Minnesota Corn Research & Promotion Council
Final Report
Project Title
Evaluation of strategies form minimizing metabolic oxidative stress in nursery pigs fed diets
containing high concentrations of DDGS
Principal Investigator and Co-Investigator(s)
Dr. Jerry Shurson, Department of Animal Science, University of Minnesota
Abstract
Energy is the most expensive nutritional component in animal feeds, and fats and oils contain 2.25
times more energy than carbohydrates. Corn oil contains the highest concentration of metabolizable
energy for swine and poultry compared to most feed grade vegetable oil and animal fats, and similar
to soybean oil. However, because of the high concentration of polyunsaturated fatty acids in corn oil,
it is highly susceptible to damage from peroxidation during heat processing and storage. Although
several peroxidation measures can be used to determine the extent of lipid damage, the numerous
compounds produced and the complexity of the peroxidation process makes it difficult to determine
the best measures to use. Therefore, determining the most useful measures of lipid peroxidation, and
understanding the effects of lipid quality (peroxidation) on metabolic oxidative stress is essential to
optimize caloric efficiency of distiller’s corn oil and reduced oil DDGS. Feeding peroxidized lipids to
pigs and poultry causes metabolic oxidative stress that can significantly reduce growth performance
and health. Achieving optimal feed and caloric efficiency, as well as minimizing animal mortality and
morbidity, are vital for maintaining profitability for Minnesota pork producers. Because the pork
industry is one of the predominant consumers of Minnesota corn, DDGS, and distiller’s corn oil,
understanding the impact of lipid quality of these co-products, and approaches to mitigate these
negative effects are essential for Minnesota corn producers to sustain current demand for DDGS, and
increase future demand for distiller’s corn oil in swine diets. Therefore, through funding support of the
Minnesota Corn Research and Promotion Council, we have continued to develop a better
understanding of potential connections between feeding diets containing DDGS and distiller’s corn oil
on metabolic oxidative stress in pigs, and communicate these findings to national and international
feed and pork industry audiences.
Introduction
Corn DDGS has become a commonly used feed ingredient in swine diets in recent years due
its abundant supply, high nutritional value, and favorable price relative to corn. In fact, the U.S. pork
industry now consumes 15 to 20% of total DDGS production annually. However, as ethanol plants are
evolving into biorefineries, the composition of DDGS is changing and new co-products are being
produced. Currently, about 85% of U.S. ethanol plants extract corn oil prior to manufacturing DDGS.
This has resulted in increased variability in oil content of DDGS (5 to 12% oil) and a new opportunity
for the feed industry to use distiller’s corn oil as an economical and high energy ingredient in animal
feeds. Extracted distiller’s corn oil, as well as corn oil present in DDGS, contains high amounts of
polyunsaturated fatty acids, especially linoleic acid, and are highly susceptible to peroxidation. A
recent University of Minnesota study from our group (Song and Shurson, 2013) showed that some
sources of DDGS contain 25 times more peroxidized oil than corn. This is a potential concern because
feeding peroxidized lipids to pigs and poultry has been shown to decrease growth performance and
may lead to adverse health effects. In fact, several years ago, some swine veterinarians reported an
increased incidence of Mulberry Heart Disease (vitamin E and selenium nutritional deficiency) in
nursery pigs, and suggested that feeding diets containing DDGS was a contributing factor. This
perception was based on the fact that the heat processes used during DDGS production destroy most
of the vitamin E content in corn oil, and that sulfur content in DDGS can sometimes exceed 1%, which
may interfere with selenium utilization by the pig. However, our research results (funded by MN Corn
Research and Promotion Council, MN Pork Board, and AURI in 2011) showed that adding high
amounts of a highly peroxidized, high sulfur DDGS source to sow and nursery pig diets had no effect
on the occurrence of Mulberry Heart Disease (Hanson et al., 2015). However, we did observe a
dramatic decline in the antioxidant status of nursery pigs in the immediate post-weaning period
(Hanson et al., 2015). These results led us to conducting the experiments described in this report
because there is limited information regarding the effects of feeding peroxidized corn oil (extracted or
in DDGS) to pigs, and the need for adding antioxidants to minimize corn oil peroxidation.
