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Glycemic response of poultries in different feeding systems

ABSTRACT.

The management of poultry feed is an important welfare promoter and the glycemic index a noninvasive evaluation. The aim was to evaluate the glycemic response of broiler breeders in restricted feeding system, and broilers receiving ad libitum feeding. Two experiments were carried out: I) 39-week-oldbroiler breeders, fed with three sources of fiber, in a completely randomized design in factorial scheme (3 fiber diets x 7 collection periods); and II) broilers, 42 days old, housed in different light systems, in a completely randomized design in factorial design (2 sexes x 2 lighting conditions x 13 collection periods). Blood glucose levels were measured at random collecting one blood drop from foot, with three replicates in each condition and treatment. In broiler breeder different fiber sources had no effect on glycemia, but the period affected circulating glucose levels, presenting a minimum of 184.3 mg dL-1 before feed and, a maximum of 242.5 mg dL-1 four hours after feeding. In broilers, there was a significant effect in glycemia for collection period and for sex, and interaction between lighting conditions and collection period. Further studies are needed to establish reference values to compare blood glucose levels in poultry.

Keywords:
broiler breeders; broilers; glycemic; welfare

Introduction

Poultry welfare is influenced by the nutrition, as metabolic factors alter blood glucose levels (Blundell & Halford, 1994Blundell, J. E., & Halford, J. C. G. (1994). Regulation of nutrient supply: the brain and appetite control. Proceedings of the Nutrition Society, 53(2), 407-418. doi: 10.1079/PNS19940046.
https://doi.org/10.1079/PNS19940046....
); therefore an important physiological response. The measurement and control of the normal responses of blood glucose levels of birds, under different conditions, allows to identify aspects of physiological and pathological state of the birds as well as its welfare conditions (Kodaira, Pereira, Soares, & Bueno, 2015Kodaira, V., Pereira, D. F., Soares, N. M., & Bueno, L. G. F. (2015). Concentração de glicose sanguínea e relação heterófilo:linfócito podem ser utilizados como indicadores de estresse térmico para aves poedeiras? Revista Brasileira de Engenharia de Biossistemas, 9(2), 182-190. doi: 10.18011/bioeng2015v9n2p182-190.
https://doi.org/10.18011/bioeng2015v9n2p...
). The poultry feed intake is regulated by a complex short and long-terms regulation depending on a negative or positive energy balance that involves the circulating glycemic levels in blood (Richards, 2003Richards, M. P. (2003). Genetic regulation of feed intake and energy balance in poultry. Poultry Science , 82(6), 907-916. doi: 10.1093/ps/82.6.907.
https://doi.org/10.1093/ps/82.6.907....
). The improvement of the knowledge of poultry glycemic response in different conditions will help to develop smart feeder or tools applicable in precision livestock farming.

Feed management of broiler breeders need be restricted due to the nutritional requirements and diets concentration, reducing the access time to the feeder. These rigid nutritional restrictions on broiler breeders may change the welfare conditions, however, different sources of fiber are able to bring satiety throughout the day. Also, other effects attributed to the use of fiber in the diet are the delay on gastric empty and gradual absorption of carbohydrates in the intestine (Graham, Maskell, Rawlings, Nash, & Markwell, 2002Graham, P. A., Maskell, I. E., Rawlings, J. M., Nash, A. S., & Markwell, P. J. (2002). Influence of a high fibre diet on glycaemic control and quality of life in dogs with diabetes mellitus. Journal of Small Animal Practice, 43(2), 67-73. doi: 10.1111/j.1748-5827.2002.tb00031.x.
https://doi.org/10.1111/j.1748-5827.2002...
), which can modulate and regulate postprandial blood glucose levels.

