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Antioxidants and physical performance in elderly persons: the

Invecchiare in Chianti (InCHIANTI) study13


Matteo Cesari, Marco Pahor, Benedetta Bartali, Antonio Cherubini, Brenda WJH Penninx, G Rhys Williams,
Hal Atkinson, Antonio Martin, Jack M Guralnik, and Luigi Ferrucci

ABSTRACT Recently, some authors suggested that age-related physical


Background: Muscle strength and physical performance in old decline might be related to oxidative damage perpetrated by
age might be related to the oxidative damage caused by free free radicals (4). A free radical has been defined as any
radicals. species capable of independent existence that contains one or
Objective: The objective was to assess the correlation of plasma more unpaired electrons (5). This situation is energetically
concentrations and daily dietary intakes of antioxidants with skel- unstable, making such species often highly reactive and short-

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etal muscle strength and physical performance in elderly persons. lived. Free radicals disrupt the equilibrium of biological sys-
Design: This study is part of the Invecchiare in Chianti (InCHI- tems by damaging their major constituent molecules, leading
ANTI) study, which was conducted in 986 Italians aged 65 y. eventually to cell death (6, 7). Oxidative damage may play a
Physical performance was assessed on the basis of walking speed, crucial role in the decline of functional activity in human
ability to rise from a chair, and standing balance. Knee extension skeletal muscle with normal aging (8, 9). This hypothesis
strength was assessed with a hand-held dynamometer. The Euro- suggests a primary role for antioxidant agents in the attempt to
pean Prospective Investigation into Cancer and Nutrition (EPIC)
avoid or reduce age-related physical decline. Antioxidants can
questionnaire was used to evaluate the daily dietary intakes of
be defined as substances whose presence significantly inhibits
vitamin C, vitamin E, -carotene, and retinol. Plasma - and
the rate of oxidation (10). The body contains an elaborate
-tocopherol concentrations were measured. Adjusted linear re-
antioxidant defense (11), and vitamin C, vitamin E, -carotene,
gression analyses were used to calculate regression coefficients per
and retinol are the primary antioxidant vitamins (12). It has
SD increase in plasma concentrations and daily dietary intakes.
Results: In adjusted analyses, plasma -tocopherol was signifi-
been suggested that DNA damage, one of the most sensitive
cantly correlated with knee extension ( 0.566, P 0.003) and biological markers of oxidative stress, might be caused by an
the summary physical performance score ( 0.044, P 0.008). imbalance between the excessive generation of free radicals
Plasma -tocopherol was associated only with knee extension and the deficient action of the antioxidant system (13).
strength ( 0.327, P 0.04). Of the daily dietary intake We hypothesize that plasma antioxidants and the dietary
measures, vitamin C and -carotene were significantly correlated intake of antioxidants may correlate with strength and physical
with knee extension strength, and vitamin C was significantly
1
associated with physical performance ( 0.029, P 0.04). From the Sticht Center on Aging, Wake Forest University Health
Conclusions: Plasma antioxidant concentrations correlate posi- Sciences, Winston-Salem, NC (MC, MP, BWJHP, and HA); the Labora-
tory of Clinical Epidemiology, Italian National Research Council of Aging,
tively with physical performance and strength. Higher dietary
Geriatric Department, Florence, Italy (BB); the Department of Gerontology
intakes of most antioxidants, especially vitamin C, appear to be and Geriatrics, University of Perugia, Perugia, Italy (AC); the Pharmaceu-
associated with higher skeletal muscular strength in elderly tical Research Institute, Bristol-Myers Squibb, Princeton, NJ (GRW); the
persons. Am J Clin Nutr 2004;79:28994. Human Nutrition Research Center on Aging, Tufts University, Boston
(AM); the Epidemiology, Demography, and Biometry Program, National
KEY WORDS Antioxidants, dietary intake, physical perfor- Institute on Aging, Bethesda, MD (JMG); the Longitudinal Studies Sec-
mance, elderly tion, Clinical Research Branch, National Institute on Aging, Baltimore
(LF).
2
Supported by Bristol-Myers Squibb Company (Princeton, NJ) and by
INTRODUCTION
an unrestricted grant from BRACCO Imaging SpA, Italy. The InCHIANTI
The assessment of physical function is becoming an increas- study was supported as a targeted project (ICS 110.1/RS97.71) by the
ingly important component in the evaluation of elderly persons, Italian Ministry of Health and in part by the US National Institute on Aging
and standardized tests of physical performance are now widely (NIA) (contracts 263 MD 9164 13 and 263 MD 821336). The work of MC
used both in research and clinical geriatric settings. In fact, was supported by the Wake Forest University Claude D Pepper Older
Americans Independence Center (NIA grant P30-AG-021332-01).
some of these performance measures, such as knee extension 3
Reprints not available. Address correspondence to M Cesari, Sticht Center
strength and performanceas assessed by walking speed, bal-
on Aging, Wake Forest University Health Sciences, 1 Medical Center Boule-
ance, and ability to rise from a chair (chair stands)have been vard, Winston-Salem, NC 27157. E-mail: mcesari@wfubmc.edu.
shown to be useful in the prediction of institutionalization, Received April 17, 2003.
disability, and mortality (13). Accepted for publication July 10, 2003.

