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Reproduction of the Oily Bird Syndrome in Broilers1
Reproduction of the Oily Bird Syndrome in Broilers1 L. S. JENSEN, I. BARTOV,2 M. J. BEIRNE, J. R. VELTMANN, Jr., and D. L. FLETCHER Department of Poultry Science, University of Georgia, Athens, Georgia 30602 (Received for publication November 19, 1979)
1980 Poultry Science 59:2256-2266 INTRODUCTION T h e Oily Bird S y n d r o m e (OBS) has been a recurring p r o b l e m in t h e commercial p r o d u c t i o n of broilers. Birds in processing plants exhibiting this condition have a very oily or greasy feel and appearance, p o c k e t s u n d e r t h e skin of the back from which an oily fluid flows when cut, and a t e n d e r skin which is easily torn during processing. Excessive water retention by t h e birds in t h e processing plant is sometimes associated with t h e s y n d r o m e . Garrett ( 1 9 7 6 ) described t h e s y n d r o m e and discussed several factors p o s t u l a t e d to affect its o c c u r r e n c e . T h e highest incidence occurs in September and O c t o b e r and is associated with high environmental t e m p e r a t u r e during t h e growing of t h e broilers. G a r r e t t ( 1 9 7 6 ) indicated t h a t females have a higher incidence of the p r o b l e m t h a n males and t h a t older broilers also have a higher incidence t h a n y o u n g e r broilers.
1 Supported by State and Hatch funds allocated to the Georgia Agricultural Experiment Station and by a grant from the Governor's contingency fund. 2 Present address: Division of Poultry Science, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel.
C o m p o s i t i o n of diets fed broilers has been considered as an etiological factor. T h e occurrence of t h e s y n d r o m e usually is associated with t h e feeding of high energy diets with relatively wide calorie to protein ratios. G a r r e t t ( 1 9 7 6 ) r e p o r t e d t h a t m a n y operations having t h e p r o b l e m were using diets with high levels of animal b y - p r o d u c t s and dried bakery p r o d u c t as replacements for p a r t of t h e soybean meal and corn. T h e fatty acid composition of t h e diets, which would be reflected in t h e fatty acid c o m p o s i t i o n of t h e broiler carcass, has also been implicated as a possible etiological factor in O B S . Feeding of diets with fat s u p p l e m e n t s containing a high level of p o l y u n s a t u r a t e d fatty acids was considered to be a possible cause of t h e s y n d r o m e , b u t Garrett ( 1 9 7 6 ) and Horvat ( 1 9 7 8 ) f o u n d n o significant differences in carcass fatty acid c o m p o s i t i o n between birds with and w i t h o u t the s y n d r o m e . A serious p r o b l e m with OBS occurred in several broiler operations in Georgia during t h e s u m m e r and fall of 1 9 7 8 . A series of studies was initiated at t h e University of Georgia in an a t t e m p t t o find a solution to this field p r o b l e m . Fletcher and T h o m a s o n ( 1 9 8 0 ) investigated t h e effects of environmental and processing conditions o n broiler carcass quality, b u t OBS was
2256
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ABSTRACT The Oily Bird Syndrome (OBS) was successfully reproduced in broilers under laboratory conditions which included elevated temperatures simulating summer conditions and feeding high energy diets with a relatively wide calorie to protein ratio. No significant difference in incidence of the syndrome was detected in broilers fed a corn-soy diet, or one with 13% animal protein concentrates and 7.5% bakery product, or with a diet containing 10% distillers dried grains with solubles. Substituting animal tallow for poultry oil significantly (P<.05) increased the incidence of the syndrome. Feeding diets with a more narrow calorie to protein ratio significantly reduced incidence in one experiment, and feeding an unpelleted diet from 3 to 7 weeks of age also significantly reduced the incidence below that of birds fed the same diet in pelleted form. Incidence of OBS was significantly less for birds housed in a separate building with lower temperature conditions than those maintained in a house with a higher environmental temperature. The OBS could best be observed under commercial processing conditions. Results of these experiments show that growing broilers at a high environmental temperature and feeding diets with wide calorie to protein ratios provide conditions conducive to the development of OBS. Further studies will be necessary to determine the specific etiology of the syndrome. (Key words: animal proteins, bakery product, calorie to protein ratio, dietary fat, distillers dried grains with solubles, energy level, Oily Bird Syndrome, pelleting, temperature)
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OILY BIRD SYNDROME TABLE 1. Composition of the starter diets (%) Diet Ingredient
A
Calculated analysis: ME, kcal/kg Crude protein, % Fat, % C/P Lysine, % Methionine + cystine, %
C
53.80 36.18
63.36 19.12 3.00 2.50 7.50
5.80 2.05
2.70
57.53 18.84 3.00 2.50 7.50 7.50 1.60
.40 .15 .37 .25 .10 .55
.35 .17 .11 .26 .09 .55
.88 .48 .26
.55 3245 22.5 8.2 144 1.27 .96
3245 22.5 6.8 144
3245 22.5 6.34 144
1.27
1.26
.96
.96
1 Constant ingredients included the following per kilogram of diet: Mn, 50 mg; Zn, 50 mg; Fe, 30 mg; I, 1.05 mg; Se, .1 mg; monensin sodium, 100 mg (except withdrawal diets); roxarsone, 50 mg; vitamin A, 4400 IU; vitamin D 3 , 800 ICU; a-toxopheryl acetate, 11 mg; menadione sodium bisulfite, 3.5 mg; riboflavin, 4.4 mg; Ca pantothenate, 9.6 mg; nicotinic acid, 44 mg; choline chloride, 220 mg; folic acid, .55 mg; vitamin B 1 2 , 6.6 Mg; and ethoxyquin, 125 mg. All diets in Experiments 2 and 3 also contained the following: Cu, 130 mg; pyridoxine, 2.2 mg; thiamine mononitrate, 2.2 mg; and biotin, .11 mg. Variable amounts of Cu and the latter three vitamins were used in Experiment 1.
not generally observed in this study. The experiments to be described here were conducted in an attempt to reproduce the syndrome under laboratory conditions and further to study dietary and environmental factors that might influence the incidence of the syndrome. GENERAL PROCEDURE Three experiments were conducted with 1-day-old male broiler chicks of the Hubbard strain maintained in floor pens with wood shavings as litter. Sixty birds in Experiments 1 and 2 and 65 birds in Experiment 3 were placed in each pen (2.44 m X 2.44 m) and four replicates were assigned to each treatment. To simulate summer temperatures in the broiler house, two forced-air space heaters fired by natural gas were used along with the infrared brooder heaters located in each pen in the house. The temperature was usually above 29 C throughout all of the experiments, but occasionally it fell below this for a few hours during the first experiment which was conducted in the
winter months. A starter diet was fed from 0 to 3 weeks of age, a grower diet from 3 to 6 weeks of age, and a withdrawal diet from 6 to 7 weeks of age. Composition of the diets used in the various experiments is detailed in Tables 1, 2, and 3. All of the diets were fed in crumbled form during the starter phase and in pelleted form during the grower and withdrawal phases except for one treatment in Experiment 3 fed in mash form after 3 weeks of age. The birds were weighed at 3 and 7 weeks of age by pens and feed weigh-backs were made at 3, 6, and 7 weeks of age. At 49 days of age a sample of 5 birds was randomly selected from each pen. These birds were processed at the University facility and the abdominal fat pad was carefully removed for weighing. Livers were also removed in Experiments 1 and 2 and weighed. The percentage of birds by treatments with an oily feel or appearance and/or with oily pockets on the back was determined in Experiment 1. In Experiment 1 liquidity of the abdominal fat
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Yellow corn Soybean meal (49% protein) Fish meal, menhaden (60% protein) Meat and bone meal (50% protein) Poultry by-product meal (58% protein) Bakery product Fat, poultry Dicalcium phosphate Limestone Salt DL-methionine L-lysine Constant ingredients'
B
1.16
157
3 300 21.0 8.56
.55
3300 21.0 6.78 157 1.16 .88
.55
3.04 .32 .09 .37 .21 .10
6.13 1.97
.82 .48 .22
66.84 15.48 3.00 2.50 7.50
57.29 32.54
3 300 21.0 6.31 157 1.16
.55
.27 .11 .11 .22 .09
61.01 15.20 3.00 2.50 7.50 7.50 1.94
3100 19.7 3.89 157 1.09 .83
.55
3300 26.0 10.4 127 1.5 1.0
.5
.4 .2
8.4 1.8
1.05 1.98 .73 .48 .20 .06
42.2 45.3
66.82 28.13
Diets
1 Constant ingredients included the following per kilogram of diet; Mn, 50 mg; Zn, 50 mg; Fe, 30 mg; I, 1.05 mg; drawal diets); roxarsone, 50 mg; vitamin A, 4400 IU; vitamin D 3 , 800 ICU; a-tocopheryl acetate, 11 mg; menadio pantothenate, 9.6 mg; nicotinic acid, 44 mg; choline chloride, 220 mg; folic acid, .55 mg; vitamin B, 2 , 6.6 Mg; and eth also contained the following; Cu, 130 mg; pyridoxine, 2.2 mg; thiamine mononitrate, 2.2 mg; and biotin, .11 mg. Vari Experiment 1.