Broilers are selected for weight gain and feed intake (Zuidhof, Schneider, Carney, Korver, & Robinson, 2014Zuidhof, M. J., Schneider, B. L., Carney, V. L., Korver, D. R., & Robinson, F. E. (2014). Growth, efficiency, and yield of commercial broilers from 1957, 1978, and 2005. Poultry Science , 93(12), 2970-2982. doi: 10.3382/ps.2014-04291
https://doi.org/10.3382/ps.2014-04291...
), so, the feed is ad libitum, in opposition to the breeders. In production system, lighting is one of the factors that can alter food intake and have potential capability to changes broilers responses in terms of feed intake and growth (Campos, 2000Campos, E. J. (2000). O Comportamento das aves. Revista Brasileira de Ciência Avícola, 2(2), 93-113. doi: 10.1590/S1516-635X2000000200001.
https://doi.org/10.1590/S1516-635X200000...
; Olanrewaju, Purswell, Collier, & Branton, 2012Olanrewaju, H. A., Purswell, J. L., Collier, S. D., & Branton, S. L. (2012). Influence of photoperiod, light intensity and their interaction on growth performance and carcass characteristics of broilers grown to heavy weights. International Journal of Poultry Science, 11(12), 739-746. doi: 10.3923/ijps.2012.739.746.
https://doi.org/10.3923/ijps.2012.739.74...
). There are few works on poultry studying glycemia levels, and the existing ones present different results, associated with genetics, type of feed and the production system.Glycemia levels in poultry is 150 to 300% higher than in mammals, considering the same body weight (Braun & Sweazea, 2008Braun, E. J., & Sweazea, K. L. (2008). Glucose regulation in birds. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 151(1), 1-9. doi: 10.1016/j.cbpb.2008.05.007.
https://doi.org/10.1016/j.cbpb.2008.05.0...
), and its maintenance is influenced by insulin and glucagon. Rajman et al. (2006Rajman, M., Juráni, M., Lamošová, D., Máčajová, M., Sedlačková, M., Košťál, Ľ., ... Výboh, P. (2006). The effects of feed restriction on plasma biochemistry in growing meat type chickens (Gallus gallus). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 145(3), 363-371. doi: 10.1016/j.cbpa.2006.07.004.
https://doi.org/10.1016/j.cbpa.2006.07.0...
) found glucose values in broiler breeders ranging from 243 mg dL-1 to 216 mg dL-1.

Most glycemic studies are focused on monitoring only one individual. Using a flock, the evaluation is less invasive, allowing indicate the most relevant environmental conditions for feed intake (Mumma, Thaxton, Vizzier-Thaxton, & Dodson, 2006Mumma, J. O., Thaxton, J. P., Vizzier-Thaxton, Y., & Dodson, W. L. (2006). Physiological stress in laying hens. Poultry Science, 85(4), 761-769. doi: 10.1093/ps/85.4.761.
https://doi.org/10.1093/ps/85.4.761....
; Nicol, Caplen, Edgar, & Browne, 2009Nicol, C. J., Caplen, G., Edgar, J., & Browne, W. J. (2009). Associations between welfare indicators and environmental choice in laying hens. Animal Behaviour, 78(2), 413-424. doi: 10.1016/j.anbehav.2009.05.016.
https://doi.org/10.1016/j.anbehav.2009.0...
; Star, Decuypere, Parmentier, & Kemp, 2008Star, L., Decuypere, E., Parmentier, H. K., & Kemp, B. (2008). Effect of single or combined climatic and hygienic stress in four layer lines: 2. Endocrine and oxidative stress responses. Poultry Science , 87(6), 1031-1038. doi: 10.3382/ps.2007-00143.
https://doi.org/10.3382/ps.2007-00143....
). The objective of this study was to evaluate the glycemic response from flocks of broiler breeders in restricted feeding system, and of broilers fed ad libitum.

Material and methods

Two experiments were conducted to evaluate average flock glycemia in breeders and broilers: experiment I - broiler breeder receiving restrict feed with different sources of dietary fiberand; Experiment II - broiler chickens receiving ad libitum diet with two lighting program.

Experiment I

A total of 168 broiler breeders Cobb 500 with 39 weeks of age, were housed in a conventional facility with wood shaving litter, pendulum drinker and tubular feeder, lighting program of 14 hours of constant light, combining natural and artificial light. The feed was offered in a single delivery in the first period of the morning (8 hours), providing 160 g day-1 bird of feed. The design was completely randomized, in a factorial arrangement 3 x 7 (three diets and seven collection times) with seven replicates of eight birds per experimental unit.

The diets were formulated according to the lineage manual, where treatments consisted of the individual use of three sources of fiber in the diet: wheat bran (WB), soybean hull (SH) or citrus pulp (CP; Table 1). The broiler breeders went through a period to adapting the diets and feed system for 14 days.

Measurements were taken by collecting one drop of blood from foot of one broiler breeder per experimental unit, randomly chosen. The calibration was done using the Accu-Chek® device, determining the glucose levels in mg dL-1 of blood, from colorimetric reagent strips. The collection periods started at 8 a.m., just before feeding, and finished at 8 p.m., with intervals of two hours.

