Metabolic Disturbances in Male Broilers of Different Strains. 1. Performance, Mortality, and Right Ventricular Hypertrophy

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1 Metabolic Disturbances in Male Broilers of Different Strains. 1. Performance, Mortality, and Right Ventricular Hypertrophy ELISABETH GONZALES,*,1 JOHAN BUYSE, TÂNIA SAYURI TAKITA,* JOSÉ ROBERTO SARTORI,* and EDDY DECUYPERE *Faculty of Veterinary and Animal Production, UNESP, CP 560, Botucatu, São Paulo, Brazil, and Faculty of Agricultural and Applied Biological Sciences, Catholic University of Leuven, Kardinaal Mercierlaan 92, 3001 Heverlee, Belgium ABSTRACT Two trials were carried out to test the susceptibility for metabolic disturbances of different strains of male broilers. In, 1,890 male chickens were allotted in a randomized block design with seven treatments (Arbor Acres, Avian Farms, Cobb-500, Hubbard-Peterson, ISA, Naked Neck, and Ross) and six blocks of 45 chickens. involved 2,184 male chickens of six strains (Arbor Acres, Avian Farms, Cobb 500, Hubbard-Peterson, ISA Naked Neck, and Ross) allotted in seven complete blocks of 52 birds. The same management system was adopted for all birds, reared up to 42 d in an open house during late winter () or late autumn (). The most marked differences observed among the strains tested was the lower BW and higher feed conversion of Naked Neck broilers. Total percentage mortalities were high among the most productive broilers, being more than 50% due to sudden death (SDS) and ascites syndrome (AS). No Naked Neck birds died as a consequence of these disturbances and the total mortalities were significantly lower (P 0.05) than the other strains. The ratio of right ventricle weight to total ventricle weight of the dead birds was over 0.25, except for Naked Neck birds, which presented a nonhypertrophic ratio. The two trials confirmed the relationship between high productivity and high incidence of SDS and AS and indicated that Naked Neck male broilers are resistant to these metabolic disturbances. (Key words: ascites syndrome, broiler, male, strains, sudden death syndrome) 1998 Poultry Science 77: INTRODUCTION The mortality incidence due to ascites syndrome (AS) and Sudden Death Syndrome (SDS) in broilers reared even under excellent management has recently increased worldwide, as well as in Brazil (Gonzales et al., 1994; Maxwell and Robertson, 1997). Although many efforts have been made to clarify the pathophysiological events of these disturbances, the primary causes inducing these syndromes remain to be clarified. There is enough evidence to support the idea that the morbidity and mortality due to AS and SDS are determined by metabolic disturbances secondary to broiler breeding programs for high weight gain and low feed conversion. The occurrence of AS and SDS could be a consequence of high metabolic rates and has been attributed to an intrinsic susceptibility of broilers to anoxic conditions, even at sea level, which could be related to a lower proportional growth of the cardiorespiratory system together with high deposition of muscle in a very early stage of posthatch development (Julian and Bowes, 1987; Peacock et al., 1990; Julian, 1993; Grashorn, 1994). Male broiler flocks with good performance show the highest AS and/or SDS incidence. Predisposition factors leading to AS and/or SDS mortality rates are high nutritional density, pelleted ration, ad libitum feeding programs, continuous illumination, and low ambient temperature among others (Ononiwu et al., 1979; Gonzales, 1992; Coello et al., 1993a,b). As BW gain is negatively correlated with reproductive performance, broiler breeding companies try to make a balance between number of chickens produced per hen with broiler weight gain by working with at least two parent lines, one male and one female (Crawford, 1990). Total mortality and that due to ascites are higher in the male parent lines, which have the capability of fast growth and high muscle deposition, Received for publication January 20, Accepted for publication June 24, To whom correspondence should be addressed: Egonzales@ botunet.com.br Abbreviation Key: AS = ascites syndrome; RV:TV = right ventricular to total ventricular ratio; SDS = Sudden Death Syndrome

