01996Applied Poulhy Science, Inr
EXCESS
DIETARY
COPPER
TRIGGERS
ENLARGEMENT
OF THE PROVENTRICULUS
IN BROILERS'
R. E WIDEMAN, JR?, Y. KOCHERA I
U
m
,T.L.BARTON, and D. CLARK
Department of Poultty Science, Universityof Ark-ansas, Fayetteville,AR 72703
Phone: (Sol) 575-4397
F M : (501) 575-3026
G. R. BAYYARI, W. E. HUFF,and I? A. MOORE, J R .
USDA,Agricultural Research Service, Poultry Production and Product S.fety Unit,
Universityof Arkansas, Fayetteville,AR 72703
I! A. DUNN
Department of VeterinatyScience, The Pennsylvania State University, UniversityPark, PA 16802
~~
Primary Audience: Nutritionists, Processors, Veterinarians
DEsCRlrPnoN
OF
The proventriculusserves as theglandular
stomach of birds. Compound glandswithin the
wall of the proventriculus secrete gastricjuice
composed of hydrochloric acid and the digestive enzyme pepsin. Specialized cells adjacent
to the inner (luminal) surface of the proventriculus produce a protective layer of mucus.
Gastric juice passes from the compound
Published as ArkansasAgriculturalExperiment Stationmanuscript No.96003with the approval
of the Experiment Station Director.
2 Address correspondence to: R.F. Wideman, Jr., 0-402Poultry Science Center, Dept. of
Poultry Science, University of Arkansas,Fayetteville, AR 72701
1
220
COPPER AND THE PROVENTRICULUS
glands into the lumen of the proventriculus
through ducts that empty through orifices in
prominent papillae protruding through the
mucus layer. Periodic contractions by the circular layer of muscle comprisingthe outer wall
of the proventriculus mix the gastricjuice with
feed and propel the mixture through a narrow
gastric isthmus connecting the proventriculus
to the gizzard. [l,2,3,4].
Proventriculitis occurs sporadically in
broilers. This syndrome includes a characteristic enlargement and dilation of the proventriculus and gastric isthmus. The walls of
the distended proventriculus become thin
and flaccid. In extreme cases, the grossly
dilated proventriculus may appear to merge
directly with the gizzard, without any evidence
of an intervening narrowing in the gastric
isthmus region. Congested secretory glands
initially appear as focal or aggregated white
"plaques" on the outer surface of an affected
proventriculus, but as widespread glandular
congestion progresses, the proventriculus
develops an overall pale and mottled external
appearance. Internally, the luminal papillae
become flattened and irregularly dispersed,
and a thick gelatinous layer of mucus may
coat the luminal surface. These changes
apparently reflect partial inhibition of
proventricular muscle tone, motility, and
glandular secretion, causing the upper gastrointestinal tract to remain engorged with feed
for over 8 hr after feed withdrawal. Affected
broilers arrive at the processing plant with
the crop, proventriculus, and gastric isthmus
distended with fluid and feed, leading to
carcass contamination when automatic
eviscerators tear the crop, proventriculus, or
gastric isthmus.
Necropsies performed on randomly
selected broilers grown under commercial
conditions in four broiler houses on a research
farm operated by the University of Arkansas,
recently revealed a high incidence of this
syndrome. In two of the houses, 20 to 40%
of the broilers exhibited proventriculitis at
2 and 3 wk of age, whereas no obviously
affected birds were found in the remaining
two houses. The chicks in all four houses had
been hatched in the same hatchery and had
been delivered to the farm at the same time.
The two highly affected broiler houses (houses
A and D) had been supplied with starter feed
from one commercial feed mill, whereas the
two apparently unaffected houses (houses B
and C) had been supplied with starter feed
formulated to similar specifications but mixed
by a second commercial feed mill. Feed from
the bin supplying each house was saved to
evaluate the responses of broiler chicks to
these feeds under controlled experimental
conditions.
