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Journal of the Science of Food and Agriculture
J Sci Food Agric 80:684±690 (2000)
Interaction between Maillard reaction products
and lipid oxidation in starch-based model
systems
Dino Mastrocola,1* Murina Munari,1 Maria Cioroi2 and Carlo R Lerici1
1
Dipartimento di Scienze degli Alimenti, Università di Udine, Via Marangoni 97, I-33100 Udine, Italy
Department of Chemistry, The University ‘Dunarea de Jos’ of Galati, Domneasca Str 47, 6200 Galati, Romania
2
Abstract: The effect of Maillard reaction products (MRPs) on the kinetics of lipid oxidation in
intermediate-moisture model systems containing pregelatinised starch, glucose, lysine and soybean
oil has been studied. The samples, either containing all components or excluding one or more of them,
were heated at 100 °C for different times. Lipid oxidation and browning indices were measured and the
results con®rmed the ability of MRPs to retard peroxide formation. Under the conditions adopted, the
rate of the Maillard reaction was increased by the presence of the oil and its oxidation products. The
antioxidant action of MRPs was also evaluated using a peroxide-scavenging test based on crocin
bleaching. The results demonstrated that antioxidant activity developed with increased browning of
the samples.
# 2000 Society of Chemical Industry
Keywords: antioxidant activity; lipid oxidation; Maillard reaction; browning, starch
INTRODUCTION
In many heated foods, amines react with carbonyl
compounds, mainly reducing sugars, leading to the
formation of a complex series of compounds called
Maillard reaction products (MRPs).1±4 On the other
hand, in fat-containing foods, lipid oxidation may take
place, but most frequently both reactions can take
place in the same food and one can in¯uence the
other.4±6
The antioxidative activity of MRPs was ®rst
observed by Franzke and Iwainsky;7 later, the formation of antioxidant MRPs from model systems was
extensively studied.1±4,8±14 Several mechanisms are
involved in the antioxidant activity of MRPs. According to Hodge's scheme,15 Grif®th and Johnson1 found
that development of the Maillard reaction led to the
formation of enediol structure reductones, which were
found to break the radical chain by donation of a
hydrogen.2 However, the compounds accounting for
this effect have not been completely identi®ed and the
mechanism of the antioxidant effect is still under
debate.13 In addition to reducing sugars, other
carbonyl compounds, including lipid peroxidation
products, are also able to react with amino groups,
producing brown macromolecular pigments with
properties similar to those of melanoidins.4,16,17 Data
are also available, but to a lesser extent, on the
interaction between the Maillard reaction and lipid
oxidation when they take place simultaneously in a
food system during heating.
In the present study the in¯uence of oil on the
kinetics of the Maillard reaction and the effect of
MRPs on the kinetics of lipid oxidation in model
systems containing pregelatinised starch, glucose,
lysine and soybean oil have been studied. The samples,
simulating a bakery product and containing all the
components or with exclusion of one or more of them,
were heated at 100 °C for different periods. The
antioxidant action of MRPs was also evaluated using
a peroxide-scavenging test based on crocin bleaching.
MATERIALS AND METHODS
Model system preparation
For model system preparation the following ingredients were used: glucose (RPE-ACS, Carlo Erba,
Milan, Italy), L-(‡)-lysine-HCL (RPE-ACS, Carlo
Erba, Milan, Italy), pregelatinised starch, distilled
water and commercial soybean oil. The fatty acid
pro®le of the soybean oil is reported in Table 1.
The formulation of model systems was chosen in
order to simulate, in simpli®ed way, a bakery product.
Starch was used as ¯our substitute and pregelatinisation was adopted in order avoid changes in waterholding capacity of the formulations during heating.