The data were submitted to analysis of variance and Tukey test with a significance of 5% and later elaborated the regression of glycemia according to collection periods using the statistical program R (R, 2016).

Experiment II

Broilers were housed in conventional facility with rice husk litter, equipped with pendulum drinker and tubular feeder, and fed with a commercial formulation ad libitum. A number of 90 broilers with 42 days of age was used, distributed in a completely randomized design, in factorial arrangement (two lighting systems, two sexes and 13 blood collection periods).

The simulated lighting systems were from conventional facility (CF) with lighting program of eight hours of dark and light intensity greater than 20 lux in the combination of natural and supplied. The other, simulated a Dark House (DH) where the maximum illumination was 4 lux. The adaption period to the systems was seven days for both facility systems.

Table 1
Energy and calculated nutrients levels of broiler breeder’s diets.

Blood samples were collected from three broilers of each sex per lighting system, every two hours, starting at 8 a.m. to 8 p.m. Measurements of glycemia levels were identical to Experiment I.

The glucose averages collected were submitted to analysis of variance and 5% of significance by F test by the statistical program R (R, 2016).

Results and discussion

Experiment I

The different sources of fiber used in conventional levels (3.5%) in broiler breeder’s diets did not affect the glycemic levels (p > 0.05; Table 2). The concentration of fiber is a determinant factor on glycemic responses (Englyst, Englyst, Hudson, Cole, & Cummings, 1999Englyst, K. N., Englyst, H. N., Hudson, G. J., Cole, T. J., & Cummings, J. H. (1999). Rapidly available glucose in foods: an in vitro measurement that reflects the glycemic response. The American Journal of Clinical Nutrition, 69(3), 448-454. doi: 10.1093/ajcn/69.3.448.
https://doi.org/10.1093/ajcn/69.3.448...
), as it causes a delay in the passage of food through the gastrointestinal tract and gradually releases glucose into the circulation (Silva Júnior et al., 2004Silva Júnior, J. W., Borges, F. M. O., Murgas, L. D. S., Valério, A. G., Medeiros, G. C., Viana, R., & Lima, L. M. S. (2004). Digestibiliade de dietas com diferentes fontes de carboidratos e sua influência na glicemia e insulinemia em cães. Ciência e Agrotecnologia, 29(2), 436-443. doi: 10.1590/S1413-70542005000200023.
https://doi.org/10.1590/S1413-7054200500...
).

The glycemia of broiler breeders was on average 184.33 mg dL-1 of circulating blood glucose, minimum average value before the first meal of the day. Similar values were observed over 24 hours of fasting, 185 mg dL-1(Belo, Romsos, & Leveille, 1976Belo, P. S., Romsos, D. R., & Leveille, G. A. (1976). Blood metabolites and glucose metabolism in the fed and fasted chicken. The Journal of Nutrition, 106(8), 1135-1143. doi: 10.1093/jn/106.8.1135.
https://doi.org/10.1093/jn/106.8.1135....
).

From the feed supply on, the glucose increased until 12 a.m., with 242.52 mg dL-1 of blood glucose, the maximum daily average, and then reduced to 209.38 mg dL-1 at 6 pm, when it resumed to increase (Figure 1). The presence of feed in feeder, observed during blood collection, possibly stimulated new intake with leftovers at 6 p.m.

Dietary fiber is important in poultry nutrition and a minimum level of dietary fiber has to be included to maintain normal physiological function in the digestive tract (Wenk, 2001Wenk, C. (2001). The role of dietary fibre in the digestive physiology of the pig. Animal Feed Science and Technology , 90(1-2), 21-33. doi: 10.1016/S0377-8401(01)00194-8.
https://doi.org/10.1016/S0377-8401(01)00...
). For broiler breeders, dietary fiber, also stimulate gut health, increase the satiety, delays gastric emptying, delays glucose absorption, slows absorption, and affect behavior and improve animal well-being (Dinsa, 2017Dinsa, N. G. (2017). Review on fiber digestion in non ruminant animals and effect of dietary fiber. International Journal of Research Studies in Agricultural Sciences, 10(3), 37-44. doi: 10.20431/2454-6224.0310004.
https://doi.org/10.20431/2454-6224.03100...
; Knudsen, Hedemann, & Lærke, 2012Knudsen, K. E. B., Hedemann, M. S., & Lærke, H. N. (2012). The role of carbohydrates in intestinal health of pigs. Animal Feed Science and Technology, 173(1-2), 41-53. doi: 10.1016/j.anifeedsci.2011.12.020.
https://doi.org/10.1016/j.anifeedsci.201...
).