MATERIALS
AND METHODS
EXPERIMENT 1: EVALUATION OF
SUSPECT FEED
W o hundred twenty male Cobb-500
chicks were wing banded, weighed, and
divided into five diet treatment groups of 44
birds each. Eighty-three chicks, including all
obvious culls, were weighed and necropsied
immediately after delivery from the hatchery.
The diet treatments consisted of starter feed
saved from each of the four broiler houses
("suspect" feeds diets A and D; apparently
unaffected feeds: diets B and C) plus a control
milo-soybean meal-based feed prepared at the
University of Arkansas Poultry Feed Mill. The
milo-soybean meal-based feed was formulated
to match the specifications of the commercial
starter feeds (approximately 21.5% protein,
3150 kcaVkg ME) without including animal
by-products.
The birds were reared in a Petersime
battery (11 birds per compartment; 4 compartment replicates per diet treatment) using
standard brooding temperatures and lighting
schedules. Feed and water were available
ad libitum. Buds received test diets during
the first 2 wk, and thereafter all treatment
groups received the control feed until they
reached 4 wk of age. On days 7, 14,21, and
28, two or three chicks were taken from
each compartment of the battery (a total of
10 chicks per diet treatment per necropsy
session) and placed in a common bin to
preclude treatment identification during the
subjective scoring phase of the necropsies.
The chicks were killed by cervical dislocation
and weighed. The proventriculus, gizzard,
liver, kidneys, spleen, pancreas, bursa, heart,
and a 10 cm length of the descending Limb
of the duodenum were then dissected, rinsed
thoroughly, blotted to remove surface moisture, and weighed. Proventriculi received
scores of 0 (unaffected), 1 (early changes
suspected), or 2 or 3 (obviously affected)
for the following criteria: enlargement or
Research Report
WIDEMAN et al.
dilation; incidence of serosal plaques; flattening or irregular dispersal of mucosal papillae; flaccidity or loss of muscle tone; and
dilation of the gastric isthmus. After fresh
organ weights were recorded, the proventriculus and gizzard were dried to constant
weight in a forced-air convection oven at
80°C, and the percent dry weight was calculated as an index of tissue fluid accumulation.
Dried affected and unaffected proventriculi
from the day 14 necropsy were analyzed for
Cu content [q. The strength of the 10 cm
length of intestine was measured [6] as described by Huff et al. [A.Novus International,
Inc. [8] performed proximate analysis and
determination of Cu levels on feed samples.
EXPERIMENT 2: EVALUATION O F
DIETARY COPPER SULFATE
To evaluate the impact of various levels
of dietary CuSO4 or energy source on the
proventriculus, the control milo-soybean
meal-based starter diet was formulated with
poultry fat (PF) or corn oil (CO) as an energy
source, and with 0, 2, 4, or 6 lb/ton CuSO4,
yielding the following diet treatment groups:
(A) PF + 0 Cu added in micro mineral mix
and 0 Cu added as CuSO4; (B) PF + 0 Cu
added as CuSO4; (C) CO + 0 CuSO4;
(D) PF + 2 lb/ton CuS04:250 ppm Cu;
(E) P F + 4 lb/ton CuS04:500 ppm Cu;
(F) CO + 4 lb/ton CuSO4; and (G) PF +
6 lb/ton CuS04:750 pprn Cu. Diets B-G all
had small amounts of Cu included with the
vitamin-mineral mix. These diets were fed for
4 wk to treatment groups of 100 Cobb-500
male chicks reared on fresh wood shavings
litter in floor pens. 'benty birds per diet treatment were necropsied at 2,3, and 4 wk of age
using a protocol that concealed their treatment identities until after completion of the
necropsies. We qualitatively evaluated proventriculi for enlargement, the incidence of
plaques, and flattening or dispersal of the
luminal papillae as described above; body
weights and organ weights, however were not
recorded. To a n a l p data, we applied the
General Linear Models (GLM) procedure
with nkey's Studentized Range (HSD) Test
option in SM" [9]. Statements regarding statistical sigoifcance are based on a probability
of P 5.05.
