Journal of the Saudi Society of Agricultural Sciences (2017) 16, 287–293

King Saud University

Journal of the Saudi Society of Agricultural Sciences

www.ksu.edu.sa
www.sciencedirect.com

FULL LENGTH ARTICLE

Health-benefits of date fruits produced in Saudi

Arabia based on in vitro antioxidant, anti-
inflammatory and human tumor cell proliferation
inhibitory assays
Chuan-Rui Zhang a, Saleh A. Aldosari b,*, Polana S.P.V. Vidyasagar b,
Paraj Shukla b, Muraleedharan G. Nair a

a
Bioactive Natural Products and Phytoceuticals Laboratory, Department of Horticulture, Michigan State University,
East Lansing 48824, MI, United States
b
Chair of Date Palm Research, Department of Plant Protection, College of Food and Agriculture Sciences,
King Saud University, Riyadh 11451, Saudi Arabia

Received 24 February 2015; revised 16 September 2015; accepted 16 September 2015

Available online 25 September 2015

KEYWORDS Abstract Date fruits are reported to exhibit health-beneficial effects in addition to its nutritional
Date palm; value. Fruits collected from commercial date palm trees were sequentially extracted with water
Phoenix dactylifera L.; and methanol. All varieties of date fruits contained sugars, phenolics, triterpenoids, triglycerides,
Functional food; fatty acids and steroids, where sugars were the predominant components. Water and methanolic
Cell proliferation; extracts of date fruits were assayed for antioxidant, antiinflammatory and human tumor cell pro-
Lipid peroxidation; liferation inhibitory activities. In MTT antioxidant assay, methanolic extracts at 250 lg/mL exhib-
Cyclooxygenase enzymes ited moderate activity with absorbance values between 0.14 and 0.41. Water and methanolic
extracts at 100 lg/mL inhibited lipid peroxidation (LPO) by 50–67% and 58–82%, respectively.
In anti-inflammatory assay using cyclooxygenase enzymes (COX-1 and -2), water and methanolic
extracts at 100 lg/mL showed COX-1 enzyme inhibition by 26–36% and 33–41%, and COX-2
by 45–48% and 48–52%, respectively. At 100 lg/mL concentrations, methanolic extracts of all date
fruits showed marginal cell proliferation inhibitory activity against human gastric, prostate, colon,
breast and lung tumor cell lines. The bioassay results suggest that varietal difference is not a

* Corresponding author. Tel.: +966 4693377.

E-mail address: [email protected] (S.A. Aldosari).
Peer review under responsibility of King Saud University.

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
288 C.-R. Zhang et al.

