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HEALTH
EFFECTS
OF
OXIDIZED HEATED OILS'
MARTIN GROOTVELD*, CHRISTOPHER J.L. SILWOOD*, PAUL ADDIS3
and
ANDREW CLAXSOP
2Department
of
Diabetes and Metabolic Medicine
St. Bartholomew
3
and the Royal
London
Hospital's School
of
Medicine and Dentistry
London
El
IBB
3Department
of
Food Science and Nutrition
University
of
Minnesota
St. Paul, Minnesota
551
08
BARTOLOME BONET SERRA
and
MARTA VIANA
Facultad de Ciencias Experimentales
y
Tkcnicas
Universidad de San Pablo Ceu
Madrid, Spain
Received
for
Publication April
30.
2001
Accepted
for
Publication August 22, 2001
ABSTRACT
The purpose
of
this report is to alert the foodsenice industry. particularly
the fast-food industry, of an emerging health issue. Considerable evidence has
accumulated over the past
two
decades that heated cooking oils, especially
polyunsaturated oils,
may
pose several types
of
health risks
to
consumers offn'ed
foods and even people working near deep fathers. Heat degrades polyunsatu-
rated fatty acids
to
toxic compounds; saturated and monounsaturated fatty acids
are resistant
to
heat-induced degradation. Several types
of
diseases
may
be
related
to
the exposure
of
humans to food-
or
air-borne breakdown products
of
heated oils including atherosclerosis, the forerunner to cardiovascular disease;
injlammatory joint disease, including rheumatoid arthritis; pathogenic conditions
of the digestive tract; mutagenicity and genotoxicity, properties that open signal
carcinogenesis; and teratogenicity, the property of chemicals that leads to the
development of birth defects. Factors that can contribute to improved oil
stability,
and
therefore fewer health concerns, are
briejly
discussed. The
literature reviewed raises serious questions concerning the willfisl addition of
large amounts of polyunsaturated fatty acids into the human diet without
accompanying measures
to
ensure the protection
of
these fatty acids against
'
This research
has
been supported in part
by
the Minnesota Agricultural Experiment Station
Author
to
whom all correspondence should be addressed. TEL: 612-624-7704; FAX: 612425-
5272; E-mail: paddisQumn.edu
Foodservice Research
International
13
(2001) 41-55.
All
Rights Reserved.
"Copyright
2001
by
Food
&
Nutrition Press, Inc., Trumbull. Connecticut.
41
42
M.
GROOTVELD
ETA.
heat- and oxidative-degradation.
It
is hoped that this review will stimulate
interest
in
the foodservice industry
in
this important area
of
potential health
concern,
and
also foster the research and development activities necessary to
reduce the exposure of humans to lipid oxidation products.
INTRODUCTION
The thermally-induced oxidation of glycerol-bound polyunsaturated fatty
acids (PUFAs) in foods and culinary oils during standard frying or cooking
episodes is a process that involves the prior generation of isomeric conjugated
hydroperoxydiene (CHPD) species. These CHPDs fragment to form alkoxyl
radicals that, in turn, undergo 8-scission to generate a wide range of aldehydic
products.
In
view of the extremely toxic nature of the aldehydic end-products
generated, the employment of PUFA-containing culinary oils for domestic or
commercial fryinghoking episodes poses health hazards that have recently
attracted much public and clinical interest.
Indeed, these cytotoxic agents have been implicated in the development and
progression of atherosclerosis (Steinberg and Wit-
1990)
and its associated
pathological sequelae such
as
ischemic heart disease and peripheral vascular
disease, and have also been shown to exert gastropathic (Jayaraj
et al.
1986),
pro-inflammatory (Benedetti
et al.
1990),
and genotoxicological (Esterbauer
1982)
properties. These phenomena are undoubtedly attributable to the extremely
high reactivity of aldehydes with critical biomolecules (e.g., thiols such
as
glutathione; DNA, forming covalently-modified base adducts; and the apolipo-
protein B component of low-density lipoprotein, altering its biological
characteristics.)