For pregelatinised starch preparation, 200 g of corn
* Correspondence to: Dino Mastrocola, Dipartimento di Scienze degli Alimenti, Università di Udine, Via Marangoni 97, I-33100 Udine, Italy
E-mail: dino.mastrocola@dsa.uniud.it
(Received 2 August 1999; revised version received 8 November 1999; accepted 13 December 1999)
# 2000 Society of Chemical Industry. J Sci Food Agric 0022±5142/2000/$17.50
684
Interaction between Maillard reaction and lipid oxidation
Table 1. Fatty acid composition of soybean oil used
in model system preparation
Content (%)
Fatty acid
C16:0
C16:1
C17:0
C18:0
C18:1
C18:2
C18:3
C20:0
C22:0
Average SD
Max
Min
10.63 0.02
0.05 0.01
0.12 0.01
4.23 0.02
24.56 0.04
53.21 0.06
6.43 0.05
0.14 0.01
0.31 0.02
10.65
0.07
0.14
4.26
24.58
53.25
6.47
0.16
0.33
10.60
0.04
0.11
4.21
24.53
53.15
6.39
0.13
0.29
starch (Carlo Erba, Milan, Italy) was dispersed in 4 l of
distilled water, boiled for 10 min and then cooled in an
ice-water bath. The starch suspension was frozen at
ÿ30 °C (Alaska, model EF 600, Bologna, Italy) and
freeze-dried in a pilot plant drier (Edwards Alto
Vuoto, Minifast 1700, Milan, Italy) at a shelf
temperature of 35 °C.
The ingredients were mixed (Ronic Ritmix, Imetec,
Milan, Italy) in order to obtain the mixtures reported
in Table 2.
Aliquots (9 g) of the different model systems were
placed into 20 ml glass vials and hermetically sealed
with butyl septa and metallic caps. Samples (three vials
per time point) were heated at 100 °C in a forced air
circulation oven (Thermocenter, Salvis, Milan, Italy).
During heat treatment, samples were removed from
the oven at different times (30, 60, 90, 120, 180 and
240 min), cooled in an ice-water bath and then
immediately tested.
Analytical methods
Fatty acid profile
Neutralisation of the free fatty acids and alkaline
methanolysis of the glycerides followed by esteri®cation of the fatty acids was the procedure used.18
The organic phase was analysed by a Varian 3300
gas chromatograph (Varian, Sunnyvale, USA)
equipped with an FID detector and a Fisons model
DP 700 integrator (Fisons, Milan, Italy). Helium was
used as carrier gas. An SP2340 capillary column
(30 m 0.32 mm id; Supelchem, Milan, Italy) was
used.
Component
Table 2. Composition (g kgÿ1) and water activity of
different model systems
J Sci Food Agric 80:684±690 (2000)
Lipid oxidation
The peroxide value in the oil fraction extracted from
model systems using 20 ml of ethyl ether was
determined and expressed as meq of active oxygen
per kg of oil according to AOAC.19
Glucose
The HPLC method described by Nicoli et al 20 was
used to determine residual glucose. A high-performance liquid chromatograph (Jasco 880PU, Tokyo,
Japan) equipped with a manual 10 ml loop injector, a
refractive index detector (RI-3, Varian, Sunnyvale,
USA) and a recorder (Varian 4290, USA) was used.
The analysis was carried out using a 250 mm 4 mm
Lichrosorb NH2 Hibar RT 250-4 prepacked column
(Merck, Dorset, UK) with acetonitrile/water (80:20)
as mobile phase at a ¯ow rate of 1.5 ml minÿ1.
For HPLC analysis, 5 g of each sample was
suspended in 30 ml of distilled water and homogenised
using a Politron (PT 3000, Kinematica AG, Littau,
Switzerland) for 1 min. Samples were centrifuged for
5 min at 4330 g at 0 °C (refrigerated centrifuge ALC,
RCF Meter, 4233R) and the aqueous phase was
®ltered on paper (Whatman no 4).
Lactose (2 10ÿ2 M) was used as internal standard.
Glucose concentration was calculated using the
response factors determined from standard solutions.
Headspace gas chromatographic (GC) analysis of carbon
dioxide
The carbon dioxide in the headspace of different
model systems considered was detected by GC
analysis using a Vega 6000 Series 2 gas chromatograph
(Carlo Erba, Milan, Italy). The instrument was
equipped with a hot wire detector (HWD) and a
2 m 2 mm id glass-packed Supelco column ®lled with
Porapack Q 80±100 mesh (Supelchem, Milan, Italy).
The operating conditions were: column temperature
100 °C; detector oven temperature 180 °C; injector
temperature 110 °C; ®lament temperature 230 °C;
carrier gas ¯ow (He) 40 ml minÿ1. A headspace volume
of 0.2 ml was injected using a Hamilton model 1750
CEST syringe (Hamilton Bonaduz AG, Bonaduz,
Switzerland) assembled on an HS 250 automatic
sampler (Carlo Erba, Milan, Italy). Gas chromatographic traces and peak areas were evaluated with a
Fisons model DP 700 integrator (Fisons, Milan,
Italy).
