Excess Dietary Copper Triggers Enlargement of the Proventriculus in Broilers1

01996Applied Poulhy Science, Inr

EXCESS DIETARY COPPER TRIGGERS ENLARGEMENT OF THE PROVENTRICULUS IN BROILERS'

~~

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

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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

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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

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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.

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.

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

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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.

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JAPR COPPER A N D THE PROVENTRICULUS

222

Figure 1A a

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Figure 1B 100

80

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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

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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).

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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

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)

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Controt

Research Report WIDEMAN et al.

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

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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

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JAPR COPPER AND THE PROVENTRICULUS

226

Pancreas, 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

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3.0020.13 2.7120.22 7.29k0.21 3.2220.13

Bursa,g

Research Report WIDEMAN et al.

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

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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

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JAPR COPPER AND THE PROVENTRICULUS

228

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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).

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3

2

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229 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.

REFERENCES AND NOTES 1.Burhol, P.G., 1971. Gastric secretion in the chicken. Scand. J. Gastroent. 6(Suppl):1-65. 2. Hill, KJ., 1971. The structure of the alimentary tract. Pages 1-23 in: Physiology and Biochemistry of the Domestic Fowl. DJ. Bell and B.M. Freeman, eds. Academic Press, New York,NY. 3. Hedge, RD., 1974. The digestive system. Pages 35-112 in: The Histolo of the Fowl. RD. Hodges, ed. Academic Press, New #I%, NY. 4. McLelland, J., 1979.Digestive system. Pa es 6P-181 in: Form and Function in Birds, Volume 1.A.8 King and J. McLelland, eds. Academic Press, New York, NY. 5. The Cu content of the proventriculus was measured using inductive cou led argon plasma emission spectrohotometry (I&l kP,Spectro Analytical Company, $itchburg, MA 0 017.

6. An Instron Model 4502 shear ress was used to measure intestine strength. Instron &rp., Canton, MA 02021. 7. Huff, W.E, J.M. Balog, G. Bayyari, and N.C. Rnlh, 1994.The effect of Mycocurb ,propionic acid, and calcium propionate on the intestinal strength of broiler

b

'

chickens. Poultry Sci. 73:1352-1356. 8. Novus International, Inc., St. Louis, MO 63141. 9. SAS Institule, 1982. SASQ User's Guide: Statistics. SAS Institute, Inc., Cary, NC.

10.Poupoulis, C. and LS.Jcnsen, 1976. Effect of high r on gizzard integrity of the chick. Poultry

E.%l?!l.

11. Jensen, LS and D.V. Maurice, 19%. Effect of hi dietary copper on the ceca of chicks. Poultry Sci. 58&-170.

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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-

