−7.61; 17.0) | 7.33 (−11.0; 25.7) | 0.399 |
| β-cryptoxanthin (µmol/L) | Ref | −17.1 (−39.6; 5.41) | −23.9 (−47.9; 0.05) | 0.042 | Ref | 6.73 (−10.2; 23.7) | −0.289 (−13.0; 12.4) | 0.990 |
| Combined Lutein/zeaxanthin (µmol/L) | Ref | 19.0 (−1.78; 39.7) | 1.25 (−24.1; 26.6) | 0.872 | Ref | 11.8 (−6.15; 29.7) | 6.95 (−14.0; 27.9) | 0.473 |
| Trans-lycopene (µmol/L) | Ref | 21.9 (4.25; 39.6) | 28.7 (9.0; 48.5) | 0.010 | Ref | 11.8 (−5.24; 28.9) | 3.32 (−9.20; 15.8) | 0.740 |
| Carotenoids (µmol/L) | Ref | 9.90 (−12.5; 32.3) | −14.1 (−37.7; 9.42) | 0.222 | Ref | 0.10 (−17.8; 18.0) | 0.17 (−18.3; 18.6) | 0.985 |
| Vitamin E (µmol/L) | Ref | 0.52 (−19.2; 20.2) | −22.9 (−41.9; −3.87) | 0.019 | Ref | 2.26 (−8.89; 13.4) | 8.71 (−8.00; 25.4) | 0.282 |
| Retinol (µg/dL) | Ref | −2.36 (−29.4; 24.7) | 21.4 (−10.1; 52.9) | 0.159 | Ref | 8.21 (−5.62; 22.0) | 11.1 (−12.8; 35.0) | 0.358 |
Model 1: unadjusted analyses. Model 2: adjusted for energy (kcal/day) and protein (g/day) intake, body mass index, sex, age, C-reactive protein (mg/dL), uric acid (mg/dL), race/ethnicity, marital status, annual household income, educational level, physical activity, smoking, hypertension, arthritis and diabetes. Bold means that the p-value is statistically significant.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Bruno, R.R.; Rosa, F.C.; Nahas, P.C.; de Branco, F.M.S.; de Oliveira, E.P. Serum α-Carotene, but Not Other Antioxidants, Is Positively Associated with Muscle Strength in Older Adults: NHANES 2001–2002. Antioxidants 2022, 11, 2386. https://doi.org/10.3390/antiox11122386
AMA Style
Bruno RR, Rosa FC, Nahas PC, de Branco FMS, de Oliveira EP. Serum α-Carotene, but Not Other Antioxidants, Is Positively Associated with Muscle Strength in Older Adults: NHANES 2001–2002. Antioxidants. 2022; 11(12):2386. https://doi.org/10.3390/antiox11122386
Chicago/Turabian StyleBruno, Renata R., Fernanda C. Rosa, Paula C. Nahas, Flávia M. S. de Branco, and Erick P. de Oliveira. 2022. "Serum α-Carotene, but Not Other Antioxidants, Is Positively Associated with Muscle Strength in Older Adults: NHANES 2001–2002" Antioxidants 11, no. 12: 2386. https://doi.org/10.3390/antiox11122386
APA StyleBruno, R. R., Rosa, F. C., Nahas, P. C., de Branco, F. M. S., & de Oliveira, E. P. (2022). Serum α-Carotene, but Not Other Antioxidants, Is Positively Associated with Muscle Strength in Older Adults: NHANES 2001–2002. Antioxidants, 11(12), 2386. https://doi.org/10.3390/antiox11122386
Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.