Lysine, % Methionine + cystine, %
C/P
Calculated analysis; ME, kcal/kg Crude protein, % Fat, %
Yellow corn Soybean meal (49% protein) Fish meal, menhaden (60% protein) Meat and bone meal (50% protein) Poultry by-product meal (58% protein) Bakery product Fat, poultry Dicalcium phosphate Limestone Salt DL-methionine L-lysine Tallow Distillers dried grains/solubles Constant ingredients 1
Ingredients
TABLE 2. Composition of grower diets (%)
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.93 .78
181 .93 .78
181
.94 .78
181
.45
3300 18.2 5.24
.45
.45
.84 .48 .19
3300 18.2 6.16
.59 .32 .13 .11 .20 .08
1.68
4.79 2.02 .36 .11 .37 .18 .08
69.97 7.95 3.00 2.50 7.50 7.50
75.53 8.24 3.00 2.50 7.50
C
65.95 25.28
B
3300 18.2 7.49
A
.27 .45
.75 .48 .17 .04
2.02
74.30 21.52
181 .88 .73
3100 17.1 3.08
D
.45
.70 .48 .27
6.83 1.94
52.76 36.57
.97
1.28
146
3300 22.6 9.19
E
3
F
1 Constant ingredients included the following per kilogram of diet: Mn, 50 mg; Zn, 50 mg; Fe, 30 mg; I, 1.05 mg drawal diets); roxarsone, 50 mg; vitamin A, 4400 IU; vitamin D 3 , 800 ICU; a-tocopheryl acetate, 11 mg; menadio pantothenate, 9.6 mg; nicotinic acid, 44 mg; choline chloride, 220 mg; folic acid, .55 mg; vitamin Bi2, 6.6 Mg: and et also contained the following: Cu, 130 mg; pyridoxine, 2.2 mg; thiamine mononitrate, 2.2 mg; and biotin, .11 mg. V in Experiment 1.
Lysine, % Methionine + cystine, %
C/P
Calculated analysis: ME, kcal/kg Crude protein, % Fat, %
Yellow corn Soybean meal (49% protein) Fish meal, menhaden (60% protein) Meat and bone meal (50% protein) Poultry by-product meal (58% protein) Bakery product Fat, poultry Dicalcium phosphate Limestone Salt DL-methionine L-lysine Tallow Distillers dried grains/solubles Purified cellulose (Solka-floc) Constant ingredients'
Ingredients
Diets
TABLE 3. Composition of withdrawal diets (%)
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JENSEN ET AL. TABLE 4. Effect of supplementation of different diets with minerals, and vitamins on performance of 7-week-old broilers (Experiment 1)'
Basal diets 2
Elements added, vitamins removed 3
Body weight (g)
Feed/gain 3—7 weeks
AAA (corn-soy)
None Cu
Cu, Cr, Mo Cu-vitamins
1984 2011 1987 2020
2.07 2.04 2.01 1.98
Mean
2000
2.02
None Cu, Cr, Mo Cu-vitamins
1945 2033 1998 1926
2.02 1.94 1.95 2.00
Mean
1975
1.98
ccc
Cu
(animal protein + bakery products)
Cu, Cr, Mo Cu-vitamins
2004 2005 1980
2.00 1.99 2.02
Mean
1996
2.00
BB B (animal protein)
1 2
Cu
None of the differences among treatments were significant (P>.05). S = starter, G = grower, and W = withdrawal; see Tables 1,2, and 3 for diet composition.
3 Cu, Cr, and Mo at a level of 125, 20, and 2.5 mg/kg, respectively, supplied as CuSO s - 5 H 2 0 , CrCl 3 - 6 H 2 0 , and Na2 Mo0 4 *2H2 O. In the treatments in which vitamins were removed pyridoxine, thiamine, and biotin of a concentration of 2.2, 2.2, and .11 mg/kg diet, respectively, were deleted from the vitamin premix.
pad was scored from 1 (relatively solid) to 3 (relatively liquid) after the samples were maintained at 25 C for 7 hr. The remainder of the birds in each experiment were processed at a local processing plant at 50 days of age. In the first experiment the birds were not identified by treatment; thus, only comparisons between the appearance of the experimental birds and commercial birds going through the plant at that time were made. In Experiments 2 and 3, birds from the various treatments were identified by leg bands. One experimental bird was placed on about every 12th shackle in the processing line so that the birds could be observed at the regular speed of the processing line. The birds were scored individually for oiliness (Fletcher and Thomason, 1980) by one person on a scale of 1 (nonoily) to 5 (extremely oily skin). Another person scored for incidence of OBS on the basis of presence or absence of oily pockets on the back on a scale of 0 (no oily pockets) to 2 (large pockets). Data were analyzed by standard statistical procedures as outlined by Steel and Torrie (1960).
SPECIFIC EXPERIMENTAL PROCEDURE AND RESULTS
Experiment 1 Procedure. This experiment was conducted from December 12, 1978, to January 9, 1979. The birds were fed three different basal diets: a corn-soy diet (A), a diet with 13% animal protein concentrates (B), and a diet with 13% animal protein concentrates plus 7.5% bakery product (C). The composition of the diets for the three different growing products are given in Tables 1, 2, and 3. Basal diets A and B were fed unsupplemented, supplemented with copper sulfate (125 ppm copper), with copper (125 ppm) plus chromium (20 ppm) and molybdenum (2.5 ppm), and with copper (125 ppm) minus the B complex vitamins — pyridoxine, thiamine, and biotin — present in the vitamin premix for the other diets. Because of limitations of space, diet C (unsupplemented with 125 ppm copper) was not included, but the other three treatments were used. The diets had the same energy and protein levels and calorie to protein ratios within each growing period. Results. No significant differences were
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S GW
OILY BIRD SYNDROME
processing plant and those after processing in the commercial plant clearly showed that to observe OBS as seen in the field, it is essential to process the birds through a commercial plant. Experiment 2 Experimental. This experiment was conducted from February 27, 1979, to April 17, 1979. The various dietary treatments outlined in Table 6 were used in this study. All of the birds were fed the same basal diet during the first 3 weeks (A, Table 1). Three series of diets were formulated to have the same energy and calorie to protein ratios, but one contained poultry oil, a second animal tallow in place of poultry oil, and the third a high level of animal proteins and bakery product. Three other treatments included a lower calorie to protein ratio with the same high energy level and low energy levels with the wide and narrow calorie to protein ratios. Results, No significant differences were observed in final body weight or feed/gain from 3 to 7 weeks of age (Table 6). Feed-gain ratios were considerably higher for birds fed die two lower energy regimens (Treatments 5 and 6),
TABLE 5. Effect of supplementation of different diets with minerals and vitamins on fatness and oiliness in 7-week-old broilers (Experiment l)1 Basal diets 2 SG W AAA (corn-soy)
BBB (animal protein)
CCC (animal protein + bakery products)
Elements added, vitamins removed
Abdominal fat (% BW)
Liver weight (g/kg BW)
Fat liquidity score
Oily birds 3
None Cu Cu, Cr, Mo Cu-vitamins
20.9 19.6 20.4 20.3
1.4 2.0 1.8 1.8
31.6 45.0 22.2 35.3
Mean
3.1 3.3 3.4 3.3 3.3b
20.3
1.8
33.8
None Cu Cu, Cr, Mo Cu-vitamins
3.5 3.5 3.3 4.0
20.6 20.4 20.5 20.5
2.0 2.0 1.9 2.2
41.2 38.9 15.8 26.7
Mean
3.6 a
20.5
2.0
30.4
Cu Cu, Cr, Mo Cu-vitamins
3.6 3.5 3.4 3.5^
21.3 21.8 21.5
1.7 1.8 1.5
15.8 10.5 20.0
21.5
1.7
15.1
Mean
(%)
a' b Average values for basal diets not followed with the same letter differ significantly (P<.05). 1
Mean of 15 to 20 birds per treatment.
