Feeding of dried sweet orange (Citrus sinensis) peel on humoral immune response of broiler chickens

Document Type: Original Article

Authors

1 Young Researchers and Elites Club, Rasht Branch, Islamic Azad University, Rasht, Iran

2 Department of Animal Science, Rasht Branch, Islamic Azad University, Rasht, Iran

3 Department of DETO, Section of Veterinary Science and Animal Production, University of Study of Bari ‘Aldo Moro’, Bari, Italy

Abstract

Purpose An experiment was conducted to evaluate the efect of dried sweet orange (Citrus sinensis) peel (DCSP) on humoral immune response of broiler chickens.
Methods Four hundred 1-day-old Ross 308 broilers were distributed according to a completely randomized design into fve treatments with four replicates of 20 chicks each. The following fve dietary treatments were applied: control group with 0% DCSP; diet containing 1.5% DCSP from 1 to 21 days of age (starter phase) and from 1 to 42 days of age, respectively; and diet containing 3% DCSP from 1 to 21 days of age (starter phase) and from 1 to 42 days of age, respectively.
Results The DCSP treatments infuenced positively total anti-SRBC and IgG titers on days 28 and 42, whereas no diferences were found for IgM titer. The anti-NDV titers were not afected by diets; conversely, the anti-AIV titers were diferent among treatments. The anti-IBD titers were diferent on days 14 and 42 among diets, whereas anti-IBV titers were not infuenced by treatments. Average white blood cell, heterophil, lymphocyte, and monocyte counts, as well as heterophil/lymphocyte (H/L) ratio, were diferent among treatments.
Conclusion The fndings suggested that the dietary inclusion of dried Citrus sinensis promoted some efects on the immune humoral response of chickens; however, these efects were not completely efective to protect birds from the main diseases.

Keywords


AOAC (1990) Official methods of analysis, 15th edn. Association of Official Analytical Chemists, Washington, DC

Azizi M, Seidavi AR, Ragni M, Laudadio V, Tufarelli V (2018) Practical applications of agricultural wastes in poultry feeding in Mediterranean and Middle East regions. Part 1: citrus, grape, pomegranate and apple wastes. World Poult Sci J 74:489–498. https ://doi.org/10.1017/S0043 93391 80004 78

Byer T, Nestle M, McTiernan A, Doyle C, Currie WA, Gansler T, Thun M (2001) American cancer society guidelines on nutrition and physical activity for cancer prevention. Can J Clin Pharmacol 52:92–119

Chanthaphon S, Chanthachum S, Hongpattarakere T (2008) Antimicrobial activities of essential oils and crude extracts from tropical Citrus spp. against food-related microorganisms. Song J Sci Technol 30:125–13

Chen HL, Li DF, Chang BY, Gong LM, Dai JG, Yi GF (2003) Effects of Chinese herbal polysaccharides on the immunity and growth performance of young broilers. Poult Sci 82:364–370. https ://doi. org/10.1093/ps/82.3.364

Ding G, Chen Z, Li W, Yang G, Xu CY (2004) Studies on effects of grass carp cell immune function by adding orange peels. Chin J Yun Agric Univ 19:727–730

Dong XF, Gao WW, Tong JM, Lia HQ, Sa RN, Zhang Q (2007) Effect of polysavone (Alfa Extract) on abdominal fat deposition and immunity in broiler chickens. Poult Sci 86:1955–1959. https ://doi.org/10.1093/ps/86.9.1955

Dragsted LO, Young JF, Loft S, Sandstrom B, Nesaretnam K, Packer L (2001) Biomarkers of oxidative stress and of antioxidative defense: relationship to intervention with antioxidant-rich foods. In: Nesratnem K, Packer L (eds) Micronutrients and health:molecular biological mechanisms. Danish Food Administration, Søborg, Denmark, pp 272–278

Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412. https ://doi.org/10.1093/jn/125.6.1401

Spinosa HS, Górniak, SL, Bernardi MM (2002) Farmacologia Aplicada à Medicina Veterinária, Ed. Guanabara Koogan, 3a Edição, Rio de Janeiro, Brazil

Guo FC, Williams BA, Kwakkel RP, Li HS, Li XP, Luo JY, Li WK, Verstegen MWA (2004) Effects of mushroom and herb polysaccharides, as alternatives for an antibiotic, on the cecal microbial
ecosystem in broiler chickens. Poult Sci 83:175–178. https ://doi.org/10.1093/ps/83.2.175

Imboden JB, Weiss A, Stobo JD (1985) The antigen receptor on a human T cell line initiates activation by increasing cytoplasmic free calcium. J Immunol 134:663–665

Karthiyaini K, Philiomina PT (2009) Effect of vitamin c supplementation on some biochemical profile stressed broiler. In: Proceedings of the national seminar of recent trends in animal welfare and sustainable livestock production, Thrissur, India

Kayvan A, Eshtiyaghi R (1992) Immunologhy Royte Principios. Jahad-E-Keshavarzi Ed. University Medical Science, Tehran, Iran

Klasing KC (1998) Nutritional modulation of resistance to infectious diseases. Poult Sci 77:1119–1125. https ://doi.org/10.1093/ps/77.8.1119

