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Critical Reviews in Food Science and Nutrition
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Strawberry As a Functional Food: An Evidence-Based
Review
Arpita Basu a , Angel Nguyen a , Nancy M. Betts a & Timothy J. Lyons b
a Department of Nutritional Sciences , 301 Human Environmental Sciences, Oklahoma State
University (OSU) , Stillwater , OK , 74078 , USA
b Harold Hamm Oklahoma Diabetes Center , Section of Diabetes & Endocrinology University
of Oklahoma Health Sciences Center (OUHSC) , OKC , OK , 73104 , USA
Accepted author version posted online: 19 Feb 2013.Published online: 17 Dec 2013.
To cite this article: Arpita Basu , Angel Nguyen , Nancy M. Betts & Timothy J. Lyons (2014) Strawberry As a
Functional Food: An Evidence-Based Review, Critical Reviews in Food Science and Nutrition, 54:6, 790-806, DOI:
10.1080/10408398.2011.608174
To link to this article: http://dx.doi.org/10.1080/10408398.2011.608174
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Critical Reviews in Food Science and Nutrition, 54:790–806 (2014)
Copyright C
Taylor and Francis Group, LLC
ISSN: 1040-8398 / 1549-7852 online
DOI: 10.1080/10408398.2011.608174
Strawberry As a Functional Food:
An Evidence-Based Review
ARPITA BASU,1ANGEL NGUYEN,1NANCY M. BETTS,1
and TIMOTHY J. LYONS2
1Department of Nutritional Sciences, 301 Human Environmental Sciences, Oklahoma State University (OSU),
Stillwater, OK 74078, USA
2Harold Hamm Oklahoma Diabetes Center, Section of Diabetes & Endocrinology University of Oklahoma
Health Sciences Center (OUHSC), OKC, OK 73104, USA
Emerging research provides substantial evidence to classify strawberries as a functional food with several preventive and
therapeutic health benefits. Strawberries, a rich source of phytochemicals (ellagic acid, anthocyanins, quercetin, and cat-
echin) and vitamins (ascorbic acid and folic acid), have been highly ranked among dietary sources of polyphenols and
antioxidant capacity. It should however be noted that these bioactive factors can be significantly affected by differences in
strawberry cultivars, agricultural practices, storage, and processing methods: freezing versus dry heat has been associated
with maximum retention of strawberry bioactives in several studies. Nutritional epidemiology shows inverse association
between strawberry consumption and incidence of hypertension or serum C-reactive protein; controlled feeding studies have
identified the ability of strawberries to attenuate high-fat diet induced postprandial oxidative stress and inflammation, or
postprandial hyperglycemia, or hyperlipidemia in subjects with cardiovascular risk factors. Mechanistic studies have eluci-
dated specific biochemical pathways that might confer these protective effects of strawberries: upregulation of endothelial
nitric oxide synthase (eNOS) activity, downregulation of NF-kB activity and subsequent inflammation, or inhibitions of car-
bohydrate digestive enzymes. These health effects may be attributed to the synergistic effects of nutrients and phytochemicals
in strawberries. Further studies are needed to define the optimal dose and duration of strawberry intake in affecting levels
of biomarkers or pathways related to chronic diseases.
Keywords Strawberries, anthocyanins, antioxidants, bioavailability, postprandial lipemia, oxidative stress
INTRODUCTION
Strawberries (Fragaria ×ananassa) have acquired signifi-
cant prominence among fruits produced and consumed in the
United States: fourth highest in terms of production, following
grapes, oranges, and apples, and fifth highest in consumption,
preceded by bananas, apples, oranges, and grapes. The United
States leads the world in strawberry production, and California
accounts for the highest commercial production of this berry
crop, followed by Florida and Oregon (Boriss et al., 2010).
While consumption of fresh strawberries is more prevalent than
the frozen berries, the US market of both fresh and frozen straw-
berries includes imports of the berry crop from Mexico, Chile,
and China (USDA, 2005). Strawberries, in addition to the fresh
or frozen forms, are also commercially available as processed
Address correspondence to Arpita Basu, Department of Nutritional Sci-
ences, 301 Human Environmental Sciences, Oklahoma State University, Still-
water, OK 74078–6141, USA. E-mail: arpita.basu@okstate.edu
products, such as, jams, juices, nectar, and puree, and are ex-
tensively used in North American cuisine as a popular berry
ingredient (Klopotek et al., 2005; CSC, 2010). Keeping in view
the widespread epidemic of obesity, and related chronic dis-
eases, especially, cardiovascular disease (CVD), diabetes melli-
tus, and cancer in the United States (Jemal et al., 2010; Nguyen
et al., 2010; Towfighi et al., 2010), public health measures to
improve diet and lifestyle factors specifically emphasize the role
of fruits and vegetables in the management of these conditions
(Bendinelli et al., 2011). The strawberry fruit is now considered
a functional food offering multiple health benefits beyond basic
nutrition as substantiated by the accumulating evidence on its
antioxidant, anti-inflammatory, antihyperlipidemic, antihyper-
tensive, or antiproliferative effects. These mechanisms of action
are directly linked to the modification of etiology of chronic
diseases. Thus, the main objective of this review is to critically
discuss the health effects associated with strawberry consump-
tion and related factors affecting its nutrient and phytochemical
composition and bioavailability, in the light of recent literature.
790
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STRAWBERRY AS A FUNCTIONAL FOOD 791
ANTIOXIDANT CAPACITY OF STRAWBERRIES
Antioxidant properties of strawberries have been mostly
attributed to their polyphenol and vitamin content. Approxi-
mately 40 phenolic compounds have been identified in straw-
berries, such as, glycosides of quercetin, kaempferol, cyanidin,
pelargonidin, ellagic acid, as well as ellagitannins. Ascorbic
acid, ellagitannins, and anthocyanins were shown to be the most
significant contributors to the antioxidant capacity of straw-
berries, as estimated by their electrochemical responses (Aaby
et al., 2007). In another study, comparing cellular antioxidant ac-
tivity (CAA) and oxygen radical absorbance capacity (ORAC),
among 25 commonly consumed fruits in the United States,
Wolfe et al. reported apples and strawberries to be the largest
contributors to dietary CAA. The data further revealed that
strawberries were among the four most commonly consumed
fruits in the United States; apples, oranges, and grapes being the
other three fruits of common choice (Wolfe et al., 2008). Straw-
berries were also ranked second in total soluble phenolic content
among eight horticultural crops, namely, nopal, papaya, guava,
black sapote, avocado, mango, and prickly pear (Corral-Aguayo
et al., 2008). While comparing ORAC activity among berries,
Wang and Lin (2000) demonstrated highest antioxidant activity
of strawberries, followed by black raspberries, blackberries, and
red raspberries.
A group of researchers conducted analyses in commonly
available fruits and vegetables in the United Kingdom, and re-
ported highest antioxidant capacity in strawberries, as measured
by trolox equivalent antioxidant capacity (TEAC) assay, among
all fruits and vegetables (Proteggente et al., 2002). In general, the
findings of this study revealed higher TEAC in berries (strawber-
ries >raspberry), in comparison to other fruits and vegetables,
such as, apples, bananas, peaches, leeks, or lettuce (value/100 g
fresh weight). In a similar study, comparing antioxidant and
antiproliferative activities of common fruits, strawberries were
ranked fourth, in both total antioxidant activity and inhibitory
effects on human liver cancer cells, while cranberries received
the highest score on these parameters (Sun et al., 2002). Thus,
while the overall grading of antioxidant index in these studies
may vary depending on the analytical methods used, strawber-
ries consistently receive higher ranking among other fruits and
vegetables.
STRAWBERRY NUTRIENTS AND PHYTOCHEMICALS
Strawberries present a unique combination of several nutri-
ents, phytochemicals, and fiber, which plays a synergistic role
in its characterization as a functional food. As summarized in
Table 1, strawberries are a significant source of B-vitamins,
vitamin C, vitamin E, potassium, folic acid, carotenoids, and
specific flavonoids, such as, pelargonidin, quercetin, and cate-
chin. Strawberries also contain significant amounts of ellagic
acid, tannins, and phytosterols (Stoner et al., 2006; Aaby et al.,
2007; Basu et al., 2010). Strawberries were recently included
among the 100 richest sources of dietary polyphenols, and fur-
ther secured a ranking on the list of 89 foods and beverages
providing more than 1 mg total polyphenols per serving (P´
erez-
Jim´
enez et al., 2010). These polyphenols have diverse structures
and functions, and account for most of the health benefits of
strawberries.
