Early feeding; Growth performance; Gut health; Hatching system; Immunity; Animals; Male; Chickens/growth & development; Chickens/physiology; Chickens/immunology; Animal Husbandry/methods; Intestines/physiology; Intestines/growth & development; Animal Husbandry; Chickens; Intestines; Animal Science and Zoology
Abstract :
[en] An alternative hatching system known as hatch on-farm (HOF) provides early access to feed compared to hatch in hatchery (HH) system. Early feeding may promote favorable gut development, potentially improving intestinal health and broiler performance. Previous studies have assessed the effects of HOF on chick quality, welfare and performance, its impacts on gut health remain inconclusive. A total of 560 Ross 308 male chicks were reared until d 38, hatched either in a hatchery (n = 280) or on-farm (n = 280), with 14 replicates per system and 20 birds per pen. Production parameters were periodically monitored. Digestive and immune organ characteristics, intestinal permeability and histomorphology were assessed on d 7, 14, and 38. High-throughput qPCR analyzed 79 ileal genes regarding barrier integrity, immune function, nutrient transporters, gut hormones, metabolism, and oxidation. HOF chicks had higher d1 body weights than HH chicks (P < 001), but this advantage disappeared within first week, with no subsequent performance differences. HOF chickens demonstrated increased duodenal villus width on d 7 and 14, and increased ileal crypt depth and submucosal thickness on d 7 (P < 0.05). Relative bursal weight was higher on d 14 (P = 0.018) and tended to be higher on d 38 in HOF chickens (P = 0.094). Intestinal permeability remained unaffected (P > 0.05), while HH chicks showed upregulation of gut barrier genes such as MUC5ac on d 7 and CLDN2 and MUC2 on d 14 (P < 0.05). HH chicks also showed upregulation of nutrient transports including VDR on d 7 and SLC30A1 and SLC5A9 on d 38, and decreased expression of the appetite-suppressing hormone CCK on d 7 (P < 0.05). HOF chicks upregulated immune-related genes, including IL-8 on d 7, IL-6, IFN-γ, AVBD9 on d 14, and NOS2 on d 38 (P < 0.05), and the oxidation gene HIF1A on d 38 (P = 0.039). In conclusion, although the HOF showed only transient growth advantages, it enhanced mucosal morphology and modulated immunity, indicating improved intestinal health.
H2020 - 955374 - MonoGutHealth - TRAINING AND RESEARCH FOR SUSTAINABLE SOLUTIONS TO SUPPORT AND SUSTAIN GUT HEALTH AND REDUCE LOSSES IN MONOGASTRIC LIVESTOCK
Funders :
EC - European Commission Marie Skłodowska-Curie Actions
Funding text :
This research received funding from the European Union's Horizon 2020 research program (agreement no. 955374).
Akram, M.Z., Everaert, N.., Dunisławska, A., In ovo sodium butyrate administration differentially impacts growth performance, intestinal barrier function, immune response, and gut microbiota characteristics in low and high hatch-weight broilers. J. Anim. Sci. Biotechnol. 15 (2024), 1–21.
Akram, M.Z., Sureda, E..A., Comer, L., Corion, M., Everaert, N., Assessing the impact of hatching system and body weight on the growth performance, caecal short-chain fatty acids, and microbiota composition and functionality in broilers. Anim. Microbiome, 6, 2024, 41.
Akram, M.Z., Sureda, E..A., Corion, M., Comer, L., Everaert, N., Linking gastrointestinal tract structure, function, and gene expression signatures to growth variability in broilers: a novel interpretation for flock uniformity. Poult. Sci., 103, 2024, 104158.
Andersen, C.L., Jensen, J..L., Ørntoft, T.F., Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64 (2004), 5245–5250.
Ballou, A.L., Ali, R..A., Mendoza, M.A., Ellis, J.C., Hassan, H.M., Croom, W.J., Koci, M.D., Development of the chick microbiome: how early exposure influences future microbial diversity. Front. Vet. Sci., 3, 2016, 2.
Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57 (1995), 289–300.
Bergoug, H., Guinebretière, M., Tong, Q., Roulston, N., Romanini, C.E.B., Exadaktylos, V., Berckmans, D., Garain, P., Demmers, T.G.M., McGonnell, I.M., Bahr, C., Burel, C., Eterradossi, N., Michel, V., Effect of transportation duration of 1-day-old chicks on postplacement production performances and pododermatitis of broilers up to slaughter age. Poult. Sci. 92 (2013), 3300–3309.
Boyner, M., A flying start : adapted hatching and post-hatch feeding in broiler chickens. Acta Univ. Agric. Sueciae, 38, 2023, 10.54612/a.35707n9nbs.
