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Food Research International 65 (2014) 193–198

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Changes in chlorophylls, chlorophyll degradation products and lutein in

pistachio kernels (Pistacia vera L.) during roasting
Gloria Pumilia a,1, Morgan J. Cichon b,1, Jessica L. Cooperstone b,1, Daniele Giuffrida a,
Giacomo Dugo a, Steven J. Schwartz b,⁎
Department of Environmental Science, Safety, Territory, of Food and Health (S.A.S.T.A.S.) University of Messina, Viale Ferdinando Stagno d'Alcontres, 31, 98166 S. Agata. Messina, Italy
Department of Food Science & Technology, The Ohio State University, 2015 Fyffe Ct., 110 Parker Food Science & Technology Building, Columbus, OH 43210, USA

a r t i c l e i n f o a b s t r a c t

Article history: Bright green pistachio kernels are desirable in the food industry and degradation of color is often associated with
Received 31 January 2014 a loss in quality. Chlorophylls (a and b) and lutein are the major pigments in raw pistachios. The heat treatment of
Received in revised form 6 May 2014 chlorophyll-containing foods results in color alteration, due to the conversion of chlorophylls (bright green color)
Accepted 29 May 2014
to pheophytins and pyropheophytins (yellow-brown olive color). In this study, changes in the concentration of
Available online 7 June 2014
chlorophylls, chlorophyll degradation products and lutein in pistachios were monitored during oven roasting.
An efficient, high performance liquid chromatography method with photodiode-array detection (HPLC-PDA)
Pistachio was developed to separate and quantitate these pigments in pistachios. Extractable chlorophylls a and b were
Pistacia vera L. higher in pistachio kernels roasted for 5 and 10 min than in the raw kernels. The most drastic losses were ob-
Chlorophylls served with pheophytins a and b, which both decreased by approximately 85% after 60 min of roasting.
Pheophytins Pyropheophytins a and b increased significantly during roasting and were 10–12 fold higher in the pistachios
Pyropheophytins roasted for 60 min than in the raw pistachios. Extractable lutein concentration increased by 37% after 5 min,
Pyrochlorophylls but did not change significantly with longer roasting times. Initial increases in chlorophylls a and b and lutein
were likely due to enhanced extractability with roasting. Color measurements of the pistachios corresponded
chlorophyll degradation products
with changes in concentration of chlorophyll pigments observed at the later roasting times. Interestingly,
pyrochlorophylls a and b were detected in pistachios as confirmed by mass spectrometry. There are no prior re-
ports of these compounds being detected in pistachios. We hypothesize that the conditions of pistachio roasting
favor the formation of pyrochlorophylls. Color changes observed after oven roasting significantly affect quality
and value perceptions of pistachios.
© 2014 Elsevier Ltd. All rights reserved.

1. Introduction 1997). Additionally, roasting is an effective method to increase the safety

of pistachios as it can potentially reduce aflatoxin content (Yazdanpanah,
Pistachios (Pistachia vera L.) are a commonly consumed tree nut cul- Mohammadi, Abouhossain, & Cheraghali, 2005).
tivated in dry and hot areas, under saline conditions (Metheney, Reyes, The popularity of pistachios is growing due in part to their proposed
& Ferguson, 1997). Iran, the United States, Turkey, Syria, Italy and health benefits. Unsaturated fats, carotenoids, vitamins and antioxi-
Greece are the main producers of pistachios, and global production is dants in pistachios increase the value of this nut to consumers (Kay,
steadily increasing (FAO, 2013). Pistachio nuts are sold shelled or un- Gebauer, West, & Kris-Etherton, 2010; Robbins, Shin, Shewfelt,
shelled, raw or roasted, with or without salt, and the kernel can be Eitenmiller, & Pegg, 2011). Pistachios have been shown to have a pos-
used in confections and pistachio nut paste to contribute flavor and itive impact on plasma lipid profiles (Kocyigit, Koylu, & Keles, 2006) and
color (Gamlı & Hayoğlu, 2007). The majority of pistachios sold directly may decrease the risk for cardiovascular disease (Gebauer et al., 2008).
to consumers are roasted; this process is responsible for the characteris- With consumer interest in pistachios increasing, continued research on
tic aroma and taste of pistachios (Nicoli, Anese, Manzocco, & Lerici, factors affecting quality is needed.
Color is an important parameter for the evaluation of pistachios with
chlorophylls (a and b) and lutein being the major pigments in raw
pistachios. Chlorophylls are heat labile and can degrade to form
⁎ Corresponding author at: 2015 Fyffe Ct., 235 Parker Food Science and Technology
Building, Columbus, OH 43210, USA. Tel.: +1 614 292 2934.
pheophytins and pyropheophytins. Degradation products of chloro-
E-mail address: (S.J. Schwartz). phylls have been reported in thermally processed green fruits and veg-
These authors contributed equally to this manuscript. etables (Heaton & Marangoni, 1996; Schwartz & Elbe, 1983). The bright
0963-9969/© 2014 Elsevier Ltd. All rights reserved.
194 G. Pumilia et al. / Food Research International 65 (2014) 193–198