2 METABOLIC DISTURBANCES IN BROILERS 1647 than in the female parent lines (Decuypere et al., 1994; Dewil et al., 1996). Also, Gonzales et al. (1994) observed differences in the incidence of SDS mortality between male and female broilers from several commercial strains. Birds known as Naked Necks contain the Na gene (Mérat, 1990). Breeder companies have been exploiting Naked Neck birds, commonly known as Label Rouge,2 in an attempt to meet increased market demand for more tasteful poultry meat. Recently, interest has increased concerning the presence of the Naked Neck gene because of its association with heat tolerance (Mérat, 1990; Ayyagari, 1996; Singh et al., 1996). Nevertheless, no indications about the susceptibility of these birds to either AS or SDS were found, especially when such birds are submitted to environmental conditions that evoke elevated metabolic rate, e.g., high density diets and cold temperature. These Naked Neck birds, different from the normally feathered broilers concerning the metabolism of energy (Touchburn et al., 1980), could be an excellent biological model to study which factors are involved in metabolic disturbances of poultry. The aim of these trials was to evaluate the influence of different broiler genotypes on performance, mortality due to AS and SDS, and right ventricular hypertrophy by comparing highly productive male broilers from commercial strains with Na male birds of low performance but excellent livability in typical Brazilian conditions. Periods MATERIAL AND METHODS Two trials were carried out, one in late winter of 1995 (August 24 to October 5) and the late autumn of 1996 (May 11 to June 22). These periods were chosen because of the great variations in temperature usually linked with high mortality of broilers in southeastern Brazil. Birds and Experimental Designs Day-old male chicks were obtained from eggs produced by 40- to 50-wk-old broiler breeders, except those from the Naked Neck breed originating from 30- to 33-wk-old breeders. A stable period of egg production, at least 3 wk after the peak, was the criterion adopted for collecting and incubating eggs. Eggs of each strain were collected on the same day, and classified by 2Collective trade mark, licensed by the France Ministry of Agriculture. 3Trade name of naked neck broiler from Granja Caipira, Porto Feliz, São Paulo, Brazil. 4Trade name of naked neck broiler from Gramado Avicola, Gramado, Rio Grande do Sul, Brazil. weight (60 g minimum, 67 g maximum) and quality of the shell (integral). Forty-eight hours after collection, all eggs were incubated in the same incubator. After hatching, the chickens were vent-sexed and vaccinated against Marek s, contagious epithelioma, and Gumboro diseases. In order to avoid bias, the name of the strains remained unknown during the experimental period (42 d). In the first trial, 1,890 male broiler chickens, 270 of each strain, were allotted in a randomized block design with seven treatments (strains: Arbor Acres, Avian Farms, Cobb-500, Hubbard-Peterson, ISA, Label Rouge,3 and Ross) and six blocks (replications) of 45 chickens each. included 2,184 male broiler chickens of six strains (Arbor Acres, Avian Farms, Cobb 500, Hubbard-Peterson, ISA-Label,4 and Ross) allotted in seven complete blocks of 52 birds per replicate and 364 birds per strain. Installation and Bird Management Birds were allocated at random to one of the 44 pens of the broiler house at 9 birds/m2 () and 10.4 birds/m2 (). Each pen was equipped with two feeders (chick and adult), two automatic drinkers (chick and adult), and an infrared lamp as heater. Heat was provided, when