Effect of Dietary Supplementation of Spirulina (Arthrospira Platensis) and Thyme (Thymus Vulgaris) on Serum Biochemistry, Immune Response and Antioxidant Status of Rabbits

Melinda Kovács 1 , Tamás Tuboly 2 , Miklós Mézes 3 , Krisztián Balogh 3 , Zsolt Gerencsér 1 , Zsolt Matics 1 , Alessandro Dal Bosco 4 , Zsolt Szendrő 1 , Gábor Tornyos 1 , Dóra Hafner 1 , Gábor Milisits 1 , Erika Balogh-Zándoki 5  and Antonella Dalle Zotte 6
  • 1 Faculty of Agricultural and Environmental Sciences, Kaposvár University, Guba S. 40, 7400, Kaposvár, Hungary
  • 2 Faculty of Veterinary Science, Szent István University, István 2, 1078 Budapest, Hungary
  • 3 Faculty of Agricultural and Environmental Sciences, Szent István University, Páter K. 1, 2001 Gödöllő, Hungary
  • 4 Department of Applied Biology, Animal Science Section, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy
  • 5 MTA-KE Mycotoxins in the Food Chain Research Group, Kaposvár University, Guba S. 40, 7400, Kaposvár, Hungary
  • 6 Department of Animal Medicine, Production and Health, University of Padova, Agripolis, Viale dell’Università 16, 35020, Legnaro, Padova, Italy

Abstract

Growing rabbits’ (42 rabbits/group, 3 rabbits/cage, 14 cages/treatment) diet was supplemented with 5% Spirulina (Arthrospira platensis) and 3% thyme (Thymus vulgaris L.) powder single (S or T) and in combination (ST) between 35 and 77 days of age. On day 0 (weaning at 35 days of age) 14 rabbits were vaccinated with 100 μg/animal ovalbumin to provoke immune response. Blood samples were taken on days 0, 14, 28 and 42 of the experimental period. Sampling dates significantly influenced total protein, albumin, glucose, cholesterol, urea, creatinine concentration and enzyme (AST, ALT, GGT) activities, with a significant age × diet interaction in the case of TP and CREA. There was a significant increase in ALT (+45 and 74%) and GGT (+87 and 102%) activity after immunisation. While Spirulina and thyme significantly ameliorated the rise in AST activity, their effect was inefficient in the case of GGT. Spirulina, both single and in combination showed a tendency in higher IgG level as compared to control (P<0.05). No significant effect of sampling date or treatment on phagocytic activity or secretory IgA was demonstrable (P>0.05). Higher MDA concentration was measured in the red blood cells of S, T and ST animals, while no other significant diet effect on the antioxidant parameters was detected, however, significant sampling date × diet interaction was found in the case of GPx activity. Plasma GGT (increase by 19-66%) was inversely associated with GSH (decrease by 66-113%) between days 0 to 42 of the experimental period (r=-0.57, P<0.05). It can be concluded that Spirulina supplementation alone resulted in higher IgG production, but none of the phytobiotics, at the dose used, affected significantly the antioxidant status of blood.

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  • AOAC (2000). Official Methods of Analysis. 17th ed. Association of Official Analytical Chemists, Arlington, VA, USA.

  • Belay A. (2002). The potential application of Spirulina (Arthrospira) asanutritional and therapeutic supplement in health management. JANA, 5: 27-48.

  • Bölükbasi S.C., Erhan M.K. (2007). Effect of dietary thyme (Thymus vulgaris) on laying hens performance and Escherichia coli (E. coli) concentration in feces. Int. J. Nat. Eng. Sci., 1: 55-58.

  • Campanella L., Crescentini G., Avino P. (1999). Chemical composition and nutritional evaluation of some natural and commercial food products based on Spirulina. Analysis, 27: 533-540.

  • Cheong S.H., Kim M.Y., Sok D.E., Hwang S.Y., Kim J.H., Kim H.R., Lee J.H., Kim Y.B., Kim M.R. (2010). Spirulina prevents atherosclerosis by reducing hypercholesterolemia in rabbits fedahigh-cholesterol diet. J. Nutr. Sci. Vitaminol., 56: 34-40.

  • Dal Bosco A., Gerencsér Z., Szendrő Z., Mugnai C., Cullere M., Kovács M., Ruggeri S., Mattioli S., Castellini C., Dalle Zotte A. (2014). Effect of dietary supplementation of Spirulina (Arthrospira platensis) and Thyme (Thymus vulgaris) on rabbit meat appearance, oxidative stability and fatty acid profile during retail display. Meat Sci., 96: 114-119.