significant factor among the 29 date fruits studied when compared for health-beneficial effects
resulting from non-nutritional components present in it.
Ó 2015 The Authors. Production and hosting by Elsevier B.V. on behalf of King Saud University. This is
an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction and sprayed with 10% sulfuric acid solution. MTT [3-(4,
5-dimethylthiazole-2-yl)-2,5-diphenyltetrazolium bromide],
Date palm Phoenix dactylifera L. (Palmaceae) is grown under tert-butylhydroquinone (TBHQ), butylatedhydroxyanisole
arid conditions primarily in the Middle East, North Africa (BHA), butylatedhydroxytoluene (BHT), Adriamycin, aspirin,
and United States. Its fruit is an important food and dietary naproxen and ibuprofen were purchased from Sigma–Aldrich
component in many countries. Dates are implicated to possess Chemical Company (St. Louis, MO, United States). Similarly,
medicinal properties in addition to its nutritional value the nonsteroidal anti-inflammatory drug (NSAIDs) CelebrexÒ
(Vayalil, 2012). Several studies have reported date fruit was physician’s professional sample provided by Dr. Subhash
with a wide range of bioactivities, such as antioxidant Gupta, Sparrow Pain Center, Sparrow Hospital, Lansing,
activity due to the presence of phenolics, carotenoids and Michigan. COX-1 and -2 enzymes were prepared in our labo-
anthocyanins in it (Mohammed and Al-Okbi, 2004; Saleh ratory from ram seminal vesicles (Oxford Biomedical
et al., 2011; Vayalil, 2002), antimutagenic (Vayalil, 2002), Research, Inc., Rochester Hills, MI, United States) and insect
anti-inflammatory (Mohammed and Al-Okbi, 2004), antihy- cells cloned with human PGHS-2 enzyme, respectively. Arachi-
perlipidemic (Tang et al., 2013), antibacterial (Sallal and donic acid was purchased from Oxford Biomedical Research,
Ashkenani, 1989) and antifungal (Sallal et al., 1996) activities. Inc. (Rochester Hills, MI, United States). 1-Stearoyl-2-lino
Over 450 date palm varieties or cultivars are grown in the leoyl-sn-glycero-3-phosphocholine (SLPC) was purchased
Kingdom of Saudi Arabia and yield more than 1 million metric from Avanti Polar Lipids (Alabaster, AL, United States).
tons of date fruits accounting for about 14% of the total world The fluorescent probe, 3-(p-(6-phenyl)-1,3,5-hexatrienyl)
production (FAOSTAT, 2014). We had earlier reported the phenylpropionic acid was purchased from Molecular Probes
functional food components in Ajwa date fruit, the most (Eugene, OR, United States). Fetal bovine serum (FBS) and
expensive date fruit in the market (Zhang et al., 2013). In this Roswell Park Memorial Institute 1640 (RPMI-1640) medium
study, we determined the health-benefits of 29 significant vari- were purchased from Gibco BRL (Grand Island, NY, United
eties of date fruits, Barni Al Madinah, Hulwa, Khashram, States). Human tumor cell lines DU-145 and LNCaP (pros-
Khodry, Khalas, Deglet Noor, Dekhaini, Rabeaa, Rushodia, tate), MCF-7 (breast) and NCI-H460 (lung) were purchased
Ruthana, Ruthana Al Sharag, Sabaka, Sukkari Al Qassim, from the National Cancer Institute (NCI, Bethesda, MD, Uni-
Sullaj, Shalabi, Shaishee, Safawi, Sefri, Segae, Ajwa, Anbara, ted States). AGS (gastric) and HCT-116 (colon) were pur-
Luban, Mabroom, Majhool, Mutwah, Meneifi, Nabtat Ali, chased from American Type Culture Collection (ATCC,
Naboot Seif and Hilali using in vitro bioassays. The antioxi- Rockville, MD, United States). All cell lines, enzymes and
dant activity was evaluated using MTT [3-(4, 5-dimethylthia reagents were stored in the Bioactive Natural Products and
zole-2-yl)-2,5-diphenyltetrazolium bromide] (Liu and Nair, Phytoceuticals Laboratory at Michigan State University (East
2010) and lipid peroxidation (LPO) assays (Bowen-Forbes Lansing, MI, United States). Centrifugation was carried out
et al., 2009; Liu and Nair, 2012; Zhang et al., 2013). Using on a Sorvall RC-5C refrigerated high-speed centrifuge
cyclooxygenase enzymes (COX-1 and -2), we determined the (DuPont, Newtown, CT, United States). MTT antioxidant
anti-inflammatory activity of the date varieties studied assay plates were read on Bio-Tek Elx800 universal microplate
(Bowen-Forbes et al., 2009; Liu and Nair, 2012; Zhang reader (Bio-Tek Instruments, Inc., Winooski, VT, United
et al., 2013). In addition, human tumor cell lines, AGS States). The fluorescent reading in the LPO assay was carried
(gastric), DU-145 and LNCaP (prostate), HCT-116 (colon), out on a Turner model 450 Fluorometer (Barnstead/Ther-
MCF-7 (breast) and NCI-H460 (lung) were employed to eval- molyne Corporation, Dubuque, IA, United States). COX
uate the cell proliferation inhibitory activity of water and assays were performed in Instech micro oxygen chamber using
methanolic extracts of all date fruits (Bowen-Forbes et al., an oxygen electrode (Instech Laboratories, Plymouth Meeting,
2009; Liu and Nair, 2012). PA, United States) attached to a YSI model 5300 biological
oxygen monitor (Yellow Springs Instrument, Inc., Yellow
2. Material and methods Springs, OH, United States).