green color of fresh vegetables is often dulled after thermal processing were monitored using HPLC and confirmed using mass spectrometry.
as a result of degradation of chlorophylls a and b to their respective Colorimetric data was collected to investigate the effects of roasting
pheophytins and pyropheophytins. Pheophytins are formed from the on quantitative color parameters that also influence pistachio quality.
displacement of the central magnesium atom from the chlorophyll
porphyrin ring with hydrogen. Previous work has reported pheophytins 2. Materials and methods
in pistachios after 11 months of storage at 25 °C (Bellomo, Fallico, &
Muratore, 2009) indicating that pheophytins can also be formed 2.1. Chemicals
under conditions other than thermal processing. Pyropheophytins,
which are formed from pheophytins after loss of the carbomethoxy All solvents were purchased from Fisher Scientific (Pittsburgh,
group at the C10 position, can be produced as a result of more extreme PA, USA). N-N-dimethyl-formamide (DMF), hexane, methyl tert-
forms of heat treatment (Fig. 1) (Canjura, Schwartz, & Nunes, 1991; butyl ether, methanol and water were HPLC grade and diethyl ether
Schwartz & Elbe, 1983). Chlorophylls a′ and b′ are the C10 epimers of was ACS grade. Sodium sulfate was purchased from Fisher Scientific
chlorophylls a and b, respectively, with an inversion of stereochemistry (Pittsburgh, PA, USA) and ammonium acetate was purchased from J.T.
between the carbomethoxy and hydrogen substituents (Schwartz, von Baker (Phillipsburg, NJ, USA). For mass spectrometry, Optima grade
Elbe, & Giusti, 2008). methanol and water were used.
The predominant carotenoid found in pistachios is lutein, a xan- Chlorophylls a and b, and lutein standards were purchased from
thophyll with a characteristic yellow color (Giuffrida, Saitta, Torre, Sigma Aldrich (St. Louis, MO, USA). Pheophytin a and b standards
Bombaci, & Dugo, 2006). Previous work shows that lutein appears were prepared by treating chlorophyll a and b standards, respectively,
to be quite heat-resistant, in contrast to chlorophylls, which are suscepti- in diethyl ether with 1 M HCl under nitrogen gas for five minutes
ble to degradation after thermal processing (Khachik et al., 1992). In one (Hynninen & Ellfolk, 1973). Standard curves were generated for
study, lutein was shown to be resistant to degradation after thermal pro- quantitation of chlorophylls a and b, pheophytins a and b, and lutein.
cessing in four different green and red vegetables (Khachik et al., 1992). Chlorophylls a′ and b′ and pheophytins a′ and b′ were quantified
Additionally, it has been shown that lutein dissolved in oil is more resis- using the standard curves for chlorophylls a and b and pheophytins
tant to thermal processing compared to some hydrocarbon carotenoids a and b, respectively; and pyropheophytins a and b were also quantified
(Henry, Catignani, & Schwartz, 1998). Previous literature has also demon- using relative slopes based on a ratio of molar extinction coefficient to
strated a perceived increase of lutein after thermal processing, which can pheophytins a and b respectively. Pyrochlorophylls were detected, but
be attributed to a loss of soluble solids into the canning medium (Weckel, not quantified.
Santos, Hernan, Laferriere, & Gabelman, 1962), inactivation of enzymes
able to oxidize the carotenoids and denaturation of carotenoid–protein 2.2. Pistachio roasting
complexes facilitating extractability (Kirk & Tilnet-Basset, 1978).
This study characterizes the effect of roasting on pistachio pigments: Raw, unshelled commercial pistachio nuts from California were pur-
changes in chlorophylls, chlorophyll degradation products and lutein chased from (Cranford, NJ, USA). Pistachios were heated in a