Model A
Model B
Model C
Model D
Gelatinised starch
Water
Glucose
Lysine
Soybean oil
320
300
160
40
180
500
300
160
40
Ð
520
300
Ð
Ð
180
700
300
Ð
Ð
Ð
Water activity (aW)
0.887 0.005
0.867 0.003
0.931 0.004
0.908 0.002
685
D Mastrocola et al
Absorbance
Absorbance measurements at 294 and 420 nm were
carried out using a Varian DMS 80 UV-vis spectrophotometer (Varian, Sunnyvale, USA) according to
Lerici et al. 21 For absorbance analysis, 5 g of each
sample was suspended in 30 ml of distilled water and
homogenised using a Politron (PT 3000, Kinematica
AG, Littau, Switzerland) for 1 min. Samples were
centrifuged for 5 min at 4330 g at 0 °C (refrigerated
centrifuge ALC, RCF Meter, 4233R) and the aqueous
phase was ®ltered on paper (Whatman no 4). Extracts
were diluted with distilled water in relation to the
degree of browning in order to have absorbance signals
on scale. A freshly prepared solution of glucose was
used as reference.
pH
The pH of the heated and unheated model systems
was measured with a Beckman 3560 digital pH meter
equipped with a penetration probe.
Water activity
Water activity aw was evaluated at 25 °C by means of
an electronic hygrometer (Hygraskop DT, Rotronic,
Zurich, Switzerland) previously calibrated with standard solutions at theoretical aw values of 0.50, 0.65,
0.80 and 0.95. Prior to aw determination the samples
were cut into small pieces and equilibrated in the
hygrometer sample cell for 6 h at least.
Colour measurements
Colour determination was made with a tristimulus
calorimeter (Chromameter CR 200 II Re¯ectance,
Minolta, Osaka Co Ltd, Japan) equipped with an
illuminant C (CIE standard 6774 K) and a microprocessor for the statistical analysis of data. The
instrument was calibrated before each series of
measurements using a white tile re¯ector plate (L*
95.3, a* ÿ1.0, b* 0.8). Chromaticity results are
expressed as L* (lightness), a* and b* (chromaticity
coordinates).22
Before each analysis the oil fraction was removed
from the samples in order to avoid interference.
Evaluation of antioxidant action
The procedure proposed by Bressa et al 13 was
adopted. In order to obtain liquid extracts, 5 g of each
sample was suspended in 20 ml of a 0.4 M KCl aqueous
solution (Carlo Erba) and homogenised using a
Politron (PT 3000, Kinematica AG, Littau, Switzerland) for 1 min. Suspensions were centrifuged for
5 min at 4330 g at 0 °C (refrigerated centrifuge ALC,
RCF Meter, 4233R) and the aqueous phase was
®ltered on paper (Whatman no 4) and diluted with
10 ml of 0.4 M KCl. Samples were frozen at ÿ18 °C for
not more than 15 h in hermetically sealed containers.
Storage for periods exceeding 24 h led to a signi®cant
loss of antioxidant activity. For kinetic analysis the
extracts were dried and weighed.
According to the procedure adopted, the ability of a
686
compound or a mixture of compounds to quench
peroxyl radicals is measured by analysing the ®rstorder rates of crocin bleaching due to the presence of
peroxyl radicals. The presence of an antioxidant
slowed down the rate of bleaching. The rate of crocin
bleaching was followed at 443 nm using a spectrophotometer (Uvikon 860, Kontron Instruments,
Milan, Italy).
The competition kinetics follows the equation13
DA0 =DA ˆ V0 =V ˆ …kc ‰CŠ ‡ ka ‰AŠ†=kc ‰CŠ
ÿ 1 ‡ …ka =kc †…‰AŠ=‰CŠ†
…1†
where DA0 and DA are the absorbance variations in the
absence and presence of antioxidant respectively, V0
and V are the bleaching rates in the absence and
presence of antioxidant respectively, kc and ka are the
rate constants of crocin bleaching in the absence and
presence of antioxidant respectively and [A] and [C]
are the concentrations of antioxidant and crocin
respectively.
