Effect of Halofuginone on Broiler Skin Strength when Used in a Shuttle Anticoccidial Program1

Effect of Halofuginone on Broiler Skin Strength when Used in a Shuttle Anticoccidial Program1 N. G. ZIMMERMANN,2 K. D. CHRISTENSEN,3 and C. L. WYATT Washington State University, Puyallup Research and Extension Center, 7612 Pioneer Way E., Puyallup, Washington 98371-4998 P. TWINING

ABSTRACT Continuous feeding of the anticoccidial halofuginone to broilers is associated with reduced skin tensile strength and increased skin tearing during processing. The possible mitigating effect of shuttle administration of halofuginone and salinomycin to female broilers was evaluated. Halofuginone or salinomycin were included in the starter and grower diets in all four possible combinations, with anticoccidial omitted from the finisher diets. Starter, grower, and finisher diets were fed to broilers through 3, 6, and 7 wk of age, respectively. Skin strength of pullets fed a diet based on milo and corn (NW) vs a diet based on corn was also compared in a factorial arrangement. Two further treatments were also included: 1) halofuginone-only NW diet supplemented with 2,500 ppm ascorbic acid from 0 to 7 wk; and 2) NW diet reared on wire floor without anticoccidial treatment. Skin tensile strength was determined at 3, 6, and 7 wk of age. Dietary composition had no effect upon skin strength or BW of broilers. Addition of ascorbic acid to the diet containing halofuginone anticoccidial did not improve skin strength. Continuous feeding of halofuginone reduced skin strength whereas withholding anticoccidial and continuous feeding of salinomycin resulted in high skin strength. When halofuginone was used in shuttle feeding programs with salinomycin, there were no differences in skin strength at 7 wk of age compared to birds that were continuously treated with salinomycin. These results suggest halofuginone may be used in a shuttle program either during the starter or grower phase without adverse affect on skin tensile strength at slaughter. (Key words: halofuginone, saHnomycin, broiler, skin strength, shuttle anticoccidial program) 1994 Poultry Science 73:326-330

INTRODUCTION

Received for publication May 10, 1993. Accepted for publication October 14, 1993. iProject 0979. Animal Sciences Scientific Paper Number 8083. College of Agriculture and Home Economics Research Center, Washington State University, Pullman, WA 99164. 2 To whom correspondence should be addressed. 3 Current Address: Draper Valley Farms, P.O. Box 838, 1000 Jason Lane, Mount Vernon, WA 98273.

Halofuginone has been shown to be an effective anticoccidial feed additive (Rotibi and McDougald, 1988; Grant and Kling, 1989; Mathis et al, 1990; Hanssens et al, 1991; Zimmermann, unpublished data). However, it has also been demonstrated that halofuginone is largely responsible for undesirable skin weakening and tearing when included in the diet of broilers (Angel et al, 1985; Casey et al, 1989, 1992; Granot et al, 1991; Crosley et al, 1992;

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Recon Inc., Taylors Island, Maryland 21669

RESEARCH NOTE

^Hubbard Farms, Walpole, NH 03608. 5 Peterson Industries, Decatur, AR 72722. 'Hunter Products, Inc., Bridgewater, NJ 08807.

tearing effect of halofuginone is not a universal phenomenon, another purpose of this experiment was to explore the interaction of shuttle anticoccidial program with dietary composition on skin strength. MATERIALS AND METHODS Each of 10 treatments was administered to 50 Hubbard4 x Peterson5 female broiler chicks reared in a 1.23 x 3.68 m pens. The main experiment was a two dietary composition by four anticoccidial treatment factorial arrangement. Broiler chickens were fed either a "Northwest" diet based on milo and corn or a "Southeast" diet based on corn as the primary cereal grain. Birds consumed starter, grower, and finisher, mash diets ad libitum (Table 1). Only starter and grower diets contained anticoccidial and were fed through 3 and 6 wk of age, respectively. All four possible combinations of halofuginone (3 mg/kg) and salinomycin (61 mg/kg) were included within the two dietary compositions. Two additional treatments were also included. The first group of chicks received the halofuginone:halofuginone (starter:grower) Northwest diet supplemented with 2,500 ppm ascorbic acid from Day 1 to 7 wk of age. The second group of chicks was fed the Northwest diet without anticoccidial treatment. This later treatment was reared on a raised wire platform to minimize bird contact with fecal material and coccidia. At the termination of the starter, grower and finisher feeding phases (3 wk, 6 wk, 7 wk of age) 14 randomly selected birds from each treatment were individually weighed and killed by cervical dislocation. Skin tensile strength was determined as described by Christensen et al (1994). Skin from both the left and right thigh regions of each bird was excised, then a template, using the superior midline as a landmark, was used to measure and cut a rectangle of skin with a 1-cm breaking width from the defeathered thigh region. A mechanical force gauge (Hunter6 Accuforce™) was used to determine the kilograms of weight needed to break 1 cm of skin. The mean value obtained from the measurement of the left and right sides was used for statistical analysis.