2.1. General experimental procedures 2.2. Date fruits

All solvents used were of ACS reagent grade (Sigma–Aldrich The 29 varieties of date fruit samples were collected from com-
Chemical Company, St. Louis, MO, United States). 250 lm mercial farms in Saudi Arabia. The varietal identity of the fruit
silica gel plates (Analtech, Inc., Newark, DE, United States) collected was determined based on the information provided
were used for thin-layer chromatography (TLC). TLC plates by the farmer and by using the database kept in the Ministry
were viewed under UV (ultraviolet) light at 254 and 366 nm of Agriculture, Saudi Arabia (Table 1) (Anonymous, 2006).
in Spectroline CX-20 ultraviolet fluorescence analysis cabinet Date fruits were packaged and shipped to Michigan State
(Spectroline Corporation, Westbury, NY, United States), University and kept in 20 °C till analyses.
Health-benefits of date fruits 289

Table 1 Date fruit variety, date palm identification number, yield of water and methanolic extracts (g) from 100 g date fruits and
percent human tumor cell proliferation inhibitory activity of methanolic extracts for DU-145 and LNCaP (prostate), MCF-7 (breast),
NCI-H460 (lung) AGS (gastric) and HCT-116 (colon). Water extracts were not active.
Date variety Plant ID* Water extract MeOH extract AGS DU-145 LNCaP HCT-116 MCF-7 NCI-H460
a
Barni Al Madinah 26 76.4 3.89 11.6 12.4 – 15.7 13.0 15.8
Hulwaa 64 72.3 5.30 16.8 – – 16.6 16.9 17.5
Khashramb 80 72.6 1.86 20.5 10.8 – 13.8 16.6 20.1
Khodryc 86 77.4 4.23 10.0 15.9 12.3 19.7 22.1 18.4
Khalasc 89 80.3 4.60 11.2 – – 22.8 19.4 14.1
Deglet Noorc 98 79.7 5.01 16.1 14.5 – 15.9 11.4 20.1
Dekhainia 100 79.9 3.93 18.5 – 10.0 24.7 15.6 17.1
Rabeaaa 111 74.3 3.96 14.7 16.2 – 13.9 17.5 17.2
Rushodiaa 114 67.2 3.77 19.4 15.2 – 22.7 19.0 18.2
Ruthanaa 116 73.3 3.60 12.5 – – 13.6 18.8 17.6
Ruthana Al Sharaga 117 80.6 4.16 27.3 – 12.0 18.7 11.2 16.6
Sabakaa 124 70.4 5.74 18.6 – – 14.4 21.6 16.2
Sukkari Al Qassima 138 73.1 4.19 – 13.1 – 18.3 16.7 20.1
Sullajc 142 81.4 2.60 12.2 17.2 – 14.3 13.5 16.6
Shalabia 159 76.4 4.75 22.8 – 10.4 14.6 22.3 18.6
Shaisheea 164 73.4 4.12 12.2 16.9 11.1 13.4 14.9 19.7
Safawia 169 80.6 3.95 12.7 14.0 10.1 14.6 16.7 19.2
Sefric 173 72.3 4.97 20.6 – – 12.5 17.2 18.2
Segaed 176 75.2 4.71 21.7 13.5 – 16.4 20.1 18.4
Ajwac 185 75.3 4.64 16.4 – 12.9 22.1 18.6 18.8
Anbaraa 191 73.3 3.98 13.1 – – 14.8 10.7 22.2
Lubana 226 74.8 4.85 19.0 – – 11.8 18.9 12.9
Mabrooma 231 77.7 4.29 – – – 16.5 15.3 18.1
Majhoolc 234 73.0 5.50 – – – 19.9 17.4 20.9
Mutwaha 246 74.8 9.43 16.0 – – 11.4 13.9 11.9
Meneific 254 76.7 4.98 12.0 13.3 – 18.4 17.7 12.7
Nabtat Alic 273 66.1 6.47 18.5 – – 12.5 11.4 20.9
Naboot Seifc 275 76.9 5.88 15.5 19.0 – 19.7 20.3 20.2
Hilalia 285 76.2 5.47 25.5 14.2 – 18.5 19.6 19.4
a
Procured on November 15, 2011.
b
Procured on June 20, 2012.
c
Procured on May 10, 2014.
d
Procured on April 26, 2014.
*
Commercial varieties, Ministry of Agriculture, Saudi Arabia. – : not active.