The following reactants were used: ABAP, 2,2'azobis(2-amidinopropane)dihydrochloride
(Wako
Chemicals Co, Osaka, Japan), as the peroxyl radical
generator; Trolox, 6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid (Aldrich, Milwaukee, WI,
USA), as the reference antioxidant (vitamin E hydrosoluble analogue); potassium dihydrogen phosphate
and potassium monohydrogen phosphate (Carlo Erba,
Milan, Italy); saffron (Sigma Chemical Co, St. Louis,
MO, USA). Crocin was isolated from saffron by
methanol extraction after repeated washing with ethyl
ether. The crocin solution was diluted with methanol
in order to obtain a 10 mmol lÿ1 crocin concentration
(the absorption coef®cient of crocin is 1.33 105 l molÿ1 cmÿ1 at 443 nm). Because of the low
solubility of Trolox in water, the Trolox solution was
obtained by dissolving 39.7 mg in a minimal volume of
absolute ethanol and diluting to 100 ml with distilled
water. The Trolox concentration was 1.59 mmol lÿ1.
Analyses were carried out at 49 °C in 2 ml of
incubation medium containing 0.1 mol lÿ1 phosphate
buffer pH 7.0, 9.5 mmol lÿ1 crocin and increasing
amounts of Trolox or sample extracts. The reaction
was started by adding 40 ml of a 97.7 mmol lÿ1 ABAP
aqueous solution. Triplicate measurements were made
for each sample.
The ability of the sample extracts to slow down the
crocin bleaching rate was measured in terms of Trolox
molar concentration. Thus, as reported by Tubaro et
al 23 and Bressa et al,13 all the dry matter of the extracts
was assumed to have antioxidant properties and, in
order to calculate the antioxidant molar concentrations, the molecular weight of Trolox (MW = 250.29)
was used.
Data analysis
All the data reported are the average of at least three
replications. The coef®cients of variation, calculated
for all the measurements taken as the ratio of the
J Sci Food Agric 80:684±690 (2000)
Interaction between Maillard reaction and lipid oxidation
standard deviation and the mean value, were lower
than 9% for colour, 4% for optical density and pH, 7%
for glucose and 5% for CO2 peroxide values and
antioxidant activity. Zero- and ®rst-order kinetic rate
constants were calculated from linear regression of the
different index values versus heating time, excluding
the induction period, when present. The induction
period was calculated using the equation21
…A ÿ A0 † ˆ k…t ÿ t†
…2†
where A is the value of the index at time t, A0 is the
value of the index at time 0, k is the kinetic rate
constant, t is the time, t = (A0ÿq)/k is the induction
time and q is the the intercept of the regression line
A = f(t).
RESULTS AND DISCUSSION
The browning kinetics in the different model systems
considered was studied using the following indicators:
optical density at 420 nm;20 Hunter L* and a*
values.21
The changes in optical density at 420 nm and
Hunter L* and a* values in the samples belonging to
models A, B, C and D during the heating time are
reported in Fig 1.
As expected, the samples without glucose and lysine
Figure 1. Optical density at 420 nm and colour L* and a* as related to
heating time at 100 °C in model systems with different compositions.
J Sci Food Agric 80:684±690 (2000)
(C and D) do not show any colour change. In contrast,
for model systems A and B it is possible to point out a
progressive change in colour (browning) due to the
Maillard reaction.15,24,25 The presence of oil in model
A seems to induce an increase in browning. In fact,
after a ®rst phase (about 100 min) during which the
reaction rate is similar in the samples belonging to
model systems A and B, after increased heating, for the
product without the lipid phase the reaction slows
down. The evolution of the absorbance and L* and a*
indices in model A could be due to the migration of
liposoluble Maillard reaction products from the
aqueous phase, where this reaction prevalently take
place, to the lipid phase. This hypothesis does not
exclude the possibility that the higher browning rate in
the presence of oil might also be due to the
participation of intermediate products of lipid oxidation in the Maillard reaction.4,16,17
In every case, all the browning indicators adopted
not only allowed us to clearly distinguish model
systems subject to the Maillard reaction (A and B)
from samples without glucose and lysine (C and D),
but were also able to put in evidence the effect of oil on
the reaction kinetics.