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Christensen et ah, 1994). Christensen et al. (1994) reported the skin weakening effect of halofuginone to be more severe in females but unrelated to ambient temperature or added dietary fat. The weakened skin is a result of reduced collagensynthesizing ability of fibroblast cells (Granot et al, 1991); which causes lower collagen concentration in the skin (Granot et al, 1991; Christensen et al, 1994) and reduced dermis thickness (Christensen et al, 1994). It could be argued that halofuginone should not be used because it has undesirable side effects. However, it is well documented that coccidia species mutate and become resistant to anticoccidials (Jeffers, 1974; Weppelman et al, 1977; Rotibi and McDougald, 1988; McDougald et al, 1990), thus warranting companies to rotate anticoccidials prior to resistance. It seems prudent to utilize halofuginone to the greatest extent possible even if only to preserve the efficacy of other anticoccidials. Proline must be hydroxylated into hydroxyproline to be incorporated into collagen (Kuhn, 1987). This reaction is mediated by the specific enzyme prolyl hydroxylase requiring ascorbic acid as a reducing agent (Blank and Peterkofsky, 1975). However, Smith et al (1977) reported that the addition of 1000 ppm ascorbic acid to the feed failed to alter skin collagen in broilers. Theoretically, halofuginone could be increasing the requirement for ascorbic acid when fed to broilers during the early growing period. Diet composition may also play a role in the response birds have to halofuginone because the incidence of skin tearing varies greatly across the United States (Herb Kling, 1989; Hoechst-Roussel Agri-Vet Company, Sommerville, NJ 08876, personal communication). The purpose of this experiment was to determine the severity of halofuginonerelated skin weakening in broilers if fed in rotation, i.e., shuttle feeding, with the anticoccidial salinomycin. Because the skin

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ZIMMERMANN ET AL. TABLE 1. Formulation of corn-soybean meal-based diets and com-milo-soybean meal-based diets labeled Southeastern and Northwestern, respectively

Ingredients and content

Southeastern formulation Finisher

51.30 36.70

58.00 30.05

63.13 25.05

.05 7.00 2.50 1.20 .35 .27 .63

.05 7.00 2.50 1.30 .25 .27 .58

3,207 9.48 22.38 .89 1.25

3,279 9.67 19.85 .84 1.08

Northwestern formulation Starter (<>/,,}

Corn Soybean meal Milo Anticoccidial1 Blended fat Meat and bone meal Defluorinated phosphate Limestone Salt Other2 Calculated nutrient content ME, kcal/kg Crude fat Protein TSAA Lysine

7.00 2.50 1.30 .275 .25 .495 3,331 9.81 17.89 .70 .94

Grower

Finisher

—...

38.23 29.80 20.00 .05 7.00 2.50 1.30 .25 .275 .595

41.45 36.54 10.00 .05 7.00 2.50 1.20 .35 .27 .64 3,193 9.38 22.33 .90 1.24

3,250 9.48 19.77 .84 1.05

38.35 24.80 25.00 7.00 2.50 1.30 .25 .285 .515 3,294 9.57 17.82 .70 .91

iDependent upon treatment, either halofuginone (3 mg/kg) or salinomycin (61 mg/kg) was used as the anticoccidial drug. 2 Trace ingredients were included to meet or exceed National Research Council (1984) requirements.

Statistical Analysis Data from the first 8 treatments (Table 2) were analyzed at 3,6, and 7 wk of age as a 2 x 4 factorial using dietary composition and anticoccidial program as the main effects. All 10 treatments were analyzed by oneway ANOVA at each age. All data from the forgoing models were also analyzed including age as a main effect. Each ANOVA was performed using SAS® (1987) General Linear Means procedures; Duncan's (1955) multiple range test (P < .05) was used to make comparisons. RESULTS AND DISCUSSION The factorial analyses of dietary composition and anticoccidial program data revealed that dietary composition had no significant main effect or interaction upon skin strength (Figure 1) or BW of broilers at 3, 6, and 7 wk of age. These results are in concurrence with Christensen et al. (1994) and suggest that dietary composition, as used in this experiment, is not

involved in halofuginone-induced skin weakening. Anticoccidial program affected skin tensile strength (P < .0005) at

H:H

H:S S:H ANTICOCCIDIAL

FIGURE 1. Effect of diet and anticoccidial program main effects on skin tensile strength (X ± SEM) at 3, 6, and 7 wk of age. Major cereal grains of the Northwest (NW) diet were corn and milo; the Southeast (SE) diet excluded milo. The anticoccidials halofuginone (H) and salinomycin (S) were fed in all combinations from 0 to 3 wk and 4 to 6 wk of age and are expressed as drug fed 0 to 3 wk:drug fed 4 to 6 wk. Anticoccidial was not fed during Week 7. Significant age by anticoccidial treatment interaction occurred; means with no common letter differ significantly (P S .05).