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12. Jensen, LS.and D.V. Mawice, 1978b. Effect of methionine on copper-induced h depression and gizzard erosion. Poultry Sci. 57:&E532. 13. Jemen, LS.,PA. Dum, and K.N. Dobson, 1991. Induction of oral lesions in broiler chicks by su lementing the diet with copper. Avian Dis. 35:969-!# 14. S(srrbcr, BC,1%9. Studies on the mechanism of copper absorption in the chick. J. Nutr. 97:321-326. 15. Flsher, C,AP. L . m nJoaes, KJ. Hill, andW.S. Hardy, 1973. The effect of copper sulphate on pe-rformance and the structure of the gizzard in broilers. Br. Poultry Sci. 145568. 16. Chen, T.C m d U . Day, 1974. Gentian violet as a possible fun I inhibitor in poul feed: Plate assays on its antifungaEctivity. Poultry S c i ? 3 1 ~ 1 - 1 ~ . 17. Slcaart, RG., RD. Wyatt, and M.D. Ashmore, 1 9 n . The effect of various antifungal agents on aflatoxin production and owth. characteristics of flaylls in liquid m ium % : 6 b 18. K d c , W-E, LE Cur,T.A. Cuter, and E& Bosserd,1981. Effect of flock and floor type on the levels of nutrients and heavy metals in broiler htter. Poultry Sci. 60:116&1164. 19. Johnson, E L , J.L Nicholson, and J.A Doerr, 1985. Etfect of dietary copper on litter microbial tion and broiler performance. Br. Poultry Sci. 26:1%%1 20. Smith, M.S., 1%9. Responses of chicks to dietary suglements of copper sulphate. Br. Poultty Sci. 14971 . 21. Aoyagi, S. and D.H. Baker, 1995. Effect of high c o w e r dosing on hemicellulose digestibility in cecectomlzed cockerels. Poultry Sci. 74u)g-211. 22. M a , A S , RD. MUes, RH. Harms, T.C Chen, B.C. wlvorth, EJ. Day, G.L Romosmr, V.G. Mate, and KJ. Shaver,1979. Fungistatic compounds in broiler production. 4. Microbiologicaland physical characteristics of litter. Poultry Sci. 5814621468. 23. K u b e ~ LF., , J.W.Denton, J.D. May, and F.N. Reece, 1974. A dietary method to correct gizzard abnormality of broilers. Poultry Sci. 53407-409. 24. B d o n , H.D., 1%2. An abnormality of the roventriculus and gizzard of chicks. Poultry Sei. 42:736-%3. 25.Riddell, C, 1976. The influence of fiber in the diet on dilation (hypertro h ) of the proventriculus in chickens. Avian Dis. 20:44f.&. 26. Wideman, RF., Y.K. Kirby, T.Rozypd, and P.A Anles, 1995. Right celvicalvagotomycausesenlargement and dilation of the mventriculus, dilation of the gastric isthmus, atroph o g h e rd,and reduced weight gain in broilers. Pourtry Sci. e u p p l ) : 3 7 (Abs). 27. Kouwenhoven, B., F.G. DaveIIppT, and J. VIM Wplsom, 1978. Infectious mntriculitis causingrunting in broilers. Avian Pathol. %83-187.

28. Bracewell, CD. pod CJ. Randall,1984. The infectiousstuntingsyndrome. World's Poultry s i . J. &31-37. 29. Brugh, M. and RL WUson, 1986. Effect of dietary histamine on broiler chickens infected with avian reovirus S1133. Avian D k 303199-2Q3.

T

31. Bayyarl, G.R, W.E H a , J.M. Balog, N.C. Rath,

and J.N. h k y , 1995a. Expenmental reproduction of provcntriculitis using homo nates of proventricular tissue. Poultry Sci. 741799-1&. 32. Bsyysri,G.R, W.E HUN,J.N. Beasley, J.M. Balog, and N.C Rn(4 1995b.The effect of dietary cop rsulfate on infectiousproventriculitis. Poultry Sci. 75:&1-1969. 33. hrner, J.W., RJ.Cole, LG.Lorna, H.G. Gosser, .adU.L Dkner. 1983. CvcloDiazonic acid Droduction bv on broiler chickens. Appl. -*and its Enw icrobiol. 6698-703. tion syndkme) in broiler chickeG J. h-p.Pithol. Tmk.

6369-386. 35. Cnlkn, J.M., M. Wilson,W.M. Hagler, J.F. Or(,

and RJ.Cole, 1988. Histologic lesions in broiler chicks n cyclopiazonic acid orally. Am. J. Vet. Res. 49728-

E

36. Newberne, P.M., M.E Muhrer, R Craghead, and ILL O'Dell, 1956. An abnormality of the proventriculus of the chick. J.A.V.M.A. 128:55>555. 37. ShiMne, M., H.E M e r , and LE Ousbrhout, 1960. The pathology of chicks fed histamine. Avian Dis. 412-21. 38. Harry,EG., J.F. Tucker, and AP. Lawsen-Jones, 1975. The role of histamine and fBh meal in the incidence of gizzard erosion and proventricular abnormalities in the fowl. Br. Poultry Sci. 1669-78. 39. Poole, D.R, 1993. Biogenic amines may be affecting the field performance ofpoultry. Pages3742 in: Proc. Degussa Tech. Symp., Indianapolis, IN.

40.Jensen, LS.and D.V. Mauflce, 1979. Influence of sulfur amino acids on coppcr toxlcity In chicks. J. Nutr. 109~91-97. 41. Jenkins, N.K., T.R Morris, and D. Valamotis, 1970. The effect of diet and co per sup lementation on chick growth. Br. Poultry Sci. 18241-248:

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.

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30.Shapiro, F. and I. Nir, 1995. Stunting syndrome in broilers: Physical, hysiological, and behavioral aspects. Poultry Sci. 74:3&.