Burke, W.H., Sex differences in incubation length and hatching weights of broiler chicks. Poult. Sci. 71 (1992), 1933–1938.
Careghi, C., Tona, K., Onagbesan, O., Buyse, J., Decuypere, E., Bruggeman, V., The effects of the spread of hatch and interaction with delayed feed access after hatch on broiler performance until seven days of age. Poult. Sci. 84 (2005), 1314–1320.
Criado-Mesas, L., Abdelli, N., Noce, A., Farré, M., Pérez, J.F., Solà-Oriol, D., Martin-Venegas, R., Forouzandeh, A., González-Solé, F., Folch, J.M., Transversal gene expression panel to evaluate intestinal health in broiler chickens in different challenging conditions. Sci. Rep. 11 (2021), 1–14.
Cuperus, T., van Dijk, A., Dwars, R.M., Haagsman, H.P., Localization and developmental expression of two chicken host defense peptides: cathelicidin-2 and avian β-defensin 9. Dev. Comp. Immunol. 61 (2016), 48–59.
Dadfar, M.J., Torshizi, R..V., Maghsoudi, A., Ehsani, A., Masoudi, A.A., Trade-off between feed efficiency and immunity in specialized high-performing chickens. Poult. Sci., 102, 2023, 102703.
Dao, H.T., Sharma, N..K., Kheravii, S.K., Bradbury, E.J., Wu, S.-B., Swick, R.A., Supplementation of reduced protein diets with L-arginine and L-citrulline for broilers challenged with subclinical necrotic enteritis. 3. Immunological parameters and gene expression. Anim. Prod. Sci. 62 (2022), 1266–1279.
De Jong, I.C., Gunnink, H.., Van Hattum, T., Van Riel, J.W., Raaijmakers, M.M.P., Zoet, E.S., Van Den Brand, H., Comparison of performance, health and welfare aspects between commercially housed hatchery-hatched and on-farm hatched broiler flocks. Animal. 13 (2019), 1269–1277.
de Jong, I.C., van Hattum, T.., van Riel, J.W., De Baere, K., Kempen, I., Cardinaels, S., Gunnink, H., Effects of on-farm and traditional hatching on welfare, health, and performance of broiler chickens. Poult. Sci. 99 (2020), 4662–4671.
de Jong, I.C., van Riel, J.., Bracke, M.B.M., van den Brand, H., A “meta-analysis” of effects of post-hatch food and water deprivation on development, performance and welfare of chickens. PLoS. One 12 (2017), 1–20.
Dibner, J.J., Knight, C..D., Kitchell, M.L., Atwell, C.A., Downs, A.C., Ivey, F.J., Early feeding and development of the immune system in neonatal poultry. J. Appl. Poult. Res. 7 (1998), 425–436.
Dieryck, I., De Backere, J., Paeshuyse, J., Effect of hatching system and prophylactic antibiotic use on serum levels of intestinal health biomarker diamine oxidase in broilers at an early age. Animal., 16, 2022, 100493.
Digby, M.R., Lowenthal, J.W., Cloning and expression of the chicken interferon-γ gene. J. Interf. Cytokine Res. 15 (1995), 939–945.
Gaweł, A., Madej, J.P., Kozak, B., Bobrek, K., Early post-hatch nutrition influences performance and muscle growth in broiler chickens. Animals, 12, 2022, 3281.
Geyra, A., Uni, Z., Sklan, D., The effect of fasting at different ages on growth and tissue dynamics in the small intestine of the young chick. Br. J. Nutr. 86 (2001), 53–61.
Giersberg, M.F., Molenaar, R.., de Jong, I.C., Souza da Silva, C., van den Brand, H., Kemp, B., Rodenburg, T.B., Effects of hatching system on the welfare of broiler chickens in early and later life. Poult. Sci, 100, 2021, 100946.
Gilani, S., Howarth, G.S., Kitessa, S.M., Forder, R.E.A., Tran, C.D., Hughes, R.J., New biomarkers for intestinal permeability induced by lipopolysaccharide in chickens. Anim. Prod. Sci. 56 (2016), 1984–1997.
Gonzales, E., Kondo, N., Saldanha, E.S., Loddy, M.M., Careghi, C., Decuypere, E., Performance and physiological parameters of broiler chickens subjected to fasting on the neonatal period. Poult. Sci. 82 (2003), 1250–1256.
Hashem, M.A., Hassan, A.E.A., Abou-Elnaga, H.M.M., Abdo, W., Dahran, N., Alghamdi, A.H., Elmahallawy, E.K., Modulatory effect of dietary probiotic and prebiotic supplementation on growth, immuno-biochemical alterations, DNA damage, and pathological changes in E. coli-infected broiler chicks. Front. Vet. Sci., 9, 2022, 964738.