2
S = starter, G = grower, and W = withdrawal; see Tables 1, 2, and 3 for diet composition.
3
Percentage of birds with an oily feel and/or pockets on back scored in University processing facility.
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observed in final body weight and feed efficiency from 3 to 7 weeks of age (Table 4). Abdominal fat as a percent of body weight was significantly higher for birds fed the basal diets containing animal by-products and animal by-products plus bakery product over that of birds fed the corn-soy diet, but the difference was relatively small (Table 5). No significant difference was observed in liver weight per unit of body weight, fat liquidity score of the abdominal fat, and percent of oily birds. No evidence was obtained that, including animal protein concentrates and bakery product in the diets, increased incidence of oily birds as measured in this experiment. The remaining birds processed through a commercial processing plant exhibited a high incidence of oiliness and of pockets on the backs. In contrast, the commercial birds being processed along with the experimental birds showed little or no evidence of OBS. Therefore, the dietary and environmental laboratory conditions under which the experimental birds were raised resulted in the reproduction of the syndrome. A comparison of the appearance of the birds after processing in the University
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JENSEN ETAL.
TABLE 6. Effect of energy level, calorie to protein ratio (C:P), tallow, and a combination of animal and bakery products on performance of 7-week-old broilers (Experiment 2) Diet description C •P
Dipt ^
SGW
1 2 3 4 5 6
AAA A G G (Tallow) A C C ( A P + BP) 3 AEE ADD AFF
G
W
Body weight2 7 weeks
157 157 157 127 157 127
181 181 181 146 181 146
1977 1980 1890 1984 1923 1953
!
ME (kcal/kg)
1
Feed/gain 3 - 7 weeks
(g)
3300 3300 3000 3300 3100 3100
2.04 2.02 2.09 2.00 2.23 2.13
S = starter, G = grower, and W = withdrawal; see Tables 1, 2, and 3 for diet composition.
2
No significant difference. Standard deviation = 85.43.
3
AP + BP = animal proteins and bakery waste.
but variability among pens was great so that no statistical significance was observed. Rubber bands of different colors were placed on some of the birds several days before the marketing period to identify specific treatments as they passed through the commercial processing plant. Some of the rubber bands were too tight and resulted in restriction of blood flow to the feet, which contributed to the variability among pens. No significant difference in percentage abdominal fat was observed between birds fed the corn-soy diet (Treatment 1) and the corn-soy diet supplemented with animal protein concentrates and bakery product (Treatment 3, Table 7). Reducing the calorie to protein ratio in either the high or low energy diets (Treatments 4 and 6) significantly reduced abdominal fat, whereas no significant reduction in fat was detected when the energy level was lowered while maintaining the same calorie to protein ratio (Treatments 3 and 5). Again, no significant differences were observed in liver weight per unit of body weight. Oiliness score of the birds at the commercial processing plant was significantly lower when birds were fed a narrow calorie to protein ratio (Table 7). Reducing the energy level of the corn-soy diet without changing the calorie to protein ratio (Treatment 5 vs. 1) also significantly reduced the oiliness score. Incidence of OBS was high among all of the dietary treatments and the incidence for birds fed the diet with animal tallow (Treatment 2) was significantly
higher than most of the other treatments. Incidence of the most severe form (score 2) of OBS tended to be lower for those fed the lower energy diets. Commercial birds passing through the processing line at the same time showed little evidence of the syndrome. Thus, OBS had been produced again under laboratory conditions. Experiment 3 Procedure. Experiment 3 was conducted from May 8, 1979, to June 26, 1979. All the birds were fed the same diet (A, Table 1) for the starter period of the study. After 3 weeks, all birds were fed diets with the same energy level, but in addition to the cornsoy basal diet one diet was formulated to contain 10% distillers dried grains with solubles. The corn-soy basal diet was also fed in pelleted and unpelleted form. Because temperature appeared to be a factor in the reproduction of the syndrome, one treatment of birds was maintained in a different broiler house without space heaters. Temperatures here were generally 3 to 5 C cooler during the study than in the house where the other birds were maintained. Two other treatments involved the raising of protein levels resulting in the feeding of diets with more narrow calorie to protein ratios. Results. No significant differences were observed in final body weight (Table 8). Feed efficiency was significantly better for birds fed the mash diet (Treatment 3) in comparison to the pelleted one (Treatment 1, Table 8). The
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Treatment no.
6
5
4
3
2
1
AAA A G G (Tallow) A C C (AP + BP) 6 AE E ADD A F F
S G W
3300 3300 3300 3300 3100 3100
(kcal/kg)
ME
157 157 157 127 157 127
G
C:P
Diet descripl:ion
181 181 181 146 181 146
W
3.5* 3.6^ 3.6a 3.0bc 3.4ab 2.7C
(% BW) 2
Abdominal fat
AP + BP = animal proteins and bakery waste.
Scores ranged from 0 for no oily pockets to 2 for large pockets.
Mean of about 225 birds per treatment.
Oiliness scores ranged from 1 for nonoily to 5 for extremely oily skin. Standard deviation = .81.
Mean of 20 birds per treatment.
S = starter, G = grower, and W = withdrawal, see Tables 1,2, and 3 for diet composition.
' ' ' Values within each column not followed by a common letter are significantly different (P<.05).
Treatment no.
Diet 1
17.9 17.0 18.6 18.7 19.4 18.0
(g/kg BW
Liver weight
TABLE 7. Effect of energy level, calorie to protein ratio (C:P), tallow, and a combination of an on fattening and incidence of OBS in 7-week-old broilers (Experiment
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JENSEN ET AL.
TABLE 8. Effect of calorie to protein ratio (C:P), distillers dried grains with solubles (DDGS), pelleting, and environmental temperature on performance of 7-vieek-old broilers (Experiment 3) Treatment description _____ SGW
G
i W
1 2 3 4 5 6
AAA AHH AAA AAA AEE AEI
157 157 157 157 127 127
181 181 181 181 146 127
Treatment
DDGS Mash3 Lower Temperature"
Body weight2 (g)
Feed/gain 3 - 7 weeks
1900 1976 1855 1865 1909 1899
2.06 a 1.94 ab 1.87b 2.08 a 1.94 ab 1.98 ab
' Values without a common letter are significantly different (P<.05). 1
S = starter, G = grower and W = withdrawal; see Tables 1, 2, and 3 for diet composition.