Fig. 1. Chlorophyll and its derivatives.

G. Pumilia et al. / Food Research International 65 (2014) 193–198 195

convection oven at 138 °C. Samples were removed from the oven after pyropheophytins. The same HPLC method was used for chromatograph-
5, 10, 30, and 60 min and frozen immediately at −80 °C. Chlorophylls, ic separation, with the following MS parameters: 7 μA corona current,
chlorophyll degradation products and carotenoids were extracted 8 eV collision energy, 3 V cone voltage, 110 °C source temperature,
from samples at each time point in triplicate and were analyzed via and 450 °C probe temperature.
HPLC-PDA. Chromatograms were integrated for quantitation at the following
wavelengths: 661 nm (chlorophyll a/a′), 642 nm (chlorophyll b/b′),
2.2.1. Pigment extraction 667 nm (pheophytin a/a′ and pyropheophytin a), 655 nm (pheophytin
The samples were extracted by liquid-phase distribution between b/b′ and pyropheophytin b) and 444 nm (lutein). For those pigments
DMF and hexane, according to a method previously described with without authentic external standards, identities were confirmed by
minor modifications (Giuffrida et al., 2006; Minguez-Mosquera, spectral characteristics and accurate mass.
Gandul-Rojas, & Gallardo-Guerrero, 1992). Briefly, approximately
50 g of pistachios were ground in order to sample 6 g for extraction 2.4. Color analysis
with 5 mL of acetone, repeated 5 times, for a total of 25 mL of extract.
Mild sonication was used during extraction with acetone to increase Color readings were taken on the raw and roasted, ground pistachios
contact between the sample and the solvent (Downes, Hrstich, & using a Hunter ColorQuest XE (Hunter Labs, Reston, VA). All samples
Vincent, 1993). The acetone extracts were pooled and dried under were read in duplicate with a D65 illuminant and a 10° observer
nitrogen. The extract was then dissolved in 6 mL of DMF, and treated angle. Color measurements were expressed using the CIELAB color
with 12 mL portions of hexane and centrifuged at 2000 ×g. The top system.
layer was then removed and extraction with hexane was repeated
two additional times. Chlorophylls, chlorophyll degradation products 2.5. Data analysis
and xanthophylls were retained in the DMF phase while the hexane
phase contained lipids and carotenes. The hexane phase was saponified Data were analyzed for differences between means using one-way
and subsequently analyzed by HPLC-PDA for carotenes. Beta-carotene analysis of variance (ANOVA) and Tukey's post-hoc test, with statistical
was detected at low levels, as previously reported (Giuffrida et al., significance when P b 0.05, using SPSS version 19 (IBM, Armonk, NY).
2006), but was not quantified.
The DMF extract was treated with 6 mL of a 2% aqueous Na2SO4 3. Results and discussion
(w/v) solution in bath of ice, followed by 3 successive 4 mL portions
of 1:1 hexane:diethyl ether. The hexane:diethyl ether phases were Chlorophylls (and their epimers), pheophytins (and their epimers),
centrifuged each time. The aqueous phase was discarded eliminating pyropheophytins and lutein were measured in raw and roasted pista-
polyphenols and other water-soluble compounds. The organic phase chios. Although the epimers have the same spectra as their parent,
was reconstituted in a known volume, aliquoted, and evaporated to they can be differentiated by their elution order. On a C30 column,
dryness under nitrogen. The dried residue was dissolved in an appropri- chlorophylls a′ and b′ eluted immediately after their corresponding a