Two of the contributors of this paper,
M.
Grootveld and
A.
Claxson, have
recently reported the detection and quantification of PUFA-derived oxidation
products (notably aldehydes and their CHPD precursors)
in
culinary oils by high
resolution proton ('H) nuclear magnetic resonance
(NMR)
spectroscopy, a
virtually noninvasive multicomponent analytical technique (Claxson
et
uZ.
1994;
Haywood
et al.
1995).
The influence of episodes of thermal stressing (i.e., those
that simulate their domestic or commercial usage) on the generation, nature and
concentrations of such products was also evaluated in these studies. We have
also employed this technique to probe the
in
vivo
absorption, metabolism and
urinary excretion of typical aldehydic lipid oxidation products in experimental
animals
and found that such agents are indeed absorbed from the gut into the
systemic circulation, metabolized (primarily via the addition of glutathione
across their electrophilic carbon-carbon double bonds), and excreted in the urine
as
C-3 mercapturate conjugates (Grootveld
et al.
1998).
HEATED
OILS:
HEALTH EFFECTS
43
The foregoing findings are especially relevant in view of the trend toward
the use of vegetable oils,
as
a replacement for
animal
fats, for the purpose of
frying/cooking practices. Vegetable oils, even those which have been subjected
to hydrogenation, are more labile than animal-derived lard and tallow. However,
neither a return to animal-derived cooking fats nor hydrogenated vegetable oils
is likely to provide an acceptable alternative
as
both are problematic with regard
to health effects (Addis
et
al.
1995). The issue of
trans
fatty acids is currently
under intense investigation and a number of potential adverse health effects have
been reported (Addis and Warner 1991; Addis
et
al.
1995). Regarding
cholesterol oxidation in the frying process, it has been demonstrated that toxic
cholesterol oxidation products (COPs) readily form in heated tallow (Park and
Addis 1986a,b). Furthermore, levels of COPs in heated tallow were predictable
by the conductivity
of
the frying medium (Zhang and Addis 1991). Moreover,
samples of French-fries obtained daily from a fast-food restaurant over a one-
month time period displayed significant though variable levels of COPs,
including the highly atherogenic
30,
5a,
60-cholestane trio1 (Zhang and Addis
1991). COPs have been shown to occur
in
the plasma lipoproteins of fasted
humans (Addis
et
al.
1989) and in chylomicrons of human subjects fed a meal
rich in fat and COPs postprandially (Emanuel
et
al.
1991). A review of the
literature of the biological and health effects of COPs and other components of
thermally-stressed oils would be enormous and will not
be
attempted here.
Several reviews of this area have been published and are recommended to the
reader (Addis 1986; Addis
et
al.
1993, 1995; Guardiola
el
al.
1996).
In
response to these foregoing issues, a tallow-based frying and baking fat has been
developed by removing cholesterol and blending the cholesterol-free tallow with
corn oil, achieving
an
oil that tends to raise serum HDL while also lowering
serum LDL (Hayes 1996). Because
the
foregoing oil
is
not
produced with
catalytic hydrogenation,
trans
fatty acids would appear not to be a problem. The
significance of this development stems from the fact that
trans
(elaidic) fatty
acids interfere with the beneficial effects of both saturated and polyunsaturated
fatty acids
-
namely, raising HDL and lowering LDL, respectively (Sundram
et
al.
1997; Hayes 1996). The removal of cholesterol is
also
advantageous in
terms of reducing serum cholesterol
in
subjects consuming the tallowhrn oil
blend (Hayes 1996).
In the following sections of this communication we review the toxicological
hazards afforded by the ingestion of aldehydes present in thermally-stressed
and/or repeatedly-utilized PUFA-rich culinary oils, and address potential
methods to limit the production of these deleterious agents during routine frying
processes.
44
M.
GROOTVELD
ETAL.