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Grower

Starter

RESEARCH NOTE

not improve skin tensile strength at any age. This observation suggests halofuginone is not reducing collagen synthesis by interference with ascorbic acid and thus reducing conversion of proline to hydroxyproline. Treatment 10, lacking any anticoccidial, had skin strength comparable with skin strength in the treatments of salinomycin only. However, despite being reared on a wire floor, some birds became infected with coccidiosis; most also developed severe breast blisters. When skin tensile strength was analyzed including age as a main effect, significant (P < .0001) age by anticoccidial program and age by treatment interactions occurred. These interactions may have occurred because 1) skin strength decreased between 6 and 7 wk of age in the salinomycin:salinomycin anticoccidial program whereas skin strength in the other programs remained constant (Figure 1) or 2) because skin tensile strength in the salinomycin:halofuginone anticoccidial program increased only 11% between 3 and 6 wk of age, whereas the average

TABLE 2. Effect of anticoccidial treatment and dietary composition on skin strength and body weight of female broilers at 3, 6, and 7 wk of age Anticoccidial treatment2 TrPAtm p n f

X 1 CCi U l IC1 H

number

0 to *•* A *" ** Dietary composition 1 wk 7 wk wk

1 Northwest 2 Southeast 3 Northwest 4 Southeast 5 Northwest 6 Southeast 7 Northwest 8 Southeast 9 Northwest 10 Northwest Pooled SEM Probability of difference

H H H H S

s s sH N

H H

s s

H H

s sH N

N N N N N N N N N N

Skin tensile strength3 3 wk 2.03b 1.85b 1.70b 1.75b 3.08" 2.73" 2.60 2.95" 1.98b 3.0ia .14 <.0001

6 wk

7 wk

• (kg/cn,> 2.77°" 2.69* 2.85** 2.97cd 3.62ab 3.34« 3.471* 3.41abc 3.27
Body weight 3 wk 642abc 65labc 604« 603<= 674ab 619*

621* 648abc 611c 685a .18 .0091

6 wk

7 wk

— (g) 1,763 1,716 1,769 1,758 1,816 1,834 1,759 1,750 1,813 1,875 36 .0819

2,091 2,169 2,119 2,051 2,222 2,182 2,122 2,219 2,173 2,157 50 .3273

"Means in columns within age group with no common superscript differ significantly (P £ .05); n = 14 with the exceptions of Treatments 4, 6, and 9 when n = 13 on Week 7. 1 The Northwest diet was based on corn and milo meal, whereas the Southeast diet was based on corn as the primary cereal. Diet of Treatment 9 was supplemented with 2,500 ppm ascorbic acid throughout experiment. Broilers in Treatment 10 were reared on a wire floor. 2 H = halofuginone; S = salinomycin; N = none. 3Skin tensile strength is the force required to break a 1-cm width of defeathered thigh region skin; mean strength from both left and right sides used for analysis.

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each age. Continuous feeding of halofuginone through 3 wk of age was associated with a significant decrease in skin strength at 3 wk of age, in agreement with Christensen et al. (1994). Continuous feeding of halofuginone to broilers through 6 wk of age resulted in significantly lower skin tensile strength compared with the other three anticoccidial feeding programs. At 6 wk of age, prior to anticoccidial withdrawal, pullets in both of the shuttle anticoccidial treatments had lower skin tensile strength than birds maintained on salinomycin exclusively. But by 7 wk of age, when halofuginone was used in a shuttle anticoccidial program with salinomycin, there were no significant differences in skin strength compared with the birds that were treated with only salinomycin. The ANOVA of data from all 10 treatments (Table 2) shows that 3-wk BW of broilers was lower in some treatments, but BW was not significantly affected at 6 or 7 wk of age. Addition of ascorbic acid to the diet containing halofuginone did