ate volume of 1:1 methanol:MTBE, filtered through a 0.22 μm nylon and b peaks; whereas pheophytins a′ and b′ eluted immediately before
filter, and analyzed by HPLC. their corresponding a and b peaks (Fig. 2). The epimers are always pres-
ent in lower concentration compared to the parent chlorophyll. Fig. 2
2.3. Pigment analysis by HPLC and mass spectrometry shows HPLC chromatograms of raw pistachios, and pistachios roasted
for 5, 10, 30 and 60 min. Table 2 shows the concentrations of the
Chlorophylls, chlorophyll degradation products and xanthophylls pigments in the pistachios at the different roasting times. Extractable
extracted from the pistachio samples were analyzed using a model chlorophylls a and b were higher in the pistachio kernels roasted for 5
2695 HPLC with a model 996 PDA (Waters Corp., Milford, MA). For and 10 min than in the raw kernels. The increase in concentration ob-
HPLC separation, an YMC C30 analytical column (250 mm × 4.6 mm served after mild roasting could be a result of the breakdown of chloro-
i.d., 3 μm) (Waters Corp.) was used at 30 °C. The mobile phase consisted phyll–protein complexes, which could improve the extractability of the
of the following: A: 90% MeOH, 3% MTBE, 5% H2O, 2% of a 2% (w/v) so- pigments from the nuts (Paulsen & Schmid, 2002; Yamane, Kashino,
lution of aqueous ammonium acetate and B: 88% MTBE, 10% MeOH, Koike, & Satoh, 1997). Concentrations of extractable pheophytins a
2% of a 2% (w/v) solution of aqueous ammonium acetate. A gradient and b were also higher in pistachio kernels roasted for 5 min compared
was employed flowing at 1.3 mL/min to separate the pigments of inter- to raw pistachios, but after 60 min of roasting concentrations decreased
est as shown in Table 1. The same model HPLC-PDA was also interfaced by approximately 85%. The presence of pheophytins a and b in raw pis-
with a QToF Premier quadrupole time-of-flight mass spectrometer tachios is likely due to the natural chlorophyll degradation observed at
(Waters Corp.) using atmospheric pressure chemical ionization (APcI) room temperature after long term storage (Bellomo et al., 2009).
in positive ion mode to confirm the identities of pyrochlorophylls and Pyropheophytin peaks showed a considerable increase in the chro-
matogram of pistachios roasted for 30 min with the highest value in pis-
Table 1 tachios roasted for 60 min (reaching levels 10–12 times higher than in
Gradient schematic for separation of pigments in pistachios by HPLC-PDA. the raw pistachios). Pyropheophytins are formed from pheophytins
during thermal processing as a result of the loss of the carbomethoxy
Time (min) Solvent A Solvent B
group at C10 (Schwartz & Elbe, 1983; Schwartz, Woo, & Von Elbe,
0 95 5 1981). Extractable lutein concentration increased by 37% after 5 min,
5 60 40
10 50 50
but did not change significantly after that; this observation is also likely
12 48 52 a result of increased carotenoid extractability from the nuts. Durmaz
14 45 55 and Gökmen report a significant decrease in lutein in oil derived from
16 40 60 pistachios roasted for 20 min, but at a higher roasting temperature
18 40 60
(180 °C) (Durmaz & Gökmen, 2011). However, other research shows
20 20 80
22 20 80 lutein in food products to be relatively resistant to heat treatments
24 5 95 (Khachik et al., 1992), as observed in this study.
27 5 95 Interestingly, two compounds were identified for the first time in
27.01 95 5 pistachio kernels: pyrochlorophylls a and b. These compounds were
30 95 5
confirmed by their spectral characteristics, retention time and mass
196 G. Pumilia et al. / Food Research International 65 (2014) 193–198