Experiment II

The lighting conditions did not influence the blood glucose values (Table 3). Broilers are more resistant to fasting hypoglycemia, since blood glucose concentrations are maintained even during long periods of food restriction (Belo et al., 1976Belo, P. S., Romsos, D. R., & Leveille, G. A. (1976). Blood metabolites and glucose metabolism in the fed and fasted chicken. The Journal of Nutrition, 106(8), 1135-1143. doi: 10.1093/jn/106.8.1135.
https://doi.org/10.1093/jn/106.8.1135....
; Rajman et al., 2006Rajman, M., Juráni, M., Lamošová, D., Máčajová, M., Sedlačková, M., Košťál, Ľ., ... Výboh, P. (2006). The effects of feed restriction on plasma biochemistry in growing meat type chickens (Gallus gallus). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 145(3), 363-371. doi: 10.1016/j.cbpa.2006.07.004.
https://doi.org/10.1016/j.cbpa.2006.07.0...
). In stress conditions, blood glucose levels increase significantly, but there is a lack of reference values for comparison (Yalçinkaya et al., 2012Yalçinkaya, I., Çinar, M., Yildirim, E., Erat, S., Başalan, M., & Güngör, T. (2012). The effect of prebiotic and organic zinc alone and in combination in broiler diets on the performance and some blood parameters. Italian Journal of Animal Science, 11(3), e55. doi: 10.4081/ijas.2012.e55.
https://doi.org/10.4081/ijas.2012.e55....
).

Table 2
Glycemia in mg dL-1 of blood glucose from broiler breeders.

Figure1
Broiler breeders glycemia levels during a day with restricted feeding system.

Table 3
Glycemia in mg dL-1of broilers in different lighting conditions.

Broilers in different lighting conditions showed different interactions between the analyzed variables (p < 0.05). Regarding sex (p < 0.001), male broilers had higher levels of circulating glucose when compared to females. These differences happen due to males having a higher growth rate, weight gain and feed intake (Marcato et al., 2010Marcato, S. M., Sakomura, N. K., Fernandes, J. B. K., Siqueira, J. C., Dourado, L. R. B., & Freitas, E. R. (2010). Crescimento e deposição de nutrientes nos órgãos de frangos de corte de duas linhagens comerciais. Revista Brasileira de Zootecnia, 39(5), 1082-1091. doi: 10.1590/S1516-35982010000500019.
https://doi.org/10.1590/S1516-3598201000...
; Martins, Taveira, Hitz, Castilhano, & Santos, 2012Martins, J. M. S., Taveira, R. Z., Hitz, F. H., Castilhano, H., & Santos, M. P. (2012). Desempenho zootécnico de linhagens de frango de corte de crescimento rápido. PUBVET, 6, 1283-1288. ; Santos et al., 2005Santos, A. L., Sakomura, N. K., Freitas, E. R., Fortes, C. M. L. S., Carrilho, E. N. V. M., & Fernandes, J. B. K. (2005). Estudo do crescimento, desempenho, rendimento de carcaça e qualidade de carne de três linhagens de frango de corte. Revista Brasileira de Zootecnia , 34(5), 1589-1598. doi: 10.1590/S1516-35982005000500020.
https://doi.org/10.1590/S1516-3598200500...
).

The interaction of the collection periods and lighting conditions (p < 0.05) is justified by the difference in the synchrony of physical activity of ingestion due to the light and dark exposition. In the two lighting conditions, different values of glycemia were observed throughout the day, obtaining alternate values of glycemia. When blood glucose levels decline, there is a stimulus in the nerve center that controls hunger, instigating food intake (Schwartz, Woods, Porte Junior, Seeley, & Baskin, 2000Schwartz, M. W., Woods, S. C., Porte Junior, D., Seeley, R. J., & Baskin, D. G. (2000). Central nervous system control of food intake. Nature, 404(6778), 661-671. doi: 10.1038/35007534.
https://doi.org/10.1038/35007534....
). These peaks may be related to ingestion timing of the flock, a collective behavior that requires further study. This study presented an initial approach on evaluating glycemia of poultry flocks, which may help to establish better feeding and lighting management methods, and can help to stablish the development of optimal feeders. The condition in which glycemia is different between male and female broilers need to be better studied, to understand if hierarchies between sexes influence the feeder access.