Hollemans, M.S., de Vries Reilingh, G.., de Vries, S., Parmentier, H.K., Lammers, A., Effects of early nutrition and sanitary conditions on antibody levels in early and later life of broiler chickens. Dev. Comp. Immunol., 117, 2021, 103954.
Hollemans, M.S., de Vries, S.., Lammers, A., Clouard, C., Effects of early nutrition and transport of 1-day-old chickens on production performance and fear response. Poult. Sci. 97 (2018), 2534–2542.
Kanayama, S., Liddle, R.A., Influence of food deprivation on intestinal cholecystokinin and somatostatin. Gastroenterology 100 (1991), 909–915.
Kogut, M.H., Lee, A.., Santin, E., Microbiome and pathogen interaction with the immune system. Poult. Sci. 99 (2020), 1906–1913.
Kogut, M.H., Rothwell, L.., Kaiser, P., Priming by recombinant chicken interleukin-2 induces selective expression of IL-8 and IL-18 mRNA in chicken heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella enterica serovar enteritidis. Mol. Immunol. 40 (2003), 603–610.
Lamot, D.M., Van De Linde, I..B., Molenaar, R., Van Der Pol, C.W., Wijtten, P.J.A., Kemp, B., Van Den Brand, H., Effects of moment of hatch and feed access on chicken development. Poult. Sci. 93 (2014), 2604–2614.
Li, D.L., Wang, J..S., Liu, L.J., Li, K., Xu, Y.B., Ding, X.Q., Wang, Y.Y., Zhang, Y.F., Xie, L.Y., Liang, S., Wang, Y.X., Zhan, X.A., Effects of early post-hatch feeding on the growth performance, hormone secretion, intestinal morphology, and intestinal microbiota structure in broilers. Poult. Sci., 101, 2022, 102133.
Liu, K., Jia, M., Wong, E.A., Delayed access to feed affects broiler small intestinal morphology and goblet cell ontogeny. Poult. Sci. 99 (2020), 5275–5285.
Lynagh, G.R., Bailey, M.., Kaiser, P., Interleukin-6 is produced during both murine and avian Eimeria infections. Vet. Immunol. Immunopathol. 76 (2000), 89–102.
Madej, J.P., Graczyk, S.., Bobrek, K., Bajzert, J., Gaweł, A., Impact of early posthatch feeding on the immune system and selected hematological, biochemical, and hormonal parameters in broiler chickens. Poult. Sci., 103, 2024, 103366.
Mahmoud, K.Z., Edens, F.W., Breeder age affects small intestine development of broiler chicks with immediate or delayed access to feed. Br. Poult. Sci. 53 (2012), 32–41.
Masum, M.A., Khan, M.Z.I., Siddiqi, M.N.H., Nasrin, M., Sultana, N., Frequency and distribution of immunoglobulin containing plasma cells in ileum representing gut-associated-lymphatic tissues in the bcrdv-vaccinated broiler. Bangladesh J. Vet. Med. 10 (2013), 15–20.
Molenaar, R., Stockhofe-Zurwieden, N., Giersberg, M.F., Rodenburg, T.B., Kemp, B., van den Brand, H., de Jong, I.C., Effects of hatching system on chick quality, welfare and health of young breeder flock offspring. Poult. Sci., 102, 2023, 102448.
Mulder, H.A., Rashidi, H., Selection on resilience improves disease resistance and tolerance to infections1. J. Anim. Sci. 95 (2017), 3346–3358.
Nelson, D.W., Murali, S..G., Liu, X., Koopmann, M.C., Holst, J.J., Ney, D.M., Insulin-like growth factor I and glucagon-like peptide-2 responses to fasting followed by controlled or ad libitum refeeding in rats. Am. J. Physiol. Integr. Comp. Physiol. 294 (2008), R1175–R1184.
Panda, A.K., Bhanja, S.K., Sunder, G.S., Early post hatch nutrition on immune system development and function in broiler chickens. Worlds. Poult. Sci. J. 71 (2015), 285–296.
Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT–PCR. Nucleic. Acids. Res., 29, 2001, e45.
Proszkowiec-Weglarz, M., Schreier, L.L., Kahl, S., Miska, K.B., Russell, B., Elsasser, T.H., Effect of delayed feeding post-hatch on expression of tight junction– and gut barrier–related genes in the small intestine of broiler chickens during neonatal development. Poult. Sci. 99 (2020), 4714–4729.
Proszkowiec-Weglarz, M., Schreier, L.L., Miska, K.B., Angel, R., Kahl, S., Russell, B., Effect of early neonatal development and delayed feeding post-hatch on jejunal and ileal calcium and phosphorus transporter genes expression in broiler chickens. Poult. Sci. 98 (2019), 1861–1871.