221
RESULTS
AND DISCUSSION
EXPERIMENT 1
Of the 83 chicks necropsied at 1 day of
age, three chicks exhibited mild proventricular
dilation or loss of tone. Solitary white opaque
plaques approximately 0.5 to 1mm in diameter were visible on the outer surface of the
proventriculus in 10 chicks. Subsequent evaluations of chicks from seven breeder flocks
demonstrated an incidence of plaques varying
between 2 and 12%.A similar variability in the
incidence of plaques occurred in consecutive
hatches of chicks from the same breeder flock.
The incidence of plaques and an overall pale
mottled external appearance of the proventriculus increased dramatically in chicks when
feed but not water was withheld for 3 days
after hatch. Providing feed to these chicks
restored an entirely normal proventricular appearance within 2 wk. Microscopic examinations indicated that the focal plaques were not
infiltrated with lymphocytes in excess of the
normal lymphocytic distribution observed in
apparently normal proventriculi. When combined, these observations raise the possibility
that plaques can develop when inactive secretory glands become congested with secretory
products and cellular debris. Such plaques
may develop primarily in chicks that hatch
early and do not have access to feed for a
prolonged period.
Compared to the groups fed the control
diet or "unaffected diets B and C, groups
fed 'lsuspect" diets A and D developed significantly higher percentages of obviously
affected proventriculi within 2 wk, as assessed qualitatively by proventricular enlargement (Figure lA), the incidence of
plaques (Figure lB), flattening and dispersal
of the mucosal papillae (Figure 2A), loss of
proventricular tone (Figure 2B), and gastric
isthmus dilation (data not shown). After all
broilers were switched to the control feed
during weeks 3 and 4 of the trial, the incidence
of proventricular symptoms in groups fed
diets A and D declined to levels similar to
those of the groups fed the control diet or
diets B and C. A low but consistent incidence
of obvious proventriculitis occurred throughout the study in broilers consumingthe control
JAPR
COPPER A N D THE PROVENTRICULUS
222
Figure 1A
a
4
A
nn
Figure 1B
100
80
0
0
7
14
21
28
Day of Age
FIGURE 1. Percentagesof broilers during weekly necropsies in Experiment 1 having an affected proventriculus
as assessed by: (A) obvious proventricular enlargement and (B) moderate to dense distributions of plaques
(congested secretory glands) visible on the outer (serosal) surface of the proventriculusmalues with different
letters within the same day of age are significantly different, Ps.05, from each other as determined by Wilcoxian
rank-sum comparisons).
Research Report
223
WIDEMAN et al.
~~
*
Figure 2A
control ~ i e t
DietA
Diet B
f DietC
Dlet D
loo
1
80
60
40
20
It--
0
I
0
7
All on Control Diet
1-
1
I
I
14
21
28
Day of Age
+
*
A
Figure 2B
Contml Diel
DelA
Diet 8
f Diet C
A
1
loo
DEtD
I
0
7
14
21
28
Day of Age
FIGURE 2. Percentage of broilers during weekly necropsies in Experiment 1 having an obviusly affected
proventriculus as assessed by: (A) flattened or irregularly distributed papillary orifices and/or a thick mucus
layer on the inner (luminal) surface of the proventriculus and (B) loss of proventricular tone v a l u e s with
different letters within the same day of age are significantly, Ps.05, from each other as determined by Wilcoxian
rank-sum comparisons).
224
COPPER A N D THE PROVENTRICULUS
diet and diets B and C, and this incidence
did not spontaneously diminish during weeks
3 and 4 of the trial.