Conclusion

Broiler breeders glycemia was not influenced by different sources of fiber, presenting a peak of 242.52 mg dL-1 of blood glucose four hours after feeding. Due to that, the effect of collection period was not significant. In broilers, glucose levels in this experiment were influenced by the interaction between collection period, sex, and lighting conditions.

References

  • Belo, P. S., Romsos, D. R., & Leveille, G. A. (1976). Blood metabolites and glucose metabolism in the fed and fasted chicken. The Journal of Nutrition, 106(8), 1135-1143. doi: 10.1093/jn/106.8.1135.
    » https://doi.org/10.1093/jn/106.8.1135.
  • Blundell, J. E., & Halford, J. C. G. (1994). Regulation of nutrient supply: the brain and appetite control. Proceedings of the Nutrition Society, 53(2), 407-418. doi: 10.1079/PNS19940046.
    » https://doi.org/10.1079/PNS19940046.
  • Braun, E. J., & Sweazea, K. L. (2008). Glucose regulation in birds. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 151(1), 1-9. doi: 10.1016/j.cbpb.2008.05.007.
    » https://doi.org/10.1016/j.cbpb.2008.05.007.
  • Campos, E. J. (2000). O Comportamento das aves. Revista Brasileira de Ciência Avícola, 2(2), 93-113. doi: 10.1590/S1516-635X2000000200001.
    » https://doi.org/10.1590/S1516-635X2000000200001.
  • Dinsa, N. G. (2017). Review on fiber digestion in non ruminant animals and effect of dietary fiber. International Journal of Research Studies in Agricultural Sciences, 10(3), 37-44. doi: 10.20431/2454-6224.0310004.
    » https://doi.org/10.20431/2454-6224.0310004.
  • Englyst, K. N., Englyst, H. N., Hudson, G. J., Cole, T. J., & Cummings, J. H. (1999). Rapidly available glucose in foods: an in vitro measurement that reflects the glycemic response. The American Journal of Clinical Nutrition, 69(3), 448-454. doi: 10.1093/ajcn/69.3.448.
    » https://doi.org/10.1093/ajcn/69.3.448
  • Graham, P. A., Maskell, I. E., Rawlings, J. M., Nash, A. S., & Markwell, P. J. (2002). Influence of a high fibre diet on glycaemic control and quality of life in dogs with diabetes mellitus. Journal of Small Animal Practice, 43(2), 67-73. doi: 10.1111/j.1748-5827.2002.tb00031.x.
    » https://doi.org/10.1111/j.1748-5827.2002.tb00031.x.
  • Knudsen, K. E. B., Hedemann, M. S., & Lærke, H. N. (2012). The role of carbohydrates in intestinal health of pigs. Animal Feed Science and Technology, 173(1-2), 41-53. doi: 10.1016/j.anifeedsci.2011.12.020.
    » https://doi.org/10.1016/j.anifeedsci.2011.12.020.
  • Kodaira, V., Pereira, D. F., Soares, N. M., & Bueno, L. G. F. (2015). Concentração de glicose sanguínea e relação heterófilo:linfócito podem ser utilizados como indicadores de estresse térmico para aves poedeiras? Revista Brasileira de Engenharia de Biossistemas, 9(2), 182-190. doi: 10.18011/bioeng2015v9n2p182-190.
    » https://doi.org/10.18011/bioeng2015v9n2p182-190.
  • Marcato, S. M., Sakomura, N. K., Fernandes, J. B. K., Siqueira, J. C., Dourado, L. R. B., & Freitas, E. R. (2010). Crescimento e deposição de nutrientes nos órgãos de frangos de corte de duas linhagens comerciais. Revista Brasileira de Zootecnia, 39(5), 1082-1091. doi: 10.1590/S1516-35982010000500019.
    » https://doi.org/10.1590/S1516-35982010000500019.
  • Martins, J. M. S., Taveira, R. Z., Hitz, F. H., Castilhano, H., & Santos, M. P. (2012). Desempenho zootécnico de linhagens de frango de corte de crescimento rápido. PUBVET, 6, 1283-1288.
  • Mumma, J. O., Thaxton, J. P., Vizzier-Thaxton, Y., & Dodson, W. L. (2006). Physiological stress in laying hens. Poultry Science, 85(4), 761-769. doi: 10.1093/ps/85.4.761.