Objectives
The objectives of this project were modified from the original proposal based on results from other
related on-going research studies after the proposal was funded. As a result, the studies conducted
in this project added much more information to our knowledge about the effects of feeding
peroxidized lipids to pigs than originally proposed. Our objectives were to:
1. Summarize the scientific literature to determine the growth performance and metabolic
oxidation effects of feeding peroxidized lipids to pigs and broilers.
2. Compare lipid peroxidation measures for corn oil subjected to varying thermal conditions.
3. Determine the impact of antioxidants on lipid peroxidation of dried distillers grains with
solubles and distiller’s corn oil stored in extreme temperature and humidity conditions.
4. Determine the effects of dietary peroxidized corn growth performance and antioxidant
status of nursery pigs.
Materials and Methods and Results and Discussion
1. Summarize the scientific literature to determine the growth performance and
metabolic oxidative effects of feeding peroxidized lipids to pigs and broilers.
Data were summarized from studies that measured growth performance of pigs (n = 16
comparisons) and broilers (n = 26 comparisons) fed diets containing peroxidized lipids. Only
studies evaluating supplemental lipid sources in isocaloric diets were included. Dietary
thiobarbituric acid reactive substances (TBARS) and peroxide value (PV) were obtained from each
study, along with response variables including ADG, ADFI, G:F, and circulating concentrations
of vitamin E and TBARS. Data were evaluated using UNIVARIATE and CORR procedures of
SAS. Overall responses for swine and broilers fed diets with peroxidized lipids showed that ADG
was 88.8 ± 12.5% (range = 49.8 to 104.6%), ADFI was 92.5 ± 9.0% (range = 67.8 to 109.8%), and
G:F was 95.7 ± 7.2% (range = 70.4 to 106.3%) relative to animals fed diets with unperoxidized
lipids. The magnitude of reduction from feeding diets with peroxidized lipids relative to diets with
unperoxidized lipids was 11.4 and 11.1% for ADG and 8.8 and 6.6% for ADFI for swine and
poultry, respectively. For swine, ADG correlated negatively with dietary TBARS content (r = 0.63, P = 0.05), but not PV. Conversely, dietary PV correlated negatively with ADG in broilers (r
= - 0.78, P < 0.01), but dietary TBARS concentrations were not reported in any of the 26 broiler
studies included in this review. The difference in magnitude of change for ADG (11.2%) compared
to ADFI (7.5%) suggests that factors in addition to caloric intake contribute to reduced ADG when
feeding peroxidized lipids. For swine and broilers fed peroxidized lipids, serum content of vitamin
E was 53.7 ± 26.3% (range = 15.2 to 105.8%, n = 18) and TBARS was 119.7 ± 23.3% (range =
97.0 to 174.8%, n = 12) relative to animals fed unperoxidized lipids, indicating that inclusion of
peroxidized lipids in diets contributes to changes in metabolic oxidative status. Historically, PV
has been used to assess lipid peroxidation, but TBARS may be a better measure for predicting the
effects of lipid peroxidation on growth in swine. Future research is necessary to develop an
accurate model for predicting reductions in growth performance and metabolic oxidative status
when feeding diets containing peroxidized lipids.
2. Compare lipid peroxidation measures for corn oil subjected to varying thermal
conditions
Lipid peroxidation results in the production and degradation of numerous compounds, but assays
commonly used to evaluate the extent of peroxidation measure a small proportion of these
compounds. Therefore, a study was conducted to compare several indicators of peroxidation when
heating refined corn oil at 185°C for 12 h (RO) or 95°C for 72 h (SO) sampled hourly or at 8 h
intervals, respectively. Air flow was maintained at 12 L/min. Samples were assayed for PUFA,
FFA, peroxide value (PV), anisidine value (AnV), thiobarbituric acid reactive substances
(TBARS), hexanal, 4-hydroxynonenol (HNE), and 2,4-decadienal (DDE). The correlation
procedure of SAS was used to evaluate associations among assays and within assays over time for
each heat treatment. Unperoxidized refined corn oil (0 h) contained 53.9% PUFA, 1.1% FFA, 2.1
meq O2/kg PV, 0.24 AnV, 17.8 mg malondialdehyde eq/kg TBARS, 1.7 ug hexanal/g, 1.1 ug
HNE/mL, and 12.6 uM DDE. Regardless of treatment, PUFA was correlated negatively (r < - 0.9,
P < 0.05), whereas TBARS, hexanal, and HNE were correlated positively (r > 0.6, P < 0.05) with
time. However, FFA was associated positively (r = 0.86, P < 0.01) with time for RO, but not for
SO, and AnV was correlated positively (r = 0.96, P < 0.01) with time for SO, but not for RO.