Anthocyanins are water-soluble plant secondary metabo-
lites responsible for the deep colors of berry fruits, such as,
blueberries, blackberries, and strawberries. Since anthocyanins
are among the principal bioactives in strawberries, food scien-
tists have conducted comprehensive analyses for their quan-
tification and characterization in strawberries (Aaby et al.,
2007; Buend´
ıa et al., 2010). Using high performance liquid
chromatography–mass spectrometry (HPLC-MS), Buend´
ıa and
colleagues (2010) compared anthocyanin content in 15 straw-
berry cultivars grown in Spain, ranging from approximately
20–47 mg/100 g fresh weight. The major forms of antho-
cyanidins identified were cyanidin-3-glucoside, pelargonidin-
3-glucoside, 3-rutinoside, and 3-malonyl glucoside. In another
analytical study, Aaby et al. (2007) identified and quantified the
antioxidant capacity of strawberries grown in Norway, and re-
ported anthocyanins to be the third highest contributors to total
antioxidant capacity (13%), preceded by vitamin C (24%) and
ellagitannins (19%). Comparing anthocyanin content in eight
different strawberry cultivars grown in the United States, Meyers
et al. (2003) reported the concentration of cyanidin-3-glucoside
to range from approximately 20 to 50 mg/100 g strawberries.
Ellagic acid and ellagitannins have been reported as signifi-
cant contributors to the antioxidant and anticarcinogenic effects
of strawberries. Ellagic acid is a widely distributed phenolic acid
in foods, such as, strawberries, raspberries, grapes, and walnuts,
and has shown to exert potent free radical scavenging, as well as
antiproliferative effects in several experimental models. Ellag-
itannins are hydrolysable tannins usually consisting of glucose
and a phenolic acid such as gallic acid or hexahydroxydiphenic
acid. Strawberry cultivars grown in Spain were shown to vary
in ellagitannin and ellagic acid content (10–23 mg/100 g and
1–2 mg/100 g fresh weight, respectively), though these were
lower than total anthocyanin content in strawberries (Buend´
ıa
et al., 2010). Ellagitannins have also been shown to be the sec-
ond potent antioxidant factor in strawberries, next to vitamin C
(Aaby et al., 2007). In comparison to other fruits, strawberries
were reported to contain approximately 1.77 mg free ellagic
acid per 100 g fresh weight, which was higher than raspberries,
pineapples, and pomegranates (0.58, 0.08, and 1.73 mg/100 g
fresh weight, respectively), but was lower than blackberries,
raspberry jam, and strawberry jam (8.77, 2.25, and 2.01 mg/
100 g fresh weight, respectively; Bakkalbasi et al., 2009).
Flavonoids, such as, catechin, quercetin, kaempferol, narin-
genin, and hesperidin have a common chemical structure and oc-
cur in plant foods as aglycones or flavonoid glycosides (Crespy
et al., 2002). Free radical scavenging activity has been shown to
be the most potent biological mode of action of flavonoids, fol-
lowed by anti-inflammatory, vasodilatory, and antiproliferative
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792 A. BASU ET AL.
Tab l e 1 Nutritional content of strawberries
Strawberries, canned,
Strawberries, Strawberries, Strawberries, frozen, Strawberries, frozen, heavy syrup pack,
Value/100 g raw frozen, unsweetened sweetened, whole sweetened, sliced solids and liquids
Water (g) 89.97 89.97 78.05 73.18 75.35
Energy (kcal) 35 35 78 96 92
Protein (g) 0.43 0.43 0.52 0.53 0.56
Total lipid (fat) (g) 0.11 0.11 0.14 0.13 0.26
Carbohydrate, by difference (g) 9.13 9.13 21 25.92 23.53
Fiber, total dietary (g) 2.12.11.91.91.7
Sugars, total (g) 4.56 4.56 18.61 24.01 21.83
Calcium, Ca (mg) 16 16 11 11 13
Iron, Fe (mg) 0.75 0.50.47 0.59 0.49
Magnesium, Mg (mg) 11 11 6 7 8
Phosphorus, P (mg) 13 13 12 13 12
Potassium, K (mg) 148 148 98 98 86
Copper, Cu (mg) 0.049 0.049 0.019 0.02 0.063
Vitamin C, total ascorbic acid (mg) 41.241.239.5 41.431.7
Vitamin E [alpha-tocopherol] (mg) 0.29 0.29 0.24 0.23 0.19
Thiamin (mg) 0.022 0.022 0.015 0.016 0.021
Riboflavin (mg) 0.037 0.037 0.077 0.051 0.034
Niacin (mg) 0.462 0.462 0.293 0.401 0.057
Folate, total (mcg) 17 17 4 15 28
Carotene, beta (mcg) 27 27 16 14 16
Lutein +Zeaxanthin (mcg) 26 26 23 21 18
Anthocyanidins (mg)
Cyanidin 1.96 1.27 — — —
Delphinidin 0.32 0.02 — — —
Malvidin 0 — — — —
Pelargonidin 31.27 19.32 — — —
Peonidin 0 — — — —
Petunidin 0.08 — — — —
Flavonols (mg)
Kaempferol 0.46 0.49 — — —
Myricetin 0 0.35 — — —
Quercetin 1.14 0.46 — — —
Flavan-3-ols (mg)
(−)-Epicatechin 0.12 — — — —
(−)-Epicatechin 3-gallate 0.15 — — — —
(−)-Epigallocatechin 0.78 — — — —
(−)-Epigallocatechin 3-gallate 0.11 — — — —
(+)-Catechin 3.32 — — — —
(+)-Gallocatechin 0.03 — — — —
Source: National Nutrient Database for Standard Reference Service Release 22 Agricultural Research Services, Unites States Department of Agriculture, 2009;
Database for the Flavonoid Content of Selected Foods Release 2.1, 2007 Beltsville MD: Agricultural Research Services, United States Department of Agriculture,
2007. (–) Not found in USDA database.
functions. Buend´
ıa et al. (2010) reported cultivar differences in
flavonol (1.5–3.4 mg/100 g fresh weight) and proanthocyanidin
content (54–163 mg/ 100 g fresh weight) in strawberries grown
in Spain. This study also identified quercetin and kaempferol
conjugates as the main flavonol compounds, and catechin or
epicatechin to account for 17–28% of total proanthocyanidins in
these strawberry cultivars. In a recent review comparing proan-
thocyanidin content of different berries, strawberries received an
intermediate ranking (1450 mg/kg fresh weight) among cran-
berries, blueberries, black currants, red currants, red raspberries,
and blackberries (Del Rio et al., 2010).
Phytosterols are plant-derived sterols that have structural
and functional similarities to cholesterol. Numerous clinical
trials have reported the serum total and low-density lipopro-
tein (LDL)-cholesterol lowering effects of dietary plant sterols
or stanols at an average dose of 2 g/day (Hernandez-Mijares
et al., 2011). Phytosterols, such as, beta-sitosterol, campesterol,
and stigmasterol are naturally present in vegetable oils, seeds,
nuts, cereals, beans, and some fruits and vegetables, and also
in phytosterol-fortified foods, such as, take Take Control Rand
Benecol Rspreads (Eussen et al., 2011). In assessing the food
sources of phytosterols in the European Prospective Investiga-
tion into Cancer (EPIC-Norfolk) (n=24,798), berries with an
average daily consumption of 20 g were shown to contribute
approximately 3.0 mg/day total plant sterols (Klingberg et al.,
2008). In another study using the Spanish National Food Con-
sumption data, strawberry was identified as a fruit source of phy-
tosterols in the Spanish diet, providing approximately 0.7 mg
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STRAWBERRY AS A FUNCTIONAL FOOD 793
total phytosterols obtained from a daily intake of 6 g straw-
berries (Jim´
enez-Escrig et al., 2006). Freeze-dried strawberries
(10% fresh weight) used in clinical studies reporting serum
cholesterol lowering effects were also analyzed for phytosterol
composition: 50 mg phytosterols/50 g freeze-dried strawber-
ries. The researchers further discuss the role of strawberry phy-
tosterols in the observed lipid lowering effects (Basu et al.,
2009).
FACTORS AFFECTING STRAWBERRY NUTRIENTS,
PHYTOCHEMICALS, AND BIOACTIVITY
Tables 2 and 3 summarize the effects of agricultural prac-
tices, cultivar differences, and processing methods, especially
drying, on the nutritional and antioxidant capacity of straw-
berries. Cultivar differences have been reported to account for
variations in total polyphenols, anthocyanins, or folate content
in strawberries grown in Europe or the United States (Meyers
et al., 2003; Str˚
alsj¨
o et al., 2003; Anttonen et al., 2006; Buend´
ıa
et al., 2010). Specific agricultural practices, such as the use of
compost socks as opposed to plastic mulch or matted rows,
were associated with higher antioxidant capacity in strawber-
ries (Wang and Millner, 2009). Evidently, agricultural practices
affecting the nutritional content of the fruit deserve significant
attention in health research.