2.3. Extraction of date fruits for bioassays was added and vortexed again for 1 min. An aliquot
(200 lL) of the reaction mixture was pipetted to a 96-well cell
The 29 varieties of date fruits, 2 or 3 fruits per variety, were culture plate and the absorbance was read at 570 nm on a
weighed and pitted separately. The pitted dates were cut in Bio-Tek Elx800 universal microplate reader. Each sample
small pieces, homogenized and extracted with water was tested in duplicate.
(50 mL  3, 1 h). After centrifugation, the supernatant from
each extraction was combined and lyophilized to yield crude 2.5. Lipid peroxidation (LPO) inhibitory assay
water extracts. The residue from water extraction was then
extracted with MeOH (100 mL  3, 2 h), centrifuged and the LPO inhibitory activity was evaluated for the extract
combined supernatant evaporated under vacuum. The result- (100 lg/mL) and positive controls (BHA, BHT and TBHQ
ing concentrate was lyophilized to yield crude methanolic at 1.802, 2.204 and 1.662 lg/mL, respectively) according to
extract. our previous report (Bowen-Forbes et al., 2009; Liu and
Nair, 2012; Zhang et al., 2013). The liposome, large unilamel-
2.4. MTT antioxidant assay lar vesicles (LUV), was prepared by re-suspension of the lipid-
probe mixture (0.15 M NaCl, 0.1 mM EDTA, and 0.01 M
MTT assay was evaluated according to our previous report MOPS maintained over chelating resin Chelex 100). The
(Liu and Nair, 2010). The stock solution of test extracts mixture was then subjected to 10 freeze–thaw cycles in a dry
(10 mg/mL) and positive controls (Vitamin C and TBHQ at ice/EtOH bath and extruded 29 times through a 100 nm pore
1 mg/mL) were prepared in DMSO. An aliquot of 10 lL of test size membrane (Avestin Inc., Ottawa, ON, Canada). The
samples and 190 lL of MTT water solution (1 mg/mL) were peroxidation was initiated by the addition of 20 lL of
vortexed in a capped glass vial (2 mL) for 1 min, which was FeCl2s_ 4H2O (0.5 mM) to the assay mixture [HEPES
then incubated at 37 °C for 24 h. To this, 200 lL of DMSO (100 lL), 1 M NaCl (200 lL), N2-sparged Millipore water
290 C.-R. Zhang et al.

