01996 Applied Poultry Science, Inc.
INTERACTION
BETWEEN
INGESTED
FEED
AND THE DIGESTIVE
SYSTEM IN POULTRY'
M. R. BEDFORD
Finnfeeds International Ltd., Market House, High St. Marlborough,
WWshire, UK SN8 IAA
Phone: + 44 (0)1672 517777
FAX: +44 (0)1672 517778
Primaw Audience: Nutritionists
SUMMARY
INTRODUCTION
The rate and efficiency of growth of the
bird is dependant upon the supply of a continuous, balanced supply of nutrients to its tissues. We attempt to determine the ability of
individual ingredients to supply such nutrients
through use of digestibility experiments and,
by assuming that these abilities (e.g., M E
value) are additive, we are able to calculate
requirements for each nutrient for maximal
growth. The assumption of additivity may be
flawed, however, since the difference between
apparent metabolizable energy (AME, the
1 Presented
parameter we measure in ingredients) and
Net Energy (NE, effectively the parameter
measured in growth trials) is the energy used
for "maintenance," which would have to be
constant for our assumption to be valid. Several observations suggest that this difference is
not constant, however. Therefore, adaptation
of the intestinal tract, which forms part of
the maintenance requirement of the bird, is
one observation which will be covered in the
present paper.
If NE were always a constant proportion
of AME, then intestinal size as a proportion
of metabolic body weight should not alter
at the 1995 Poultry Science Association Informal Poultry Nutrition Symposium:
"Advancements in Diet Modification and Digestion in Poultry."
Symposium
BEDFORD
sig~dkantly
with diet/aging. The ability of the
digestive system to adapt to various stresses is
well documented, however, if not fully understood. It is quite evident that the pancreas, the
primary source of intestinal lumenal enzymes,
is not static in its output since it can alter
enzymatic output in terms of relative and
absolute amounts on a short-term (2 hr) and
medium- to long-term basis in response to diet
changes [l] or simply as a function of aging of
the animal [2, 3). Similarly, the intestine responds in terms of length, weight, absorptive
area, and rate of turnover of enterocytes in
response to changes in diet [4, 5, 61. The
impact of such changes on our ability to predict the feeding value of a particular dietary
regimen is not well understood.
Questions such as variability in cereal
quality only confirm our lack of understanding
of the interaction of many of the parameters at
work in determining the bird’s overall nutrient
extraction. Data will indicate that the classical
measure of energy value, AME, is not always
a good predictor of subsequent bird performance. The objective of this paper is to investigate what changes in the digestive system
may account for these observations.
87
surface area does not reach a mature structure
until 20-30 days of age 1111.The consequences
of these changes in digestive capacity have
been highlighted in recent work by Scott [12],
where faecal AME was determined at 7, 21,
and 35 days of age in five samples of wheat.
The determined values were on average 2637
(at 7 days), 2748 (at 21 days), and 2933 (at
35 days) kcaVkg total diet. This consistent
increase in AME with age is what would be
expected if the digestive system had not
reached optimum nutrient extraction rate for
the reasons suggested above.
The increase in these absolute ME values
with age should not present a problem to modern day feed formulation, provided that the
relative ranking of ingredients did not change
with bird age since the requirements are all
based on a static table of relative values. For
example, maize was always 10% higher in
AME than wheat at all ages. This may not be
the case, however, and has yet to be thoroughly
investigated. But suspicion exists that the viscous grains (rye, oats, barley, triticale, and
wheat) may improve proportionately more
with age than the non-viscous grains (maize,
sorghum, rice).