Processing of fresh fruits into products, such as puree, juices,
or jams, is necessary to ensure availability in all seasons and
cater to consumer preferences. However, processing is also as-
sociated with some inevitable loss of strawberry bioactives. In
a comparative study, Asami et al. (2003) reported significantly
higher polyphenols in frozen strawberries produced under con-
ventional or sustainable agricultural practices than freeze-dried
or air-dried strawberries grown under similar conditions. This
study also showed the lowest content of both ascorbic acid as
well as polyphenols in air-dried strawberries versus frozen or
freeze-dried forms, further explaining these effects due to the
oxidation or decomposition as a result of air drying at high
Tab l e 2 Effects of cultivar and agricultural systems on the polyphenol and antioxidant content of strawberries
Cultivar/culture Total antioxidant Total
system Free phenolics Flavonoids Anthocyanins antioxidant activity ORAC flavonols
(mg gallic acid (mg catechin (mg cyanidin (μmol
Meyers equivalents/100 g equivalents/100 g 3-glucoside/100 g vitamin C/g
et al. (2003)∗strawberry) strawberry) strawberry) strawberry)
Annapolis 256a76a39a45a——
Evangeline 266ab 68ab 48ab 52a——
Earliglow 294abc 67ab 28abc 133ab ——
Jewel 228bcd 56bc 37a45a——
Sable 228bcd 56bc 37a45a——
Mesabi 242bcd 52bc 41a50a——
Sparkle 242bcd 52cd 41a50a——
Allstar 180de 39d22bcd 20abc ——
Total phenolics (mg/100 g Total anthocyanins (mg/100 g
Buend´
ıa et al. (2010) fresh weight) (mg/100 g fresh weight) fresh weight)
Aguedilla 1.8±0.2fg— 46.6±2.9a——1.9±0.1defg
Albi´
on 1.5±0.1g— 23.5±1.9ef ——2.9±0.2b
Camarosa 2.5±0.1de — 47.4±0.4a——1.6±0.1fg
Candonga 4.2±0.3c— 29.7±2.5cde ——1.9±0.1defg
Carmela 3.1±0.1d— 29.0±2.2cde ——2.3±0.1cd
Chifl´
on 2.8±0.3de — 36.1±1.4b——1.5±0.0g
Cisco 4.0±0.4c— 32.1±2.9bc ——2.1±0.2cdef
Coral 0.8±0.1h— 20.2±0.4f——2.9±0.2b
Festival 2.3±0.2ef — 31.9±1.8bc ——1.7±0.1efg
Galexia 2.4±0.3e— 29.2±1.4cde ——3.4±0.3a
Macarena 1.7±0.2g— 25.0±1.1cde ——2.0±0.2cdef
Marina 6.7±0.5a— 44.8±1.8a——1.9±0.2defg
Medina 3.1±0.3d— 30.7±0.7cd ——2.1±0.2cde
Rubygem 2.7±0.5de — 32.0±1.0bc ——2.5±0.2bc
Ventana 5.2±0.4b— 26.0±1.9cde ——2.1±0.2cde
Wang and Millner (2009) (mg/100 g fresh weight) (mg/100 g fresh weight) (μmol TE/g fresh weight)
Allstar (matted row) 97.9±4.5i— 36.8±1.6f— 26.2 ±0.3h—
Allstar (black plastic mulch) 98.5±3.0i— 46.8±1.8d— 28.3 ±0.2g—
Allstar (compost socks) 47.7±2.0d— 47.7±2.0d— 32.8 ±0.1f—
Chandler (matted row) 157.1±3.0f— 55.1±2.3c— 41.3 ±0.4e—
Chandler (black plastic mulch) 174.7±3.1c— 60.1±2.1b— 46.0 ±0.1c—
Chandler (compost socks) 205.1±2.9a— 68.2±2.1a— 53.1 ±0.2a—
∗mean ±SD, adapted data from figures; (–) not reported. Values in the same column with no superscripts in common are significantly different for each set of
observations.
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794 A. BASU ET AL.
Tab l e 3 Effects of processing methods and storage on ascorbic acid, polyphenols and antioxidant capacity of strawberries1,2,3
Cultivar/processing method Total polyphenols Total anthocyanins ABTS FRAP Ascorbic acid TEAC
Wojdylo et al. (μM Trolox/ (μM Trolox/ (μmol/100gdw
(2009) (mg/100gdw) (mg/100gdw) 100gdw) 100gdw) (mg/100gdw) or%)
Kent
Fresh 1901.9 294.4 3.1±0.4b17.2±0.3b340.2±2.9f—
FD 1802.7 302.1 2.3±0.9e12.4±0.2f333.7±3.3g—
VD 1331.7 72.6 1.6±0.2f9.6±0.5i138.0±1.9l—
VM-240W 1702.0 227.9 2.3±0.5d13.1±0.3e298.5±2.6h—
VM-360W 1649.5 228.7 2.4±0.0d14.0±0.6e276.5±3.4i—
VM-480W 1657.4 211.8 2.5±0.3d13.8±0.0e264.7±3.2j—
CD 1220.5 79.4 2.1±0.5g10.4±0.3h94.9±1.9m—
Elsanta —
Fresh 2405.9 372.6 3.6±0.0a18.1±0.9a680.2±3.2a—
FD 2411.5 375.2 2.9±0.2c 16.8±0.7c676.2±1.9b—
VD 1667.6 88.2 2.4±0.1d11.7±0.2e260.4±1.5j—
VM-240W 2302.4 305.8 2.9±0.5c14.4±0.1d593.1±0.9c—
VM-360W 2277.8 312.2 2.1±0.6f12.5±0.8f450.6±2.6d—
VM-480 W 2253.2 318.6 3.0±0.0b16.2±0.5c437.2±2.7e—
CD 1541.5 135.8 2.7±0.1f13.6±0.9g185.1±3.5k—
Klopotek et al. (2005) (mg/100 g or%) (mg/100 g or%) (μg/100 g or%) (mg/100 g or%) (μg/100 g or%)
Strawberries 257.1±2.4A42.2±0.3A— 2466 ±97A104.1±1.7A1190 ±30A
Pasteurized strawberry juice 35.6±0.5I67.3±6.0G— 41.8±2.1H36.0±1.9I34.4±2.3H
Pasteurized strawberry nectar 42.1±0.3J56.8±1.8H— 48.1±2.8I39.8±1.1J47.0±0.8I
Strawberry wine (from juice) 46.9±0.9N20.7±0.7K— 50.3±3.8M34.0±2.1M56.5±3.8L
Hartmann et al. (2008) (%) (%) (%) (%) (%)
Bottle pasteurized juice (glass) 62.3±0.9b61.4±0.8b— 73.5±4.3a63.5±0.8a71.1±5.3ad
Pasteurized enzymatic juice (PET) 78.3±0.6c76.2±1.0c— 88.0±4.4b46.1±1.9b87.7±3.5ad
After 3 weeks storage
Bottle pasteurized juice (glass) 60.2±1.4ej 49.0±0.2f— 67.1±3.1ac 28.6±2.7f69.8±2.7ad
Pasteurized enzymatic juice (PET) 76.1±2.1f65.4±1.2g— 78.6±10bd 32.8±2.7g86.8±2.5b
After 11 weeks storage
Bottle pasteurized juice (glass) 58.9±0.8j35.8±0.8n— 66.1±3.8g15.6±2.7hj 68.3±4.5d
Pasteurized enzymatic juice (PET) 72.4±1.4d46.3±0.8m— 78.6±4.6def 26.5±2.7f79.7±4.4c
FD, freeze-drying; VD, vacuum-drying; VM, vacuum-microwave drying; CD, convection drying; DP, degree of polymerization; ABTS, 2,2’-azinobis(3-
ethylbenzothiazoline-6-sulfonate); FRAP, the ferric reducing antioxidant power; TEAC, trolox equivalent antioxidant capacity; dw, dry weight; PET, hot filled
bottles using flow pasteurization unit.