Rao, J.N., Wang, J.Y., Luminal Nutrients and Microbes in Gut Mucosal Growth Regulation of Gastrointestinal Mucosal Growth, 2010, Morgan & Claypool Life Sciences Available from: https://www.ncbi.nlm.nih.gov/books/NBK54100/.
Rehfeld, J.F., Cholecystokinin-from local gut hormone to ubiquitous messenger. Front. Endocrinol. 8 (2017), 1–8.
Reis, L.H., Gama, L..T., Soares, M.C., Effects of short storage conditions and broiler breeder age on hatchability, hatching time, and chick weights. Poult. Sci. 76 (1997), 1459–1466.
Richards, M.P., Proszkowiec-Weglarz, M.., Rosebrough, R.W., McMurtry, J.P., Angel, R., Effects of early neonatal development and delayed feeding immediately post-hatch on the hepatic lipogenic program in broiler chicks. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 157 (2010), 374–388.
Santhakumar, D., Rubbenstroth, D., Martinez-Sobrido, L., Munir, M., Avian interferons and their antiviral effectors. Front. Immunol., 8, 2017, 49.
Shira, E.B., Sklan, D.., Friedman, A., Impaired immune responses in broiler hatchling hindgut following delayed access to feed. Vet. Immunol. Immunopathol. 105 (2005), 33–45.
Simon, K., de Vries Reilingh, G., Kemp, B., Lammers, A., Development of ileal cytokine and immunoglobulin expression levels in response to early feeding in broilers and layers. Poult. Sci. 93 (2014), 3017–3027.
Souza da Silva, C., Molenaar, R., Giersberg, M.F., Rodenburg, T.B., van Riel, J.W., De Baere, K., Van Dosselaer, I., Kemp, B., van den Brand, H., de Jong, I.C., Day-old chicken quality and performance of broiler chickens from 3 different hatching systems. Poult. Sci., 100, 2021, 100953.
Sun, L., Li, T., Tang, H., Yu, K., Ma, Y., Yu, M., Qiu, Y., Xu, P., Xiao, W., Yang, H., Intestinal epithelial cells-derived hypoxia-inducible factor-1α is essential for the homeostasis of intestinal intraepithelial lymphocytes. Front. Immunol. 10 (2019), 1–12.
Tachibana, T., Matsuda, K., Kawamura, M., Ueda, H., Khan, M.S.I., Cline, M.A., Feeding-suppressive mechanism of sulfated cholecystokinin (26–33) in chicks. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 161 (2012), 372–378.
Turnbaugh, P.J., Ridaura, V..K., Faith, J.J., Rey, F.E., Knight, R., Gordon, J.I., The effect of diet on the Human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med., 1, 2009, 6ra14.
Uni, Z., Ganot, S., Sklan, D., Posthatch development of mucosal function in the broiler small intestine. Poult. Sci. 77 (1998), 75–82.
Van de Ven, L.J.F., Van Wagenberg, A.V., Debonne, M., Decuypere, E., Kemp, B., Van Den Brand, H., Hatching system and time effects on broiler physiology and posthatch growth. Poult. Sci 90 (2011), 1267–1275.
van Dijk, A., Veldhuizen, E.J.A., Kalkhove, S.I.C., Tjeerdsma-van Bokhoven, J.L.M., Romijn, R.A., Haagsman, H.P., The β-defensin gallinacin-6 is expressed in the chicken digestive tract and has antimicrobial activity against food-borne pathogens. Antimicrob. Agents Chemother. 51 (2007), 912–922.
Vasalou, V., Kotidis, E., Tatsis, D., Boulogeorgou, K., Grivas, I., Koliakos, G., Cheva, A., Ioannidis, O., Tsingotjidou, A., Angelopoulos, S., The effects of tissue healing factors in wound repair involving absorbable meshes: a narrative review. J. Clin. Med., 12, 2023, 5683.
Williams, M.A., Lallo, C.H.O., Sundaram, V., The effect of early post hatch feeding times on the growth and development of the gastrointestinal tract of mule ducklings to five days of age. Brazilian J. Poult. Sci., 23, 2021, eRBCA-2019.
Xiong, F., Zhang, L., Role of the hypothalamic–pituitary–adrenal axis in developmental programming of health and disease. Front. Neuroendocrinol. 34 (2013), 27–46.
Yeh, H.-Y., Winslow, B.J., Junker, D.E., Sharma, J.M., In vitro effects of recombinant chicken interferon-gamma on immune cells. J. Interf. Cytokine Res. 19 (1999), 687–691.
Zulkifli, I., Shakeri, M., Soleimani, A.F., Dietary supplementation of L-glutamine and L-glutamate in broiler chicks subjected to delayed placement. Poult. Sci. 95 (2016), 2757–2763.