Am J Clin Nutr 2004;79:289 94. Printed in USA. 2004 American Society for Clinical Nutrition 289
290 CESARI ET AL

performance. The purpose of this study was to assess the semitandem position, and a full-tandem position. Good to
correlation of plasma antioxidant concentrations and daily di- excellent reliability of these tests has been shown, which sup-
etary intakes of antioxidants with skeletal muscle strength and ports the utilization of these measures in aging research (16).
physical performance in elderly persons. An arithmetic summary performance score was calculated to
obtain a continuous measure (17). The timed scores of the
performance tests were rescaled to values ranging from 0 to 1,
SUBJECTS AND METHODS where 1 indicates the best performance and 0 the worst per-
formance. The worst performers were participants who were
The present study is part of the Invecchiare in Chianti
unable to complete the task or those who had a performance
(InCHIANTI) study, a prospective population-based study of
above the 99th percentile (walking time: 15.5 s; chair-stand
elderly people in Italy designed by the Laboratory of Clinical
time: 27.3 s; standing-balance test: 30 s). The following for-
Epidemiology of the Italian National Research Council of
mulas were applied to rescale measures: 1) walking speed, 1
Aging (Florence, Italy). The aims of the study are to identify
(15.5/speed in centimeters per second); 2) chair-stand test, 1
risk factors for the onset of disability in elderly persons, to
(time in seconds/27.3); and 3) standing-balance test, time in
study physiologic subsystems critical for walking, and to de-
seconds/30. A summary physical performance score ranging
fine critical ranges for tests that evaluate the integrity of the
from 0 to 3 was calculated by adding these 3 rescaled scores.
physiologic subsystems that are important for walking. The
Such a summary score has been shown to have excellent
study population included 1156 participants aged 65102 y,
predictive validity for mortality, institutionalization, hospital-
who were randomly selected from residents in 2 towns of the
ization, and incident disability (1, 3, 18, 19). The internal
Chianti geographic area (Greve In Chianti and Bagno a Ripoli,
consistency (Cronbachs ) of the summary scale in our study
Tuscany, Italy) with the use of a multistage stratified sampling