  • Dalle Zotte A., Cullere M., Sartori A., Bosco A.D., Gerencsér Z., Matics Z., Ko - vàcs M., Szendrő Zs. (2014). Effect of dietary supplementation of Spirulina (Arthrospira platensis) and Thyme (Thymus vulgaris) on carcass composition, meat physical traits, and vitamin B12 content of growing rabbits. World Rabbit Sci., 22: 11-19.

  • Deng R., Chow T.J. (2010). Hypolipidemic, antioxidant and anti-inflammatory activities of microalgae Spirulina. Cardiovascular Therapeutics, 28: e33-e45.

  • Dorman H.J.D., Deans M. (2000). Antimicrobial agents from plants: Antibacterial activity of plant volatile oils. J. Appl. Microbiol., 88: 308-316.

  • EC (1998). Commission Directive 98/64/ECof 3 September 1998 establishing Community methods of analysis for the determination of amino acids, crude oils and fats and olaquindox in feeding stuffs and amending Directive 71/393/EEC. Official J. EU, 19.9.1998 L257/14-L257/28.

  • Gerencsér Z., Szendrő Z., Matics Z., Radnai I., Kovács M., Nagy I., Cullere M., Dal Bosco A., Dalle Zotte A. (2014). Effect of dietary supplementation of Spirulina (Arthrospira platensis) and Thyme (Thymus vulgaris) on apparent digestibility and productive performance of growing rabbits. World Rabbit Sci., 22: 1-9.

  • Harcourt-Brown F. (2002). Textbook of rabbit medicine. Oxford, UK, Elsevier, 410 pp.

  • Hayashi O., Katoh T., Okuwaki Y. (1994). Enhancement of antibody production in mice by dietary Spirulina platensis. J. Nutr. Sci. Vitaminol., 40: 431-441.

  • Hoffmann-Pennesi D., Wu C. (2010). The effect of thymol and thyme oil feed supplementation on growth performance, serum antioxidant levels, and caecal Salmonella population in broilers. J. Appl. Poultry Res., 19: 432-443.

  • Jafari S.M.A., Rabbani M., Emtyazjoo M., Piryaei F. (2014). Effect of dietary Spirulina platensis on fatty acid composition of rainbow trout (Oncorhynchus mykiss) fillet. Aquacult. Int., 22: 1307-1315.

  • Kato T., Takemoto K., Katayama H., Kuwabara Y. (1984). Effects of Spirulina (Spirulina platensis) on dietary hypercholesterolemia in rats. J. Jap. Soc. Nutr. Food Sci., 37: 323-332.

  • Kaysen G.A., Dubin J.A., Müller H.G., Rosales L., Levin N.W., Mitch W.E. (2004). Inflammation and reduced albumin synthesis associated with stable decline in serum albumin in hemodialysis patients. Kidney Intern., 65: 1408-1415.

  • Kim M.Y., Cheong S.H., Lee J.H., Kim M.J., Sok D.E., Kim M.R. (2010). Spirulina improves antioxidant status by reducing oxidative stress in rabbits fedahigh-cholesterol diet. J. Med. Food, 13: 420-426.

  • Lawrence R.A., Burk R.F. (1978). Species, tissues and subcellular distribution of non-selenium dependent glutathione peroxidase activity. J. Nutr., 108: 211-215.

  • Lee D.H., Blomhoff R., Jacobs D.R. (2004). Is serum gamma glutamyltransferaseamarker of oxidative stress? Review. Free Radical Res., 38: 535-539.

  • Makhlouf R., Makhlouf I. (2012). Evaluation of the effect of Spirulina against Gamma irradiation induced oxidative stress and tissue injury in rats. Int. J. Appl. Sci. Engin. Res., 1: 152-164.

  • Meineri G., Ingravalle F., Radice E., Aragno M., Peiretti P.G. (2009). Effects of high fat diets and Spirulina platensis in New Zealand White rabbits. J. Anim. Vet. Adv., 8: 2735-2744.

  • Mertens D.R. (2002). Gravimetric determination of amylase-treated detergent fibre in feeds with refluxing beakers or crucibles: collaborative study. J. AOAC Int., 85: 1217-1240.

  • Mikulski D., Zduńczyk Z., Jankowski J., Juśkiewicz J. (2008). Effects of organic acids or natural plant extracts added to diets for turkeys on growth performance, gastrointestinal tract metabolism and carcass characteristics. J. Anim. Feed Sci., 17: 233-246.

  • Mohebbifar A., Torki M. (2011). Growth performance and humoral immune response of broiler chicks fed diets containing graded levels of ground date pits withamixture of dried garlic and thyme. Global Veterinaria, 6: 389-398.