necessary, up to 14 d of age. Wood shavings (5 cm) were used as litter. Lighting schedule during the whole experimental period provided 23 h of light/d. The feed program in was divided into two periods, starter (1 to 21 d) and grower (22 to 42 d). In this trial, a mash diet was used. In, the birds were fed high density pelleted diets in a three-phase program (starter from 1 to 21 d, grower from 22 to 39 d, and finisher from 40 to 42 d). Table 1 shows the composition of the diets. Environmental temperature was continuously registered on a thermograph. Measurements At Day 1 and weekly afterwards, birds were weighed on a pen basis. Average feed consumption was calculated by considering the average number of chickens per pen for the given period. Feed conversion was calculated from total feed consumption, total weight gain, and mortality data. Daily mortality was recorded and dead birds were weighed, put in the refrigerator and, when possible, necropsied in the same day. Sudden death syndrome diagnosis was made when dead birds showed good development, similar or better weight than average, full gastrointestinal tract, gall bladder small or empty, enlarged heart with atria full of blood and clots, contracted ventricles, and no lesions due to other diseases (Gonzales, 1992). Ascitic fluid in the abdominal cavity, generalized congestion, abnormal liver and spleen, right cardiac hypertrophy with or without hydropericardium, and low performance were characteristics considered in the diagnosis of AS (Maxwell, 1990). Independently of these criteria, when the ratio of the right ventricle to total

3 1648 GONZALES ET AL. TABLE 1. Composition of the rations 1 Ration Composition Starter Grower Finisher Corn, ground Soybean meal Soybean oil Dicalcium phosphate Limestone DL methionine Salt Vitamin premix Micromineral premix BHT (antioxidant) - 99% Coxistac Calcium propionate (antifungic) - 99% Colistin (growth promoter) Olaquindox (growth promoter) Calculated analysis ME, kcal/kg 3,050 3,150 3,200 Crude protein, % Methionine, % Methionine + cystine, % Lysine, % Calcium, % Available phosphorus, % Starter = 1 to 21 d for Trials 1 and 2. Grower = 22 to 42 d and 22 to 39 d for Trials 1 and 2, respectively. Finisher = 40 to 42 d for. 2Agroceres Ross Melhoramento Genético de Aves S/A, Rio Claro, Brasil. 3Salinomicin. Laboratóries, Pfizer Ltda., Guarulhos, Brasil. ventricle weight (RV:TV) was greater than 0.25, ascites was considered as the cause of death (Silversides et al., 1997). In order to determine the index of right ventricle cardiac hypertrophy, the hearts of necropsied birds were dissected and the right ventricle and the left ventricle plus septum were weighed. (%) Statistical Evaluations Statistical analysis was done using the General Linear Models procedure of SAS (SAS Institute, 1988). Arc sine transformation of percentage mortality prior to ANOVA analysis was the method used to normalize data (Bartlett, 1947). When appropriate, differences between means were analyzed by Tukey s test (P 0.05). RESULTS AND DISCUSSION The average temperature registered during the experimental period was greater than normal for this area of São Paulo State as a consequence of a mild winter. Temperatures were as follows: average maximum, 27C; average minimum, 15.5C; absolute maximum, 34.5C; and absolute minimum, 11C. Temperatures below 15C were recorded on 18 d during the experimental period. Temperature ranges above 10C were observed on 26 d. Although the climate did not interfere with bird performance, some differences among strains were observed (Table 2). Among the strains selected for high growth rate, the greatest final weight and weight gain were achieved by Ross broilers, numerically higher (P > 0.05) than those of ISA and Hubbard-Peterson and significantly different (P 0.05) from those of Avian Farms, Arbor Acres, and Cobb, which were similar (P > 0.05) to each other. Ross broilers also showed the lowest feed