Results reported as mean ±SD; (–) not reported. Values in the same column with no superscripts in common are significantly different for each set of observations.
temperatures (Asami et al., 2003). In a study reported from
Poland, Wojdylo et al. (2009) compared different drying meth-
ods, namely, freeze-drying, vacuum-drying, vacuum-microwave
drying, and convection drying in two different strawberry culti-
vars. Results of this study showed that vacuum-drying at 240 W
was the most effective in preserving the total antioxidants, ascor-
bic acid, and color of strawberries compared to other methods,
while freeze-dried strawberries had the greatest antioxidant ca-
pacity (Wojdylo et al., 2009). Processing of strawberries to prod-
ucts, such as juices and puree, has also been associated with
significant loss of ascorbic acid, polyphenols, and antioxidant
capacity (Klopotek et al., 2005; Hartmann et al., 2008). Factors
involved in the processing of strawberries, such as nonenzymatic
mash treatment, bottle versus flash pasteurization, fermentation,
storage time, and temperature, are critical factors that should
be carefully controlled to maximize the preservation of straw-
berry bioactives and antioxidant capacity (Klopotek et al., 2005;
Hartmann et al., 2008). In assessing the nutritional values of
processed products from Oregon grown strawberries, Ngo et al.
(2007) reported significant losses of anthocyanins and total phe-
nolic content in canned strawberries or strawberry jam. In an
interesting comparative study in fresh-cut strawberries versus
whole fruits, Gil et al. (2006) reported no losses in phenolic
content of fresh-cut pineapples, mangoes, cantaloupes, water-
melons, strawberries, and kiwifruits, after six days of storage at
5◦C, though visual appearance and texture started deteriorating
before then. Thus, while processed strawberry products, such as
puree, juices, and jams, provide alternative sources of the fresh
fruit in all seasons, the choice of fresh or frozen strawberries
seems to be the most prudent for health and nutrition benefits.
BIOAVAILABILITY OF STRAWBERRY
PHYTOCHEMICALS
Bioavailability of dietary polyphenols, involving factors af-
fecting their absorption and metabolism, is a complex process
and several pathways have been proposed in rat, pig, or human
model. Selected anthocyanins have been shown to be absorbed
intact as glycosides (Cao et al., 2001; Wu et al., 2002). Though
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STRAWBERRY AS A FUNCTIONAL FOOD 795
the mechanism of absorption is not clear, it has been suggested
that bilitranslocase, an organic anion membrane carrier, may
play a role in the bioavailability of anthocyanins (Vanzo et al.,
2008).
In a recent report, Azzini et al. (2010) have specifically elu-
cidated the pathways for strawberry anthocyanin absorption
and metabolism. Pelargonidin-3-glucoside has been proposed
to undergo gastric conversion to pelargonidin glucuronide, fol-
lowed by small intestinal and colonic microbial metabolism to
4-hydrobenzoic acid. Pelargonidin-3-O-glucoside, the principal
anthocyanin in strawberries, has been shown to be bioavail-
able in pharmacokinetic studies in humans. Felgines et al.
(2003) identified pelragonidin-3-glucoside and its metabolites,
such as pelargonidin, monoglucoronides, and sulfoconjugates of
pelargonidin in urine, following a 200 g strawberry intervention
in healthy volunteers. Urinary excretion of these metabolites was
observed to continue until 24-hour period. Similar findings were
also reported by Hollands et al. (2008) on increasing urinary
excretion of strawberry anthocyanins with increasing doses of
fresh strawberries (100–400 g). In a study comparing bioavail-
ability of strawberry anthocyanins in 300 g fresh or stored (+4◦C
for four days) in healthy volunteers, Azzini et al. (2010) reported
significantly higher mean plasma α-carotene levels in subjects
consuming fresh versus stored strawberries, while no differences
were observed in plasma phenolic acids between two varieties.
Total concentration of 24-hour urinary excretion of pelargoni-
din glucoside and pelargonidin glucoronide was significantly
higher in case of fresh versus stored strawberry consumption.
Thus, while these findings show higher bioavailability of phy-
tochemicals in fresh strawberries versus those refrigerated for
four days, subsequent differences in bioactivity need to be con-
firmed, especially in the context of limited shelf life of fresh
strawberries. In another comparative study, Cerda et al. (2005)
assessed the urinary excretion of ellagitannins and the microbial
metabolite, urolithin B in healthy volunteers consuming 250 g
fresh strawberries, 225 g frozen red raspberries, 35 g walnuts,
or 300 mL oak-aged red wine. While ellagitannins or ellagic
acid were not detected in urine at any time point, the excretion
of urolithin B was lowest in the case of strawberry interven-
tion and highest following walnut intake (2.8% versus 16.6%).
Thus, ellagitannins and ellagic acid were not detected as parent
compounds in urine, and metabolism by colonic microflora is
less efficient for strawberries when compared to raspberries, red
wine, or walnuts (Cerda et al., 2005).
Bioavailability has also shown to be influenced by compo-
nents in the food matrix. Mullen et al. (2008) reported a study
in eight healthy nonsmoking volunteers who consumed 200 g
defrosted frozen strawberries, with or without 100 mL double
cream. Peak plasma concentration (C max) of the main straw-
berry anthocyanin metabolite, pelargonidin-O-glucuronide was
not significantly affected, though there was a significant delay
in plasma C max when strawberries were consumed with cream.
Also, zero to two-hour urinary excretion of strawberry antho-
cyanins was lower in the case of cream intake versus without
cream (Mullen et al., 2008). Thus, on the basis of these findings,
strawberry anthocyanins are better absorbed when consumed as
the fresh fruit or puree, and anthocyanin absorption may be af-
fected when consumed as part of a mixed meal, especially along
with fat-rich foods.
EPIDEMIOLOGICAL DATA: STRAWBERRIES,
HYPERTENSION, INFLAMMATION, AND CANCER
Nutritional epidemiology provides convincing evidence on
the cardio-protective effects of frequent consumption of fruits
and vegetables high in fiber, micronutrients, and several phy-
tochemicals (Liu et al., 2000; Joshipura et al., 2001; Bazzano
et al., 2002; Holt et al., 2009). The findings of the INTER-
HEART study, comprising dietary patterns from 52 countries,
revealed a significant inverse association between the prudent
dietary pattern high in fruits and vegetables and the risk of acute
myocardial infarction (Iqbal et al., 2008). Studies have also re-
ported specific associations between berries or berry flavonoid
(anthocyanins) intakes and cardiovascular health. Though lim-
ited, epidemiological studies support the protective effects of
strawberries against hypertension, inflammation, cancer, and
cardiovascular mortality.
Analyses of dietary flavonoid intakes in 46,672 women from
the Nurses’ Health Study I (NHS I), 87,242 women from the
Nurses’ Health Study II (NHS II), and 23,043 men from the
Health Professionals Follow-Up Study (HPFS), in a 14-year
follow-up, revealed significant cardiovascular health benefits of
strawberry and blueberry anthocyanins (Cassidy et al., 2010).
As the main dietary sources of anthocyanins in these cohorts,
higher intakes of strawberry and blueberry anthocyanins
(16–22 mg/day) were associated with a significant 8% risk
reduction of hypertension, versus in those with lower consump-
tion (5–7 mg/day of berry anthocyanins). These findings were
significant upon adjustments for covariates, such as family his-
tory, physical activity, body mass index (BMI), and other dietary
factors associated with blood pressure (Cassidy et al., 2010).
These observational data corroborate the experimental and
clinical findings on the antihypertensive effects of strawberries
(Erlund et al., 2008; Cheplick et al., 2010). In another cohort,
postmenopausal women (n=34,489) participating in the Iowa
Women’s Health Study showed a significant reduction in CVD
mortality associated with strawberry intake in a 16-year follow-
up period. Study findings showed that a mean anthocyanin
intake of 0.2 mg/day was associated with a significantly reduced
risk of CVD mortality in these postmenopausal women (Mink
et al., 2007). Strawberry intake has also been associated with
lower C-reactive protein (CRP) levels, a stable inflammatory
biomarker among female US health professionals enrolled in
the Women’s Health Study (n=38,176) (Sesso et al., 2007).
These participants provided dietary information using a 131-
item validated semiquantitative food frequency questionnaire.
Strawberry intake was described as “never” or “less than one
serving per month” up to “6+servings per day” of fresh,
frozen, or canned strawberries. During a follow-up period for
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796 A. BASU ET AL.
approximately 11 years, a decreasing trend for CVD was
observed in subjects consuming higher amounts of strawberries
(p=0.06), while a borderline significant risk reduction of
elevated CRP levels (≥3 mg/L) was observed among women
consuming higher amounts of strawberries (≥2 servings/week).
Elevated CRP has been significantly associated with inflam-
mation and is a high-risk factor of CVD (Ridker et al., 2000).
Analyses of NHANES data (1999–2002) revealed a significant
inverse association between serum CRP and anthocyanin in-
takes among US adults (Chun et al., 2008). These observational
data suggest antihypertensive and anti-inflammatory effects of
strawberry consumption, which may contribute to overall risk
reduction of CVD.