INDEPENDENT
DIETARY GENOTYPE
Improvements in the genotype of the
FACTORS
CONTRIBUTING
broiler chicken have accounted for a large
proportion of the gains in bird performance
TO CHANGE
AGE
Allometric growth is applicable to the digestive system as it is with any organ. Several
authors have investigated the changes in relative size and/or output of the small intestine,
the pancreas, and other sections of the gastrointestinal tract (GIT) with aging [2,3, 7, 8,9,
101. Whereas there is some disagreement on
the exact point of maturation, it can be concluded that the GIT is potentially immature at
hatch, particularly with respect to digestion of
fat. Several weeks of maturation are required
before the relative size of the small intestine
and output of the pancreas reach a level which
will not constrain growth rate. However, it
has yet to be unequivocally demonstrated
that the rate of growth is indeed constrained
by GIT development. Nevertheless, investigations into the ontogeny of the microscopic
structure of the intestine have shown that in
both broilers and Leghorns, the absorptive
made over the past twenty-five years. Comparisons between broilers and laying hen
strains have indicated that broilers achieve
greater rates of growth of the small intestine
and liver in the first 10-14 days post hatching
[3, 101 although some data suggests that
this situation is reversed as the birds age [lo,
131. In fact, Mitchell and Smith [13] suggested
that one of the reasons for greater efficiency
in modern day broiler lines is due to greater
absorptive efficiency per unit GIT weight,
thereby minimizing the total amount of intestinal tract required, which in turn reduces
maintenance costs and allows for greater feed
efficiency. Even so, Nir et al. [3] claimed that
digestion in the young broiler may be limited
by digestive enzyme production since lumenal
enzyme activities were higher in the Leghorn
(because of much smaller amounts of digesta)
although this finding contrasts with data from
Dunnington and Siege1 [lo], who used two
lines of White Plymouth Rock selected over
88
MEPERFORMANCE RELATIONSHIP
thirty-three generations for high and low body
weight. It seems that in the pancreas enzyme
activities are equivalent if not slightly greater
in the broiler. But once expressed on a relative basis in the small intestine, the differences
between strains are significantlyreduced if not
reversed [3, 101. This result of greater digesta
mass in the broiler probably stems from far
greater feed intake. Nevertheless, the maturation of enterocytes in a broiler strain has been
shown to be more rapid than that in a layer
strain [ll],implying significant benefits in the
efficiency of digestion in broilers compared
with Leghorns. Thus, the overall digestive
capability is greater in the broiler than in
the Leghorn.
Scanning electron micrographs and light
microscopy of the villi surface indicate that
the broiler-type bird has larger and more
numerous villi, a greater density and size of
microvilli, and a faster rate of extrusion of
enterocytes from the villus tip compared to
Leghorns [ll, 131. Calculated villus surface
area in the duodenum, jejunum, and ilea of
a highly selected l i e was found to be significantly greater than that in a relaxed selected or random bred line of broilers [13].
It is interesting to note that the villus surface
area was three times greater in the duodenum
than in the ileum, despite the fact that the
ileum was twice the length and nearly twice
the weight of the duodenum in all lines of bird.
The rate of absorption of alanine into villus
tips has also been shown to be greater in highly
selected than in random-bred lines of broilers
~31.
There is, therefore, a difference in absorptive area and capacity, if not lumenal
enzymatic activity, between genotypes (depending upon the pressures under which
they have been selected) which manifests itself
in terms of better growth rates and feed efficiencies in broilers compared with Leghorns
when they are offered similar diets.
Evidently, for maximum accuracy, digestibility studies should be undertaken with
strains that bear some relationship to the
strains for which the data will subsequently
be applied.
physiological status. Physiological status is
most often overlooked but has an over-riding
effect on the morphology of the gut. Age
effects aside, laying hens, brooding hens, and
pullets, for example, will place different demands on their digestive systems, resulting in
different kinds of impact on their relative
structure.
OTHER FACTORS
Other factors, which undoubtedly aFfect
the digestive system in poultry but which are
beyond the scope of this paper include sexand
DIETARY-DEPENDENT
FACTORS
CONTRIBUTING
TO CHANGE
GENERAL
Nutrient density is known to influence
both pancreatic output and the size of the
intestinal tract [lo]. The use of a high as opposed to a low nutrient density diet (in which
both energy and protein/amino acid specifications were modulated in concert) resulted in a
16% reduction in GIT size [lo]. Since it is
recognized that the duodenal mucosa has an
extremely high oxygen requirement (7 times
that of the animal as a whole [14]), it is easy to
conclude that maintainingthe rate of digestion
with a smaller GIT will enable a greater proportion of absorbed energy to be utilized for
carcass accretion. The focus of this paper is,
however, not on nutrients but on ingredients
and the problems they may introduce to the
digestive tract.