conversion, which was significantly different (P 0.05) from Arbor Acres birds. The most significant performance differences could be stated for the Naked Neck strain, which showed much lower (P 0.05) final weight and BW gain as well as the highest (P 0.05) feed conversion. TABLE 2. Initial weight (IW), final weight (FW), weight gain (WG), cumulative feed intake (FI) and feed conversion (FC) of 42-d-old male broilers from different strains 1 Strain IW FW WG FI FC (g) Arbor Acres 45 ± 0.4 a 2,334 ± 44 b 2,289 ± 44 b 4,204 ± 10 ab 1.87 ± 0.04 b Avian Farms 44 ± 0.2 bc 2,381 ± 16 b 2,337 ± 16 b 4,265 ± 25 a 1.84 ± 0.01 bc Cobb ± 0.3 ab 2,356 ± 19 b 2,311 ± 19 b 4,087 ± 30 b 1.79 ± 0.01 bc ISA 41 ± 0.2 d 2,433 ± 13 ab 2,392 ± 13 ab 4,249 ± 57 ab 1.79 ± 0.01 bc Hubbard 45 ± 0.2 ab 2,409 ± 54 ab 2,364 ± 54 ab 4,198 ± 46 b 1.80 ± 0.03 bc Ross 43 ± 0.2 c 2,520 ± 21 a 2,473 ± 21 a 4,293 ± 36 a 1.77 ± 0.01 c Label Rouge 2 42 ± 0.2 d 1,154 ± 8 c 1,112 ± 7 c 2,275 ± 20 c 2.05 ± 0.02 a Arbor Acres 42 ± 0.2 ab 2,479 ± 16 b 2,438 ± 16 b 4,197 ± 32 cd 1.78 ± 0.01 bc Avian Farms 41 ± 0.2 b 2,493 ± 65 b 2,452 ± 65 b 4,427 ± 49 ab 1.86 ± 0.04 b Cobb ± 0.2 c 2,509 ± 11 b 2,469 ± 11 b 4,105 ± 29 d 1.76 ± 0.01 c Hubbard 43 ± 0.1 a 2,530 ± 10 b 2,488 ± 10 b 4,322 ± 36 bc 1.80 ± 0.01 bc Ross 41 ± 0.2 b 2,722 ± 12 a 2,681 ± 12 a 4,518 ± 47 a 1.74 ± 0.02 c ISA-Label 2 40 ± 0.3 c 1,210 ± 6 c 1,171 ± 6 c 2,253 ± 16 e 1.93 ± 0.01 a a-emeans ± SEM in a column within a trial with no common superscript differ significantly (P 0.05) by Tukey s test. 1Values are means ± SEM (n = 6 or 7 for and 2, respectively). 2Naked Neck strain.

4 METABOLIC DISTURBANCES IN BROILERS 1649 TABLE 3. Cumulative mortality of male broilers from different strains 1 Strain (%) Arbor Acres ab 9.63 a Avian Farms ab 5.19 ab Cobb ab a ISA a 9.63 a Hubbard ab 8.89 a Ross a a Label Rouge b 1.85 b Arbor Acres ab 6.87 b b Avian Farms ab 6.32 b c Cobb a a a Hubbard ab 8.52 b b Ross ab ab b ISA-Label b 1.92 c 2.20 d a-dmeans in the same column within each trial with no common superscript differ significantly (P 0.05) by Tukey s test. 1Percentage of mortality transformed Arc sine (percentage/ ) 0.5 before ANOVA analysis. Values are means of 270 initial birds per strain in and 364 initial birds per strain in. 2Naked Neck strain. Day The differences in performance at 42 d of age cannot be attributed to differences in the hatch weight of the chickens, as there was no correlation (P > 0.05) between initial and final weight. On the 1st d, the ISA broilers showed the lowest hatch weight (P 0.05) among all the high productivity strains, which was similar (P > 0.05) to that of naked-neck chickens (Table 2); whereas at 42 d, ISA broilers had mean BW equal to those of the top three performers. The Naked Neck strain had performed as expected for this age when receiving a diet containing 3,150 kcal/kg (Cothenet et al., 1996). Therefore, the weight of 42-d-old broilers has little to do with the weight at hatch, but the final weight follows a genetic standard fixed in its progeny if conditions for the full expression of the genetic potential are given, as demonstrated by Pinchasov (1991). The strain with the best productive performance (Ross) showed the highest incidence of mortality, which was high for all strains except for the Naked Necks, mainly from the 3rd wk of age (Table 3). At the end of the experimental period the Naked Neck birds presented a lower incidence of mortality, which was significantly different from the remaining strains, except for Avian Farm chickens. TABLE 4. Causes of death of Arbor Acres (AA), Avian Farms (AF), Cobb-500 (CO), Hubbard (HU), ISA (IS), Ross (RO), and Label Rouge (LR) male broilers, Mortality AA AF CO HU IS RO LR Total n Percentage AS 2 n Percentage Percentage/Total SDS 3 n Percentage Percentage/Total Others 4 n Percentage Percentage/Total initial birds per strain. 2Ascites syndrome. 3Sudden death syndrome. 4Including culled birds.