Body weights and organ weights at 14 days
of age during the peak of the diet-induced
proventriculitis are shown in Table 1. Diet D
increased the fresh weight of the proventriculus and decreased the percentage dry weight,
indicating that a significant portion of the proventricular enlargement was associated with
fluid accumulation (Table 1). At the same
time, diet A increased kidney weights and reduced intestine weights. Pooling these data to
compare all buds receiving entirely normal
proventricular scores (Pooled Normal) vs. all
birds with an obviously affected proventriculus (Pooled Affected scores of 2 to 3 for three
or more categories) independent of the diet
treatments showed that affected birds had a
higher proventriculus fresh weight, a lower
proventriculus percentage dry weight, and
heavier kidneys (Table 2). Despite gizzard
DI~TREATMENTS
PARAMETER
MEASURED
Controt
I
A
I
B
I
C
I
D
TABLE 2. Comparison of data pooled, independent of diet treatment, from all broilers evaluated as having an
entirely normal proventriculus or from all broilers having an obviously affected proventriculusat 14 days of age
in Experiment 1 (values are shown as the mean+SEM)
Research Report
WIDEMAN et al.
erosion and occasional perforation of the
gizzard lining in broilers fed all of the commercial starter diets, there were no diet-related
(Table 1) or proventriculitis-related (Table 2)
influences on gizzard fresh or percentage dry
weight, nor were gizzard erosions or perforations consistently associated with obviously
affected proventriculi. The most severely
affected proventriculi had a thick luminal
layer of mucus, and applying pressure to the
serosal surface of congested secretory glands
caused copious quantities of fluid to flow
through the luminal papillae.
Table 3 shows body and organ weights at
28 days of age, after all groups had consumed
the control feed for at least 2 wk. No consistent trends differentiated the diet treatment
groups. Comparing all birds having normal
proventriculi (Pooled Normal) to all birds
having obviously affected proventriculi
(Pooled Affected) independent of the diet
treatments showed that affected birds had
higher body weights, proventriculus fresh
weights, gizzard and liver weights, and a lower
percentage dry weight for the proventriculus
(Table 4). Comparison of Pooled Normal and
Pooled Affected buds over the course of
the entire experiment revealed that only the
proventriculus was consistently affected
(Table 5 ) . Otherwise, broilers with proventriculitis had heavier kidney weights at 7
225
and 14 days of age, and heavier liver and
gizzard weights at 21 and 28 days of age. There
were no consistent effects of proventriculitis
on body weight or other organ weights, and
the strength of the duodenum was unaffected
(Table 5).
Feed analysis indicated that the suspect
diets A and D contained 264 and 259 ppm Cu
respectively, whereas the control diet and
diets B and C contained 17,191, and 118 pprn
Cu respectively. Dietary fiber was 2.16 and
2.12% in diets A and D, and 1.76, 1.64, and
1.68%in the control diet and diets B and C.
The diet-induced incidence of proventriculitis
did not appear to be consistently associated
with calcium (range: 1.01 to 1.16%), total
phosphorus (range: 0.74 to 0.87%), selenium
( e 1 ppm), 4 or 24 hr AOM (range: 54 to
196 meq/kg fat), initial peroxide value
(range: 0.1 to 1.4 meqkg fat), crude protein
(range: m.3 to 22.7%), fat (range: 7.39 to
8.83%), or the amino acid profile (lysine: 1.12
to 1.27%;methionine: 0.33 to 0.37%; cystine:
0.34 to 0.39%). Proventriculi collected on
day 14 from six obviously affected broilers
(diets A and D) and six unaffected broiIers
(control diet, diets B and C) were analyzed
for Cu. Affectedproventriculi contained Cu at
20 to 75 ppm dry matter (mean: 48.5+9 pprn),
whereas normal proventriculi contained Cu at
4 to 12 ppm dry matter (mean: 7.2&1ppm).
TABLE 3. Body and organ weights at 28 days of age in Experiment 1 (values are shown as the mean+SEM)
MEASURED
JAPR
COPPER AND THE PROVENTRICULUS
226
Pancreas, g
3.0020.13
2.7120.22
7.29k0.21
3.2220.13
Bursa,g
Heart, g
Intestine, g
3.0820.13
25420.13
7.95k0.29
35420.11
TABLE 5. Presence or absence of significant differences for comparison of data pooled, independent of diet
treatment, from all broilers having an entirely normal proventriculusvs. all broilers having an obviously affected
proventriculus during Experiment 1 (NS = Not signficant; Ps.05: significant)
Intestine weight
Intestine strength
NS
NS
NS
NS
0.0105
NS
NS
NS
Research Report
WIDEMAN et al.