(1.64 mL), DMSO or test sample (20 lL)] and 20 lL of enzymes (20 lL) were then added and incubated for 2 min.
liposome suspension. The fluorescence was monitored at 0, 1, The substrate arachidonic acid (10 lL of solution at 1 mg/mL
3 and every 3 min thereafter up to 21 min on a Turner model 1 mM Tris-phenol buffer, pH = 7) was added to initiate the
450 Fluorometer. The decrease in fluorescence intensity over enzyme reaction or formation of prostaglandin endoperoxide.
time (21 min) indicated the rate of peroxidation. Each sample The data were recorded using QuickLog for windows data
was assayed in duplicate, and the percent inhibition was acquisition and control software. Each sample was tested in
calculated with respect to DMSO control. duplicate, and the percent inhibition was calculated with
respect to DMSO control. The varying concentration of
2.6. Cyclooxygenase enzymes (COX-1 and -2) inhibitory assays positive controls used in the assay was to obtain comparable
enzyme inhibitions between 50% and 100%.
The COX-1 and -2 enzyme inhibitory activities were measured
for extracts (100 lg/mL) and the positive controls (commercial 2.7. Human tumor cell proliferation inhibitory assay
Aspirin, Celebrex, Naproxen, and Ibuprofen at 108, 1, 15 and
12 lg/mL, respectively) following the published procedure The human tumor cell proliferation inhibitory activities
(Bowen-Forbes et al., 2009; Liu and Nair, 2012; Zhang were evaluated for the extracts at 100 lg/mL and positive
et al., 2013). The test was carried out by monitoring the initial control adriamycin at 1.5 lg/mL as per published method
rate of O2 uptake using an Instech micro oxygen chamber and (Bowen-Forbes et al., 2009; Liu and Nair, 2012). AGS
electrode attached to an YSI model 5300 Biological Oxygen (gastric), DU-145 and LNCaP (prostate), HCT-116 (colon),
Monitor at 37 °C. The test samples (6 lL) were initially added MCF-7 (breast), and NCI-H460 (lung) human tumor cells
to the chamber full of assay buffer (1 mM Tris-phenol buffer, were cultured in RPMI-1640 medium containing penicillin–
600 lL, pH = 7, and hemoglobin (17 lg)). COX-1 or -2 streptomycin and 10% fetal bovine serum (FBS). Aliquots of

Figure 1 Absorbance values at 570 nm of (A) water and (B) methanolic extracts of 29 varieties of date fruit extracts at 250 lg/mL
obtained after reaction with MTT at 37 °C. Vitamin C and TBHQ were used as positive controls at 25 lg/mL. Vertical bars represent the
standard deviation of each data point (n = 2).
Health-benefits of date fruits 291

100 lL of test samples were added to each well of 96-well cell Khalas, Deglet Noor, Dekhaini, Ruthana Al Sharag, Sullaj,
culture plate containing the tumor cells (2000–4000 cells). Safawi and Mutwah gave the highest yield of total extracts,
After incubation for 48 h at 37 °C, an aliquot (25 lL) of about 84%, while Khashram, Rushodia and Nabtat Ali gave
MTT in Phosphate Buffer Saline (PBS) solution (5 mg/mL) the lowest yield, about 72%. Khalas, Deglet Noor, Dekhaini,
was added and plates were incubated for another 3 h at Ruthana Al Sharag, Sullaj and Safawi showed the highest yield
37 °C. The wells were then aspirated followed by the addition of water extract, about 80%, while Mutwah showed the high-
of DMSO (200 lL) to dissolve the formazan blue crystals pro- est yield of methanolic extract, about 9.43%. The TLC profiles
duced by viable cells. The plates were shaken and the absor- of water extracts showed only sugars and no indication of the
bance was measured on a Bio-Tek Elx800 universal presence of secondary metabolites in all date fruits studied.
microplate reader at 570 nm. Each sample was assayed in Fructose was predominant along with glucose in all varieties
triplicate. of dates except Nabtat Ali, Sukkari Al Qassim and Deglet
Noor showed additional sucrose. In Sukkari Al Qassim and
3. Results and discussion Deglet Noor sucrose was the predominant sugar. Between
fructose and glucose, fructose was higher in these varieties con-
The date fruits were extracted sequentially with water and taining sucrose. The major components in the methanolic
methanol to afford the respective crude extracts. The yield of extracts of all date fruits by TLC were still the same sugars
total extracts varied among the varieties of date fruits studied detected in water extracts. In order to profile the minor com-
(Table 1) and was between 70.97% and 84.90%. Among them, ponents or secondary metabolites in all varieties of date fruits

