Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-20T04:53:57.304Z Has data issue: false hasContentIssue false

The effects of superoxide dismutase-rich melon pulp concentrate on inflammation, antioxidant status and growth performance of challenged post-weaning piglets

Published online by Cambridge University Press:  18 June 2018

A. S. M. L. Ahasan
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
G. Invernizzi
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
G. Farina
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
A. Pilotto
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
F. Barbé
Affiliation:
Lallemand SAS, 31700 Blagnac, France
V. Bontempo
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
R. Rossi
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
F. Bellagamba
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
C. Lecchi
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Milano, 20133 Milano, Italy
G. Savoini
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
A. Agazzi*
Affiliation:
Dipartimento di Scienze Veterinarie per la Salute, la Produzione Animale e la Sicurezza Alimentare, Università degli Studi di Milano, 20133 Milano, Italy
*
Get access

Abstract

Piglets can often suffer impaired antioxidant status and poor immune response during post-weaning, especially when chronic inflammation takes place, leading to lower growth rates than expected. Oral administration of dietary antioxidant compounds during this period could be a feasible way to balance oxidation processes and increase health and growth performance. The aim of the trial was to study the effects of an antioxidant feed supplement (melon pulp concentrate) that contains high concentration of the antioxidant superoxide dismutase (SOD) on inflammation, antioxidant status and growth performance of lipopolysaccharide (LPS) challenged weaned piglets. In total, 48 weaned piglets were individually allocated to four experimental groups in a 2×2 factorial design for 29 days. Two different dietary treatments were adopted: (a) control (CTR), fed a basal diet, (b) treatment (MPC), fed the basal diet plus 30 g/ton of melon pulp concentrate. On days 19, 21, 23 and 25 half of the animals within CTR and MPC groups were subjected to a challenge with intramuscular injections of an increasing dosage of LPS from Escherichia coli (serotype 0.55:B5) (+) or were injected with an equal amount of PBS solution (). Blood samples were collected at the beginning of the trial and under the challenge period for interleukin 1β, interleukin 6, tumour necrosis factor α, haptoglobin, plasma SOD activity, total antioxidant capacity, reactive oxygen species, red blood cells and plasma resistance to haemolysis, and 8-oxo-7, 8-dihydro-2’-deoxyguanosine. Growth performance was evaluated weekly. A positive effect of melon pulp concentrate was evidenced on total antioxidant capacity, half-haemolysis time of red blood cells, average daily gain (ADG) and feed intake, while LPS challenge increased pro-inflammatory cytokines and haptoglobin serum concentrations, with a reduced feed intake and gain : feed (G : F). The obtained results show that oral SOD supplementation with melon pulp concentrate ameliorates the total antioxidant capacity and the half-haemolysis time in red blood cell of post-weaning piglets, with positive results on growing performance.

Type
Research Article
Copyright
© The Animal Consortium 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Present address: Department of Anatomy and Histology, Faculty of Veterinary Medicine, Veterinary and Animal Sciences University, 4225, Chittagong, Bangladesh.