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was 0.871.
method (14). The data collection started in September 1998 and
was completed in March 2000. A detailed description of the
sampling procedure and data collection method was previously Plasma antioxidants
published (14). The Italian National Research Council of Ag- Plasma vitamin E (- and -tocopherol) concentrations were
ing Ethical Committee approved the study protocol. measured by reversed-phase HPLC as previously described
The present analyses were conducted in 986 participants; we (20). Briefly, 100 mL plasma was mixed with 100 mL ethanol;
excluded subjects in whom daily nutrient intakes were not after being mixed by vortex, tocopherol was extracted into 500
assessed or in whom tests of physical performance and of knee mL hexane containing 0.002% butylated hydroxytoluene
extension strength were not conducted (n 136). We also (Sigma, St Louis). Tocol, a gift from Hoffmann-La Roche
excluded 34 participants who were vitamin supplement users. (Nutley, NJ), was added to the mixture as an internal standard.
Sociodemographic characteristics showed that the excluded Samples were centrifuged at 180 g for 5 min at 4 C. The
participants were elderly (79.8 compared with 75.3 y), more supernatant fluid was collected and dried under a stream of
likely to be female (67.1% compared with 55.3%), and less nitrogen gas and was reconstituted in 100 mL methanol. To-
educated (4.7 compared with 5.4 y) than were those eligible for copherols were separated by HPLC with a 3-m C18 reversed-
the present analyses. phase column (Perkin-Elmer, Norwalk, CT). The mobile phase,
delivered at a flow rate of 1.0 mL/min, consisted of 1% water
Physical performance tests in methanol containing 10 mmol lithium perchlorate/L. Sam-
ples were injected with an autosampler (1100 series; Hewlett-
Knee extension strength was measured with a hand-held
Packard, Palo Alto, CA). Eluted peaks were detected at an
dynamometer (Nicholas Muscle Tester; Sammon Preston Inc,
applied potential of 0.6 V by an LC 4B amperometric elec-
Chicago). Participants, lying in lateral decubitus (opposite to
trochemical detector (Bioanalytical System, West Lafayette,
the examined limb) with the hip and knee in 45 and 60
IN). Peaks were integrated with ChemStation software
flexed positions, respectively, were asked to perform the task
(Hewlett-Packard). Tocopherol concentrations were expressed
twice with each leg. The average of the best results obtained for
in mol/L. The reproducibility and accuracy of the procedures
each leg was used for the present analyses. In our study we
used were tested by analyzing representative samples in trip-
found a high correlation between the 2 strength measures done
licate from a sample provide by the American Association for
for each leg (r 0.896, P 0.001). This measurement of knee
Laboratory Accreditation (Washington, DC), which contained
extension strength has been proven to be reliable on the basis
known concentrations of -tocopherol. Intra- and interbatch
of high test-retest and interrater reliabilities (0.85 and 0.74,
CVs were 3% and 4.2%, respectively.
respectively) (15).
Performance of the lower extremities was assessed with the
use of 3 tests: walking speed, ability to stand from a chair, and EPIC questionnaire
ability to maintain balance in progressively more challenging To determine daily nutritional intakes, we used the EPIC
positions. Walking speed was defined as the best performance (European Prospective Investigation into Cancer and Nutrition)
(time in s) of two 4-m walks at usual pace along a corridor. For questionnaire (21, 22). This questionnaire was designed and
the chair-stand test, the participants were asked to rise and sit validated in a multicenter study performed in 10 European
down 5 times as quickly as possible with their hands folded countries, with the aim to evaluate the relation between diet
across the chest. The performance was expressed as total time and the onset of cancer. Participants were asked how many
(in s) to complete the test. For the standing-balance test, the times in a year each food (or food category) and beverage were
subjects were asked to stand in 3 progressively more difficult consumed. All of the answers provided by the participants were
positions for 10 s each: a side-by-side feet standing position, a reported through specific software in a database, and the daily
ANTIOXIDANTS AND PHYSICAL PERFORMANCE 291
intakes of micro- and macronutrients were calculated. The TABLE 1
software for the estimate of food composition was created and Participant characteristics1
verified by the EPIC study group according to food-composition Value
tables compiled in 1998 by researchers at the European Institute of
Oncology. Sociodemographic characteristics
Age (y) 75.3 0.22
In a previous study (23), data on dietary intake collected in
Female sex (%) 55.3
the InCHIANTI study were compared with data collected in a
Residents of Greve, Italy (%) 47.8
nationwide study in which a direct method of measure based on Education (y) 5.4 (0.1)
7-d weighted and registered food consumption was used. De- Mini-Mental State Examination Score 24.6 (0.2)
spite different populations and different methods used for data Smoking (%)
collection, the distributions of dietary intake from the 2 studies Never 59.0
were remarkably similar for most macro- and micronutrients, Former 30.1
both in men and women, which suggests that the EPIC food- Current 10.9
frequency questionnaire provides a good estimate of dietary BMI (kg/m2) 27.5 (0.1)
intake. In the present analyses, we considered the EPIC 20 (%) 1.9
2024.9 (%) 26.0
questionnairederived daily intakes of 4 antioxidant agents:
2530 (%) 43.5
vitamin C, vitamin E, -carotene, and retinol.
30 (%) 23.9
Covariates Missing (%) 4.7
Physical activity (%) 37.0
The covariates included sociodemographic variables (age, Plasma lipids (mg/dL)