2
Standard deviation = 75.73.
3 Diets in this treatment were fed in mash form from 3 to 7 weeks. Diets for all other treatments were fed in pelleted form. 4
Birds in this treatment were kept in a separate house where space heaters were not used.
mash feed tended to bind in the tube feeders used in the study and had to be checked two or three times a day to be sure feed was available to the birds. Less feed wastage may have occurred as a result of this practice. Abdominal fat as a percent of body weight was significantly less for the treatment fed the narrow calorie to protein ratio (127) from 3 to 7 weeks of age (Treatment 6) in comparison to the birds fed the corn-soy diet in the same house (Treatment 1, Table 9). Other treatment means were not significantly different. Oiliness score was significantly less for birds maintained in the lower temperature house (Treatment 4) than those in the higher temperature house (Treatment 1) even though the diets were the same. Feeding mash diets with more narrow calorie to protein ratios also significantly reduced the oiliness score below that of the birds fed the corn-soy control diet (Table 9). Incidence of OBS was significantly lower for birds fed mash and for those maintained in the lower temperature house. Incidence of OBS was reduced by feeding more narrow calorie to protein ratios during the growing and withdrawal stages (Treatments 5, and 6, Table 9). Differences in the more severe form of OBS (score 2) were particularly striking among the various treatments. Distillers dried grains with solubles did not significantly reduce abdominal fat pad, oiliness score, or incidence of OBS.
DISCUSSION The oily bird syndrome was successfully reproduced in these experiments under laboratory conditions. The experimental birds with the condition had a "greasy" appearance and large pockets filled with an oily fluid on their back. These birds were similar to those seen in commercial processing plants at the height of the oily bird problem in Georgia during the summer and fall of 1978. Processing of the laboratory-reared broilers apparently must be done in a commercial processing plant for OBS to be fully expressed. The birds processed in the University facility failed to exhibit the same incidence and severity of OBS as seen in the commercial plant. Garrett (1976) emphasized that stress in commercial processing plants was a major factor affecting the incidence of OBS. Apparently the batch picker used in the University facility coupled with perhaps a different scalding temperature and time did not sufficiently stress the skin tissues to precipitate a high incidence of OBS. Fletcher and Thomason (1980) observed higher skin oiliness scores in birds subjected to higher scald temperatures and longer picking times. Although the specific cause of OBS was not discovered in these investigations, some factors appear to have been eliminated and others confirmed as being involved in the production of the syndrome. The idea that feeding diets
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Treatment no.
7
6
5
4
3
2
157 157 157 157 127 127
G
C:P .
181 181 181 181 146 127
W
DDGS Mash 6 Lower t e m p e r a t u r e 7
Treatment
T r e a t m e n t descriiption
3.9a 3.6ab 3.5*b 3.7ab 3.5ab 3.3b
Abdominal fat <% BW) 2
Birds in this treatment were kept in a separate house where space heaters were not used.
Diets in this treatment were fed in mash form 3 to 7 weeks. Diets for all other treatments were fed in pelleted form
OBS scores ranged from 0 for no oily pockets to 2 for large pockets.
Oiliness scores ranged from 1 for nonoily to 5 for extremely oily skin. Standard deviation = 1.09.
Mean of about 160 birds per treatment.
S = starter, G = grower and W = withdrawal; see Tables 1, 2, and 3 for diet composition. Mean of 20 birds per treatment.
' ' Values within each column without a common letter are significantly different (P<.05).
AAA A H H AAA AAA A E E A E I
1 2 3 4 5 6
1
SG W
no.
Diet
1
TABLE 9. Effect of calorie to protein ratio (C:P), distillers dried grains with solubles (DDGS), pelleting, fattening and OBS in 7-week-old broilers (Experiment 3)
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2266
JENSEN ETAL.
under high temperature conditions. The specific reason for the development of OBS under conditions of elevated ambient temperature and high energy rations with wide calorie to protein ratios is not apparent from these studies. The basic biochemical changes occurring in the skin and other tissues of the animal by these environmental and dietary conditions need to be determined in order to discover means by which the syndrome can be prevented under all conditions. Garrett (1976) hypothesized that a nutritional deficiency or imbalance resulted in a reduced rate of connective tissue synthesis resulting in an impairment in the structural integrity of the skin and adipose tissue. Smith et al. (1976) obtained evidence for a reduced collagen content in broiler skin tissue by feeding high energy diets during a period of high environmental temperature. Subsequent studies, however, failed to confirm this observation in birds raised under cooler temperature conditions (Smith et al, 1977). Further work is needed on the effect of environmental temperature and dietary changes on collagen content and other possible changes in the tissues of broilers to attempt to find the basic cause of OBS. ACKNOWLEDGMENTS
The authors are indebted to W. J. Schimmel and John Kiker, Central Soya, Athens, GA, for their cooperation in allowing the birds to be observed and scored in a commercial processing plant and to Hoffmann-LaRoche, Inc., Nutley, NJ for supplying the vitamin premixes used in Experiment 1. REFERENCES Fletcher, D. L., and D. M. Thomason, 1980. The influence of environmental and processing conditions on the physical carcass quality factors associated with Oily Bird Syndrome (OBS). Poultry Sci. 59:731-736. Garrett, R. L., 1976. Update on the "Oily Bird" Syndrome. Proc. 11th Nat. Mtg. Health and Condemnation. DE-MD, Oct. 20. Horvat, R. J., 1978. Oily bird skin lipids. Poultry Sci. 57:1187. Smith, T. W., Jr., J. R. Couch, C. R. Creger, and R. L. Garrett, 1976. The relationship of sex, dietary energy and meat protein with collagen in broiler skin tissue. Poultry Sci. 55:2093-2094. Smith, T. W., Jr., J. R. Couch, R. L. Garrett, and C. R. Creger, 1977. The effect of sex, dietary energy, meat protein, ascorbic acid and iron on broiler skin collagen. Poultry Sci. 56:1216-1220. Steele, R.G.D., and J. H. Torrie, I960. Principles and procedures of statistics. McGraw-Hill, New York, NY.
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with a high concentration of polyunsaturated fatty acids is a major etiological factor for OBS apparently can be eliminated. Neither Garrett (1976) nor Horvat (1978) were able to demonstrate any differences in fatty acid composition of the skin lipids in birds with and without the syndrome. In the second experiment of the present investigations, feeding a diet with a more saturated fat (tallow) to chicks from 3 to 7 weeks of age increased the incidence of OBS over that of birds fed a more unsaturated fat (poultry oil). Garrett (1976) indicated that many broiler operations reporting OBS fed high levels of animal by-products and dried bakery product. Direct comparison of birds fed diets containing 13% animal by-products coupled with 7.5% bakery product with those fed a corn-soybean meal diet failed to reveal any major difference in the incidence of OBS between the two types of diets. A significantly higher percent of abdominal fat was observed in Experiment 1 in birds fed diets with a higher level of animal products, but this was not confirmed in the second experiment. Garrett (1976) also suggested that nutrient deficiencies might be involved in the etiology of OBS. Distillers dried grains with solubles, a concentrated source of several minerals and vitamins and perhaps other unidentified factors, failed to reduce the incidence of OBS. Adding a high level of copper, supplements of molybdenum and chromium, and elimination of pyridoxine, thiamine, and biotin from the vitamin premix did not seem to affect appearance of broilers (but only the birds processed at the University facility were identified by treatments). Feeding rations with more narrow calorie to protein ratios reduced the incidence of OBS but did not completely prevent it under the environmental and other dietary conditions used to produce the syndrome. Other factors must play an important role. Feeding of the corn-soy diet as a mash from 3 to 7 weeks of age significantly reduced the incidence of the syndrome (Table 9). Growth rate was slightly less for these birds than for those fed the pelleted diets which may have influenced the incidence of the syndrome. A major factor in reproducing OBS under laboratory conditions appears to be the ambient temperature at which the birds are maintained. Observations in the commercial broiler industry and the data from this study indicate that the problem is much more severe in birds raised
1980 Poultry Science 59:2256-2266 INTRODUCTION T h e Oily Bird S y n d r o m e (OBS) has been a recurring p r o b l e m in t h e commercial p r o d u c t i o n of broilers. Birds in processing plants exhibiting this condition have a very oily or greasy feel and appearance, p o c k e t s u n d e r t h e skin of the back from which an oily fluid flows when cut, and a t e n d e r skin which is easily torn during processing. Excessive water retention by t h e birds in t h e processing plant is sometimes associated with t h e s y n d r o m e . Garrett ( 1 9 7 6 ) described t h e s y n d r o m e and discussed several factors p o s t u l a t e d to affect its o c c u r r e n c e . T h e highest incidence occurs in September and O c t o b e r and is associated with high environmental t e m p e r a t u r e during t h e growing of t h e broilers. G a r r e t t ( 1 9 7 6 ) indicated t h a t females have a higher incidence of the p r o b l e m t h a n males and t h a t older broilers also have a higher incidence t h a n y o u n g e r broilers.