Figure 2 Inhibition of LPO by (A) water and (B) methanolic extracts of date fruits at 100 lg/mL. Commercial antioxidants BHA, BHT
and TBHQ were tested at 1.802, 2.204 and 1.662 lg/mL. The oxidation of lipid was initiated by the addition of Fe2+ ions. The varying
concentrations of positive controls were to yield a comparable activity profiles between 0% and 100% by test extracts and positive
controls alike. Vertical bars represent the standard deviation of each data point (n = 2).
292 C.-R. Zhang et al.

studied, an aliquot of 400 mg of methanolic extract of each are capable of reducing or removing oxidative agents while the
variety was separately stirred with CHCl3–MeOH (4:1, v/v) LPO assay detects components in the extract that are free rad-
to yield a sugar free fraction, respectively. Interestingly, the ical scavengers. In MTT assay, water extracts from all date
sugar free fractions of all varieties showed identical TLC pro- fruits at 250 lg/mL showed weak activity with absorbance val-
files with variations in concentration of some of its compo- ues between 0.10 and 0.16 at 570 nm. However, all methanolic
nents. The secondary metabolites detected by TLC profiles extracts at 250 lg/mL exhibited better activity with absorbance
for all varieties of date fruits were similar to phenolics, triter- values between 0.14 and 0.41 (Fig. 1). Among these, methano-
penoids, triglycerides, fatty acids and steroids reported for lic extracts of Khashram, Ruthana and Luban showed the
Ajwa date fruit (Zhang et al., 2013). Therefore, characteriza- highest antioxidant activity on par with the absorbance dis-
tion of bioactive compounds was not further carried out for played by the positive controls. In the LPO assay, water and
the date fruit extracts evaluated in this study for antioxidant, methanolic extracts of all varieties at 100 lg/mL showed inhi-
antiinflammatory and tumor cell proliferation inhibitory bition by 50–67% and 58–82%, respectively (Fig. 2). Again,
activities. similar to MTT assay results, the methanolic extracts showed
The water and methanolic extracts of all varieties of date better activity than water extracts. For example, among the
fruits were evaluated for antioxidant activity using MTT and water extracts, Shaishee, Safawi, Sefri, Ajwa, Mabroom and
LPO assays (Bowen-Forbes et al., 2009; Liu and Nair, 2010, Hilali showed the highest LPO inhibition by about 65% and
2012; Zhang et al., 2013). MTT assay detects compounds that the methanolic extracts of Khashram, Rabeaa, Sefri, Anbara,

Figure 3 COX-1 and -2 enzyme inhibitory activities of (A) water and (B) methanolic extracts of date fruits at 100 lg/mL and commercial
NSAIDs aspirin, CelebrexÒ, naproxen and ibuprofen used as positive control at 108, 1, 15, and 12 lg/mL, respectively. The varying
concentrations of positive controls were to yield a comparable activity profiles between 0% and 100% by test extracts and positive
controls alike. Vertical bars represent the standard deviation of each data point (n = 2).
Health-benefits of date fruits 293

Mabroom, Mutwah and Meneifi by around 75%. Methanolic Conflict of interest

extract of Mutwah showed the highest LPO inhibitory activity,
about 82%, and was similar in activity with respect to the pos- Authors certify that they have no financial or other conflicts of
itive controls used in the assay. The enhanced activity of interest on this research.
methanolic extracts in these assays over water extracts was
not surprising since sugars do not function as antioxidants.
Acknowledgments
The anti-inflammatory activity of all date fruits studied was
determined by percent inhibition of COX-1 and -2 enzymes by
This research is a contribution from Michigan State University
their water and methanolic extracts (Bowen-Forbes et al.,
AgBioResearch and the Vice-Deanship of Scientific Research
2009; Liu and Nair, 2012; Zhang et al., 2013). Cyclooxygenase
Chairs, King Saud University, Riyadh, Saudi Arabia.
enzymes, especially COX-2 produce inflammatory intermedi-
ates and partakes in gene regulations that cause many diseases.
Therefore, potential inhibition of COX-2 enzyme by date fruits References
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