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sex, site, smoking habit, and education), cognitive status (Mini- Total cholesterol 217.6 (1.3)
Mental State Examination score), plasma lipid concentrations Triacylglycerols 110.5 (84.0150.0)3
(total cholesterol and triacylglycerols), comorbidity (self- Comorbid conditions (%)
reported diagnoses of hypertension, angina, myocardial infarc- Hypertension 44.4
tion, stroke, cancer, diabetes, congestive heart failure, and Angina or myocardial infarction 7.6
Stroke 5.8
chronic obstructive pulmonary disease), body mass index
Cancer 10.3
(computed as weight in kg/height in m2), the number of med- Diabetes 11.6
ications taken by participants at the baseline assessment, and Congestive heart failure 5.8
physical activity (defined as a moderate-to-high intensity ex- COPD 6.3
ercise performed for 12 h/wk or a light-intensity exercise Number of medications taken 2.2 (0.1)
performed for 4 h/wk). To adjust for overall food intake, we Plasma antioxidants (mol/L)
also adjusted our analyses for daily dietary energy intake, as -Tocopherol 29.96 (0.27)
assessed by the EPIC questionnaire. Participants were asked to -Tocopherol 1.45 (0.02)
report any medication taken in the last 2 wk. Drugs were coded EPIC questionnaire measures
according to the Anatomical Therapeutic and Chemical codes Vitamin C (mg) 110.78 (1.54)
Vitamin E (mg) 6.22 (0.06)
(24).
-Carotene (g) 2167.35 (36.91)
Statistical analyses Retinol (g) 492.76 (17.70)
Energy intake (kcal) 1920.17 (17.95)
Because the plasma concentrations of -tocopherol and - Performance tests
tocopherol, and daily dietary intakes of vitamin C, vitamin E, Physical performance4 2.18 (0.02)
-carotene, and retinol were not normally distributed, analyses Knee extension strength (kg) 15.17 (0.19)
were performed with the use of their log values. Spearman 1
n 986. COPD, chronic obstructive pulmonary disease; EPIC,
correlation tests were used to evaluate correlations of antioxi- European Prospective Investigation into Cancer and Nutrition.
dants plasma concentrations and daily dietary intakes with knee 2
x SE.
extension strength and summary physical performance score. 3
Median; interquartile range in parentheses.
All analyses were adjusted for age, sex, site, Mini-Mental State 4
Possible score ranges from 0 to 3.
Examination score, smoking habit, education, body mass in-
dex, total cholesterol, triacylglycerol (log value), hypertension,
angina or myocardial infarction, congestive heart failure, dia- RESULTS
betes, stroke, number of medications taken, and daily dietary The main characteristics of the participants are shown in
energy intake; all these variables showed a significant correla- Table 1. The mean (SE) age of the participants was 75.3
tion with outcome measures. Linear regression analyses were 0.2 y, and 55.3% were female. The most common diagnoses
used to identify regression coefficients for strength and perfor- reported by the participants were hypertension (44.4%), diabe-
mance outcomes per SD increase in plasma antioxidant con- tes (11.6%), cancer (10.3%), and angina or myocardial infarc-
centrations and daily dietary intakes. To calculate adjusted tion (7.6%).
knee extension strength and summary physical performance Mean (SE) plasma concentrations of - and -tocopherol
scores, analyses of covariance were performed for tertiles of were 29.96 0.27 and 1.45 0.02 mol/L, respectively.
antioxidants (plasma concentrations and dietary intakes) and Plasma concentrations of -tocopherol were correlated with
daily energy intake. Sex interactions were assessed by adding plasma concentrations of -tocopherol (r 0.373, P 0.001)
the interaction term for sex antioxidant concentration in the and with daily dietary intake of vitamin E (r 0.126, P
adjusted model. 0.001). No significant correlation was found between plasma
292 CESARI ET AL

TABLE 2 -carotene were significantly correlated with knee extension


Spearman correlations between physical performance and muscular strength (vitamin C: 0.383, SE 0.162, P 0.02; -caro-
strength tests and plasma concentrations and dietary intakes of tene: 0.311, SE 0.159, P 0.05). Only the daily intake of
antioxidants
vitamin C was significantly associated with physical performance
Knee extension Physical ( 0.029, SE 0.014, P 0.04). No significant sex interaction
strength performance score was found between dietary intake and physical performance (all
P values 0.05).
kg
Plasma antioxidants Adjusted means for knee extension strength and summary
-Tocopherol 0.054 0.1151 physical performance score according to tertiles of plasma
-Tocopherol 0.057 0.1071 antioxidant concentrations and daily dietary intakes were as-
Daily dietary intakes sessed. Greater knee extension strength was found at higher
Vitamin C 0.2101 0.2191 concentrations of -tocopherol (lowest compared with highest
Vitamin E 0.2811 0.2431 tertile: P 0.003 and P for trend 0.01). Higher plasma
-Carotene 0.2161 0.2021 concentrations of -tocopherol were found at higher physical
Retinol 0.0951 0.0732 performance scores (lowest compared with highest tertile: P
1
P 0.01. 0.009 and P for trend 0.003). Similar results were found for
2
P 0.05. higher daily intakes of vitamin C and greater knee extension
strength (lowest compared with highest tertile: P 0.008 and
-tocopherol and daily dietary intake of vitamin E. This finding P for trend 0.03) and physical performance (lowest com-
could have been due to a higher consumption of olive oil (x pared with highest tertile: P 0.03 and P for trend 0.08).
Higher daily intakes of -carotene tended to be associated with