1 Supported by State and Hatch funds allocated to the Georgia Agricultural Experiment Station and by a grant from the Governor's contingency fund. 2 Present address: Division of Poultry Science, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel.
C o m p o s i t i o n of diets fed broilers has been considered as an etiological factor. T h e occurrence of t h e s y n d r o m e usually is associated with t h e feeding of high energy diets with relatively wide calorie to protein ratios. G a r r e t t ( 1 9 7 6 ) r e p o r t e d t h a t m a n y operations having t h e p r o b l e m were using diets with high levels of animal b y - p r o d u c t s and dried bakery p r o d u c t as replacements for p a r t of t h e soybean meal and corn. T h e fatty acid composition of t h e diets, which would be reflected in t h e fatty acid c o m p o s i t i o n of t h e broiler carcass, has also been implicated as a possible etiological factor in O B S . Feeding of diets with fat s u p p l e m e n t s containing a high level of p o l y u n s a t u r a t e d fatty acids was considered to be a possible cause of t h e s y n d r o m e , b u t Garrett ( 1 9 7 6 ) and Horvat ( 1 9 7 8 ) f o u n d n o significant differences in carcass fatty acid c o m p o s i t i o n between birds with and w i t h o u t the s y n d r o m e . A serious p r o b l e m with OBS occurred in several broiler operations in Georgia during t h e s u m m e r and fall of 1 9 7 8 . A series of studies was initiated at t h e University of Georgia in an a t t e m p t t o find a solution to this field p r o b l e m . Fletcher and T h o m a s o n ( 1 9 8 0 ) investigated t h e effects of environmental and processing conditions o n broiler carcass quality, b u t OBS was
2256
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ABSTRACT The Oily Bird Syndrome (OBS) was successfully reproduced in broilers under laboratory conditions which included elevated temperatures simulating summer conditions and feeding high energy diets with a relatively wide calorie to protein ratio. No significant difference in incidence of the syndrome was detected in broilers fed a corn-soy diet, or one with 13% animal protein concentrates and 7.5% bakery product, or with a diet containing 10% distillers dried grains with solubles. Substituting animal tallow for poultry oil significantly (P<.05) increased the incidence of the syndrome. Feeding diets with a more narrow calorie to protein ratio significantly reduced incidence in one experiment, and feeding an unpelleted diet from 3 to 7 weeks of age also significantly reduced the incidence below that of birds fed the same diet in pelleted form. Incidence of OBS was significantly less for birds housed in a separate building with lower temperature conditions than those maintained in a house with a higher environmental temperature. The OBS could best be observed under commercial processing conditions. Results of these experiments show that growing broilers at a high environmental temperature and feeding diets with wide calorie to protein ratios provide conditions conducive to the development of OBS. Further studies will be necessary to determine the specific etiology of the syndrome. (Key words: animal proteins, bakery product, calorie to protein ratio, dietary fat, distillers dried grains with solubles, energy level, Oily Bird Syndrome, pelleting, temperature)
2257
OILY BIRD SYNDROME TABLE 1. Composition of the starter diets (%) Diet Ingredient
A
Calculated analysis: ME, kcal/kg Crude protein, % Fat, % C/P Lysine, % Methionine + cystine, %
C
53.80 36.18
63.36 19.12 3.00 2.50 7.50
5.80 2.05
2.70
57.53 18.84 3.00 2.50 7.50 7.50 1.60
.40 .15 .37 .25 .10 .55
.35 .17 .11 .26 .09 .55
.88 .48 .26
.55 3245 22.5 8.2 144 1.27 .96
3245 22.5 6.8 144
3245 22.5 6.34 144
1.27
1.26
.96
.96
1 Constant ingredients included the following per kilogram of diet: Mn, 50 mg; Zn, 50 mg; Fe, 30 mg; I, 1.05 mg; Se, .1 mg; monensin sodium, 100 mg (except withdrawal diets); roxarsone, 50 mg; vitamin A, 4400 IU; vitamin D 3 , 800 ICU; a-toxopheryl acetate, 11 mg; menadione sodium bisulfite, 3.5 mg; riboflavin, 4.4 mg; Ca pantothenate, 9.6 mg; nicotinic acid, 44 mg; choline chloride, 220 mg; folic acid, .55 mg; vitamin B 1 2 , 6.6 Mg; and ethoxyquin, 125 mg. All diets in Experiments 2 and 3 also contained the following: Cu, 130 mg; pyridoxine, 2.2 mg; thiamine mononitrate, 2.2 mg; and biotin, .11 mg. Variable amounts of Cu and the latter three vitamins were used in Experiment 1.
not generally observed in this study. The experiments to be described here were conducted in an attempt to reproduce the syndrome under laboratory conditions and further to study dietary and environmental factors that might influence the incidence of the syndrome. GENERAL PROCEDURE Three experiments were conducted with 1-day-old male broiler chicks of the Hubbard strain maintained in floor pens with wood shavings as litter. Sixty birds in Experiments 1 and 2 and 65 birds in Experiment 3 were placed in each pen (2.44 m X 2.44 m) and four replicates were assigned to each treatment. To simulate summer temperatures in the broiler house, two forced-air space heaters fired by natural gas were used along with the infrared brooder heaters located in each pen in the house. The temperature was usually above 29 C throughout all of the experiments, but occasionally it fell below this for a few hours during the first experiment which was conducted in the
winter months. A starter diet was fed from 0 to 3 weeks of age, a grower diet from 3 to 6 weeks of age, and a withdrawal diet from 6 to 7 weeks of age. Composition of the diets used in the various experiments is detailed in Tables 1, 2, and 3. All of the diets were fed in crumbled form during the starter phase and in pelleted form during the grower and withdrawal phases except for one treatment in Experiment 3 fed in mash form after 3 weeks of age. The birds were weighed at 3 and 7 weeks of age by pens and feed weigh-backs were made at 3, 6, and 7 weeks of age. At 49 days of age a sample of 5 birds was randomly selected from each pen. These birds were processed at the University facility and the abdominal fat pad was carefully removed for weighing. Livers were also removed in Experiments 1 and 2 and weighed. The percentage of birds by treatments with an oily feel or appearance and/or with oily pockets on the back was determined in Experiment 1. In Experiment 1 liquidity of the abdominal fat
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Yellow corn Soybean meal (49% protein) Fish meal, menhaden (60% protein) Meat and bone meal (50% protein) Poultry by-product meal (58% protein) Bakery product Fat, poultry Dicalcium phosphate Limestone Salt DL-methionine L-lysine Constant ingredients'
B
1.16
157
3 300 21.0 8.56
.55
3300 21.0 6.78 157 1.16 .88
.55
3.04 .32 .09 .37 .21 .10
6.13 1.97
.82 .48 .22
66.84 15.48 3.00 2.50 7.50
57.29 32.54
3 300 21.0 6.31 157 1.16
.55
.27 .11 .11 .22 .09
61.01 15.20 3.00 2.50 7.50 7.50 1.94
3100 19.7 3.89 157 1.09 .83
.55
3300 26.0 10.4 127 1.5 1.0
.5
.4 .2
8.4 1.8
1.05 1.98 .73 .48 .20 .06
42.2 45.3
66.82 28.13
Diets
1 Constant ingredients included the following per kilogram of diet; Mn, 50 mg; Zn, 50 mg; Fe, 30 mg; I, 1.05 mg; drawal diets); roxarsone, 50 mg; vitamin A, 4400 IU; vitamin D 3 , 800 ICU; a-tocopheryl acetate, 11 mg; menadio pantothenate, 9.6 mg; nicotinic acid, 44 mg; choline chloride, 220 mg; folic acid, .55 mg; vitamin B, 2 , 6.6 Mg; and eth also contained the following; Cu, 130 mg; pyridoxine, 2.2 mg; thiamine mononitrate, 2.2 mg; and biotin, .11 mg. Vari Experiment 1.