In Fig 2 the evolution of the optical density at
294 nm and the percentage of carbon dioxide in the
different model systems considered are reported. As
expected, signi®cant changes in CO2 content in the
headspace of samples A and B and absorbance at
294 nm of their aqueous extracts during heating have
been observed. In fact, in these models the presence of
glucose and lysine allows the Maillard reaction to take
place and both carbon dioxide and optical density in
the ultraviolet zone can be considered as early
indicators of this reaction.21
Figure 2. Optical density at 294 nm and CO2 content in headspace as
related to heating time at 100 °C in model systems with different
compositions.
687
D Mastrocola et al
Figure 5. Antioxidant activity as related to heating time at 100 °C in model
systems with different compositions.
Figure 3. Glucose content and pH as related to heating time at 100 °C in
model systems with different compositions.
The data reported in Fig 2 also show that the
presence of oil slightly decreases the amount of CO2
that it is possible to detect in the gaseous phase at
equilibrium. Probably the lower concentration of
carbon dioxide in the headspace of samples belonging
to model A is due to the distribution of this gas in the
two phases (aqueous and lipid), with the consequent
reduction of its molar ratio in the vapour phase.
Fig 3 describes the changes in pH and glucose
concentration in the heat-treated model systems. As is
well known, the decrease in pH observed in the
samples in which the Maillard reaction takes place (A
and B) can be attributed to the reaction of amines to
form compounds of lower basicity and to the
degradation of glucose to acids.26,27 In fact, in these
model systems the glucose consumption follows the
same behaviour as the pH decrease (Fig 3).
In Fig 4 the peroxide values of the lipid fraction of
Figure 4. Peroxide values as related to heating time at 100 °C in model
systems with different compositions.
688
models A and C as a function of heating time are
reported. As also observed in a previous work,12 the
oxidative process, very evident in model C, is strongly
inhibited in model A by the well-known antioxidant
activity of Maillard reaction products (MRPs).7,8,10,11
In Fig 5 the antioxidant capacity of the model
systems considered as a function of heating time is
reported. From the data reported in Fig 5, it is evident
that only the samples in which the Maillard reaction
takes place generate a detectable antioxidant activity
during heating. After the initial period (about 100 min)
in which the behaviour of models A and B appears very
similar, the samples with oil show a deceleration of the
formation of compounds with antioxidant activity. In
this model system, in fact, the presence of a lipid
phase, although favouring the development of the
Maillard reaction, on the other hand can involve a
`consumption' of antioxidants.
Zero- and ®rst-order kinetic constants related to the
reactive model systems only and calculated from linear
regression analysis of the data plotted versus heating
time and their determination coef®cients are reported
in Table 3. In the case of absorbance, colour a* and
peroxide values and antioxidant activity the reaction
kinetic constants are signi®cantly different also from a
statistical point of view. According to the literature,21,26 zero order was more in keeping with changes
in optical density and peroxide values, headspace CO2
concentration and antioxidant activity, while for
colour, glucose loss and pH the ®rst-order determination coef®cients were slightly higher than the zeroorder ones.