Laudadio V, Nahashon SN, Tufarelli V (2012) Growth performance and carcass characteristics of guinea fowl broilers fed micronized-dehulled pea (Pisum sativum L.) as a substitute for soybean
meal. Poult Sci 91:2988–2996. https ://doi.org/10.3382/ps.2012-02473

Leonard SS, Cutler D, Ding M (2002) Antioxidant properties of fruit and vegetable juices: more to the story than ascorbic acid. Ann Clin Lab Sci 32:193–200

Leshchinsky TV, Klasing KC (2001) Relationship between the level of dietary vitamin E and the immune response of broiler chickens.Poult Sci 80:1590–1599. https ://doi.org/10.1093/ps/80.11.1590

Malterud KE, Rydland KM (2000) Inhibitors of 15-lipoxygenase from orange peel. J Agric Food Chem 48:5576–5580. https ://doi.org/10.1021/jf000 613v

Manthey JA (2004) Fractionation of orange peel phenols in ultrafiltered molasses and mass balance studies of their antioxidant levels. J Agric Food Chem 15:7586–7592. https ://doi.org/10.1021/jf049
083j

Marech I, Ammendola M, Leporini C, Patruno R, Luposella M, Zizzo N, Passantino G, Sacco R et al (2018) C‐Kit receptor and tryptase expressing mast cells correlate with angiogenesis in breast cancer patients. Oncotarget 9:7918–7927

Mc-Farland K, Catalano JF, Thrope SR, Baynes JW (2005) Nonenzymatic glucosylation of serum proteins in diabetes mellitus. Diabetes 28:1011–1014. https ://doi.org/10.2337/diab.28.11.1011

Mogenet LY, Youbicier-Simo BJ (1998) Determination of reliable biochemical parameters of heat stress and application to the evaluation of medications: example of erythromycin E. In: Proceedings of 10th European poultry conference, Jerusalem, Israel, pp 538–541

Mona SR, Hanan A (2007) Effects of using dried egyptian clover and orange peels as natural feed additives on egg production egg quality and immune response of laying hens. Fay J Agric Res Dev
21:188–205

Nijveldt RJ, Boelens Nood EV (2001) Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 74:418–425. https ://doi.org/10.1093/ajcn/74.4.418

NRC (1994) Nutrient requirements of poultry, 9th edn. National Academy Press, Washington, DC
Nysather JO, Katz AE, Lenth JL (1976) The immune system: its development and functions. Am J Nurs 76:1614–1618

Oluremi OIA, Ebe AI, Ngi J, Aku EO (2010) Effect of naturally fermented sweet orange (Citrus sinensis) peel meal on its maize replacement value in broiler diet on performance and carcass indices. In: Proc. of 35th Ann. Conf. Nig. Soc. for Anim. Prod. 14–17 March, University of Ibadan, Nigeria, pp 449–542

Pourhossein Z, Qotbi AAA, Seidavi A, Laudadio V, Centoducati G, Tufarelli V (2015) Effect of different levels of dietary sweet orange (Citrus sinensis) peel extract on humoral immune system responses in broiler chickens. Anim Sci J 86:105–110. https ://doi.org/10.1111/asj.12250

Puthpongsiriporn U, Scheideler SE (2005) Effects of dietary ratio of linoleic to linolenic acid on Performance, antibody production,and in vitro lymphocyte proliferation in two strains of leghorn
pullet chicks. Poult Sci 84:846–857. https ://doi.org/10.1093/ps/84.6.846

Qorbanpour M, Fahi T, Javandel F, Nosrati M, Paz E, Seidavi A, Ragni M, Laudadio V, Tufarelli V (2018) Effect of dietary ginger (Zingiber officinale Roscoe) and multi-strain probiotic on growth and carcass traits, blood biochemistry, immune responses and intestinal microflora in broiler chickens. Animals 8:117. https ://doi.org/10.3390/ani80 70117

Qureshi MA, Hussain I, Heggen CL (1998) Dietary exposure of broiler breeders to aflatoxin results in immune function in progeny chicks.Poult Sci 77:1126–1129. https ://doi.org/10.1093/ps/77.6.812

SAS Institute (2002) SAS proprietary software release 9.2. SAS Inst.Inc., Cary

Scott LA (1993) Diffusion across a sheep red blood cell membrane.Test Stud Lab Teach 14:115–140

Tufarelli V, Crovace AM, Rossi G, Laudadio V (2017) Effect of a dietary probiotic blend on performance, blood characteristics, meat quality and faecal microbial shedding in growing-finishing pigs. S Afr J Anim Sci 47:875–882. https ://doi.org/10.4314/sajas.v47i6 .15

Wegmann TG, Smithies O (1965) A simple hemagglutination system requiring small amounts of red blood cells and antibodies. Transfusion 6:67–73. https ://doi.org/10.1111/j.1537-2995.1966.tb046
96.x

Weinstock D, Schat KA, Calnet BW (1989) Cytotoxic T lymphocytesin reticulo endotheliosis virus-infected chickens. Eur J Immunol 19:267–272. https ://doi.org/10.1002/eji.18301 90208

Yamamoto Y, Glick B (1982) A comparison of the immune response between two lines of chickens selected for differences in the weight of the bursa fabricius. Poult Sci 61:2129–2132. https ://
doi.org/10.3382/ps.06121 29