Lysine, % Methionine + cystine, %
C/P
Calculated analysis; ME, kcal/kg Crude protein, % Fat, %
Yellow corn Soybean meal (49% protein) Fish meal, menhaden (60% protein) Meat and bone meal (50% protein) Poultry by-product meal (58% protein) Bakery product Fat, poultry Dicalcium phosphate Limestone Salt DL-methionine L-lysine Tallow Distillers dried grains/solubles Constant ingredients 1
Ingredients
TABLE 2. Composition of grower diets (%)
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.93 .78
181 .93 .78
181
.94 .78
181
.45
3300 18.2 5.24
.45
.45
.84 .48 .19
3300 18.2 6.16
.59 .32 .13 .11 .20 .08
1.68
4.79 2.02 .36 .11 .37 .18 .08
69.97 7.95 3.00 2.50 7.50 7.50
75.53 8.24 3.00 2.50 7.50
C
65.95 25.28
B
3300 18.2 7.49
A
.27 .45
.75 .48 .17 .04
2.02
74.30 21.52
181 .88 .73
3100 17.1 3.08
D
.45
.70 .48 .27
6.83 1.94
52.76 36.57
.97
1.28
146
3300 22.6 9.19
E
3
F
1 Constant ingredients included the following per kilogram of diet: Mn, 50 mg; Zn, 50 mg; Fe, 30 mg; I, 1.05 mg drawal diets); roxarsone, 50 mg; vitamin A, 4400 IU; vitamin D 3 , 800 ICU; a-tocopheryl acetate, 11 mg; menadio pantothenate, 9.6 mg; nicotinic acid, 44 mg; choline chloride, 220 mg; folic acid, .55 mg; vitamin Bi2, 6.6 Mg: and et also contained the following: Cu, 130 mg; pyridoxine, 2.2 mg; thiamine mononitrate, 2.2 mg; and biotin, .11 mg. V in Experiment 1.
Lysine, % Methionine + cystine, %
C/P
Calculated analysis: ME, kcal/kg Crude protein, % Fat, %
Yellow corn Soybean meal (49% protein) Fish meal, menhaden (60% protein) Meat and bone meal (50% protein) Poultry by-product meal (58% protein) Bakery product Fat, poultry Dicalcium phosphate Limestone Salt DL-methionine L-lysine Tallow Distillers dried grains/solubles Purified cellulose (Solka-floc) Constant ingredients'
Ingredients
Diets
TABLE 3. Composition of withdrawal diets (%)
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2260
JENSEN ET AL. TABLE 4. Effect of supplementation of different diets with minerals, and vitamins on performance of 7-week-old broilers (Experiment 1)'
Basal diets 2
Elements added, vitamins removed 3
Body weight (g)
Feed/gain 3—7 weeks
AAA (corn-soy)
None Cu
Cu, Cr, Mo Cu-vitamins
1984 2011 1987 2020
2.07 2.04 2.01 1.98
Mean
2000
2.02
None Cu, Cr, Mo Cu-vitamins
1945 2033 1998 1926
2.02 1.94 1.95 2.00
Mean
1975
1.98
ccc
Cu
(animal protein + bakery products)
Cu, Cr, Mo Cu-vitamins
2004 2005 1980
2.00 1.99 2.02
Mean
1996
2.00
BB B (animal protein)
1 2
Cu
None of the differences among treatments were significant (P>.05). S = starter, G = grower, and W = withdrawal; see Tables 1,2, and 3 for diet composition.
3 Cu, Cr, and Mo at a level of 125, 20, and 2.5 mg/kg, respectively, supplied as CuSO s - 5 H 2 0 , CrCl 3 - 6 H 2 0 , and Na2 Mo0 4 *2H2 O. In the treatments in which vitamins were removed pyridoxine, thiamine, and biotin of a concentration of 2.2, 2.2, and .11 mg/kg diet, respectively, were deleted from the vitamin premix.
pad was scored from 1 (relatively solid) to 3 (relatively liquid) after the samples were maintained at 25 C for 7 hr. The remainder of the birds in each experiment were processed at a local processing plant at 50 days of age. In the first experiment the birds were not identified by treatment; thus, only comparisons between the appearance of the experimental birds and commercial birds going through the plant at that time were made. In Experiments 2 and 3, birds from the various treatments were identified by leg bands. One experimental bird was placed on about every 12th shackle in the processing line so that the birds could be observed at the regular speed of the processing line. The birds were scored individually for oiliness (Fletcher and Thomason, 1980) by one person on a scale of 1 (nonoily) to 5 (extremely oily skin). Another person scored for incidence of OBS on the basis of presence or absence of oily pockets on the back on a scale of 0 (no oily pockets) to 2 (large pockets). Data were analyzed by standard statistical procedures as outlined by Steel and Torrie (1960).
SPECIFIC EXPERIMENTAL PROCEDURE AND RESULTS
Experiment 1 Procedure. This experiment was conducted from December 12, 1978, to January 9, 1979. The birds were fed three different basal diets: a corn-soy diet (A), a diet with 13% animal protein concentrates (B), and a diet with 13% animal protein concentrates plus 7.5% bakery product (C). The composition of the diets for the three different growing products are given in Tables 1, 2, and 3. Basal diets A and B were fed unsupplemented, supplemented with copper sulfate (125 ppm copper), with copper (125 ppm) plus chromium (20 ppm) and molybdenum (2.5 ppm), and with copper (125 ppm) minus the B complex vitamins — pyridoxine, thiamine, and biotin — present in the vitamin premix for the other diets. Because of limitations of space, diet C (unsupplemented with 125 ppm copper) was not included, but the other three treatments were used. The diets had the same energy and protein levels and calorie to protein ratios within each growing period. Results. No significant differences were
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S GW
OILY BIRD SYNDROME
processing plant and those after processing in the commercial plant clearly showed that to observe OBS as seen in the field, it is essential to process the birds through a commercial plant. Experiment 2 Experimental. This experiment was conducted from February 27, 1979, to April 17, 1979. The various dietary treatments outlined in Table 6 were used in this study. All of the birds were fed the same basal diet during the first 3 weeks (A, Table 1). Three series of diets were formulated to have the same energy and calorie to protein ratios, but one contained poultry oil, a second animal tallow in place of poultry oil, and the third a high level of animal proteins and bakery product. Three other treatments included a lower calorie to protein ratio with the same high energy level and low energy levels with the wide and narrow calorie to protein ratios. Results, No significant differences were observed in final body weight or feed/gain from 3 to 7 weeks of age (Table 6). Feed-gain ratios were considerably higher for birds fed die two lower energy regimens (Treatments 5 and 6),
TABLE 5. Effect of supplementation of different diets with minerals and vitamins on fatness and oiliness in 7-week-old broilers (Experiment l)1 Basal diets 2 SG W AAA (corn-soy)
BBB (animal protein)
CCC (animal protein + bakery products)
Elements added, vitamins removed
Abdominal fat (% BW)
Liver weight (g/kg BW)
Fat liquidity score
Oily birds 3
None Cu Cu, Cr, Mo Cu-vitamins
20.9 19.6 20.4 20.3
1.4 2.0 1.8 1.8
31.6 45.0 22.2 35.3
Mean
3.1 3.3 3.4 3.3 3.3b
20.3
1.8
33.8
None Cu Cu, Cr, Mo Cu-vitamins
3.5 3.5 3.3 4.0
20.6 20.4 20.5 20.5
2.0 2.0 1.9 2.2
41.2 38.9 15.8 26.7
Mean
3.6 a
20.5
2.0
30.4
Cu Cu, Cr, Mo Cu-vitamins
3.6 3.5 3.4 3.5^
21.3 21.8 21.5
1.7 1.8 1.5
15.8 10.5 20.0
21.5
1.7
15.1
Mean
(%)
a' b Average values for basal diets not followed with the same letter differ significantly (P<.05). 1
Mean of 15 to 20 birds per treatment.