Epidemiological observations also support a protective asso-
ciation between increasing consumption of colorful fruits and
vegetables and the incidence of cancer (Feskanich et al., 2000;
Michaud et al., 2000; Siegel et al., 2010). In a prospective five-
year cohort study in an elderly population (n=1271), higher
consumption of fresh strawberries, categorized among green
and yellow vegetables including tomatoes, dried fruits, broc-
coli, carrots or squash, and salads, was associated with signif-
icantly reduced cancer mortality. The authors attribute these
observations to the carotenoid content of fruits and vegetables
known to exert anticarcinogenic effects (Colditz et al., 1985).
In a larger five-year prospective cohort study (n=2,193,751
person-years), higher consumption of Rosaceae botanical sub-
group, including strawberries, was associated with a protective
effect against esophageal squamous cell carcinoma versus those
in the lower quintiles of this fruit group (Freedman et al., 2007).
Reduced risks of head and neck cancer were also reported in the
same cohort among those consuming higher number of serv-
ings of Rosaceae botanical subgroup representing strawberries,
plums, pears, apples, peaches, and nectarines, in comparison
to lower intakes and other botanical groups (Freedman et al.,
2008). These population-based studies provide some insight
into the potential protective effects of strawberries against can-
cer, which have also been postulated in several experimental
cell and animal models (Table 4). These observational data pro-
vide a rationale for further investigation of the effects of whole
strawberries on both surrogate markers and hard clinical end
points of CVD and cancer.
CLINICAL STUDIES: STRAWBERRIES, OXIDATIVE
STRESS, HYERLIPIDEMIA, AND POSTPRANDIAL
STAT US
Health benefits of strawberries have been investigated in
healthy or overweight subjects, in patients with mild to moderate
elevations in serum cholesterol and in subjects with metabolic
syndrome (Table 5). Strawberry intervention has been re-
ported to increase plasma antioxidant capacity, reduce oxidized
LDL and lipid peroxidation, decrease serum total and LDL-
cholesterol, and attenuate postprandial glycemia or lipemia as
summarized in Table 5. In a single study reported in healthy vol-
unteers, administration of strawberries was also shown to signif-
icantly decrease urinary excretion of N-nitrosodimethylamine
(NDMA), corresponding to inhibition of nitrosation of carcino-
genic precursors (Chung et al., 2002).
Oxidative stress, defined as an imbalance between free rad-
ical production and antioxidant defense mechanisms, resulting
in accumulation of oxidative products, has been implicated in
the pathogenesis of cancer and CVD (Valko et al., 2007). Hu-
man intervention studies, using fresh, frozen, or freeze-dried
strawberries, have been shown to reduce oxidant stress associ-
ated with high-fat meal, hyperlipidemia, or metabolic syndrome,
thus suggesting a therapeutic role of strawberries as dietary an-
tioxidants in counteracting these oxidative challenges (Paiva
et al., 1998; Basu et al., 2010; Burton-Freeman et al., 2010;
Henning et al., 2010). Flavonoids, the principal class of straw-
berry phytochemicals, have demonstrated antioxidant effects,
mainly via scavenging free radicals, inducing phase 2 enzymes
involved in antioxidant defense and detoxification, and modu-
lating expression of antioxidant genes (Rice-Evans and Packer,
2003). While few clinical studies have reported the antihyper-
lipidemic effects of berry flavonoid extracts (Lee et al., 2008;
Qin et al., 2009), strawberry-specific flavonoids warrant further
investigation on the basis of the reported studies using fresh or
frozen strawberries.
Hyperlipidemia is an independent risk factor for atheroscle-
rosis and subsequent CVD, mainly via upregulation of both
oxidative stress and inflammatory responses (Stokes et al.,
2002). The observed lowering of elevated serum total and LDL-
cholesterol (Basu et al., 2010), or raising serum high-density
lipoprotein (HDL)-cholesterol (Erlund et al., 2008), following
strawberry intervention, can be attributed to the synergistic ef-
fects of fiber, phytosterols, and polyphenols in strawberries.
These individual constituents have been independently shown to
exert antihyperlipidemic effects in clinical trials principally via
decreasing serum total and LDL-cholesterol, increasing HDL-
cholesterol, decreasing intestinal cholesterol absorption, and
mass and activity of plasma cholesteryl ester transfer protein
(Lee et al., 2008; Qin et al., 2009; Marangoni and Poli, 2010;
Wolever et al., 2010). Thus, some of these effects on cardiovas-
cular health have also been reported following consumption of
strawberries, and thus, the inclusion of the whole berry fruit is
recommended in the dietary strategies against CVD.
Postprandial hyperglycemia and hyperlipidemia directly con-
tribute to endothelial dysfunction and the development of
atherosclerosis (Temelkova-Kurktschiev et al., 2000; Tushuizen
et al., 2010). The efficacy of dietary polyphenols in attenuat-
ing postprandial hyperglycemia, hyperlipidemia, oxidant, and
inflammatory responses has been investigated in clinical trials
following a high-fat or high-glucose challenge (Unno et al.,
2005; Bogani et al., 2007; Burton-Freeman, 2010). Strawberry
or mixed berry (including strawberry) intervention in healthy
volunteers or in patients with hyperlipidemia was shown to in-
crease postprandial plasma antioxidant capacity (Prior et al.,
2007), produce a lower postprandial glucose response versus
control meal (Kurotobi et al., 2010; T¨
orr¨
onen et al., 2010), or
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Tab l e 4 Summary of mechanistic studies on anticarcinogenic effects of strawberries
Reference Cell line/animal model Duration and dose of strawberry/anthocyanin intervention Mechanisms proposed
Xue et al. (2001) Syrian hamster embryo (SHE) cell transformation
model
Freeze-dried black raspberry or strawberry fractions
(2–100 μg/mL) or ellagic acid (0.3–4.5 μg/mL)
treatment along with carcinogen (B[a]P) for seven days
Methanol fractions of black raspberries and strawberries, or
ellagic acid significantly inhibited cell transformation
via interfering with the uptake, activation, and/or
detoxification of (B[a]P) leading to chemopreventive
effects (p<0.05)
Carlton et al. (2001) Male F344 rats (five to six-week old) injected with
carcinogen NMBA or vehicle (DMSO) for once
per week for 15 weeks or single dose of NMBA,
or three times per week for five weeks to induce
tumor in the esophagus
Thirty weeks, 2 weeks, or 25 weeks intervention of
AIN-76A diet containing 5% or 10% freeze-dried
strawberries
Strawberry supplementation caused a significant decrease
in NMBA-induced esophageal tumor incidence and
tumor multiplicity versus control group (AIN-76A +
NMBA); 5% and 10% freeze-dried strawberries reduced
tumor multiplicity in the range of 24–38% and 31–56%,
respectively; significant decrease in O6-methylguanine
in esophageal DNA of strawberry-fed animals (p<0.05)
Meyers et al. (2003) Human liver cancer cells [HepG(2)] Strawberry extracts of eight cultivars (0–80 mg/mL); cells
treated with extracts for 96 hours
Strawberry extracts showed a dose-dependent inhibition of
human liver cancer cell proliferation; Earliglow cultivar
exhibited the highest antiproliferative effect while
Annapolis showed the lowest (p<0.05)
Ramos et al. (2005) Human liver cancer cells [HepG(2)] Strawberry extracts (0.1, 0.2, 0.4, 0.6, 0.8 mg/mL); plum
extracts and pure polyphenols (quercetin, chlorogenic
acid, epicatechin) were also used in the study; cells
treated for 4 and 18 hours
Strawberry extracts exhibited higher cell death rate than
plum extracts (IC50 for strawberry extracts: 0.6 mg/mL);
strawberry and plum extracts also induced apoptosis of
cancer cells versus controls (p<0.05)
Wang et al. (2005) Human lung epithelial cancer cells (A549) and
mouse epidermal cells (JB6 P+)
Strawberry fruit extracts at different levels of dilution: 0,
1:20, 1:40, 1:80, 1:125, 1:160, 1:250, 1:500, 1:1000;
cells pre-treated for one hour with extracts
Strawberry extract treatment showed downregulation of
AP-1 and NF-kappaB activities, blocking of MAPK
signaling, and decreased proliferation of human lung
cancer cells (p<0.05)
Seeram et al. (2006) Human oral (KB, CAL-27), breast (MCF-7), colon
(HT-29, HCT116), and prostate (LNCaP) tumor
cell lines
Strawberry extracts (25–200 μg/mL); other berry extracts
used were derived from blueberry, blackberry, raspberry,
black raspberry, and cranberry; cells treated for 48 hours
Strawberry and black raspberry extract exhibited
significant pro-apoptotic activity in HT-29 colon cancer