Cardiovascular
Diseases
Peroxidation of PUFA components of low-density lipoprotein (LDL)
in vivo
stimulates the subsequent production of foam cells from macrophages, a crucial
stage in the pathogenesis of atherosclerosis (Addis and Warner 1991; Van
Hinsbergh 1984), and this oxidative modification occurs from the following
sequential steps: (1) generation of aldehydes from the decomposition of pre-
formed, PUFA-derived CHPDs; and (2) alteration of the apolipoprotein
B
(apo
B)
moiety’s structure via Maillard reactions involving the above carbonyl
compounds. Hoff
ef
al.
(1989) demonstrated that
4-hydroxy-trans-2-nonenal
(HNE), an a,P-unsaturated aldehyde arising from the autoxidation of PUFAs,
reacted with selected
amino
acids of apo
B,
rendering it susceptible to uptake by
the macrophage scavenger receptor. Apo
B
lysine residues are readily
derivatized by aldehydic CHPD fragmentation products (Jurgens
e?
al.
1987).
Therefore, subsequent to their
in
vivo
absorption, aldehydes present in
thermally/ oxidatively-stressed frying
oils
ingested in the diet will have the
ability to directly effect structural modification of the apo
B
component of LDL,
a process that induces the generation of foam cells from macrophages
-
the
hallmark of atherosclerosis.
Interestingly, Smith and Kummerow (1987) have demonstrated that the
dietary consumption of peroxidized culinary oils escalated the accumulation of
‘oxidized lipids’
in
macrophages and monocytes, and previous animal feeding
studies have shown that diets containing thermally-stressed, PUFA-rich oils are
more atherogenic than those containing corresponding unheated oils. More
recently, Staprans
ef
al.
(1996) conducted investigations
aimed
at evaluating the
ability of oxidized dietary lipids to accelerate the development of atherosclerosis
in New Zealand White rabbits and found that such a diet increased levels of fatty
streak lesions, a “fingerprint” of atherosclerosis, by 100% compared to unheated
oils. These findings clearly indicate that the consumption of PUFA-derived
oxidation products in the diet represents a hazard to human health. Furthermore,
Kritchevsky and Tepper (1967) provided evidence for the atherogenicity of
thermally-stressed PUFA-rich oils
as
early
as
1967. These researchers found that
heating corn oil [PUFA-content
=
57%
(w/w)] at 215C for a period of 20
min
substantially increased its atherogenicity, whereas the heating of olive oil [PUFA
content
=
9% (w/w)] in the same manner had no effect on its atherogenic
properties.
Figure 1 shows expanded regions of high resolution ‘H NMR spectra of a
corn (maize) oil sample acquired prior to and subsequent to heating at a
temperature of 180C for a period of
30
min.
The results in Fig. 1 clearly reveal
the generation of CHPDs and their aldehydic fragmentation products during the
subjection of a commonly-utilized PUFA-laden culinary oil to episodes of
thermal stressing according to standard frying practices. Therefore, it is likely
HEATED
OILS:
HEALTH EFFECTS
45
that consumption of foods subjected to standard frying procedures is a health
concern to the consumer, especially regarding cardiovascular disease.
,~""'"'l""'"'I'"'~''''l'~"~'"'I'"'~'""''''~''''
G--Z
on
85
8.0
75
70
85
80
55
ppm
FIG.
1.
PROTON ('H) NMR ANALYSIS OF LIPID OXIDATION PRODUCTS IN
Partial
(5.00-10.00
ppm) region
of
a onedimensional
'H NMR
spectrum
of
a sample
of
corn (maize)
oil
subjected
to
an episode
of
heating according
to
standard frying practices
(30
min at
180C). A
typical spectrum is shown. Abbreviations:
'H
nuclear labels
of
lipid oxidation products correspond
to
labeled protons in the accompanying molecular stlllctllres
([a,
cis,
trans-conjugated hydroxy-
peroxydiene; trans,transconjugated hydroxyperoxydiene;
[IIII,
cis,
rranr-conjugated
hydroxydiene;
N,
n-alkanal;
IV),
rrans-2-alkenal;
[vr],
rrans,trans-alka-2,4- dienal).