2
S = starter, G = grower, and W = withdrawal; see Tables 1, 2, and 3 for diet composition.
3
Percentage of birds with an oily feel and/or pockets on back scored in University processing facility.
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observed in final body weight and feed efficiency from 3 to 7 weeks of age (Table 4). Abdominal fat as a percent of body weight was significantly higher for birds fed the basal diets containing animal by-products and animal by-products plus bakery product over that of birds fed the corn-soy diet, but the difference was relatively small (Table 5). No significant difference was observed in liver weight per unit of body weight, fat liquidity score of the abdominal fat, and percent of oily birds. No evidence was obtained that, including animal protein concentrates and bakery product in the diets, increased incidence of oily birds as measured in this experiment. The remaining birds processed through a commercial processing plant exhibited a high incidence of oiliness and of pockets on the backs. In contrast, the commercial birds being processed along with the experimental birds showed little or no evidence of OBS. Therefore, the dietary and environmental laboratory conditions under which the experimental birds were raised resulted in the reproduction of the syndrome. A comparison of the appearance of the birds after processing in the University
2261
2262
JENSEN ETAL.
TABLE 6. Effect of energy level, calorie to protein ratio (C:P), tallow, and a combination of animal and bakery products on performance of 7-week-old broilers (Experiment 2) Diet description C •P
Dipt ^
SGW
1 2 3 4 5 6
AAA A G G (Tallow) A C C ( A P + BP) 3 AEE ADD AFF
G
W
Body weight2 7 weeks
157 157 157 127 157 127
181 181 181 146 181 146
1977 1980 1890 1984 1923 1953
!
ME (kcal/kg)
1
Feed/gain 3 - 7 weeks
(g)
3300 3300 3000 3300 3100 3100
2.04 2.02 2.09 2.00 2.23 2.13
S = starter, G = grower, and W = withdrawal; see Tables 1, 2, and 3 for diet composition.
2
No significant difference. Standard deviation = 85.43.
3
AP + BP = animal proteins and bakery waste.
but variability among pens was great so that no statistical significance was observed. Rubber bands of different colors were placed on some of the birds several days before the marketing period to identify specific treatments as they passed through the commercial processing plant. Some of the rubber bands were too tight and resulted in restriction of blood flow to the feet, which contributed to the variability among pens. No significant difference in percentage abdominal fat was observed between birds fed the corn-soy diet (Treatment 1) and the corn-soy diet supplemented with animal protein concentrates and bakery product (Treatment 3, Table 7). Reducing the calorie to protein ratio in either the high or low energy diets (Treatments 4 and 6) significantly reduced abdominal fat, whereas no significant reduction in fat was detected when the energy level was lowered while maintaining the same calorie to protein ratio (Treatments 3 and 5). Again, no significant differences were observed in liver weight per unit of body weight. Oiliness score of the birds at the commercial processing plant was significantly lower when birds were fed a narrow calorie to protein ratio (Table 7). Reducing the energy level of the corn-soy diet without changing the calorie to protein ratio (Treatment 5 vs. 1) also significantly reduced the oiliness score. Incidence of OBS was high among all of the dietary treatments and the incidence for birds fed the diet with animal tallow (Treatment 2) was significantly
higher than most of the other treatments. Incidence of the most severe form (score 2) of OBS tended to be lower for those fed the lower energy diets. Commercial birds passing through the processing line at the same time showed little evidence of the syndrome. Thus, OBS had been produced again under laboratory conditions. Experiment 3 Procedure. Experiment 3 was conducted from May 8, 1979, to June 26, 1979. All the birds were fed the same diet (A, Table 1) for the starter period of the study. After 3 weeks, all birds were fed diets with the same energy level, but in addition to the cornsoy basal diet one diet was formulated to contain 10% distillers dried grains with solubles. The corn-soy basal diet was also fed in pelleted and unpelleted form. Because temperature appeared to be a factor in the reproduction of the syndrome, one treatment of birds was maintained in a different broiler house without space heaters. Temperatures here were generally 3 to 5 C cooler during the study than in the house where the other birds were maintained. Two other treatments involved the raising of protein levels resulting in the feeding of diets with more narrow calorie to protein ratios. Results. No significant differences were observed in final body weight (Table 8). Feed efficiency was significantly better for birds fed the mash diet (Treatment 3) in comparison to the pelleted one (Treatment 1, Table 8). The
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Treatment no.
6
5
4
3
2
1
AAA A G G (Tallow) A C C (AP + BP) 6 AE E ADD A F F
S G W
3300 3300 3300 3300 3100 3100
(kcal/kg)
ME
157 157 157 127 157 127
G
C:P
Diet descripl:ion
181 181 181 146 181 146
W
3.5* 3.6^ 3.6a 3.0bc 3.4ab 2.7C
(% BW) 2
Abdominal fat
AP + BP = animal proteins and bakery waste.
Scores ranged from 0 for no oily pockets to 2 for large pockets.
Mean of about 225 birds per treatment.
Oiliness scores ranged from 1 for nonoily to 5 for extremely oily skin. Standard deviation = .81.
Mean of 20 birds per treatment.
S = starter, G = grower, and W = withdrawal, see Tables 1,2, and 3 for diet composition.
' ' ' Values within each column not followed by a common letter are significantly different (P<.05).
Treatment no.
Diet 1
17.9 17.0 18.6 18.7 19.4 18.0
(g/kg BW
Liver weight
TABLE 7. Effect of energy level, calorie to protein ratio (C:P), tallow, and a combination of an on fattening and incidence of OBS in 7-week-old broilers (Experiment
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2264
JENSEN ET AL.
TABLE 8. Effect of calorie to protein ratio (C:P), distillers dried grains with solubles (DDGS), pelleting, and environmental temperature on performance of 7-vieek-old broilers (Experiment 3) Treatment description _____ SGW
G
i W
1 2 3 4 5 6
AAA AHH AAA AAA AEE AEI
157 157 157 157 127 127
181 181 181 181 146 127
Treatment
DDGS Mash3 Lower Temperature"
Body weight2 (g)
Feed/gain 3 - 7 weeks
1900 1976 1855 1865 1909 1899
2.06 a 1.94 ab 1.87b 2.08 a 1.94 ab 1.98 ab
' Values without a common letter are significantly different (P<.05). 1
S = starter, G = grower and W = withdrawal; see Tables 1, 2, and 3 for diet composition.
2
Standard deviation = 75.73.