Peroxide value was correlated negatively (r = - 0.81, P < 0.01) with time for RO, but correlated
positively (r = 0.94, P < 0.01) with time for SO. Regardless of thermal treatment, hexanal (r < 0.9) and HNE (r < - 0.6) were associated negatively (P < 0.05) with PUFA. Anisidine value was
correlated negatively with PUFA (r = - 0.95, P < 0.01) for SO, but not RO. In RO, FFA content
was correlated positively (P < 0.02) with TBARS (r = 0.87), hexanal (r = 0.79), and HNE (r =
0.64), but not for SO. These results indicate that thermal processing and storage conditions should
be considered when selecting indicators of peroxidation, but this information is seldom available.
Peroxide value, AnV, and FFA measurements are variable indicators of peroxidation in oil exposed
to different heating duration and temperatures. However, HNE and hexanal increased with heating
duration and were reflected in PUFA degradation for both RO and SO, indicating that hexanal and
HNE are reliable indicators of peroxidative damage in corn oil regardless of time and temperature
conditions.
3. Determine the impact of antioxidants on lipid peroxidation of dried distillers grains
with solubles and distiller’s corn oil stored in extreme temperature and humidity
conditions
An experiment was conducted to assess indicators of peroxidation in distillers corn oil (DCO) and
dried distillers grains with solubles (DDGS) during storage. Reduced oil-DDGS (RO-DDGS; 5.0
± 0.15% crude fat), high oil DDGS (HO-DDGS; 13.0 ± 0.19% crude fat), and 2 sources of DCO
(DCO-1, 1.2, 0.08, and 0.48% moisture, impurities, and unsaponifiables [MIU]; and DCO-2, 1.2,
0.01, and 0.1% MIU) were obtained. Each ingredient was divided into 18 representative
subsamples (~908 g for DDGS or 2 kg of corn oil). Six subsamples were mixed with either no
supplemental antioxidants (CON), Rendox-CQ® (REN; active ingredient: tertiary butyl
hydroquinone [TBHQ]; Kemin, Industries, Des Moines, IA), or Santoquin-Q4T® (SAN; active
ingredient: ethoxyquin and TBHQ; Novus Intl., St. Louis, MO) for a total of 72 batches. Batches
were formulated to contain 0 (CON), 1,000 mg REN/kg crude fat, or 1,500 mg SAN/kg crude fat.
Three samples of each batch were obtained. One sample was immediately frozen (-20°C) for later
analysis. Two samples were placed in an environmental chamber set to maintain 38°C and 90%
relative humidity (actual = 38.6 ± 0.1°C and 94.0 ± 0.3%), and removed after 14 or 28 d. Peroxide
value (PV), p-anisidine value (AnV), and thiobarbituric acid reactive substances (TBARS) of DCO
and DDGS increased (P < 0.05) from d 14 to 28 of storage. The PV of DCO-1 and HO-DDGS
(12.3 and 12.6 ± 0.3 meq O2/kg oil, respectively) exceeded (P < 0.05) that of DCO-2 or RO-DDGS
(9.6 and 9.3 ± 0.3 meq O2/kg oil, respectively) overall (averaged across d 14 and 28), and on d 14
and 28. Similarly, the TBARS concentration of DCO-2 was less (P < 0.05) than DCO-1, and less
(P < 0.05) for RO-DDGS than HO-DDGS overall and on d 14. The AnV was lower (P < 0.05) in
DCO-1 compared to the other ingredients across sampling days. Concentrations of PV overall, and
on d 14 or 28 declined (P < 0.05) relative to CON by adding either REN or SAN to ingredients.