THERMALLY-STRESSED CULINARY OILS
Pro-inflammatory Properties
The oxygen radical-mediated peroxidation
of
polyunsaturates in the knee-
joint of patients with inflammatory joint diseases (e.g., rheumatoid arthritis)
have been investigated in some detail, and elevated levels
of
lipid oxidation
products have been measured in inflammatory knee-joint synovial fluid,
an
apparent consequence of a cascade
of
radical reactions induced by localized
46
M.
GROOTVELD
ETA.
episodes of ‘oxidative stress’ in vivo. In view of their aggressive reactivity
toward many essential biomolecules, aldehydic lipid oxidation products exert
powerful pro-inflammatory actions, and Benedetti
er
al.
(1980) found that
injection of a mixture of peroxidized PUFA-derived carbonyl compounds
(predominantly
4-hydroxy-trans-2-nonenal
at a concentration of only 0.15
pM)
induced a significant inflammatory response (i.e. edema) in the hind paw of rats.
Intriguingly, Selley
ef
al.
(1992) used gas chromatography coupled with
mass
spectrometric detection to determine levels of
4-hydroxy-trans-2-nonenal
in blood plasma of patients with rheumatoid and osteoarthritis, and found that
although concentrations of this terminal peroxidation product in the osteoarthrit-
ics’ biofluids were similar to those of healthy vqlunteers (ca. 0.10
pM),
those
of rheumatoid patients’ plasma were significantly greater. Although at least some
of this cytotoxic agent could arise from the oxidative degradation of PUFAs in
vivo, there may be an association between these levels and the frequency of
thermally-stressed PUFA consumption in the diet.
Several of the authors have recently investigated the pro-inflammatory
properties of control and thermally-stressed culinary oils using an appropriate
animal model system (foot pad edema in the hind paw of male Wistar albino
rats), and Fig. 2 demonstrates that preheating corn and olive oils at a tempera-
ture of 250C for a period of 60 min gives rise to a marked elevation in the pro-
inflammatory properties of these materials. The increase in edema size with time
observed for the heated
corn
oil samples is significantly greater than that arising
from heated olive oil samples, a phenomenon explicable by the much higher
content of PUFAs in the former which, of course, give rise to the generation
of
higher concentrations
of
aldehydic peroxidation products.
Gastropathic
Conditions
Oral administration of the a$-unsaturated aldehyde 4-hydroxy-rrans-2-
nonenal to rats at a dose level of only 0.26
pM,
a concentration similar to that
of healthy human blood plasma,
has
been found to induce peptic ulcers in the
animals (Jayaraj
er
al.
1986). Therefore, dietary consumption of such agents,
present at extremely high levels in thermally-stressed PUFA-rich culinary oils,
may account for a high fraction of such gastopathic conditions in humans.
In contrast to the acute toxicity observed shortly after the systemic
administration of CHPDs (experimental animals dying from severe lung damage
within 24 h), oral administration of these primary lipid oxidation products were
found to be nonlethal, a phenomenon indicating that they fail to be effectively
absorbed across the gastric or intestinal epithelium. However, it is important to
note that isomeric CHPDs could also give rise to gastropathic conditions in
humans consuming culinary oils subjected to domestic or commercial frying
episodes.
HEATED
OILS:
HEALTH EFFECTS
47
Mutagenicity
and
Genotoxicity
Further toxicological investigations regarding thermally-stressed culinary
oils and fats have focussed on their mutagenic properties. Indeed, recent studies
by Wu
ef
al.
(1999) and Zhong
ef
al.
(1999) have shown that volatile emissions
from heated culinary oils utilized for the purpose of Chinese-style cooking
are
mutagenic and exposure to such indoor air pollution may render humans to
an
increased risk of contracting lung cancer. Indeed, in view of the temperatures
employed in standard frying practices
(ca.