While it is well known that a variety of
ingredients have profound and specific direct
effects on the digestive system (e.g. raw soybeans, rapeseed, beandpeas) due to the presence of various antinutritive factors (trypsin
inhibitors, lectins, tannins, etc.), it is not the
intention of this paper to cover this area. In
fact, several recent papers go into far greater
detail than is possible here [15, 161. A great
proportion of the problems described in these
papers come from heat labile compounds
which are mostly inactivated in normal feed
ingredient processing. It is the intention of
this paper to concentrate on more practically
relevant factors which apply to typical finished
feed, and which emanate principally from the
fiber component of the diet.
INGREDIENT VARIABILITY
Generally, it would be expected that given
a consistent bird age, sex, and physiological
status, the measurement of digestibility of a
diet should allow for an accurate prediction of
Symposium
89
BEDFORD
its feeding value. Although ileal digestibility
values of amino acids often allow for accurate
predictions of performance [17,there are well
documented failures of this measure [18, 191
with heat-processed protein supplements.
Similar problems with the AME procedure
have been highhghted by the work of Rose and
Bedford [20], who indicated that the determined AME of six samples of wheat did not
predict the subsequent performance of birds
fed these same wheats in a standard diet base
(Table 1). A review of the literature by the
same authors indicated that in three previous
publications where both AME and growth
trials had been performed on the same
samples of wheat (in a total of five experiments), no correlations between AME and
feed conversion ratio (FCR) or gain were
found.
Explanationsfor such poor correlationsin
these trials probably lies with the characteristics of what are commonly becoming known as
the viscous grains, i.e. rye, barley, oats,
triticale, and wheat in order of descending
viscosity. The viscous grains are known to increase the viscosity of the intestinal contents.
This condition reduces nutrient diffusion
(increasing solution viscosity from 1 to 5 CP
decreases the rate of diffusion of bradykinin,
Mwt 1000, by 40% [21]) and hence absorption
rate, thereby limitingbird performance [21,22,
231. Ranges in intestinal viscosity observed in
a total of fifty experiments conducted between
1992and 1994in diets based on60-65% cereal
inclusion rate appear in Table 2.
Intestinal viscosity is generally influenced by:
1. Grain inclusion level - The greater the
inclusion level, the greater the intestinal
viscosity, the relationship being exponential [23,24]
2. Grain genotype and environment in
which it is grown [20,25]
3. Processing of the diet - Pelleting tends
to increase intestinal viscosity [%I
4. Age of bird - The older the bird, the
lower the measured viscosity [27]
Reduced rates of diffusion alone would
not lead to a poor AMEFCR correlation, but
when the effects of intestinal viscosity on intestinal physiology and on the endogenous
microflora are considered, these changes can
account for a large part of the discrepancy
observed above.
TABLE 1. Relationship between determined diet
AME and FCR
WHEAT
SAMPLE
1
WHOLE
DIETAME
1
FCR
MJ/kg Fresh
Weight
1
GAIN^
g/MJ Intake
Tonic
1258
1.338
59.41
Hussar
12.81
1.236
63.16
Beaver
12.72
1.306
60.20
Alexandria
12.46
1.292
62.12
Estica
12.92
1.344
57.59
Mixed
13.00
1.325
58.06
TABLE 2. Mean, minimum, and maximum intestinal
viscosities (cP) determined in 21-day old broilers by
the method of Bedford and Classen [28]
CHANGES IN INTESTINAL PHYSIOLOGY
Feeding diets based on viscous grains results in signiticant increases in the relative size
of the digestive tract [6,291. Reduction of intestinal viscosity through use of the relevant
exogenous enzymes has been shown to reduce
relative weights and length of the crop, gizzard, proventriculus, duodenum,jejunum, and
ileum [6] in barley and wheat-fed birds, although the effect in wheat-fed birds was far
less dramatic. The performance of birds fed
either grain was improved with enzyme supplementation.
ALmirall et al. [30] determined that pancreas mass was greatest in broilers fed a
diet based on a high viscosity barley, less in
those fed a low viscosity barley, and even
less in broilers (21 days) offered a maizebased control. Reduction of viscosity through
use of a /3-glucanase reduced pancreatic size
in both barley-fed groups to maize control
levels. Ileal digestibility of protein, starch,
and fat were improved to equal that of the
maize control by /3-glucanase addition to
90
both barley diets, despite the reduction in
pancreas weight. Interestingly, the same
diets were offered to l-year-old Leghorn-type
birds. These proved to be almost inert to
dietary changes, demonstrating further the
ageigenotype differences discussed earlier.