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SD: 26.1 13.0 g/d) than of other vegetable oils (x SD: 1.0
1.6g/d) and animal fats (x SD: 0.7 1.0 g/d) in our greater knee extension strength (lowest compared with highest
sample. Confirming our hypothesis, Spearman correlations tertile: P 0.05 and P for trend 0.06).
showed a significant positive relation between olive oil con-
sumption and -tocopherol (r 0.073, P 0.02) but not with
-tocopherol. DISCUSSION
In unadjusted analyses (Table 2), daily dietary intakes of This study evaluated the relation between antioxidants and
vitamin C, vitamin E, and -carotene were significantly and objective performance assessments in elderly persons. We in-
positively correlated with knee extension strength. Plasma con- vestigated whether plasma concentrations and daily dietary
centrations of - and -tocopherol and daily dietary intakes of intakes of antioxidants were associated with physical perfor-
vitamin C, vitamin E, and -carotene were similarly correlated mance and muscular skeletal strength in an elderly population.
with summary physical performance scores. To our knowledge, this is the first study that evaluated simul-
Adjusted regression coefficients per SD increase in plasma taneously the effects of dietary antioxidant intakes and plasma
antioxidants for knee extension strength and physical perfor- antioxidant concentrations on physical performance in an el-
mance are described in Table 3. -Tocopherol was signifi- derly population. Previous studies were focused on younger
cantly correlated with both performance measures (knee exten- samples, especially athletes, and principally aimed at assessing
sion: 0.566, SE 0.193, P 0.003; physical performance: whether antioxidant supplementation reduces the rate of oxi-
0.044, SE 0.017, P 0.008). -Tocopherol was associated dation or helps promote faster recovery from the damage
only with knee extension strength ( 0.327, SE 0.165, P generated by exercise (11, 12, 2527). Our analyses suggest a
0.04). No significant sex interaction was found between plasma relation between plasma concentrations of antioxidants and
antioxidants and knee extension strength or physical performance physical performance and strength. A significant positive as-
(all P values 0.05). Daily dietary intakes of vitamin C and sociation, especially on muscular skeletal strength, was also

TABLE 3
Adjusted regression coefficients for knee extension strength and summary physical performance scores per SD increase (log) in plasma antioxidants
and in dietary intakes of antioxidants1