Fig. 2. The HPLC chromatograms (combined 665 and 650 nm) of the pistachio extracts from raw and 5, 10, 30 and 60 min of roasting. Peak identification: 1, chlorophyll b; 2, chlorophyll b′;
3, chlorophyll a; 4, chlorophyll a′; 5, pheophytin b′; 6, pheophytin b; 7, pheophytin a′; 8, pheophytin a; 9, pyrochlorophyll b; 10, pyrochlorophyll a; 11, pyropheophytin b; 12,
pyropheophytin a.

spectrometry (Figs. 3 and 4). Concentrations of pyrochlorophylls a and b the loss of a carbomethoxy group (Fig. 1). As pyrochlorophylls have
were highest in pistachios roasted for 60 min. Pyrochlorophylls are less the same absorption spectra to their parent chlorophylls, accurate
common chlorophyll degradation products than pheophytins and mass was used to differentiate between these compounds. We hypoth-
pyropheophytins. They can be formed directly from chlorophylls from esize that the high roasting temperatures and low moisture content of

Table 2
Changes in pistachio pigments from raw during roasting at 138 °C for 5, 10, 30 or 60 min. Different letters in the same row denote statistically significant differences (P b 0.05).

Pigment Quantity of Pigment (mg/kg wet weight)

Raw 5 min 10 min 30 min 60 min

Chlorophyll a 3.63 ± 0.57a 7.64 ± 1.25b 7.75 ± 1.39b 4.10 ± 0.46a 2.00 ± 0.47a
Chlorophyll a′ 0.80 ± 0.20a 1.92 ± 0.21bc 2.49 ± 0.29c 1.65 ± 0.27b 0.89 ± 0.12
Chlorophyll b 1.81 ± 0.38a 3.29 ± 0.27b 3.28 ± 0.61b 1.47 ± 0.10a 0.46 ± 0.09c
Chlorophyll b′ 0.68 ± 0.09a 1.40 ± 0.03b 1.37 ± 0.09b 0.64 ± 0.03a 0.22 ± 0.05a
Pheophytin a 6.29 ± 1.56a 7.16 ± 0.88a 5.93 ± 0.84ab 3.58 ± 0.78b 0.90 ± 0.29c
Pheophytin a′ 1.12 ± 0.21a 1.28 ± 0.11a 1.13 ± 0.11a 0.71 ± 0.14b 0.21 ± 0.07c
Pheophytin b 0.81 ± 0.07a 1.00 ± 0.06b 0.93 ± 0.07ab 0.39 ± 0.0303c 0.11 ± 0.10d
Pheophytin b′ 0.15 ± 0.02a 0.23 ± 0.03b 0.20 ± 0.05ab 0.05 ± 0.01c 0.01 ± 0.03c
Phyropheophytin a 0.54 ± 0.03a 0.70 ± 0.03a 1.05 ± 0.09a 4.59 ± 0.81b 6.70 ± 0.22b
Phyropheophytin b 0.13 ± 0.13a 0.22 ± 0.04a 0.34 ± 0.08a 0.93 ± 0.03b 1.37 ± 0.21b
Lutein 8.12 ± 0.71a 10.83 ± 0.77b 10.83 ± 1.54b 10.62 ± 0.60b 11.14 ± 0.25b
G. Pumilia et al. / Food Research International 65 (2014) 193–198 197

Fig. 3. Extracted ion chromatograms for pyrochlorophyll a (tentative) and pyropheophytin a Fig. 4. Extracted ion chromatograms for pyrochlorophyll b (tentative) and pyropheophytin b
in the pistachios roasted for 60 min. Mass chromatograms (top two) are aligned with the in the pistachios roasted for 60 min. Mass chromatograms (top two) are aligned with the
HPLC chromatogram (bottom) at 665 nm. HPLC chromatogram (bottom) at 650 nm.