  • Namkung H., Li M., Gong J., Yu H., Cottrill M.,de Lang C.F.M. (2004). Impact of feeding blends of organic acids and herbal extracts on growth performance, gut microbiota and digestive function in newly weaned pigs. Can. J. Anim. Sci., 4: 697-704.

  • Ocak N., Erener G., Burak AK.F., Sungu M., Altop A., Ozmen A. (2008). Performance of broilers fed diets supplemented with dry peppermint (Mentha piperita L.) or thyme (Thymus vulgaris L.) leaves as growth promoter source. Czech J. Anim. Sci., 53: 169-175.

  • Peiretti P.G., Meineri G. (2008). Effects of diets with increasing levels of Spirulina platensis on the performance and apparent digestibility in growing rabbits. Livest. Sci., 118: 173-199.

  • Peiretti P.G., Meineri G. (2009). Effects of two antioxidants on the morpho-biometrical parameters, apparent digestibility and meat composition in rabbits fed low and high fat diets. J. Anim. Vet. Adv., 8: 2299-2304.

  • Peiretti P.G., Meineri G. (2011). Effects of diets with increasing levels of Spirulina platensis on the carcass characteristics, meat quality and fatty acid composition of growing rabbits. Livest. Sci., 140: 218-224.

  • Placer Z.A., Cushman L.L., Johnson B.C. (1966). Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Anal. Biochem., 16: 359-364.

  • Rahimi S., Teymouri Zadeh Z., Karimi Torshizi M.A., Omidbaigi R., Rokni H. (2011). Effect of three herbal extracts on growth performance, immune system, blood factors and intestinal selected bacteria population in broiler chickens. J. Agr. Sci. Tech., 13: 527-539.

  • Ravi M., Lata De S., Azharuddin S., Paul S.F.D. (2010). The beneficial effects of spirulina focusing on its immunomodulatory and antioxidant properties. Nutr. Diet. Suppl., 2: 73-83.

  • Sadeghi G.H., Karimi A., Padidar Jahromi S.H., Azizi T., Daneshmand A. (2012). Effects of cinnamon, thyme and turmeric infusions on the performance and immune response in of 1- to 21-day-old male broilers. Braz. J. Poultry Sci., 14: 15-20.

  • Sedlak I., Lindsay R.H. (1968). Estimation of total, protein-bound and non-protein sulfhydryl groups in tissues with Ellmann’s reagent. Anal. Biochem., 25: 192-205.

  • Simpson D.W., Roth R., Loose L.D. (1979). Arapid, inexpensive and easily quantified assay for phagocytosis and microbicidal activity of macrophages and neutrophils. J. Immunol. Methods, 29: 221-226.

  • Toghyani M., Tohidi M., Gheisari A.A., Tabeidian S.A. (2010). Performance, immunity, serum biochemical and hematological parameters in broiler chicks fed dietary thyme as alternative for an antibiotic growth promoter. Afr. J. Biotechnol., 9: 6819-6825.

  • Toghyani M., Toghyani M., Mohammadrezaei M., Gheisari A., Tabeidian S.A., Ghalamkari G. (2011). Effect of Cocoa and Thyme powder alone or in combination on humoral immunity and serum biochemical metabolites of broiler chicks. Proc. 2nd International Conference on Agricultural and Animal Science, IACSIT Press, Singapore, pp. 114-118.

  • Van Soest P.J., Robertson J.B., Lewis B.A. (1991). Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci., 74: 3583-3597.

  • Vántus V., Bónai A., Zsolnai A., Dal Bosco A., Szendro Z., Tornyos G., Bodnár Z., Morsy W.A., Pósa R., Toldi M., Bóta B., Kovács M., Dalle Zotte A. (2012). Single and combined effect of dietary Thyme (Thymus vulgaris) and Spirulina (Arthrospira platensis) on bacterial community in the caecum and caecal fermentation of rabbits. Acta Agr. Slov., 100 (Supplement 3): 77-81.

  • Voltarelli F.A.,de Mello M.A. (2008). Spirulina enhanced the skeletal muscle protein in growing rats. Eur. J. Nutr., 47: 393-400.

  • Weichselbaum T.E. (1948). An accurate and rapid method for the determination of protein in small amounts of serum and plasma. Am. J. Clin. Pathol., 16: 40-43.

  • Yan L., Meng Q.W., Kim I.H. (2011). The effect of an herb extract mixture on growth performance, nutrient digestibility, blood characteristics and fecal noxious gas content in growing pigs. Livest. Sci., 141: 143-147.

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