EXPERIMENT 2
The results of the first experiment, coupled with previous evidence that dietary Cu
exceeding 200 ppm can trigger proventricular
enlargement and gizzard erosions [lo, 11, 12,
131, strongly implicated high dietary Cu levels
as at least one factor capable of triggering
or amplifying broiler proventriculitis. Adding copper sulfate to feed at approximately
2 lb/ton yields Cu levels calculated at 240 to
250 ppm, depending on the purity and state
of hydration of the CuSO4. In the second
experiment, regardless of the energy source,
diets containing 2 2 lb/ton CuSO4 caused
significant increases in proventricular size
(Figure 3A), an increased incidence of
plaques (week 2, Figure 3B), and flattening
or dispersal of the mucosal papillae (data
not shown) during one or more of the
necropsy periods. Diets supplemented
with 1 4 Ib/ton CuSO4 also caused a thick
gelatinous layer of mucus to accumulate on
the luminal surface of the proventriculus. All
of these Cu-induced changes in proventricular
morphology are similar to those previously
observed by Jensen and Maurice [12]. No
proventricular differences attributable to the
use of corn oil or poultry fat as an energy
source occurred in this experiment. These observations clearly demonstrate that dietary Cu
levels above 200 pprn can directly amplify all
of the gross lesions commonly associated with
proventriculitis. Subsequent to these observations, field trials conducted by a commercial
integrator also implicated dietary CuSO4 in
excess of 200 pprn as an amplifer of proventriculitis. In some cases, feeds formulated
to contain Cu at 250 pprn were assayed to
contain 160 to 3u) ppm Cu,apparently due to
variability in feed mixing. A similar degree
of variability in Cu content occurred in the
"suspect"and "unaffected"feeds in the present
study, providing a probable explanation for
flock-to-flock differences in the incidence of
proventriculitis in broiler complexes where
all flocks consume feedfornuluted to contain
250 ppm Cu.
Dietary Cu levels clearly should be
evaluated during commercial outbreaks of
proventriculitis in broilers. Copper may
accumulate in and alter the function of the
proventriculus as a secondary consequence of
the substantial absorption of Cu across the
proventricular mucosa [141. Similarly, the
227
gizzard lining binds large quantities of Cu
[14, q,providing a biological basis for the
discoloration and erosion of the gizzard lining
commonly associated with excess dietary Cu
[lo, 11,12,13,15]. In addition to the Cu provided in feed, Cu also is present in drinking
water supplements intended to treat fungal
disorders of the upper gastrointestinal tract
[16,171.Such treatments may be inappropriate
if the gastrointestinal disorders include
proventriculitis. High levels of Cu accumulate
in the litter [18, 191 and may contribute to
the onset of proventriculitis when broilers eat
litter. In this context, it is of interest that the
commercial use of copper sulfate as a feed
supplement for improving growth performance and feed conversion [lo, 15, 20, 211
may be most effective after consecutive flocks
of broilers are reared on the same litter, leading to suggestionsthat the beneficial effects of
supplemental dietary Cu and other antifungal
treatments are mainly derived primarily from
alterations in the fungal and microbiological
characteristics of litter [15,19,22]. It also has
been reported that the demarcation between
the proventriculus and gizzard is less distinct
in cage-reared than in floor-reared broilers,
and that the demarcation becomes more
prominent if 3% ground litter is added to the
diet of cage-reared broilers [B].The absence
of fiber or roughage can cause proventricular
enlargement and gizzard atrophy in cagereared broilers [24, 251, which may help
explain why, in the present study, "suspect"
diet D triggered a 40% incidence of proventriculitis in the original broiler house and
a 100% incidence of proventriculitis in the
Petersime battery. Litter roughage may be
beneficial to proventricular and gizzard function as long as litter consumption does not
excessivelyincrease Cu intake.
Excess Cu intake was not the sole cause of
proventriculitis in the broilers we evaluated
under controlled experimental conditions. A
low but consistent incidence of obviously
affected proventriculi occurred in both experiments when broilers received control diets
containing no supplemental copper sulfate.