References

Association of Official Analytical Chemists (AOAC) 2005. Official methods of analysis, 18th edition. AOAC, Arlington, VA, USA.Google Scholar
Bontempo, V, Jiang, XR, Cheli, F, Lo Verso, L, Mantovani, G, Vitari, F, Domeneghini, C and Agazzi, A 2014. Administration of a novel plant extract product via drinking water to post-weaning piglets: effects on performance and gut health. Animal 8, 721730.Google Scholar
Campbell, JM, Crenshaw, JD and Polo, J 2013. The biological stress of early weaned piglets. Journal of Animal Science and Biotechnology 4, 19.Google Scholar
Carillon, J, Rouanet, JM, Cristol, JP and Brion, R 2013a. Superoxide dismutase administration, a potential therapy against oxidative stress related diseases: several routes of supplementation and proposal of an original mechanism of action. Pharmaceutical Research 30, 27182728.Google Scholar
Carillon, J, Fouret, G, Feillet-Coudray, C, Lacan, D, Cristol, JP and Rouanet, JM 2013b. Short-term assessment of toxicological aspects, oxidative and inflammatory response to dietary melon superoxide dismutase in rats. Food and Chemical Toxicology 55, 323328.Google Scholar
Carroll, JA, Fangman, TJ, Hambach, AK and Wiedmeyer, CE 2004. The acute phase response in pigs experimentally infected with Escherichia coli and treated with systemic bactericidal antibiotics. Livestock Production Science 85, 3544.Google Scholar
Carroll, JA, Matteri, RL, Dyer, CJ, Beausang, LA and Zannelli, ME 2001. Impact of environmental temperature on response of neonatal pigs to an endotoxin challenge. American Journal of Veterinary Research 62, 561566.Google Scholar
Cray, C, Zaias, J and Altman, NH 2009. Acute phase response in animals: a review. Comparative Medicine 59, 517526.Google Scholar
Ceciliani, F, Ceron, JJ, Eckersall, PD and Sauerwein, H 2012. Acute phase proteins in ruminants. Journal of Proteomics 75, 42074231.Google Scholar
Cooke, RF and Arthington, JD 2013. Concentrations of haptoglobin in bovine plasma determined by ELISA or a colorimetric method based on peroxidase activity. Journal of Animal Physiology and Animal Nutrition 97, 531536.Google Scholar
de Ridder, K, Levesque, CL, Htoo, JK and de Lange, CFM 2012. Immune system stimulation reduces the efficiency of tryptophan utilization for body protein deposition in growing pigs. Journal of Animal Science 90, 34853491.Google Scholar
Frank, JW, Mellencamp, MA, Carroll, JA, Boyd, RD and Allee, GL 2005. Acute feed intake and acute-phase protein responses following a lipopolysaccharide challenge in pigs from two dam lines. Veterinary Immunology and Immunopathology 107, 179187.Google Scholar
Gessner, DK, Ringseis, R and Eder, K 2017. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. Journal of Animal Physiology and Animal Nutrition 101, 605628.Google Scholar
Jiang, XR, Agazzi, A, Awati, A, Vitari, F, Bento, H, Ferrari, A, Alborali, GL, Crestani, M, Domeneghini, C and Bontempo, V 2015b. Influence of a blend of essential oils and an enzyme combination on growth performance, microbial counts, ileum microscopic anatomy and the expression inflammatory mediators in weaned piglets following an Escherichia coli infection. Animal Feed Science and Technology 209, 219229.Google Scholar
Jiang, XR, Awati, A, Agazzi, A, Vitari, F, Ferrari, A, Bento, H, Crestani, M, Domeneghini, C and Bontempo, V 2015a. Effects of a blend of essential oils and an enzyme combination on nutrient digestibility, ileum histology and expression of inflammatory mediators in weaned piglets. Animal 9, 417426.Google Scholar
Kick, AR, Tompkins, MB, Flowers, WL, Whisnant, CS and Almond, GW 2012. Effects of stress associated with weaning on the adaptive immune system in pigs. Journal of Animal Science 90, 649656.Google Scholar
Lallès, JP, Lacan, D and David, JC 2011. A melon pulp concentrate rich in superoxide dismutase reduces stress proteins along the gastrointestinal tract of pigs. Nutrition 27, 358363.Google Scholar
Le Floc’h, N and Seve, B 2007. Biological roles of tryptophan and its metabolism: potential implications for pig feeding. Livestock Science 112, 2332.Google Scholar
Muchová, J, Śustrová, M, Garaiová, I, Liptáková, A., Blazíček, P, Kvasnička, P, Pueschel, S and Duračková, Z 2001. Influence of age on activities of antioxidant enzymes and lipid peroxidation products in erythrocytes and neutrophils of Down syndrome patients. Free Radical Biology and Medicine 31, 499508.Google Scholar
National Research Council (NRC) 2012. Nutrient requirements of swine, 11th revised edition. National Academic Press, Washington, DC, USA.Google Scholar
Niekamp, SR, Sutherland, MA, Dahl, GE and Salak-Johnson, JL 2007. Immune responses of piglets to weaning stress: impacts of photoperiod. Journal of Animal Science 85, 93100.Google Scholar
Notin, C, Vallon, L, Desbordes, F and Leleu, C 2010. Oral supplementation with superoxide dismutase in Standardbred trotters in training: a double blind placebo controlled study. Equine Veterinary Journal 42 (suppl. 38), 375381.Google Scholar
Pié, S, Lallès, JP, Blazy, F, Laffitte, J, Seve, B and Oswald, IP 2004. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. The Journal of Nutrition 134, 641647.Google Scholar
Rakhshandeh, A and de Lange, CF 2012. Evaluation of chronic immune system stimulation models in growing pigs. Animal 6, 305310.Google Scholar
Royer, E, Barbé, F, Guillou, D, Rousseliere, Y and Chevaux, E 2016. Development of an oxidative stress model in weaned pigs highlighting plasma biomarkers’ specificity to stress inducers. Journal of Animal Science 94, 4853.Google Scholar
Rossi, R, Pastorelli, G and Corino, C 2013. Application of KRL test to assess total antioxidant activity in pigs: sensitivity to dietary antioxidants. Reseach in Veterinary Science 94, 372377.Google Scholar
Salamano, G, Mellia, E, Candiani, D, Ingravalle, F, Bruno, R, Ru, G and Doglione, L 2008. Changes in haptoglobin, C-reactive protein and pig-major acute phase protein (porcine) during a housing period following long distance transport in swine. The Veterinary Journal 177, 110115.Google Scholar
Sartorelli, P, Paltrinieri, S and Comazzi, S 2000. Non-specific immunity and ketone bodies. II: in vitro studies on adherence and superoxide anion production in ovine neutrophils. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine 47, 18.Google Scholar
van de Crommenacker, J, Horrocks, NP, Versteegh, MA, Komdeur, J, Tieleman, BI and Matson, KD 2010. Effects of immune supplementation and immune challenge on oxidative status and physiology in a model bird: implications for ecologists. The Journal of Experimental Biology 213, 35273535.Google Scholar
Van Soest, PJ, Robertson, JB and Lewis, BA 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 35833597.Google Scholar
Vouldoukis, I, Conti, M, Krauss, P, Kamate, C, Blazquez, S, Tefit, M, Mazier, D, Calenda, A and Dugas, B 2004a. Supplementation with gliadin-combined plant superoxide dismutase extract promotes antioxidant defences and protects against oxidative stress. Phytotherapy Research 18, 957962.Google Scholar
Vouldoukis, I, Lacan, D, Kamate, C, Coste, P, Calenda, A, Mazier, D, Conti, M and Dugas, B 2004b. Antioxidant and anti-inflammatory properties of a Cucumis melo LC extract rich in superoxide dismutase activity. Journal of Ethnopharmacology 94, 6775.Google Scholar
Zhang, R, Chae, S, Lee, JH and Hyun, JW. 2012. The cytoprotective effect of butin against oxidative stress is mediated by the up-regulation of manganese superoxide dismutase expression through a PI3K/Akt/Nrf2-dependent pathway. Journal of Cellular Biochemistry 113, 19871997.Google Scholar
Zhu, LH, Zhao, KL, Chen, XL and Xu, JX 2012. Impact of weaning and an antioxidant blend on intestinal barrier function and antioxidant status in pigs. Journal of Animal Science 90, 25812589.Google Scholar