cell line versus untreated controls (p<0.05); strawberry
extracts significantly decreased cell proliferation of all
cell lines versus untreated controls
Olsson et al. (2006) Human colon cancer (HT 29) and breast cancer
(MCF-7) cell lines
Organically and conventionally grown strawberries; cells
treated with four different concentrations of strawberry
extracts: 0.025, 0.05, 0.25, or 0.5% for 24 hours
Organically grown strawberries had higher antiproliferative
activity than conventional strawberries; 53% inhibition
of HT-29 and 43% inhibition of MCF-7 cells at highest
concentrations versus controls (p<0.05)
Zhang et al. (2008) Human oral (CAL-27, KB), colon (HT29, HCT-116),
and prostate (LNCaP, DU145) cell lines
Strawberry crude extracts (250 μg/mL) and purified
compounds (100 μg/mL); 10 phenolic compounds:
cyanidin-3-glucoside, pelargonidin, pelargonidin-
3-glucoside, pelargonidin-3-rutinoside, kaempferol,
quercetin, kaempferol-3-(6’-coumaroyl)glucoside),
3,4,5-trihydroxyphenyl-acrylic acid, glucose ester of
(E)-p-coumaric acid, and ellagic acid; cells treated for
48 hours
Significant inhibition of human oral, colon, and prostate
cancer cells with both crude extracts and purified
compounds from strawberries (p<0.05)
(Continued on next page)
797
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Tab l e 4 Summary of mechanistic studies on anticarcinogenic effects of strawberries (Continued)
Reference Cell line/animal model Duration and dose of strawberry/anthocyanin intervention Mechanisms proposed
Li et al. (2008) Mouse epidermal JB6 CI 41 cell line Freeze-dried black raspberries and strawberries
fractionated for cell treatment (1–100μg/mL for 30
minutes)
Strawberry fractions significantly inhibited NFAT and
TNF-αtranscription, induced by BaPDE; similar
anticancer effects were also exerted by black raspberry
fractions (p<0.05)
McDougall et al. (2008) Human cervical cancer (HeLa) and colon cancer
(CaCo-2) cell lines
Strawberry, rowan berry, raspberry, lingonberry,
cloudberry, arctic bramble, blueberry, sea buckthorn, or
pomegranate extracts; cells treated for 72 hours
Strawberry extracts showed the highest antiproliferative
effects, followed by arctic bramble, cloudberry, and
lingonberry; ellagitannins being the common agent in
these berries
Weaver et al. (2009) Human normal and tumorigenic breast (B42,
MCF-7) and prostate (P21, LNCaP, PC-3) cell
lines
Strawberry-derived polyphenol-rich extract, anthocyanin or
tannin-rich subfractions; cells treated for 72 hours
Cytotoxic effects of strawberry extracts at 5 μg/mL leading
to a 50% decrease in cell survival in normal and cancer
cells; tannin-rich subfraction more cytotoxic than
anthocyanin-rich fraction
Sharma et al. (2010) Human 293T cell line with reconstituted canonical
Wnt signaling
ET-enriched strawberry, jamun, or pomegranate fruit
extracts; cells treated with ET extracts, EA, or UA for
48 hours
Strawberry ET extracts, EA, or UA caused inhibition of
Wnt signaling; IC50 for strawberry ET extracts:
28 μg/mL; implicated in prevention of colon
carcinogenesis
Stoner et al. (2010) Male F344 rats (four to five-week old) injected with
carcinogen NMBA or vehicle (DMSO) for five
weeks to induce tumor in the esophagus
Thirty week intervention of AIN-76A diet containing 5%
strawberries or other berries (black or red raspberries,
blueberries, noni, wolfberry, or acai berry); total
phenolics from strawberries: 103–230 mg/100 g fresh
weight; fiber: 2000 mg/100 g fresh weight
Strawberry supplementation caused a significant decrease
in esophageal tumor incidence and tumor multiplicity
versus control group (AIN-76A +NMBA), decreased
serum cytokines and increased serum antioxidant
capacity (p<0.05); similar effects were also noted for
other berries
Wang et al. (2010) Male F344 rats (four to five-week old) injected with
carcinogen NMBA or vehicle (DMSO) for 15
weeks to induce tumor in the esophagus
Thirty-two weeks (including 2 weeks prior to NMBA or
DMSO treatment) intervention of AIN-76A diet
containing 5% or 10% strawberries or other berries
(black raspberries or blueberries) as freeze-dried whole
berries or berry residues; strawberry diet providing
27.3% residues with ET in the range of 0.08–0.17 g/kg
diet
Both whole strawberry or strawberry residue-supplemented
diets were equally effective in reducing NMBA-induced
esophageal tumor multiplicity and volume versus control
(AIN-76A +NMBA) (p<0.05); no significant
difference noted between high- and low-dose ET; similar
effects were also noted for other berries
Notes: B[a]P: Benzo[a]pyrene; NMBA: N-nitrosomethylbenzylamine; DMSO: Dimethyl sulfoxide; MAPK: Mitogen-Activated Protein Kinase; NFAT: nuclear factor of activated T cells; TNF-α: tumor
necrosis factors-α; B[a]PDE: Benzo[a]pyrene-7,8-diol-9,10-epoxide; ET: ellagitannins; EA: ellagic acid; UA: urolithin A.
798
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Tab l e 5 Summary of human intervention studies using fresh or processed strawberry products
Source Duration Study design Study subjects Control Strawberry intervention Significant findings
Cao et al. (1998) Postprandial Controlled trial Eight healthy female
subjects (mean age, 67 ±
0.6 years)
Coconut drink 240 g strawberries added to the
control drink
Increase in plasma vitamin C,
serum, and urine antioxidant
capacity (p<0.05)
Paiva et al. (1998) Postprandial Controlled trial Seven healthy elderly
women (mean age, 67 ±
0.6 years)
378 mL coconut drink 240 g fresh, whole, and
homogenized strawberries
added to the control drink
Decreased plasma carotenoids
versus baseline (p<0.02)
Chung et al.
(2002)
Four days Three consecutive control days
followed by experimental
agents on the fourth day
Forty healthy volunteers
(27 males and 13
females, mean age, 24.0
±3.0 years)
Control diet: low in NDMA,
nitrate, amine, sulfur
compounds, ascorbic
acid, and phenolic-
compound-containing
food items
Experimental diet containing
whole strawberries (300 g),
garlic juice (200 g), or kale
juice (200 g) with
administration of nitrate
(400 mg/day)
Decrease in NDMA excretion
following whole strawberry
consumption versus nitrate only
(p<0.05)
Prior et al. (2007) Postprandial Randomized cross-over
multicentered trial (Study
#3—grapes, kiwifruit,
strawberries)
Seven healthy women
(18–40 years)
None Seascape’ strawberries (300 g)
purchased from Watsonville,
CA
Increase in postprandial whole
plasma antioxidant capacity in
strawberry group versus
baseline (p<0.05)
Erlund et al.
(2008)
Eight weeks Randomized, single-blind,
placebo-controlled, trial
Seventy-two subjects with
cardiovascular risk
factors (mean age,
control- 58.4 ±5.6 years,
berry- 57.5 ±6.3 years)
One of four control
products each day to
match the energy intake
in the berry group; 2 dL
sugar-water, 100 g sweet
semolina porridge, 100 g
sweet rice porridge, or
40 g marmalade sweets
Two portions of berries daily;
whole bilberries (100 g) and
a nectar of 50 g crushed
lingonberries every other
day; black currant or
strawberry puree (100 g, 80%
black currants) and
cold-pressed chokeberry and
raspberry juice (0.7 dL, 80%
chokeberry) on alternating
days
Inhibition of platelet function;
increase in HDL-cholesterol;
decrease in systolic blood
pressure in berry versus control
group (p<0.05)
Jenkins et al.
(2008)
Ten weeks Randomized cross-over study
with two-week washout
phase
Twenty-eight
hyperlipidemic subjects
(62.0 ±1.0 years);
subjects were on a
cholesterol-lowering
dietary portfolio for
2.5 years
Oat bran bread (65 g/day) Fresh strawberries (454 g/day);
purchased from local stores
Reduction in oxidative damage to
LDL in strawberry group
versus baseline (p<0.05);
maintained reduction in
LDL-cholesterol as result of
previous dietary regimen;
enhanced dietary palatability
Basu et al. (2009) Four weeks Baseline and Postintervention
effects
Sixteen women with
metabolic syndrome
(mean age,
51±9.1 years)
None 50 g of freeze-dried strawberry
powder as beverage
(California Strawberry
Commission, CA, USA)
Decrease in total and
LDL-cholesterol and lipid
peroxidation at four weeks
versus baseline (p<0.05)
(Continued on next page)
799
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Tab l e 5 Summary of human intervention studies using fresh or processed strawberry products (Continued)
Source Duration Study design Study subjects Control Strawberry intervention Significant findings
Basu et al. (2010) Eight weeks Randomized controlled trial Twenty-seven men and
women with metabolic
syndrome (mean age,
47.0±3.0 years)
Four cups water 50 g of freeze-dried strawberry
powder as beverage
(California Strawberry
Commission, CA, USA)
Decrease in total and
LDL-cholesterol, small LDL
particles, and vascular cell
adhesion molecule-1 at 8 weeks
versus controls (p<0.05)
T¨
orr¨
onen et al.