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ACKNOWLEDGMENTS

The authors thankfully acknowledge the support given by Draper Valley Farms, Mount Vernon, WA 98273, and the Hoechst-Roussel Agri-Vet Company, Somerville, NJ 08876. REFERENCES Angel, S., Z. G. Weinberg, O. Polishuk, M. Heit, I. Plavnik, and I. Bartov, 1985. A connection between a dietary coccidiostat and skin tears of female broiler chickens. Poultry Sci. 64:294-296. Blank, T. J., and B. Peterkofsky, 1975. The stimulation of collagen secretion by ascorbate as a result of increased proline hydroxylation in chick embryo fibroblasts. Arch. Biochem. Biophys. 171: 259-267. Casey, N. H., R. I. Crosley, and G. A. Smith, 1992. Influence of continuous dietary halofuginone on broiler skin tensile strength and growth performance. J. S. Afr. Vet. Assoc. 63:16-19. Casey, N. H., G. A. Smith, and R. I. Crosley, 1989. The influence of breed and sex on the incidence on mortalities and skin tears in broiler chickens. J. S. Afr. Vet. Assoc. 60:102-103. Christensen, K. D., N. G. Zimmermann, C. L. Wyatt, R. J. Buhr, and P. Twining, 1994. Dietary and environmental factors affecting skin strength in broiler chickens. Poultry Sci. 73:224-235. Crosley, R. I., N. H. Casey, G. A. Smith, and B. Roosendaal, 1992. Influence of phased inclusion of halofuginone on broiler skin tensile strength

and growth performance. J. S. Afr. Vet. Assoc. 63:5-11. Duncan, D. B., 1955. Multiple range and F tests. Biometrics 11:1-42. Granot, I., I. Bartov, I. Plavnik, E. Wax, S. Hurwitz, and M. Pines, 1991. Increased skin tearing in broilers and reduced collagen synthesis in skin in vivo and in vitro in response to coccidiostat halofuginone. Poultry Sci. 70:1559-1563. Grant, R., and H. Kling, 1989. The efficacy of halofuginone hydrobromide against field isolates of Eimeria species during three years of use. Poultry Sci. 68:(Suppl. l):61.(Abstr.) Hanssens, Q. J., R. J. Grant, and H. F. Kling, 1991. Comparative efficacy of commonly used anticoccidials from 1987 to 1990. Poultry Sci. 70: (Suppl. l):162.(Abstr.) Jeffers, T. K., 1974. Eimeria acervulina and E. maxima: Incidence and anticoccidial drug resistance of isolants in major broiler-producing areas. Avian Dis. 18:331-342. Kafri, I., J. A. Cherry, D. E. Jones, and P. B. Siegel, 1985. Breaking strength and composition of the skin of broiler chicks: Response to dietary calorie-protein ratios. Poultry Sci. 64:2143-2149. Kuhn, K., 1987. The classical collagens: Types I, II, and HI. Pages 1-42 in: Structure and Function of Collagen Types. R. Mayne and R. E. Burgeson, ed. Academic Press, Inc., New York, NY. Mathis, G. R., A. L. Fuller, and L. R. McDougald, 1990. Turkey coccidiosis: Effect of control programs on oocyst shedding patterns and sensitivity to anticoccidial drugs. Poultry Sci. 69:(Suppl. l):89.(Abstr.) McDougald, L. R., J. M. Gilbert, L. Fuller, X. M. Quan, and A. Rotibi, 1990. Improvements in coccidiosis control by the use of roxarsone in combination with ionophores. Poultry Sci. 69: (Suppl. l):90.(Abstr.) National Research Council, 1984. Nutrient Requirements of Poultry. 8th rev. ed. National Academy Press, Washington, DC. Rotibi, A., and L. R. McDougald, 1988. Response of Canadian field isolates of chicken coccidia to commercial anticoccidial drugs. Poultry Sci. 67: (Suppl. l):31.(Abstr.) SAS Institute, 1987. SAS/STAT® Guide for Personal Computers. Version 6 Edition. SAS Institute Inc., Cary, NC. Smith, T. W., 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. Weinberg, Z. G., S. Angel, and C. Navrot, 1986. The effects of sex, age, and feed on tensile strength of broiler skin. Poultry Sci. 65:903-906. Weppelman, R. M., G. Olson, D. A. Smith, T. Tamas, and A. Van Iderstine, 1977. Comparison of anticoccidial efficacy, resistance, and tolerance of narasin, monensin, and lasalocid in chicken battery trials. Poultry Sci. 56:1550-1559.

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increase in the other programs was 47%. Decreasing skin strength during the withdrawal period (7 wk) has also been observed by Kafri et al. (1985) and Christensen et al. (1994). Broiler skin strength, especially in pullets, is highly variable but has been demonstrated to increase erratically with age (Kafri et al, 1985; Weinberg et al, 1986; Casey et al, 1992; Christensen et al, 1994). Crosley et al. (1992) suggested withdrawal of halofuginone from broiler diets for 7 d could result in compensatory overstrengthening of skin. This hypothesis is not supported either by the results of this experiment nor those of Christensen et al. (1993). However, agreement exists that broiler skin strength can be maintained by shuttle administration of halofuginone.