Knee extension strength (kg) Physical performance score


Regression coefficient (SE) P Regression coefficient (SE) P

Plasma
-Tocopherol (mol/L) 0.566 (0.193) 0.003 0.044 (0.017) 0.008
-Tocopherol (mol/L) 0.327 (0.165) 0.04 0.004 (0.015) 0.80
Daily intake
Vitamin C (mg) 0.383 (0.162) 0.02 0.029 (0.014) 0.04
Vitamin E (mg) 0.277 (0.204) 0.17 0.013 (0.018) 0.47
-Carotene (g) 0.311 (0.159) 0.05 0.015 (0.014) 0.29
Retinol (g) 0.012 (0.147) 0.94 0.010 (0.013) 0.31
1
The coefficients were adjusted for age, sex, site, Mini-Mental State Examination score, smoking, education, BMI, physical activity, total cholesterol,
triacylglycerol (log value), hypertension, coronary heart disease, stroke, congestive heart failure, number of medications taken, and daily dietary energy
intake. The -tocopherol SD 0.278, -tocopherol SD 0.441, daily vitamin C intake (log) SD 0.449, daily vitamin E intake (log) SD 0.323, daily
-carotene intake (log) SD 0.508, and daily retinol intake (log) SD 0.910.
ANTIOXIDANTS AND PHYSICAL PERFORMANCE 293
found for the daily dietary intakes of several antioxidants, nonsignificant association between the dietary intake of vita-
including vitamin C and -carotene. min E and physical performance and strength measures.
Free radical oxidative stress has been implicated in the Even though antioxidant supplementation has been sug-
pathogenesis of a variety of diseases, and natural antioxidant gested as a mean to perform better and recover more quickly
defenses have been found to be defective in many diseases and fully from vigorous exercise, the theoretical basis for why
(10). A free radical is a molecule that contains an unpaired antioxidants may enhance performance is not clear. An im-
electron in its outer orbit and that can exist independently (5, proved antioxidant status is one adaptation to regular exercise
12). Stability is achieved by the removal of electrons from training (32), and an acute increase in plasma antioxidant
surrounding molecules to produce an electron pair. The re- activity has been observed after exercise (33). This finding
mainder of the attached molecule then possesses an unpaired suggests that antioxidant status may be important in healthy
electron and therefore becomes a free radical. In this way, the muscle function, especially during the recovery phase after
presence of a single radical may initiate a chain sequence of exercise. To our knowledge, no evidence is available that
electron transfer (redox) reactions. Several studies suggest an documents the suppression of oxidative damage in muscle by
important role of oxidation in physiologic decline with normal antioxidant supplements, but it seems reasonable that an ade-
aging (8, 9, 13). Oxidative stress can come from a variety of quate antioxidant intake is needed to maintain healthy muscular
sources, from abnormal metabolic pathways to inflammatory activity (10, 34).
cells (eg, macrophages and neutrophils producing hydrogen Several limitations of our study should be mentioned. The
peroxide and hypochlorus acid as means of bacterial killing) cross-sectional design of the study did not permit us to evaluate
(28), smoking, and radiation (10). the effect of daily nutrient intakes on changes in physical
Our results confirmed previous findings that suggest a strong performance. Further longitudinal studies are needed to eval-

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correlation of plasma antioxidant concentrations with physical uate the role that antioxidant intakes may have on physical
performance and strength. In fact, we found a significantly high performance in the elderly. The study population was charac-
correlation of -tocopherol, the predominant form of circulat- terized by high nutritional indexes and tended to be over-
ing vitamin E (29), with physical performance and strength weight. These characteristics did not allow us to assess the
tests. We also reported a strong correlation between skeletal effect of very poor nutrition. The general overweight status of
muscular strength and -tocopherol, a vitamin E form indicated participants may have influenced our findings. To better iden-
by some studies to be a more effective trap for lipophilic-free tify the effects of antioxidants on physical performance, it may
radicals than -tocopherol (29). In our study, we found no be useful to evaluate a population in which under- and normal-
significant sex interaction between performance and antioxi- nourished persons are used as comparison groups. Finally,
dants. another limitation of our study was its limited assessment of
biological measures. The evaluation of both dietary intake
We also examined the effects of the dietary intake of major
estimates and biological measures would have been the ideal
antioxidants on physical performance and strength. Vitamin C
combination, especially given the significant association found
is a water-soluble vitamin that represents a first-line antioxi-
between dietary intakes of vitamin C and -carotene and knee
dant defense in plasma. It is a powerful inhibitor of lipid
extension strength.
peroxidation and regenerates vitamin E in lipoproteins and
In conclusion, our study indicates a significant positive cor-
membranes. -Carotene is a lipid-soluble antioxidant and a
relation between plasma antioxidant concentrations and phys-
precursor of retinol that works synergistically with vitamin C.
ical performance and strength. Higher dietary intakes of anti-
Vitamin E is a major lipid-soluble chain-breaking antioxidant
oxidants, especially of vitamin C, in the elderly were also
that prevents lipid peroxidation in lipoproteins and biological
found to be associated with greater skeletal muscular strength.
membranes. Its antioxidant function is strongly supported by However, the potentially positive effects of antioxidant intakes
regeneration promoted by vitamin C (10, 12). on performance and strength need to be confirmed in future
Our findings suggest an association between higher daily prospective studies and clinical trials.
dietary intakes of vitamin C and -carotene and skeletal muscle
strength. Whether higher antioxidant intakes are beneficial in The EPIC-Italy food-frequency questionnaire was developed as a coop-
promoting better physical performance and muscular strength erative project supported by the Italian Association for Cancer Research.
is controversial. Although the findings of some studies do not We are particularly grateful to Domenico Palli and Simonetta Salvini
(Molecular and Nutritional Epidemiology Unit, CSPO, Scientific Institute
support a beneficial effect of increased antioxidant intakes on
of Tuscany, Florence, Italy) and Vittorio Krogh (National Cancer Institute,
physical performance (11, 12, 30), other studies have shown Milan, Italy) for their help in processing and developing the InCHIANTI
improvements in the recovery from exercise with antioxidant nutritional database.
intake and a preventive role of antioxidant supplements against MC helped design the study, analyze the data, and write the manuscript.
oxidative damage (10, 27, 31). MP and BWJHP helped design the study, write the manuscript, and
In our study we showed a nonsignificant correlation between critically review the manuscript. BB helped collect and analyze the data
the dietary intake of vitamin E and -tocopherol but a signif- and critically review the manuscript. AC and AM helped collect the data
icant correlation with -tocopherol. The nonsignificant associ- and critically review the manuscript. GRW and HA helped critically review
the manuscript. JMG helped design the study and critically review the
ation between vitamin E and -tocopherol may have been due
manuscript. LF helped design the study, collect and manage the data, and
to the participants high consumption of olive oil, which was critically review the manuscript. None of the authors had any financial or
the major source of vitamin E in the study. Dietary intake of personal conflict of interest. Bristol-Myers Squibb sponsored the data
vitamin E includes the sum intake of all tocopherol and toco- analyses but had no influence on the design of the study, the data collec-
trienols with vitamin activity. Therefore, such a summary mea- tion, the analyses and interpretation of the data, or the decision to publish
sure is probably not precise and specific and may explain the the results.
294 CESARI ET AL