However, the PV was lower (P < 0.05) overall and on d 14 and 28 for ingredients treated with
REN compared to SAN. On d 14 and 28, the concentration of TBARS and AnV declined (P <
0.05) relative to CON by adding either REN or SAN, but there was no difference between the 2
antioxidants (overall mean = 11.0, 6.1, and 5.9 ± 0.2 mg malondialdehyde eq/kg oil and 6.5, 1.9
and 1.8 ± 0.2, respectively for TBARS and AnV). These results suggest that lipids in DCO and
DDGS peroxidize during 28 d of storage at a high temperature and relative humidity. Based on
these findings, peroxidation of DCO is influenced negatively by MIU content. Antioxidants
effectively impeded peroxidation, but neither antioxidant evaluated completely stabilized the
ingredients in this experiment.
4. Determine the effects of dietary peroxidized corn on growth performance and
antioxidant status of nursery pigs
Two experiments were conducted to assess the impact of increasing dietary levels of peroxidized
corn oil on the growth performance and antioxidant status of nursery pigs. In experiment one, 249
weanling barrows were blocked by initial body BW and assigned to 32 pens. Pens were randomly
assigned to 1 of 4 dietary treatments in a 3-phase feeding program and consisted of control diets
containing no supplemental corn oil, or similar diets containing 2, 4, and 6% of slowly peroxidized
corn oil (SO). Diets were formulated to similar SID Lys:ME ratios. Corn oil was heated for 72 h
at 95°C (air flow rate = 12 L/min) to yield SO (peroxide value [PV] = 134.9 meq O2/kg;
thiobarbituric acid reactive substances [TBARS] = 19.0 mg malondialdehyde [MDA] eq/kg. In
Exp. 2, 128 weanling barrows were blocked by initial BW and randomly assigned to 1 of 32 pens.
Pens were assigned to 1 of 4 dietary treatments in a 3-phase feeding program and contained 9%
unheated oil + 0% rapidly peroxidized corn oil (RO), 6% unheated oil + 3% RO, 3% unheated oil
+ 6% RO, or 0% unheated oil + 9% RO. Therefore, diets were formulated to be isocaloric and
contain equal levels of SID Lys:ME. Corn oil was heated for 12 h at 185°C (air flow rate = 12
L/min) to yield RO (PV = 5.7 meq O2/kg; TBARS = 26.7 mg MDA eq/kg). In both experiments,
diets were fed for 35 d, and ADG, ADFI, G:F, and caloric efficiency (ADG/ME intake) were
determined. Serum was collected on d 0, 14, and 35 from 1 pig per pen that was subsequently
harvested to obtain liver and heart tissue. Serum and liver samples were analyzed for
concentrations of α-tocopherol and Se. In Exp. 1, feeding SO resulted in a linear reduction in ADFI
(P = 0.05), no effect on ADG, and thus, resulted in improved G:F (linear and quadratic; P < 0.01)
with increased dietary SO. However, these responses were likely a result of increasing dietary
energy density with increasing dietary concentrations of SO. Conversely, caloric efficiency
declined by 1.2 to 2.4% (linear; P < 0.04) in pigs fed diets with 2 to 6% SO relative to those fed
diets without SO. In Experiment 2, increasing dietary RO tended to linearly reduce final (d 35)
BW (P = 0.11), ADG (P = 0.10), and reduced G:F (P = 0.03) and caloric efficiency (P = 0.03)
without affecting ADFI. When pigs were fed diets with 3 to 9% RO, caloric efficiency declined
by 2.4 to 4% relative to pigs fed diets without RO (linear; P < 0.03). The α-tocopherol content of
serum declined with increasing dietary concentrations of SO (linear and quadratic; P < 0.03) and
RO (linear and cubic; P < 0.01). These data suggest that SO and RO negatively affect the
efficiency of energy utilization and serum α-tocopherol content of nursery pigs.