3 Diets in this treatment were fed in mash form from 3 to 7 weeks. Diets for all other treatments were fed in pelleted form. 4
Birds in this treatment were kept in a separate house where space heaters were not used.
mash feed tended to bind in the tube feeders used in the study and had to be checked two or three times a day to be sure feed was available to the birds. Less feed wastage may have occurred as a result of this practice. Abdominal fat as a percent of body weight was significantly less for the treatment fed the narrow calorie to protein ratio (127) from 3 to 7 weeks of age (Treatment 6) in comparison to the birds fed the corn-soy diet in the same house (Treatment 1, Table 9). Other treatment means were not significantly different. Oiliness score was significantly less for birds maintained in the lower temperature house (Treatment 4) than those in the higher temperature house (Treatment 1) even though the diets were the same. Feeding mash diets with more narrow calorie to protein ratios also significantly reduced the oiliness score below that of the birds fed the corn-soy control diet (Table 9). Incidence of OBS was significantly lower for birds fed mash and for those maintained in the lower temperature house. Incidence of OBS was reduced by feeding more narrow calorie to protein ratios during the growing and withdrawal stages (Treatments 5, and 6, Table 9). Differences in the more severe form of OBS (score 2) were particularly striking among the various treatments. Distillers dried grains with solubles did not significantly reduce abdominal fat pad, oiliness score, or incidence of OBS.
DISCUSSION The oily bird syndrome was successfully reproduced in these experiments under laboratory conditions. The experimental birds with the condition had a "greasy" appearance and large pockets filled with an oily fluid on their back. These birds were similar to those seen in commercial processing plants at the height of the oily bird problem in Georgia during the summer and fall of 1978. Processing of the laboratory-reared broilers apparently must be done in a commercial processing plant for OBS to be fully expressed. The birds processed in the University facility failed to exhibit the same incidence and severity of OBS as seen in the commercial plant. Garrett (1976) emphasized that stress in commercial processing plants was a major factor affecting the incidence of OBS. Apparently the batch picker used in the University facility coupled with perhaps a different scalding temperature and time did not sufficiently stress the skin tissues to precipitate a high incidence of OBS. Fletcher and Thomason (1980) observed higher skin oiliness scores in birds subjected to higher scald temperatures and longer picking times. Although the specific cause of OBS was not discovered in these investigations, some factors appear to have been eliminated and others confirmed as being involved in the production of the syndrome. The idea that feeding diets
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Treatment no.
7
6
5
4
3
2
157 157 157 157 127 127
G
C:P .
181 181 181 181 146 127
W
DDGS Mash 6 Lower t e m p e r a t u r e 7
Treatment
T r e a t m e n t descriiption
3.9a 3.6ab 3.5*b 3.7ab 3.5ab 3.3b
Abdominal fat <% BW) 2
Birds in this treatment were kept in a separate house where space heaters were not used.
Diets in this treatment were fed in mash form 3 to 7 weeks. Diets for all other treatments were fed in pelleted form
OBS scores ranged from 0 for no oily pockets to 2 for large pockets.
Oiliness scores ranged from 1 for nonoily to 5 for extremely oily skin. Standard deviation = 1.09.
Mean of about 160 birds per treatment.
S = starter, G = grower and W = withdrawal; see Tables 1, 2, and 3 for diet composition. Mean of 20 birds per treatment.
' ' Values within each column without a common letter are significantly different (P<.05).
AAA A H H AAA AAA A E E A E I
1 2 3 4 5 6
1
SG W
no.
Diet
1
TABLE 9. Effect of calorie to protein ratio (C:P), distillers dried grains with solubles (DDGS), pelleting, fattening and OBS in 7-week-old broilers (Experiment 3)
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JENSEN ETAL.
under high temperature conditions. The specific reason for the development of OBS under conditions of elevated ambient temperature and high energy rations with wide calorie to protein ratios is not apparent from these studies. The basic biochemical changes occurring in the skin and other tissues of the animal by these environmental and dietary conditions need to be determined in order to discover means by which the syndrome can be prevented under all conditions. Garrett (1976) hypothesized that a nutritional deficiency or imbalance resulted in a reduced rate of connective tissue synthesis resulting in an impairment in the structural integrity of the skin and adipose tissue. Smith et al. (1976) obtained evidence for a reduced collagen content in broiler skin tissue by feeding high energy diets during a period of high environmental temperature. Subsequent studies, however, failed to confirm this observation in birds raised under cooler temperature conditions (Smith et al, 1977). Further work is needed on the effect of environmental temperature and dietary changes on collagen content and other possible changes in the tissues of broilers to attempt to find the basic cause of OBS. ACKNOWLEDGMENTS
The authors are indebted to W. J. Schimmel and John Kiker, Central Soya, Athens, GA, for their cooperation in allowing the birds to be observed and scored in a commercial processing plant and to Hoffmann-LaRoche, Inc., Nutley, NJ for supplying the vitamin premixes used in Experiment 1. REFERENCES Fletcher, D. L., and D. M. Thomason, 1980. The influence of environmental and processing conditions on the physical carcass quality factors associated with Oily Bird Syndrome (OBS). Poultry Sci. 59:731-736. Garrett, R. L., 1976. Update on the "Oily Bird" Syndrome. Proc. 11th Nat. Mtg. Health and Condemnation. DE-MD, Oct. 20. Horvat, R. J., 1978. Oily bird skin lipids. Poultry Sci. 57:1187. Smith, T. W., Jr., J. R. Couch, C. R. Creger, and R. L. Garrett, 1976. The relationship of sex, dietary energy and meat protein with collagen in broiler skin tissue. Poultry Sci. 55:2093-2094. Smith, T. W., Jr., J. R. Couch, R. L. Garrett, and C. R. Creger, 1977. The effect of sex, dietary energy, meat protein, ascorbic acid and iron on broiler skin collagen. Poultry Sci. 56:1216-1220. Steele, R.G.D., and J. H. Torrie, I960. Principles and procedures of statistics. McGraw-Hill, New York, NY.
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with a high concentration of polyunsaturated fatty acids is a major etiological factor for OBS apparently can be eliminated. Neither Garrett (1976) nor Horvat (1978) were able to demonstrate any differences in fatty acid composition of the skin lipids in birds with and without the syndrome. In the second experiment of the present investigations, feeding a diet with a more saturated fat (tallow) to chicks from 3 to 7 weeks of age increased the incidence of OBS over that of birds fed a more unsaturated fat (poultry oil). Garrett (1976) indicated that many broiler operations reporting OBS fed high levels of animal by-products and dried bakery product. Direct comparison of birds fed diets containing 13% animal by-products coupled with 7.5% bakery product with those fed a corn-soybean meal diet failed to reveal any major difference in the incidence of OBS between the two types of diets. A significantly higher percent of abdominal fat was observed in Experiment 1 in birds fed diets with a higher level of animal products, but this was not confirmed in the second experiment. Garrett (1976) also suggested that nutrient deficiencies might be involved in the etiology of OBS. Distillers dried grains with solubles, a concentrated source of several minerals and vitamins and perhaps other unidentified factors, failed to reduce the incidence of OBS. Adding a high level of copper, supplements of molybdenum and chromium, and elimination of pyridoxine, thiamine, and biotin from the vitamin premix did not seem to affect appearance of broilers (but only the birds processed at the University facility were identified by treatments). Feeding rations with more narrow calorie to protein ratios reduced the incidence of OBS but did not completely prevent it under the environmental and other dietary conditions used to produce the syndrome. Other factors must play an important role. Feeding of the corn-soy diet as a mash from 3 to 7 weeks of age significantly reduced the incidence of the syndrome (Table 9). Growth rate was slightly less for these birds than for those fed the pelleted diets which may have influenced the incidence of the syndrome. A major factor in reproducing OBS under laboratory conditions appears to be the ambient temperature at which the birds are maintained. Observations in the commercial broiler industry and the data from this study indicate that the problem is much more severe in birds raised