As intestinal viscosity increases, the rate
of digestion would be expected to decrease,
a situation which would result in the bird’s
perceiving a lower nutrient density diet. The
response to this condition includes increased
intestinal mass and pancreatic size. Presumably gross changes in intestinal size require
greater extremes in viscosity to become apparent. Certainly changes in pancreatic size seem
to more dramatic and sensitive in both wheat
and barley-fed birds, indicating that enzyme
output is modulated before changes in size
of the digestive tract [6]. The sensitivity of
the pancreas to increased arabinoxylans was
confirmed by Anghanaporn et al. [31], who
observed that the addition of graded levels
of wheat arabinoxylans to a synthetic diet resulted first in the increased loss of endogenous
nitrogen followed by a reduction in true protein digestibility at the extremes of addition.
Thus, one of the first responses to increased
viscosity is not a reduction in true digestibility
due to poorer kinetics, but a greater endogenous loss due to attempts of the bird to overcome such poor kinetics. At higher and higher
viscosities even these attempts are overwhelmed and diffusional constraints will slow
down digestion as a whole.
Structure as well as gross size seem to be
affected by intestinal environment. Viscous
gums have been shown to increase stomach
size and intestinal length in rats and decrease the density of crypts and villi, but these
gums increase the rates of enterocyte division
by 80% [32, 331. Similar results have been
seen in rye-fed chicks, for which the rate of
enterocyte turnover was significantly increased compared to maize-fed controls, and
the addition of a xylanase reduced turnover
to almost equivalent levels as the control [34].
Similarly, reductions in crypt depth and
villi height have been observed in barley-fed
chicks (compared with corn), a situation which
is reversed on j?-glucanase supplementation
[B].
The mechanism by which these changes
are brought about may well involve microbial
interaction and are discussed in the next
section.
AMEPERFORMANCE RELATIONSHIP
Viscous gums have also been shown to
increase transit time in chickens [35, 361, directly reduce amylase activity in the stomach
of pigs [37l, decrease the rate of gastric emptying [32], and delay the rate and kinetics of
sugar absorption [32, 331. In addition to the
soluble fibre effects, the insoluble fibre fractions can have direct and indirect effects on
digestive function. Several authors have reported that cellulose has an inhibitory effect
in vitro [38] on the activity of lipase and proteases from the pancreas; this finding is borne
out by in vivo data. Almirall et al. [30] showed
that lumenal activities of amylase and lipase
were depressed with barley compared to
maize-based diets. The availability of bile
acids for lipase is certainly compromised by
both insoluble and soluble fibers [38]. The
addition of varying levels of grass has been
shown to increase the mass of the intestines in
chickens signifcantly [39],while increasing dietary fiber levels has been shown to increase
cellular proliferation in both the colon and
small intestine of rats [4].
There are also data to suggest that soluble,
indigestible oligosaccharides (from lupins)
have a profound effect on the digestive system,
increasing the mass of the crop and duodenum
significantly [MI.
Taken as a whole, the dietary-dependent
factors presented in this paper indicate that
there is very likely a microbial interaction in
many of these observations, since the effects
observed are very much associated with fermentable materials. Many of the negative effects of rye and barley, for example, are
overcome when the diets are supplemented
with an antibiotic [41,42,43,44]which further
proposes a bacterial interaction. This interaction is discussed below.
MICROFLORAL IMPLICATIONS
The ingested feed can significantly influence the bacterial populations by either providing fermentable materials, i e . substrate, or
changing the environment in which they live,
e.g. increasing viscosity. Increasing viscosity is
known to reduce mixing and feed passage rate
[35,36] which would presumably decrease lumenal oxygenation and allow for increased
bacterial reproduction due to increased residence time. The bacterial population in the
intestine can have an effect on the efficiency of
host digestion by one of three mechanisms:
Symposium
BEDFORD
1. InvasionlDisease: Disease will inevitably alter the energy status of the bird, which
mounts an immune response to defend itself,
thereby increasingmaintenance costs and subsequently reducing feed efficiency. Interestingly, there is evidence that ingestion of some
ingredients predisposes the bud to certain
diseases: wheat and necrotic enteritis [45];
wheat and coccidiosis [&I; barley and necrotic
enteritis [47) Mechanisms for such relationships have yet to be proposed, but may be
linked with viscosity of the intestinal contents.