Conclusions
Identifying the appropriate laboratory methods to determine the extent of lipid peroxidation
is challenging because no individual measure fully characterizes lipid damage. Furthermore,
connecting these measurements to changes in animal health and growth performance has been a
challenge for nutritionists. Our summary of experimental evidence revealed that feeding
peroxidized lipids to broilers and pigs reduced gain efficiency by an average of 4.3%. Negative
relationships were shown to exist between dietary concentrations of TBARS or PV and ADG for
pigs and broilers, respectively. However, is has been well documented that PV and TBARS
concentrations increase, and then decrease over time during peroxidation, particularly in lipids
exposed to temperatures exceeding 150⁰C (Danowska‐Oziewicz and Karpińska‐Tymoszczyk,
2005; Liu, 2012). Unfortunately, PV was the only measure used to estimate the extent of lipid
peroxidation in some studies (Inoue et al., 1984; Cabel et al., 1988; Lin et al., 1989; Takahashi and
Akiba, 1999; Anjum et al., 2002, 2004; Upton et al., 2009; McGill et al., 2011a,b; Tavárez et al.,
2011) which prohibits assessment of the value of using other measures of lipid peroxidation.
Two experiments were conducted to identify the optimal indictors for lipid peroxidation in
corn oil exposed to varying thermal conditions. We determined that TBARS, hexanal, and 4hydroxynonenol consistently indicated the extent of peroxidation in corn oil exposed to high
(185°C) or low (95°C) temperatures for 12 or 72 h, respectively. Interestingly, PV and AnV
effectively indicated peroxidation in oil exposed to low temperatures, but not at high temperatures.
Therefore, assessment of secondary and tertiary products of peroxidation is more appropriate for
lipids exposed to high temperatures.
We learned that PV, AnV, and TBARS of DCO and DDGS continue to increase throughout
28 days of storage at 38°C with 90% relative humidity. These data suggest that PV, AnV, and
TBARS are reliable indicators of peroxidation under these conditions (≤ 38°C). One of the main
findings of this research was the appropriate selection of indicators of peroxidation depends on
thermal conditions of storage and processing. However, information on historical processing,
storage, and handling conditions is generally not available to feed formulators and nutritionists.
Ultimately, the concentration of secondary products of peroxidation, such as hexanal, 2,4hydroxynonenol, and TBARS, may indicate peroxidation in lipids subjected to either high or low
temperatures. We also learned that 2 commonly used commercial antioxidants (Rendox and
Santoquin), were effective in reducing peroxidation of distiller’s corn oil and DDGS over a 28 day
storage period under hot, humid conditions, but adding antioxidants did not completely stop
peroxidation. This is a significant finding because no other data are available to address concerns
of domestic and import markets on the extent of lipid damage of these co-products, and the
effectiveness of antioxidants, under high temperature and humidity storage conditions. However,
further studies are needed to determine the benefits of using antioxidants to inhibit peroxidation of
these co-products relative to growth performance and health of pigs.
We also conducted experiments to investigate the effects of feeding peroxidized corn oil
on the growth and antioxidant status of pigs. Feeding highly peroxidized DDGS increased the
vitamin E status of nursery pigs, and did not affect growth performance. We speculate that high
levels of dietary sulfur from DDGS increased levels of sulfur-containing antioxidants in vivo,
resulting in a sparing effect on vitamin E. These findings suggest that feeding highly peroxidized
DDGS is not detrimental for nursery pigs if the DDGS source contains high levels of sulfur.
Feeding DDGS to sows reduced the vitamin E status of pigs at weaning, but this effect did not
persist post-weaning when antioxidant deficiency diseases can be an issue. These results indicate
that feeding DDGS is not a concern for the development of metabolic oxidative stress.
To eliminate the confounding influence of dietary sulfur concentrations on lipid
peroxidation effects of corn oil in DDGS, nursery pigs were fed increasing levels of peroxidized
corn oil. Results of this study confirmed findings reported by others that feeding peroxidized lipids
(corn oil) results in reduced growth performance and antioxidant status in nursery pigs. Feeding
slowly heated corn oil reduced the caloric efficiency of nursery pigs from 1.2 to 2.4% with 2 to
6% dietary inclusion. However, feeding rapidly heated corn oil reduced caloric efficiency from
2.4 to 4% with 3 to 9% dietary inclusion. It is unknown if the reduced growth performance during
the nursery phase from feeding peroxidized corn oil may have lasting effects on the growth
performance of pigs to harvest. The difference in magnitude of responses across these 2
experiments suggests that the effects of peroxidized lipids on growth performance depend on the
temperature and duration of thermal exposure. Interestingly, the concentration of TBARS in diets
containing the rapidly heated corn oil was 4-fold that of the slowly heated corn oil. Furthermore,
the concentration of hexanal in diets containing the rapidly heated corn oil was approximately
double that of diets with slowly heated corn oil. These findings indicate that TBARS or hexanal
may be associated negatively with efficiency of nutrient utilization when pigs are fed diets with
peroxidized lipids.