(2010)
Postprandial Randomized controlled
cross-over trial
Twelve healthy men and
women (age range,
25–69 years)
Control meal: 250 mL
water, 35 g sucrose, 4.5 g
glucose, 5.1 g fructose
Mixed berry puree (150 g)
consisting of black currants,
bilberries, European
cranberries and strawberries,
with 35 g sucrose
Lower postprandial glucose at 15
and 30 minutes and higher at
150 minutes in berry versus
control group; smaller peak
increase in glucose from
baseline in berry group (p<
0.05)
Henning et al.
(2010)
Three weeks Baseline and Postintervention
effects
Twenty-one healthy female
volunteers (mean age,
29.0 ±6.3 years)
None 250 g frozen (Camarosa and
Ventana) strawberries daily
for three weeks (California
Strawberry Commission, CA,
USA)
Increase in serum antioxidant
capacity (p<0.05);
nonsignificant decreasing trend
of lymphocyte oxidative DNA
damage
Burton-Freeman
et al. (2010)
Postprandial and 12
weeks (two sequences
of six weeks each
consuming strawberry
or placebo beverage)
Randomized
placebo-controlled
cross-over trial
Twenty-four hyperlipidemic
men and women (mean
age, 50.9 ±15 years)
Placebo beverage matched
for calories,
carbohydrates and sugars
10 g freeze-dried strawberries
∼110 g/day of fresh
strawberries (California
Strawberry Commission, CA,
USA)
Postprandial lipemia and oxidized
LDL were significantly reduced
following high-fat meal
challenge with strawberries
versus placebo (p<0.05)
Kurotobi et al.
(2010)
Postprandial Cross-over design Thirty healthy subjects (20
women, 10 men), (mean
age, 29.4 ±11.7 years)
Glucose: 50 g (reference
food)
Five kinds of strawberry jams
containing sugar, corn syrup
and sugar, sugar and glucose,
apple juice, or polydextrose
Postprandial blood glucose
significantly lower in the case
of strawberry jams versus
reference glucose load
(p<0.05)
Ellis et al. (2011) Six weeks Cross-over design Fourteen women and ten
men (mean age,
50.9±15 years)
Placebo beverage matched
for calories,
carbohydrates, and
sugars
10 g freeze-dried strawberries
∼100 g/day of fresh
strawberries (California
Strawberry Commission, CA,
USA)
Significant attenuation of
postprandial inflammatory
(IL-1β) and thrombotic (PAI-1)
markers following high
carbohydrate/fat meal in the
strawberry group versus
placebo intervention for six
weeks (p<0.05)
Notes: NDMA: N-nitrosodimethylamine; IL-1β: Interleukin-1β; PAI-1: plasminogen activator inhibitor-1.
800
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STRAWBERRY AS A FUNCTIONAL FOOD 801
reduce postprandial hyperlipidemia or plasma lipid oxidation
following a high-fat meal challenge versus placebo (Burton-
Freeman et al., 2010). These favorable postprandial effects of
strawberries or mixed berries on glucose and lipid profiles pro-
vide evidence for their potential role in the dietary management
of CVD.
MECHANISTIC STUDIES: STRAWBERRIES AND CVD
Emerging research in animal and cell culture models pro-
vides evidence on the effects of strawberries in ameliorating
obesity, hyperglycemia, hyperlipidemia, hypertension, and ox-
idative stress, the well-known risk factors for CVD. Phyto-
chemicals in strawberries, such as anthocyanins, ellagic acid,
catechin, quercetin, and kaempferol have exhibited antioxida-
tive, antidiabetic, antihypertensive, or antithrombotic effects in
several experimental models, which may explain the observed
cardio-protective effects of strawberries in epidemiological and
clinical studies.
Anthocyanin treatment was shown to upregulate endothe-
lial nitric oxide synthase (eNOS) in bovine artery endothelial
cells, and increase protein level of eNOS in human umbili-
cal vein endothelial cells (Xu et al., 2004; Lazz`
e et al., 2006).
Treatment of rabbit aortic rings with aqueous extract of freeze-
dried strawberry powder produced a dose-dependent endothe-
lial relaxation, which was attributed to the phosphorylation of
eNOS by the strawberry extract (Edirisinghe et al., 2008). Since
eNOS plays a crucial role in maintaining cardiovascular home-
ostasis by favorably modulating blood pressure and reducing
endothelial dysfunction, strawberry phytochemicals, by upreg-
ulating eNOS, may reverse endothelial dysfunction and subse-
quent initiation of atherosclerosis. Pelargonidin-3-O-glucoside,
a strawberry-specific anthocyanidin, was shown to significantly
inhibit glucose uptake and transport by human intestinal Caco-2
cells, which may have implications in glucose absorption in the
management of diabetes mellitus (Manzano and Williamson,
2010). Using an animal model of obesity, Prior et al. (2008,
2009) demonstrated that purified anthocyanins from blueberries
and strawberries added to drinking water could prevent the de-
velopment of dyslipidemia and obesity in mice fed a high-fat
diet during a 90-day period. Oral administration of pelargoni-
din was also shown to prevent streptozotocin-induced diabetic
neuropathic hyperalgesia in male Wistar rats at eight weeks
(Mirshekar et al., 2010). Intraperitoneal injection of pelargoni-
din has also been shown to normalize elevated blood glucose
levels in diabetic rats at five weeks (Roy et al., 2008). Though
limited, these data provide some evidence on the role of straw-
berry extracts or strawberry-specific anthocyanins in counter-
acting obesity, diabetes mellitus, dyslipidemia, and endothelial
dysfunction contributing to CVD. Antioxidant effects and in-
hibition of platelet aggregation have also been observed in the
case of other strawberry phytochemicals, such as catechin, el-
lagic acid, kaempferol, and quercetin, suggesting their role in
reversing or inhibiting oxidative stress and thrombotic events
underlying CVD (Tzeng et al., 1991; Meyer et al., 1998; Rein
et al., 2000). Ellagic acid treatment was also shown to suppress
oxidized LDL-induced proliferation of rat aortic smooth muscle
cells, which may have implications in inhibiting the initiation
and development of atherosclerosis (Chang et al., 2008).
Purified ellagitannins and ellagic acid from strawberries have
been evaluated for their antihyperglycemic and antihypertensive
effects. Pinto Mda et al. (2010) reported the α-glucosidase, α-
amylase, and angiotensin I-converting enzyme (ACE) inhibitory
activities of strawberry phytochemicals using in vitro models,
which may be linked to the management of hyperglycemia and
hypertension. McDougall and associates (2005) conducted com-
parative analyses of berry polyphenols in inhibiting carbohy-
drate digestive enzymes, as a potential phytotherapy in obesity
and hyperglycemia. Strawberry and raspberry extracts contain-
ing significant amounts of soluble tannins exhibited greater inhi-
bition of α-amylase in comparison to blueberry, black currant,
or red cabbage extracts. These researchers also reported the
protease and lipase inhibitory activities of berry polyphenols,
thereby suggesting a novel therapy using berries, such as straw-
berries as macronutrient enzyme inhibitors in obesity, dyslipi-
demia, and hyperglycemia (McDougall et al., 2005; McDougall
and Stewart, 2005). Cheplick et al. (2010) provide further ev-
idence on the cultivar-specific α-amylase, α-glucosidase, and
ACE-inhibitory activities of strawberries. Among all strawberry
cultivars, Ovation exhibited the highest α-glucosidase inhibitory
activity, Honeoye, Idea, and Jewel cultivars showed moderate
α-amylase inhibition, while water extracts of Jewel and Ova-
tion exhibited moderate ACE inhibition (Cheplick et al., 2010).
In conclusion, these mechanistic data elucidate the role of in-
dividual strawberry pytochemicals or extracts as antioxidants,
antiobesity, antidyslipidemic, antihyperglycemic, or antihyper-
tensive agents. However, further studies are needed in support
of these observations.