5 1650 GONZALES ET AL. TABLE 5. Number (n), mean BW, right ventricle weight (RV), left ventricle + septum weight (LV), and RV:TV ratio (x ± SEM) of necropsied broilers of different strains Strain n BW RV LV RV:TV (g) Arbor Acres 23 1, ± 0.02 Avian Farms 10 1, ± 0.03 Cobb , ± 0.03 Hubbard 20 1, ± 0.02 ISA 25 1, ± 0.02 Ross ± 0.01 Label Rouge ± 0.03 Arbor Acres 60 1, ± a Avian Farms 35 1, ± a Cobb , ± a Hubbard 56 1, ± a Ross 56 1, ± a ISA-Label ± b a,bmeans ± SEM in the same column within each trial with no common superscript differ significantly (P 0.05) by Tukey s test. 1Naked Neck strain. Analysis of mortality data according to cause revealed that more than 50% of cases of mortality, except in the Naked Neck birds, were due to metabolic diseases (Table 4). High mortality rates by SDS and AS, as observed during this trial, mainly for strains of high productivity and for male birds have already been reported previously (Maxwell, 1990; Gonzales et al., 1994; Olkowski and Classen, 1995). During a worldwide survey carried out in 1996, Maxwell and Robertson (1997) found an average rate of 4.7% of mortality incidence due to ascites. This rate is very similar to that registered in the present study for all strains of high productivity. In contrast, there were no Naked Neck birds that died from metabolic diseases, which corroborates the positive relationship between high productivity and mortality due to metabolic diseases as observed previously (Decuypere et al. 1994; Lubritz et al., 1995; Dewil et al., 1996). Necropsies proved that mortality due to ascites was accompanied by aspects of hemorrhagic and congestive enteritis (confirmed by histopathological exam) that were not observed to such extent in former experiments. It was suspected that the enteritis was due to the quality of corn, which might have been contaminated with mycotoxins. Subsequent laboratory analysis of corn and feed, however, did not demonstrate the presence of mycotoxins. It was also impossible to relate these lesions to infectious diseases, as attempts to isolate pathogenic agents gave negative results. Mortality in the Naked Neck strain was low, without presenting any of the congestive aspects normally observed in AS (Randall, 1986; Maxwell, TABLE 6. Number (n), BW, right ventricle weight (RV), left ventricle + septum (LV), and RV:TV ratio (x ± SEM) of necropsied broilers of different ages (strains combined) Day n BW RV LV RV:TV 1 (g) 01 to ± b 08 to ± b 15 to ± b 22 to ± ab 29 to ± a 36 to ± a 01 to ± c 08 to ± c 15 to ± bc 22 to ± b 29 to ± a 36 to ± a a-cmeans ± SEM in the same column within each trial with no common superscript differ significantly (P 0.05) by Tukey s test.

6 METABOLIC DISTURBANCES IN BROILERS 1651 TABLE 7. Causes of death of Arbor Acres (AA), Avian Farms (AF), Cobb-500 (CO), Hubbard (HU), Ross (RO), and ISA-Label (IL) male broilers, Mortality 1 AA AF CO HU RO IL Total n Percentage AS 3 n Percentage Percentage/Total SDS 4 n Percentage Percentage/Total Other 5 n Percentage Percentage/Total initial birds per strain. 2Number of birds. 3Ascites syndrome. 4Sudden death syndrome. 5Including culled birds. 1990). Thus, it was concluded that the enteritis was secondary and not determining ascites. Coherent with the clinical aspect of mortality observed in the most productive strains, the RV:TV ratio of dead birds of these strains (Table 5) was high and exceeded 0.25, which indicates the occurrence of right cardiac hypertrophy secondary to the ascitic state (Coello et al., 1993a; Lubritz and McPherson, 1994; Lubritz et al., 1995). This effect was not be observed for Naked Neck birds, which showed an average ratio of RV:TV less than Indeed, in the Naked Neck chickens, AS was not the cause of mortality. Independent from the strain, it was observed that RV:TV indices over 0.25 occurred only after the 4th wk of age (Table 6), being significantly greater than the ratios observed until the 3rd wk of age, which characterized AS as the main cause of mortality in the high productive broilers after 21 d of age. Temperature data showed that rearing conditions in this experiment were similar to those of, and did not include a severe winter period. However, there were more days (31) with minimum temperatures below 15 C, and the average maximum (24.4 C) and minimum (14.6 C) temperatures were lower than in. The absolute maximum (28 C) was also lower in this experiment, but not the absolute minimum (12 C). There were 14 d with temperature ranges above 10 C. Linked with the influence of temperature, the use of a pelleted ration induced an increase in feed consumption and a higher performance of the birds compared with (Table 2). This result was already be noted after 1 wk of age, and at the end of the 4th wk (28 d), all strains