2. Competitionfor ResourceslProvision of
Resources: Evidence for the energy costs of a
gut microflora comes from work with conventional vs. germ-free chicks. In an experiment
using Leghorn-type chicks from 0-15 days of
age, Muramatsu et al. [ a ] determined that
while the conventional chicks on average extracted more than 1MJ extra energy from a
semi-synthetic diet, their rate of growth was
almost 10% less than that of the equivalent
germ-free chicks. These data suggest that
under these conditions, the microflora was
accounting for at least 1 MJ of dietary AME
(8% of total) and probably more (since the
growth rate of the conventional chicks was
poorer). In older birds with a more numerous
and mature bacterial flora [49], these effects
would be considerably greater, particularly
when a commercial diet containing considerably more fermentable substrates is offered.
More dramatic and perhaps more relevant to this paper is the work described by
Choct et al. [50] in which a sorghum-based
control diet was offered to broilers from 4-28
days of age with and without supplementation
with isolated wheat arabinoxylans, the known
viscous agent in wheat. The arabinoxylansupplemented diet was fed in either the presence or absence of a xylanase-based enzyme.
Gain and FCR were significantly depressed
with inclusion of the arabinoxylan; both were
restored to control levels when the xylanase
accompanied the arabinoxylan. The most
interesting finding of this work, however,
was that the inclusion of the arabinoxylan
dramatically increased total ileal volatile fatty
acid (VFA) levels nearly fifteen-fold. In contrast, the addition of the xylanase brought levels back to control values. No effect of the
arabinoxylan appeared on caecal fermentation, but addition of the enzyme increased
caecal VFA levels three-fold. Gain per MJ
91
intake was 3% poorer with inclusion of the
arabinoxylan, probably reflecting the energy
cost of the additional microflora and suspected increase in intestinal size/digestive
activity.Addition of the xylanase, however, not
only increased AME and improved FCR but
also improved gai4/1w by almost 10% compared to the sorghum control. Since the sorghum control and xylanase-supplemented
diets were of similar intestinal viscosity and
AME, diffusional constraints would be similar, suggesting that either significantly less
energywas being used to digest and absorb the
nutrients in the xylanase-supplemented diet or
the nutrients in the xylanase-supplemented
diet were absorbed in a fashion more balanced
for growth.
Bacteria can also provide resources by
fermentation of indigestible components and
supply of utilizable sugardacids to the bird.
Certainly the data of Choct et al. [50]indicates
considerable caecal fermentation of what
would presumably have been unavailable material. Further, there is good evidence that in
rats resistant starch, another source of fiber, is
poorly digested but readily fermented [51].
Ideally, the bird should extract as much of
the nutrients as it can before the small intestinal bacteria - which increase in numbers in the
duodenum,jejunum, and ileum, respectivelyare exposed to the digesta. The slower the rate
of host digestion, the greater the opportunity
for ingested nutrients to be metabolized by
bacteria. The kinetics of digestion are therefore of great importance. It is interesting to
note that an estimated 85% of all nutrients
digested in the small intestine are digested by
the mid-jejunum [ a ] . Intestinal viscosity has a
signifcant effect on rate of digestion, and this
ability can markedly influence the partitioning
of energy between the bird and the microflora.
Although intestinal viscosity is known to decrease with age [27], this tendency is offset by
the markedly greater bacterial colonization of
the gut by bacteria in the older bird [ll], which
can take advantage of the viscous environment. The net result is that reduction of viscosity is of greater significance in terms of FCR
improvements in the older bird [21], despite
the fact that intestinalviscosityis alreadylower
than that in the young bird [27].
3. Secondary Effects of Metabolites:
The fermentation of substrates by bacteria
may result in the production of many
92
MEPERFORMANCE RELATIONSHIP
metabolites/products which may directly or
indirectly affect the digestive system. These
metabolites include biogenic amines (particularly polyamines) and short chain fatty acids,
while the products include enzymes. Feighner
and Dashkevicz [43] demonstrated that feeding rye-based diets si&icantly increased the
production of cholyltaurine hydrolase, which
deconjugates bile acids, directly influencing
the digestion of fats and also producing secondary bile acids which have been implicated
as carcinogens.