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Letter to the Editor

Vegetarian diets and exposure to organochlorine biphenyls and phthalate esters) have been found in human serum in the
pollutants, lead, and mercury following relative concentrations: urban fish eaters rural fish eaters
urban vegetarians rural vegetarians (7). Vegetarian vegans from
Hong Kong who consumed no fish or shellfish were shown to have very
Dear Sir: low concentrations of hair mercury compared with nonvegetarians (8).
Passos et al (9) suggest that an increased consumption of fruit can lower
The practice of feeding animal meat and bone meal to cattle has the body burden of mercury in Brazilian Amazon fish-eating popula-
been linked to the recent epidemic of bovine spongiform encepha- tions. After 12 mo of changing from an omnivorous diet to a lactoveg-
lopathy. Bovine spongiform encephalopathy, in turn, has been etarian diet, healthy adults had decreased hair concentrations of mercury
linked to the human prion disease variant Creutzfeldt-Jakob disease and lead (10). Therefore, a predominance of plant food in human diets
(1). In that recent issue of the Journal, Trevitt and Singh introduced is an important step in lowering the body burden of harmful substances
an interesting issue that has escaped previous discussions regarding in populations exposed to pollutants.
vegetarian diets and human health. Not only are harmful prions Strict vegetarianism, or veganism, is defined as the practice of
found in the meats of animals that have consumed animal products,
consuming plant food only (no animal products). However, variants
but also found in these meats are persistent lipophilic organic pol-
of vegetarianismsuch as lactoovovegetarianisminvolve the
lutants (PLOP), such as pesticides, polychlorinated dibenzo-p-
practice of consuming eggs and dairy products. Although a vegetar-
dioxins, dibenzofurans, polychlorinated biphenyls, and polybromi-
nated compounds. Animal products can also contain other ian lifestyle can lower the body burden of PLOP, MMHg, and lead,
neurotoxic substances, such as monomethyl mercury (MMHg) and such benefits can be undermined by the consumption of contami-
lead. nated milk and egg products. Farm animals that have been fed con-
Substances that are resistant to degradation and that are released taminated animal products produce contaminated milk and egg
in the environment accumulate in the food web and often end up products.
being consumed by humans. The chemical characteristics of these In summary, the inclusion of animal products in some forms of
persistent pollutants determine the location of accumulation, the vegetarianism can increase the exposure of humans to persistent
metabolism, and the half-time within animal tissues. Lipophilic sub- pollutants. Vegetarians with a desire to reduce their exposure to
stances such as PLOP accumulate in fat tissues, whereas lead accu- neurotoxic substances (eg, PLOP, MMHg, and lead) should be
mulates in bones as a function of age and diet. Although organo- aware of farming practices that introduce these pollutants into the
chlorine pesticides are a significant contaminant of crops, animal human diet.
byproducts are the major carriers of these harmful substances (2).
MMHg is also a fat-soluble substance, but it is complexed with
hydrophilic sulfhydril-containing molecules of protein matrices in Jos G Dorea
animal tissues. A series of chemical reactions involving mercury and
sulfate-reducing bacteria produce MMHg, which is then introduced Department of Nutrition
in the aquatic food chain and is thereby acquired by humans through CP 04322
the consumption of fish and shellfish. Animals and humans share Universidade de Brasilia
some of the bioaccumulation features of these persistent substances, 70919.970 Brasilia DF
but, because of different dietary habits, humans may or may not be Brazil
exposed to them. E-mail: dorea@rudah.com.br
The trend among affluent countries is to feed animal byproducts
to poultry and ruminants (herbivores such as cows, sheep, and goats).
These animals are used in milk production or are consumed as meat.
Fishmeal is mainly used as feed for dairy cows (3). Fishmeal con- REFERENCES
sumption results in an increase in milk production and stimulates an 1. Trevitt CR, Singh PN. Variant Creutzfeldt-Jakob disease: pathology,
increase in docosahexaenoic and eicosapentaenoic acids (4). Cow epidemiology, and public health implications. Am J Clin Nutr 2003;
feed may also contain significant proportions of bone meal (5). 78(suppl):651S 6S.
The health benefits of vegetarian diets have been a topic of health 2. Singh PP, Chawla RP. Insecticide residues in total diet samples in Pun-
and nutrition research since long before the emergence of modern jab, India. Sci Total Environ 1988;76:139 46.
3. Yeo JM, Knight CH, Chamberlain DG. Effects of changes in dietary
environmental concerns. However, because of increases in environ-
amino acid balance on milk yield and mammary function in dairy cows.
mental pollution, dietary habits have become an increasingly important J Dairy Sci 2003;86:1436 44.
public health issue. Studies have shown that a primarily vegetarian diet 4. Gulati SK, McGrath S, Wynn PC, Scott TW. Preliminary results on the
results in decreased exposures to bioconcentrated environmental pol- relative incorporation of docosahexaenoic and eicosapentaenoic acids
lutants. Vegetarian mothers have been shown to secrete substantially into cows milk from two types of rumen protected fish oil. Int Dairy J
fewer organochlorine substances in breast milk than do nonvegetarian 2003;13:339 43.
mothers (6). Environmental estrogenic substances (polychlorinated 5. Akayezu JM, Hansen WP, Otterby DE, Crooker BA, Marx GD. Yield