180C), such fumes are rich in
CHPD-derived volatile aldehydic fragments, including acrolein, one of the most
highly toxic crJ3-unsaturated aldehydes generated from the thermally-induced
oxidation of PUFAs.
Intriguingly, Shields
et
al.
(1995) found that volatile emissions from
unrefined Chinese rapeseed, refined U.S. rapeseed (Canola), Chinese soybean
and Chinese peanut oils contained the mutagens acrolein and formaldehyde in
addition to 1,3-butadiene and benzene, which represent important risk factors in
the etiology of lung cancer. As expected, lowering of the cooking temperature,
or pre-addition of lipid-soluble antioxidants such
as
butylated hydroxyanisole
(BHA) decreased the levels of these mutagenic volatile components, and,
interestingly, the mutagenicity of individual volatile emission condensates
correlated strongly with the linolenate content of the oils investigated.
Hence, the inhalation of vaporized aldehydes by subjects conducting
commercial or domestic frying practices involving PUFA-rich culinary oils
affords a potential hazard to human health.
The mutagenic properties of repeatedly-used deep-frying fats have been
previously evaluated using the Ames test (Hageman
et
al.
1988). In this study,
fat samples were fractionated into polar and nonpolar fractions by column
chromatography and the former increased the number of revertants without S-9
mix in various strains, strain TA97 being the most sensitive. The mutagenic
activity of these polar fractions was positively correlated with the level of
thiobarbituric acid-reactive substances (TBARS), an observation strongly
suggesting the involvement of lipid oxidation products in mutagenicity.
Teratogenicity
The possibility that heated culinary oils might stimulate the development of
birth defects has been studied only recently.
Two
of the contributors of this
paper, B. Serra and
M.
Viana, have obtained evidence indicating that both
in
vifro
and
in vivo,
the generation
of
oxygen-derived free radical species can lead
to embryo malformations (Bonet
ef
al.
1995; Viana
ef
al.
1996). These findings
are consistent with reports from other laboratories on the embryonic malforma-
tions due to oxygen-derived free radicals induced by diabetes (Eriksson and Borg
48
M.
GROOTVELD
ETA.
I
I
1991; Sivan
er
al.
1996) and the ameliorating effects
of
vitamin
E
(Bonet
ec
al.
1995;
Siman
and Eriksson 1997).
I
30
B
v
W
u
3
25
E
I2
u
ri
3
d
20
I
15
-
-0
O.lOmL
of
unheated
corn
oil
0.lOmL
of
heated
corn
oil
***
***
T
r
ns
i/
‘
,’
cj
I
***
I
I
*
1
rn
ns
I
TIME
(hr.)
HEATED
OILS:
HEALTH EFFECTS
I
I
I
I
30
25
20
15
!I
0
0.lOmL
Of
UNHEATED olive oil
-m
O.lOrnL
of
HEATED olive oil
**
**
ns
*
r
I
I
T\
'\
+I
T
ns
ns
Xh
1-
ns
rn
I
0
1.0
2.0
3.0
4.0
5.0
6.0
'
24.0
TIME
(hr.)
FIG. 2. PRO-INFLAMMATORY PROPERTIES
OF
THERMALLY-STRESSED CULINARY
OILS
Rat (male Wistar) foot pad edema induced by application of
0.10
mL
volumes of (A) control
(unheated) and preheated corn oil and
(B)
control and preheated olive oil
(oils
were subjected to a
60
min thermal saessing episode at 250C and then cooled
to
ambient temperature prior
to
testing).
Paw circumferences were measured with a cotton loop
localized
at the hindmost spur on the
subplatar surface. Data
points
are the mean values of groups of
6
experimental animals, and the
error bars represent associated
standard
deviations. Abbreviations:
ns,
not significantly significant;
*, **,
***,
statistically significant at the
5,
1
and
0.10%
levels, respectively.
50
M. GROOTVELD
ETA.