Rye-based diets and isolated wheat
arabinoxylans have been shown to increase the
concentration of short chain fatty acids in the
lumen of the intestine significantly [34,50,52].
These fatty acids are themselves signals for
increased mucosal growth [53, 54,551. These
acids can also reduce the pH of the gut [56].
In fact, feeding a viscous cellulose has been
shown to result in decreased pH in the small
intestine of chicks [36]. The pH change in
itself can have profound negative effects on
pancreatic secretion as documented by
Garcia et al. [57.
Polyamines, which are produced by lumenal bacteria, have been shown to directly increase the small intestinal and colonicmucosal
growth rate [58, 591, and their concentration
has been shown to increase considerablywhen
bacterial numbers have increased due to colonic obstruction, for example [58].
The fact that conventional chicks have
significantly heavier intestines than the
equivalent germ-free counterparts bears out
the effect of bacteria on the digestive system
for example, the bird is coping well, then stimulating intestinal growth unnecessarily will
only increase maintenance costs and thereby
reduce feed efficiency.
F31.
Whether such effects of the metabolites
are beneficial or detrimental depends very
much upon the status of the intestinal tract. If,
IMPLICATIONS
FOR
POULTRY
NUTRITION
Current digestibility trials rely on the assumption that the energy required for digestion is a constant and that the proportion of
energy extracted from a ration during its passage through the intestine by the bird is a
constant. The evidence is building up that in
the case of the viscous grains this hypothesis
may not necessarilybe true, with the result that
AME and FCR, for example, do not always
correlate.
The fact that bacterial populations and/or
intestinal development in response to the
dietary ingredients are responsible for such
lack of correlation suggests that rapid energy
evaluation procedures may be inappropriate,
since both the microflora and intestine will
adapt over a period of several days to a change
in diet. Indeed, results from ileal cannulated
roosters fed a corn-based diet and then rapidly
changed to a barley-based diet (Table 3)
confiim that adaptation of the intestines to
the new diet as judged by viscosity alone can
take as long as three days. Presumably the
reduction of viscosity with time after switching
to the barley-based diet is the result of microfloral acclimation, some species of which
(lactobacilli) are suspected of producing
p-glucanases.
TME in particular would ignore these
adaptive changes and therefore potentially
offer misleading results. Even more long-term
M E tests will not differentiate between en-
TABLE 3. Effect of sudden diet change on water and feed intake and ileal viscosity in cannulated roosters
_ _ _ _ ~ ~
Symposium
BEDFORD
93
ergy utilized by the bacteridextra intestinal
mass and energy accreted into tissues.
Further, the inclusion rate has been identified as an impacting factor on the determined
AME of wheat [29]. Many AME/TME procedures utilize high inclusion rates of the test
ingredient ( > 80% to 100% in TME) in order
to minimize the effects of the diluent, yet the
determined ME values are applied to diets
which rarely see greater than 65% inclusion of
any cereal. McCracken et al. [24] determined
the average AME of two samples of wheat to
be 14.8, 14.4, and 13.9 MJIkg when included
in the test diet at 65%, 72%, and 80%, respectively. The accompanying intestinal viscosity
values were 7.5,10.6, and 25.9 cP, respectively.
Thus, the whole procedure may not be particularly accurate for determining the feeding
value of viscous grains. Performance data, particularly FCR data, should probably always
accompanyAME data if the true feedingvalue
is to be determined.
CONCLUSIONS
AND APPLICATIONS
1. The response of the intestines and its gut-associated microflora to feed related and
unrelated factors has significant implications for one of the most commonly used tools in
ingredient evaluation, viz.the AME/TME procedure. The use of older birds for prediction
of AME for young birds, for example, is evidently incorrect when physiological data are
reviewed. Practical data also support this statement.
2. Very rarely are AME determinations concomitantlyrun with performance trials.When they
are, they tend not to give the consistencythat would be expected, particularly with viscous
grains. Several hypotheses as to why this finding may occur have been presented. Ideally,
AME, and any digestibility parameter for that matter, should be backed up with supporting
performance data. Certainly where viscous grains are concerned, the consequences of
relying on AME alone could be dramatic.
REFERENCES
AND NOTES
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1AO. Personal communication.
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