the pistachio may be responsible for the conversion of chlorophylls to pistachios significantly decreased during roasting, which indicates less
pyrochlorophylls. The formation of pyrochlorophylls has been previous- yellow color. These observed color changes are considered to be less de-
ly observed in spinach leaves during microwave heat treatment (Teng & sirable. Similar trends in L*-, a*- and b*-values were reported for oils
Chen, 1999), which supports our hypothesis. However, additional work from pistachios roasted at 180 °C for 5, 10, 20, 30 and 40 min
is needed to test the specific effect of low moisture, and high tempera- (Durmaz & Gökmen, 2011).
ture conditions on the formation of these compounds. Color is one of the most important quality attributes evaluated by
The pigment extraction used in this paper was faster than the most consumers, producers and distributors. Chlorophylls a and b are the pre-
common method used to extract chlorophylls and xanthophylls dominant pigments responsible for the green color of pistachios. Pig-
(Minguez-Mosquera et al., 1992) due to smaller sample sizes versus ment concentrations are influenced by a number of factors, including
the method presented in the literature. Previous pigment extractions geographic origin, degree of ripeness, storage conditions and processing
from pistachios have used sample sizes of 37 g where this study used methods. The concentrations and ratios of these pigments can be quan-
a smaller sample size (6 g) for a faster sample preparation requiring tified and used to determine the geographic origin of a sample (Bellomo
less solvent (Giuffrida et al., 2006). Extraction efficiencies of the two & Fallico, 2007). For quality and import purposes, region of origin may
methods were evaluated and found to be comparable. Additionally, a affect the value of pistachios, thus authentication of geographic origin
more efficient HPLC method was developed for the separation and anal- is valuable in preventing adulteration or mislabeling of pistachios.
ysis of these pigments in pistachios. This improved method has a shorter
run time while retaining good peak separation (Giuffrida et al., 2006). Table 3
Ammonium acetate was added to the mobile phase for better peak Color analysis of raw and roasted pistachios in duplicate. Different letters in the same
resolution, shape and on column recovery among the analytes (Hart & column denote statistically significant differences, as determined by ANOVA (P b 0.05)
and Tukey's post-hoc test for multiple comparisons.
Scott, 1995).
Colorimetric measurements of the pistachio samples after different Roasting time L* a* b* C* h* dE*
roasting times correspond with changes in concentration of chlorophyll Raw 60.7 a
1.3 a
26.9 ab
26.9 ab
87.3 a
pigments determined by HPLC-PDA (Table 3). The L*-value of the pista- 5 min 60.8a 0.5b 27.1a 27.1b 88.9b 66.8a
chios decreased with roasting time, indicating a darkening of the nuts. 10 min 58.4b 2.5c 26.1a 26.2a 84.6c 64.0b
Additionally, the a*-value significantly increased during roasting, 30 min 53.8c 5.6d 21.0c 21.1c 75.0d 58.0c
60 min 50.2d 5.1d 17.2d 18.3d 70.9e 53.4d
which indicates less green in the sample, while the b*-value of the
198 G. Pumilia et al. / Food Research International 65 (2014) 193–198

Additionally, roasting pistachios can affect other nut parameters by Gamlı, Ö. F., & Hayoğlu, İ. (2007). The effect of the different packaging and storage
conditions on the quality of pistachio nut paste. Journal of Food Engineering, 78(2),
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It has been shown that nut roasting decreases reducing sugars, as of pistachios on cardiovascular disease risk factors and potential mechanisms of
action: A dose-response study. American Journal of Clinical Nutrition, 88(3), 651–659.
these sugars likely take part in Maillard browning reactions (Kashani Giuffrida, D., Saitta, M., Torre, L., Bombaci, L., & Dugo, G. (2006). Carotenoid, chlorophyll
& Valadon, 1984) and can lead to the formation of important aroma and chlorophyll-derived compounds in pistachio kernels (Pistachia vera L.) from
compounds (Aceña, Vera, Guasch, Busto, & Mestres, 2010). Pistachio Sicily. Italian Journal of Food Science, 18, 309–317.
Hart, D. J., & Scott, K. J. (1995). Development and evaluation of an HPLC method for the
nut oils produced from roasted nuts were found to have lower peroxide analysis of carotenoids in foods, and the measurement of the carotenoid content of
and TBARS values after 30 days of storage compared to unroasted nut vegetables and fruits commonly consumed in the UK. Food Chemistry, 54, 101–111.
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