The mechanisms of these teratogenic effects are the subject of much
speculation. Among the cell components, PUFAs are readily oxidized by free
radicals, leading to the generation of cytotoxic aldehydic fragments (Gutteridge
and Halliwell
1994;
Pryor
1994).
These compounds can cause chromosomal
breakage (Emerit
ef
al.
1985;
Emerit
1994),
and if
this
process occurs in the
embryo,
it
could lead to malformations.
To
study whether culinary oils oxidized
by heat, materials rich in CHPDs and aldehydes, are teratogenic in rats, we
developed the following experiment (Bonet
et al.
1996).
Pregnant rats were fed
by gavage with
0.3
mL
of either thermally-stressed (with a content of TBARS
of
120
mmol) or nonheated sunflower
seed
oils from day
1
of pregnancy until
day
11,
the end of the rat gestational period.
A
control group was investigated.
The animals were sacrificed and the embryos examined.
In
Table
1,
the rate of
neural tube malformations, reabsorptions, crown-rump length and the number
of somites (parameters related with the embryo size and development) in the
three experimental groups are shown. Clearly, the administration of preheated
(oxidized) oil increased the mean rate of malformations from the
6%
found in
controls animals to a value of
26%.
The administration of nonheated oil did not
give rise to any changes in the rate of fetal malformations (the administration of
either preheated or nonheated culinary oil did not lead to any modifications
in
the rate
of
reabsorptions, crown-rump length, or the somite number). These
results demonstrate that the administration of aldehyde-containing thermally-
stressed culinary oil is highly teratogenic in the rat, and an attractive hypothesis
is that the intake of such oxidized oils during pregnancy may be partially
responsible for the neural tube defects found in humans. Differences in the type
of heated oil used in standard frying or cooking processes may also be
responsible for the differing rates of neural tube defects found among different
populations. Further investigations are required in this research area.
TABLE
1.
AND SOMITE NUMBER IN THE DIFFERENT EXPERIMENTAL GROUPS
RATE OF EMBRYO MALFORMATIONS, REABSORPTIONS, CROWN-RUMP LENGTH
Unheated
oil
Control Heated oxidized oil
Total embryos
132 50 105
Neural tubes malformed,
%
4.6 6.0 26.0
Reabsorptions,
%
9.5 10.0 7.5
Somites. number
29.5ko.i 2a.6ko.2 2a.5+0.3
Crown-rump, mm
4.1+0.03 3.9k0.05 3.9+0.05
HEATED
OILS:
HEALTH EFFECTS
51
Suggested
Research Activities
Several areas of research could potentially be fruitful with regard to
building upon what is currently known about the chemical breakdown and
toxicity of heated polyunsaturated oils and other frying fats. These include
surveys of foods provided in fast food restaurants, studies of improved
maintenance of oils during restaurant usage by, for example, improved use of
antioxidants, improved filtration efficiency, determining the optimum
type
of oil
(fat) to use in a frying operation, and in some cases development of alternative
cooking procedures i.e. those which create food with fried characteristics but in
fact do not employ oils in the cooking process. In addition, although not
specifically reviewed in this article, precooked (uncured) meats and irradiated
meats are two types of food that may well contain lipid oxidation products
similar to those in heated polyunsaturated oils and therefore parallel studies
should be conducted.
Surveys of foods are needed to ascertain the actual consumption of lipid
oxidation products by the public. Given the complexities involved, i.e. the many
different types of fats, oils and shortenings; the many types of maintenance
schedules and equipment; the numerous foods, extremely variable in composition
and properties, that are fried, such a survey would be a major undertaking but
it must be conducted. It would also be valuable to compare restaurants that are
subjected to governmental regulation regarding oil quality, specifically regulating
maximum polar materials allowable, and those that are not. Methodology used
to monitor oil quality is also an important issue. One way to insure minimum
acceptable oil quality would be to incorporate the oil quality requirements and
maintenance schedule into the restaurant's HACCP (hazard analysis critical
control point) program. The implementation of a HACCP program for frying
oils would require the development of effective quality control (rapid, simple)
tests for oil quality.
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