selected for fast growth rate attained an average BW of more than 1,300 g (data not shown). The nutritional composition of starter and grower feeds were the same in both experiments (Table 1). Again, in this trial the best performance was observed for Ross broilers, which attained the highest (P 0.05) weight and weight gain. Also, Ross broiler feed conversion was the lowest but it was statistically different only from Avian Farms and Naked Neck birds. The latter had the worst performance (P 0.05) among the strains studied but it was considered normal for its genetic background. Confirming the observations of, greater initial weight did not correspond to superior final weight and weight gain (Table 2). Ross and Cobb broilers had low initial weight but high final weights. Up to 28 d of age, cumulative mortality of all strains, as in, occurred within a range considered normal for age, sex, nutritional level, and weight gain (Table 3). During the 4th wk and until the end of the experimental period, mortality increased considerably, reaching 26.65% for Cobb chickens, which was significantly higher than the also very high rates of the other strains. Once again, the Naked Neck strain, which is not selected for rapid growth rate, was the only strain without an occurrence of death due to SDS or AS (Table 7) and had a mortality that could be considered within normal limits for this strain. This result confirms the conclusion that sensitivity to metabolic diseases is related to the fast increase of the BW of broilers. When comparing the incidence of mortality of strains with high productivity in this experiment with that of, it was much higher and even double that of some of the strains. Cases of death were determined to be an even larger proportion by metabolic disturbances, mainly by the ascites syndrome (Table 7). Some factors may have contributed to this occurrence: lower average temperature, use of a pelleted ration, higher feed consumption,

7 1652 and better performance. All of these factors are related to the occurrence of high incidences of ascites in flocks of male broilers (Ononiwu et al., 1979; Julian, 1993; Maxwell and Robertson, 1997). Maxwell (1990) and Coello et al. (1993a) mentioned a mortality up to 50% in flocks of male broilers as being almost all due to AS. The main physiopathological explanation for this high occurrence of ascites due to low temperatures, high feed consumption, and good performance is the high demand of oxygen of the birds in these conditions (Julian, 1993; Wideman et al., 1998). Rapid temperature declines may also contribute to the increase of death due to ascites because they cause an increase in the demand for oxygen. Gleeson (1986) demonstrated that the consumption of oxygen of female Leghorn chickens increased twice as much when they were exposed to sudden decreases in temperature from 20 to 2C. A similar hemorraghic/congestive enteritis observed during the necropsy in was found in. Again, it was also impossible to isolate pathogenic agents or to find other reasons for the observed high mortality than that determined by the ascitic syndrome, the major cause of death in this study. As seen in the previous trial, the average RV:TV ratio of the dissected birds (Table 5) was high and all ratios were over 0.25 except for birds of the ISA-label strain, which presented a nonhypertrophic RV:TV ratio of 0.18, statistically less than that of the other strains, which were similar to each other. Regardless of strain, a RV:TV ratio over 0.25 was observed after the 4th wk of age, characterizing AS as the major cause of mortality. Because ascites incidence in was proportionally higher than in and RV: TV ratio was measured on necropsied birds, this result explains the higher RV:TV ratio observed in this trial compared to. In conclusion, both trials confirmed the relationship between high productivity and high incidence of sudden death and ascites syndrome, especially if the birds are submitted to risk factors such as cold environment and high nutritional density of the diet. Also, the results indicated that Naked Neck strain is comparatively resistant to SDS and AS and can be used as comparative model in physiologic studies of these pathologies. ACKNOWLEDGMENTS The authors acknowledge the financial support provided by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). REFERENCES Ayyagari, V., Effect of feathering genes and dietary protein levels and their interactions on juvenile growth and carcass traits in broilers. Page 71 in: Proceedings 20th World s Poultry Congress, New Delhi, India. GONZALES ET AL. Bartlett, M. S., The use of transformation. Biometrics 3: Coello, C. P., J. A. Menocal, and E. A. González, 1993a. 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