Am J Clin Nutr 2004;80:237 8. Printed in USA. 2004 American Society for Clinical Nutrition 237
238 ERRATUM

response of lactating Holstein dairy cows to dietary fish meal and bone 8. Dickman MD, Leung CK, Leong MK. Hong Kong male subfertility links
meal. J Dairy Sci 1997;80:2950 63. to mercury in human hair and fish. Sci Total Environ 1998;214:16574.
6. Noren K. Levels of organochlorine contaminants in human milk in 9. Passos CJ, Mergler D, Gaspar E, et al. Eating tropical fruit reduces
relation to the dietary habits of the mothers. Acta Paediatr Scand 1983; mercury exposure from fish consumption in the Brazilian Amazon.
72:811 6. Environ Res 2003;93:12331.
7. Rozati R, Reddy PP, Reddanna P, Mujtaba R. Role of environmental 10. Srikumar TS, Johansson GK, Ockerman PA, Gustafsson JA, Akesson B.
estrogens in the deterioration of male factor fertility. Fertil Steril 2002; Trace element status in healthy subjects switching from a mixed to a
78:118794. lactovegetarian diet for 12 mo. Am J Clin Nutr 1992;55:88590.

Erratum

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 94.

On page 290, column 2, paragraph 3, the unit mL is used incorrectly in 4 instances; the correct unit is L.
The text should have been presented as follows: Briefly, 100 L plasma was mixed with 100 L ethanol; after
being mixed by vortex, tocopherol was extracted into 500 L hexane containing 0.002% butylated hydroxy-
toluene (Sigma, St Louis). Tocol, a gift from Hoffmann-La Roche (Nutley, NJ), was added to the mixture as an
internal standard. Samples were centrifuged at 180 g for 5 min at 4 C. The supernatant fluid was collected
and dried under a stream of nitrogen gas and was reconstituted in 100 L methanol.

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