In Table 4, correlation equations and correlation
coef®cients (r) of antioxidant activity as a function of
different Maillard indices for all samples considered
together, samples with oil and samples without oil are
reported. The high correlation coef®cients suggest
that, for a given food product under given processing
and storage conditions, the determination of some
appropriate indices could give useful indications on
the antioxidant capacity of the product. In every case
there is a perceptible difference between samples with
and without oil. In fact, for all analytical indices
considered, the antioxidant activity of the samples
J Sci Food Agric 80:684±690 (2000)
Interaction between Maillard reaction and lipid oxidation
Model
k0
r2
Abs 420 nm
A
B
0.0269 0.0028
0.0161 0.0021
0.968
0.952
Colour (L*)
A
B
Colour (a*)
A
B
0.0786 0.0121
0.0563 0.0111
0.913
0.865
19.3179 1.6398
14.2243 1.2191
Abs 294 nm
A
B
0.2586 0.0364
0.1917 0.0257
0.927
0.933
54.9906 16.3381 0.739
40.7785 11.9405 0.745
CO2
A
B
0.1031a 0.0021 0.998
0.1095a 0.0049 0.992
23.6960a 3.2488 0.930
25.5337a 2.9025 0.951
Glucose
A
B
ÿ0.0155a 0.0034 0.837
ÿ0.0164a 0.0035 0.849
ÿ4.0084a 0.2663 0.983
ÿ4.2095a 0.2674 0.982
pH
A
B
ÿ0.0095a 0.0023 0.774
ÿ0.0099a 0.0024 0.768
ÿ1.8714a 0.2193 0.948
ÿ1.8456a 0.2431 0.935
Peroxide value
A
C
0.0103 0.0034
0.1835 0.0113
0.694
0.981
1.9728 1.1007
42.1855 4.5887
Ð
0.958
Antioxidant activity
A
B
0.0393 0.0040
0.0552 0.0028
0.960
0.990
9.3154 1.0621
12.6248 1.9286
0.949
0.914
Index
Table 3. Zero- (k0) and first-order (k1) kinetic rate
constants and determination coefficients (r2)
calculated from linear regression analysis for
changes in absorbance (294 and 420nm), colour
(L* and a*) and peroxide values, headspace CO2
and glucose concentration, pH and antioxidant
activity in different model systems
0.757
0.748
ÿ0.2466a 0.0202 0.974 ÿ58.5191a 5.3489 0.967
ÿ0.2081a 0.0342 0.900 ÿ51.9493a 2.3794 0.990
0.972
0.971
For the same index, values in a column with a common superscript are not signi®cantly different
(p 0.05).
Samples
Equation a (y = antioxidant activity)
Abs 420 nm
All
With oil
Without oil
y = 2.2542 ( 0.274) x ‡ 0.5014
y = 1.7625 ( 0.190) x ‡ 0.2828
y = 4.0189 ( 0.342) x ‡ 0.2441
Colour (L *)
All
With oil
Without oil
y = ÿ0.1836 ( 0.012) x ‡ 16.3827
y = ÿ0.1573 ( 0.006) x ‡ 13.7935
y = ÿ0.2260 ( 0.015) x ‡ 20.3343
Colour (a *)
All
With oil
Without oil
y = 0.6224 ( 0.049) x ‡ 0.8375
y = 0.4997 ( 0.014) x ‡ 0.6628
y = 0.8737 ( 0.063) x ‡ 0.8983
0.931
0.995
0.970
Abs 294 nm
All
With oil
Without oil
y = 0.2056 ( 0.020) x ‡ 0.4407
y = 0.1606 ( 0.019) x ‡ 0.3919
y = 0.2955 ( 0.023) x ‡ 0.2887
0.898
0.930
0.963
CO2
All
With oil
Without oil
y = 0.4536 ( 0.012) x ÿ0.1485
y = 0.4110 ( 0.017) x ‡ 0.0067
y = 0.4864 ( 0.011) x ÿ0.2766
0.991
0.992
0.996
Glucose
All
With oil
Without oil
y = ÿ1.8307 ( 0.314) x ‡ 27.6102
y = ÿ1.5818 ( 0.338) x ‡ 23.6288
y = ÿ2.2310 ( 0.481) x ‡ 33.6716
ÿ0.859
ÿ0.912
ÿ0.901
pH
All
With oil
Without oil
y = ÿ2.7029 ( 0.284) x ‡ 15.6899
y = ÿ2.4561 ( 0.334) x ‡ 14.2346
y = ÿ2.9225 ( 0.458) x ‡ 17.0024
ÿ0.885
ÿ0.911
ÿ0.878
a
r
0.854
0.942
0.959
ÿ0.948
ÿ0.991
ÿ0.974
For all correlation equations, p 0.001.
containing an oxidisable lipid fraction is signi®cantly
lower (lower values of x coef®cients). In addition, the
separation of samples with oil and samples without oil
allowed us to obtain higher correlation level (higher
values of correlation coef®cients) between antioxidant
activity and Maillard reaction indices.
J Sci Food Agric 80:684±690 (2000)
5.1521 1.4579
3.1070 0.9026
r2
a
Index (x value
Table 4. Correlation equations and correlation
coefficients (r) of antioxidant activity as a function of
different Maillard indices (absorbance at 294 and
420nm, colour L* and a* values, headspace CO2
and glucose concentration, pH) for analysed
samples considered all together or collected as
‘with oil’ or ‘without oil’ samples
k1
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