Furthermore, field outbreaks of proventriculitis have occurred in flocks reared on feeds
containing no supplemental copper sulfate.
Evidently proventriculitis in broilers can be
aggravated by several factors, one of which is
excessive Cu intake. Because of the location
JAPR
COPPER AND THE PROVENTRICULUS
228
Figure 3A
a
3
2
4
Weeks of Age
OOCuadjed
O C u S 0 4 PF
oCuS04
co
2CuS04 PF
Figure 3B
e
a-J-J
4 CuS04 PF
lCuSO,
co
6 WSO, PF
"1
a
a
a
L
i
a
3
4
Weeks of Age
FIGURE 3. Average proventriculus scores as a function of dietary copper sulfate supplementation (0,2, 4, or
6 lbhon CuSO4) and the use of poultry fat (PF) or corn oil (CO) as an energy source. Higher scores indicate
more severe proventriculitis/proventriculosis as assessed by: (A) the degree of proventricular enlargement and
(B) the incidence or density of serosal plaques (bdValueswith different letters within the same weekly necropsy
interval are significantly different, Ps.05, from each other as determined by Wilcoxian rank-sum comparisons).
Research Report
WIDEMANecal.
229
and function of the proventriculus and gizzard,
multiple factors may independently affect the
muscle tone and activity of these organs, leading in turn to delayed feed passage and engorgement of the upper gastrointestinal tract.
For example, cutting the right vagus nerve
inhibits proventricular and gizzard function,
thereby triggering gizzard atrophy and all of
the classic symptoms of proventriculitis [XI.
Additional factors known to trigger some or all
of the symptoms of proventriculitis include
infectious agents [27,28,29,30,31,32], toxins
[33, 34, 351, biogenic amines or their derivatives [29,34,36,37,38,39], and lack of dietary
fiber [g.
Aside from the obvious problems encountered during evisceration, the commercial integrator did not report a negative association
between the incidence of proventriculitis and
body weight gain or feed conversion during
the outbreak we investigated. Similarly, sus-
pect diets A and D affected mainly the proventriculus, without reducing body weights
or consistently affecting the weights of other
organs. Jensen and Maurice [12] previously
reported that diets supplemented with 500
and 700 pprn Cu, added as copper sulfate,
triggered proventriculitis and gizzard erosions
without affecting gizzard weights. Diets
containing 500 pprn Cu also did not affect
body weights and feed efficiency as long as
such diets were supplemented with sulfur
amino acids [12, 401. In earlier studies, Cu
depressed growth only when added to diets
in concentrations greater than 300 pprn [20,
15, 411. In contrast, the proventriculitis
associated with runting-stunting syndrome or
transmissible agents consistently is coupled
with other more severe symptoms, including
gizzard atrophy, accelerated feed passage,
poor feed conversion, and reduced body
weight gain [27,29,30,34].
CONCLUSIONS
AND APPLICATIONS
1. Under controlled experimental conditions, starter feeds containing in excess of 200 pprn
Cu (added to the feed as copper sulfate) induced proventriculitis in broiler chicks.
2. The gross enlargement of the proventriculus was reversed when the starter feed was
replaced with a control feed containing no supplemental copper sulfate.
3. Control feeds formulated to contain dietary Cu in excess of 200 ppm, added as copper
sulfate, reproducibly amplified the incidence of proventriculitis.
4. A low but consistent incidence of proventriculitis persisted in broilers receiving diets
that contained no supplemental CuSO4. The cause of the background incidence of
proventriculitis remains unknown.
5. Proventriculitis in broilers can be triggered or amplified by multiple factors, one of which
is excess Cu intake. Potential sources of excess Cu intake include feed, supplements added
to the drinking water, and litter.
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AND NOTES
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ACKNOWLEDGEMENTS
T h e a u t h o r s thank Dr. Leo S. Jensen and
Dr. Roland M. Leach for their valuable comments
during the course of this research.