These experiments also uncovered a potential connection between endogenous catabolism
of the amino acid, tryptophan, and peroxidized corn oil that must be further explored. Our
preliminary results suggest that tryptophan catabolism is increased in response to rapidly
peroxidized corn oil, but the practical implications on the availability of tryptophan for protein
synthesis are unclear. Feeding peroxidized corn oil resulted in metabolic oxidative stress,
suggesting that a metabolic antioxidant imbalance contributes to reduced growth and efficiency.
Additional research is need to evaluate if the negative effects of feeding peroxidized corn oil is
ameliorated by adding dietary antioxidants.
Mechanisms underlying the negative effects of peroxidized lipids are not well established.
Inefficiencies in growth performance may result from consequences of altered metabolic oxidative
status (Cabel et al., 1988; McGill et al., 2011b; Tavárez et al., 2011) or altered energy value and
nutrient digestibility (Inoue et al., 1984; Liu and Huang, 1995; Engberg et al., 1996; Yuan et al.,
2007). The information obtained from this study will facilitate future research to better understand
specific mechanisms and develop predictive models of effects of peroxidized lipids on growth
performance, energetic efficiency, and metabolic oxidation status of pigs.
Education, Outreach, and Publications
Abstracts presented and published
Hanson, A.R., P.E. Urriola, L.J. Johnston, S.K. baidoo, C. Chen, B.J. Kerr, and G.C. Shurson.
2014. Evaluation of strategies from minimizing metabolic oxidative stress in nursery pigs fed
diets containing high concentrations of DDGS. MN Ag Expo., January 9, 2014, Mankato, MN.
Hanson, A.R., L. Wang, C. Chen, B. J. Kerr, and G. C. Shurson. 2014. Comparison of lipid
peroxidation measures for corn oil subjected to different heating times and temperatures. J.
Anim. Sci. 91(Suppl. 2):144. (Abstr.)
Hanson, A.R., P. E. Urriola, L. J. Johnston, S.K. Baidoo, C. Chen, B. J. Kerr, and G. C. Shurson.
2014. Dietary peroxidized corn oil reduces growth performance of nursery pigs. J. Anim. Sci.
91(Suppl. 2):39. (Abstr.)
Hanson, A.R., P.E. Urriola, and G.C. Shurson. 2014. Peroxide value (PV) and thiobarbituric
acid reactive substaances (TBARS) as indicators of dietary lipid peroxidation, reduced growth
performance, and metabolic oxidation status when feeding peroxidized lipids to pigs and
broilers. J. Anim. Sci. 91(Suppl. 2):144. (Abstr.)
Hanson, A.R., P.E. Urriola, L.J. Johnston, and G.C. Shurson. 2015. Antioxidants reduce lipid
peroxidation of dried distillers grains with solubles (DDGS) and distillers corn oil (DCO) stored
under high temperature and humidity conditions. Midwest Section ASAS/ADSA, Des Moines,
IA.
Manuscripts in preparation for publication
Hanson, A.R., P.E. Urriola, and G.C. Shurson. 2015. Impact of antioxidants on lipid peroxidation
of distillers dried grains with solubles and distiller’s corn oil in extreme temperature and
humidity conditions. J. Anim. Sci.
Hanson, A.R., and G.C. Shurson. 2015. Peroxidized lipids reduce growth performance and
metabolic oxidative status of pigs and broilers. J. Anim. Sci.
Hanson, A.R., B.J. Kerr, and G.C. Shurson. 2015. Comparison of lipid peroxidation measures for
corn oil subjected to varying thermal conditions. J. Anim. Sci.
Hanson, A.R., P.E. Urriola, L.J. Johnston, C. Chen, and G.C. Shurson. 2015. Dietary peroxidized
corn oil affects growth performance and antioxidant status of nursery pigs. J. Anim. Sci.
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