    » https://doi.org/10.1093/ps/85.4.761.
  • Nicol, C. J., Caplen, G., Edgar, J., & Browne, W. J. (2009). Associations between welfare indicators and environmental choice in laying hens. Animal Behaviour, 78(2), 413-424. doi: 10.1016/j.anbehav.2009.05.016.
    » https://doi.org/10.1016/j.anbehav.2009.05.016.
  • Olanrewaju, H. A., Purswell, J. L., Collier, S. D., & Branton, S. L. (2012). Influence of photoperiod, light intensity and their interaction on growth performance and carcass characteristics of broilers grown to heavy weights. International Journal of Poultry Science, 11(12), 739-746. doi: 10.3923/ijps.2012.739.746.
    » https://doi.org/10.3923/ijps.2012.739.746.
  • Rajman, M., Juráni, M., Lamošová, D., Máčajová, M., Sedlačková, M., Košťál, Ľ., ... Výboh, P. (2006). The effects of feed restriction on plasma biochemistry in growing meat type chickens (Gallus gallus). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 145(3), 363-371. doi: 10.1016/j.cbpa.2006.07.004.
    » https://doi.org/10.1016/j.cbpa.2006.07.004.
  • Richards, M. P. (2003). Genetic regulation of feed intake and energy balance in poultry. Poultry Science , 82(6), 907-916. doi: 10.1093/ps/82.6.907.
    » https://doi.org/10.1093/ps/82.6.907.
  • Santos, A. L., Sakomura, N. K., Freitas, E. R., Fortes, C. M. L. S., Carrilho, E. N. V. M., & Fernandes, J. B. K. (2005). Estudo do crescimento, desempenho, rendimento de carcaça e qualidade de carne de três linhagens de frango de corte. Revista Brasileira de Zootecnia , 34(5), 1589-1598. doi: 10.1590/S1516-35982005000500020.
    » https://doi.org/10.1590/S1516-35982005000500020.
  • Schwartz, M. W., Woods, S. C., Porte Junior, D., Seeley, R. J., & Baskin, D. G. (2000). Central nervous system control of food intake. Nature, 404(6778), 661-671. doi: 10.1038/35007534.
    » https://doi.org/10.1038/35007534.
  • Silva Júnior, J. W., Borges, F. M. O., Murgas, L. D. S., Valério, A. G., Medeiros, G. C., Viana, R., & Lima, L. M. S. (2004). Digestibiliade de dietas com diferentes fontes de carboidratos e sua influência na glicemia e insulinemia em cães. Ciência e Agrotecnologia, 29(2), 436-443. doi: 10.1590/S1413-70542005000200023.
    » https://doi.org/10.1590/S1413-70542005000200023.
  • Star, L., Decuypere, E., Parmentier, H. K., & Kemp, B. (2008). Effect of single or combined climatic and hygienic stress in four layer lines: 2. Endocrine and oxidative stress responses. Poultry Science , 87(6), 1031-1038. doi: 10.3382/ps.2007-00143.
    » https://doi.org/10.3382/ps.2007-00143.
  • Wenk, C. (2001). The role of dietary fibre in the digestive physiology of the pig. Animal Feed Science and Technology , 90(1-2), 21-33. doi: 10.1016/S0377-8401(01)00194-8.
    » https://doi.org/10.1016/S0377-8401(01)00194-8.
  • Yalçinkaya, I., Çinar, M., Yildirim, E., Erat, S., Başalan, M., & Güngör, T. (2012). The effect of prebiotic and organic zinc alone and in combination in broiler diets on the performance and some blood parameters. Italian Journal of Animal Science, 11(3), e55. doi: 10.4081/ijas.2012.e55.
    » https://doi.org/10.4081/ijas.2012.e55.
  • Zuidhof, M. J., Schneider, B. L., Carney, V. L., Korver, D. R., & Robinson, F. E. (2014). Growth, efficiency, and yield of commercial broilers from 1957, 1978, and 2005. Poultry Science , 93(12), 2970-2982. doi: 10.3382/ps.2014-04291
    » https://doi.org/10.3382/ps.2014-04291

Publication Dates

  • Publication in this collection
    25 Feb 2019
  • Date of issue
    2019

History

  • Received
    04 June 2018
  • Accepted
    05 Sept 2018
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