MECHANISTIC STUDIES: STRAWBERRIES
AND CANCER
As summarized in Table 4, strawberries, both as extracts or
purified strawberry phytochemicals, have been shown to exert
anticarcinogenic effects mediated principally via detoxification
of carcinogens, protection against DNA damage, decrease in
cancer cell proliferation via apoptosis, downregulation of acti-
vator protein-1 (AP-1) and nuclear factor kappa B (NF-kappa
B), inhibition of Wnt signaling and tumor necrosis factor-αtran-
scription (TNF-α), and increase in serum antioxidant capacity
(Carlton et al., 2001; Xue et al., 2001; Meyers et al., 2003;
Ramos et al., 2005; Wang et al., 2005). These observations are
supported by treatment effects of strawberries versus controls in
human cancer cells, Syrian hamster embryo cells, in mouse epi-
dermal cells, and also in rodent models of carcinogen-induced
esophageal cancer (Table 4).
Stoner et al. (2006, 2010) have conducted extensive labo-
ratory studies on the effects of freeze-dried black raspberries,
blackberries, and strawberries on the inhibition of tumors in
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802 A. BASU ET AL.
N-nitrosomethylbenzylamine (NMBA)-treated rodents. The
findings of their group, validated by several bioassays, may be
summarized as follows: inhibition of NMBA metabolism and
DNA adduct formation, reduced frequency of preneoplastic
lesions and subsequent initiation of malignancy, and downregu-
lation of inflammatory cyclooxygenase-2 (COX-2), as potential
chemopreventive mechanisms of black raspberries and straw-
berries. Stoner and associates have further commented that the
doses of freeze-dried berries used in these animal studies are
achievable in the human diet, which further strengthens the
applicability of their findings. These intriguing data, though
limited, warrant further investigation of freeze-dried strawberry
supplementation in animal models of other common forms of
gastrointestinal malignancies, such as colon and gastric cancer.
Data further suggest a synergistic effect among phytochemicals
and micronutrients in strawberries in exerting protection against
carcinogenesis (Stoner et al., 2006, 2010).
In a comparative evaluation, Weaver et al. (2009) have re-
ported higher cyto-toxicity of tannin-rich versus anthocyanin-
rich strawberry extracts in human breast and prostate cancer
cells. Several lines of evidence support the chemopreventive ef-
fects of anthocyanins and tannins in human cancer cells. The
anti-invasive activities of anthocyanins through suppression of
matrix metalloproteinases and inhibition of tumor growth and
angiogenesis have been demonstrated in human colon and breast
cancer cells and in human breast cancer xenografts in BALB/c
nude mice, respectively (Hui et al., 2010; Shin et al., 2011). Spe-
cific pathways, such as stimulation of adenosine monophosphate
(AMP)-activated protein kinase α1(AMPKα1) and inhibition of
mammalian target of rapamycin (mTOR), and downregulation
of proteinases involved in metastasis, have also been identi-
fied as principal chemopreventive mechanisms of anthocyanins
(Lee et al., 2010; Ho et al., 2010). Tannins, as specific straw-
berry polyphenols, have also been known to exert significant
anticancer effects in human breast, cervix, and colon carcinoma
cells via antioxidative and apoptotic effects leading to inhibition
of cell proliferation (Barraj´
on-Catal´
an et al., 2010; Kasimsetty
et al., 2010; Stanojkovi´
c et al., 2010).
Purified ellagic acid from strawberries has been shown to
contribute to the anticarcinogenic effects of strawberries in sev-
eral human cancer cell models (Zhang et al., 2008; Sharma et al.,
2010). Ellagic acid has been independently shown to exert an-
tiproliferative effects via apoptosis through inhibition of NF-kB
and suppress lipopolysaccharide (LPS)-induced inflammatory
gene expressions in cell and animal models of carcinogenesis
(Edderkaoui et al., 2008; Karlsson et al., 2010; Umesalma and
Sudhandiran, 2010).
STRAWBERRIES AND NEURONAL HEALTH
Several lines of evidence substantiate the role of strawber-
ries in reversing age-related neurodegenerative disorders. The
most significant findings have been reported by the researchers
at the USDA Human Nutrition Research Center on Aging at
Tufts (Joseph et al., 1998; Shukitt-Hale et al., 2008). In an ani-
mal model of age-related neuronal signal-transduction and cog-
nitive behavioral deficits, strawberry extract supplementation
(9.5 g/kg) caused a significant reversal of parameters related
to age-induced neuronal deficits, especially, GTPase activity
(Joseph et al., 1998). In another animal model of exposure to
cosmic radiations, pre-treatment of animals using a 2% straw-
berry diet for two months prior to exposure was shown to sig-
nificantly improve performance than the controls, showing pro-
tective effects of strawberries against radiation-induced damage
(Rabin et al., 2005). Shukitt-hale et al. (2008) have summa-
rized the proposed mechanisms underlying the neuroprotective
effects of berry polyphenols, such as strawberries, as follows:
lowering oxidative stress and inflammation, altering signaling
in neuronal communication and calcium buffering ability, and
favorably modulating stress signaling pathways. These mecha-
nisms of action of berry fruits including strawberries have also
been implicated in the reversal of Alzheimer’s or Parkinson’s
disease (Joseph et al., 2009).
Berry anthocyanidins have also been shown to inhibit
monoamine oxidases A and B, and this has been implicated in
protective effects against neurodegenerative disorders (Dreisei-
tel et al., 2009). Strawberry-specific anthocyanidin, pelargoni-
din, has also been shown to inhibit proteasome activity and con-
sequently confer neuroprotective effects (Dreiseitel et al., 2008).
These pre-clinical studies provide substantial evidence on the
role of strawberries in reversing oxidative stress-related neu-
ronal damage and warrant further investigation in patients with
neurodegenerative diseases, as an alternative phytochemistry-
based therapy.
CONCLUSIONS
Thus, on the basis of the preceding sections reviewed in
this article, strawberries can be termed as a “functional food,”
providing health benefits beyond basic nutrition (Hasler and
Brown, 2009). As one of the most popular fruits produced and
consumed in the United States, strawberries contain significant
amounts of phytochemicals (polyphenols and ellagic acid) and
micronutrients (vitamins and carotenoids). These constituents
in strawberries can be affected by differences in cultivars, agri-
cultural practices, and processing methods. However, fresh and
frozen strawberries, available throughout the year, are signifi-
cant dietary sources of polyphenols and vitamins, which have
been shown to contribute to their observed health effects. Stud-
ies involving cellular and animal models provide evidence on
the anticarcinogenic and antiproliferative effects of strawber-
ries, principally via downregulation of NF-kB activity and sub-
sequent inflammation; ellagitannins in strawberries have been
shown to exert significant chemotherapeutic effects. Mechanis-
tic studies have also shown the protective effects of strawber-
ries against endothelial dysfunction and hyperglycemia, mainly
via upregulation of eNOS activity, and inhibitions of ACE and
carbohydrate digestive enzymes. Epidemiological and clinical
Downloaded by [Oklahoma State University] at 07:16 18 September 2014
STRAWBERRY AS A FUNCTIONAL FOOD 803
observations further strengthen the evidence on the health ben-
efits of strawberries. Existing data from human studies mainly
highlight the antioxidant, anti-inflammatory, and antihyperten-
sive effects of strawberries, and attenuation of high-fat diet in-
duced postprandial lipemia or oxidative stress with strawberry
intervention. Emerging research also indicates the potential of
strawberries in reversing age-related neurodegenerative disor-
ders, which deserves further investigation. Thus, the role of
strawberry as a functional food is supported by several lines
of evidence and warrants further research on its preventive and
therapeutic health outcomes.
RECOMMENDATIONS
Based on the existing literature, strawberries have a signif-
icant impact on health and disease as a popular nutrient dense
low-calorie fruit. However, future research is needed to further
define these effects while considering some recommendations
below:
•Identify processing and storage methods for maximum preser-
vation of strawberry nutrients and phytochemicals and related
consumer education.
•Identify bioavailability of strawberry phytochemicals and
metabolites in humans with one or more risk factors for
chronic diseases, such as aging, obesity, dyslipidemia, hy-
pertension, or exposure to carcinogens.
•Identify optimal dose of strawberries (via dose–response
study) that would affect specific biomarkers of chronic dis-
eases related to oxidative stress and inflammation.
•Conduct mechanistic studies on interaction (synergistic or an-
tagonistic) effects of strawberries with commonly used pre-
scription drugs in the treatment of cancer, CVD, or neurode-
generative diseases.
•Conduct long-term prospective studies to assess temporal re-
lationship between strawberry consumption and incidence of
cancer, CVD, or neurodegenerative diseases.
ACKNOWLEDGMENTS
Supported by the California Strawberry Commission. This
publication was made possible by NIH Grant Number P20 RR
024215 from the COBRE Program of the National Center for
Research Resources.
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