Effects of dietary conjugated linoleic acid on haematological and humoral responses in the grower pig
E. Ostrowska A B , A. Knowles C , M. Muralitharan D , R. F. Cross B , D. E. Bauman E and F. R. Dunshea A D F GA Department of Primary Industries, 600 Sneydes Rd, Werribee, Vic. 3030, Australia.
B School of Engineering and Science, Swinburne University of Technology, Hawthorn, Vic. 3122, Australia.
C Faculty of Veterinary Science, University of Sydney, NSW 2006, Australia.
D School of Biological and Chemical Sciences, Deakin University, Geelong, Vic. 3220, Australia.
E Department of Animal Science, Cornell University, Ithaca, NY 14853, USA.
F School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia.
G Corresponding author; email: Frank.Dunshea@dpi.vic.gov.au
Australian Journal of Agricultural Research 55(7) 711-718 https://doi.org/10.1071/AR04002
Submitted: 5 January 2003 Accepted: 19 May 2004 Published: 2 August 2004
Abstract
The effects of conjugated linoleic acid (CLA) on the levels of total serum leucocytes, granulocytes including neutrophils, basophils, and eosinophils, as well as on monocytes and leucocytes were measured in pigs selected from a clean (minimal disease) herd. Thirty pigs were fed different rates of dietary CLA (0, 1.25, 2.5, 5.0, 7.5, and 10.0 g CLA-55/kg diet) for 8 weeks. Blood samples were collected at the end of the study for assessment of haematological and humoral responses to CLA supplementation. No difference in total white blood cells including the neutrophil, monocyte, and lymphocyte counts was observed among different dietary groups. A dose-dependent reduction (P = 0.02) in eosinophil concentrations suggests that CLA exerts anti-inflammatory activities. A 2-fold increase in the level of basophils was recorded in pigs fed lower levels of CLA (1.25 and 2.5 g CLA/kg diet) but the levels decreased gradually (P = 0.05) and were below the detection limit at the highest rate (10 g/kg) of CLA supplementation. The level of IgG was reduced by over 50% in CLA-fed pigs (P < 0.001), although the response was quadratic in nature (P < 0.001). T-cell population analysis showed that CD4+ cells tended (P = 0.06) to be reduced linearly with increasing inclusion of CLA in the diet. Our results suggest that dietary CLA modulates haematological and humoral responses in a dose-dependent manner.
Acknowledgments
The authors thank Carl Skarie from ConLinco Pty Ltd for providing CLA, and acknowledge the technical assistance of Doug Kerton, Danny Suster, and Shamila Khan. EO gratefully acknowledges a Swinburne University Postgraduate Research Award. The authors acknowledge the financial assistance of Australian Pork Limited (formally the Pig Research and Development Corporation) for partial funding of this project and for the award of a top-up scholarship to EO. These data were presented in part at the 24th Annual Scientific Meeting of the Nutrition Society of Australia [Ostrowska E, Knowles A, Muralitharan M, Cross RF, Bauman DE, Dunshea FR (2000) Dietary conjugated linoleic acid modulates the immune system of growing pigs. Proceedings of the Nutrition Society of Australia 24, 258].
Bassaganya-Riera J,
Hontecillas-Magarzo R,
Bregendahl K,
Wannemuehler MJ, Zimmerman DR
(2001) Effects of dietary conjugated linoleic acid in nursery pigs of dirty and clean environments on growth, empty body composition, and immune competence. Journal of Animal Science 79, 714–721.
| PubMed |
Belury MA, Kempa-Steczko A
(1997) Conjugated linoleic acid modulates hepatic lipid composition in mice. Lipids 32, 199–204.
| PubMed |
Belury MA,
Nickel KP,
Bird CE, Wu Y
(1996) Dietary conjugated linoleic acid modulation of phorbol ester skin tumor promotion. Nutrition and Cancer 26, 149–157.
| PubMed |
van den Berg JJ,
Cook NE, Tribble DL
(1995) Reinvestigation of the antioxidant properties of conjugated linoleic acid. Lipids 30, 599–605.
| PubMed |
Black JL,, Liges LRM, Wynn PC, Knowles AG, Kerr CA, Jones MR, Strom AD, Gallagher NL, Eamens GJ
(2001) A review—factors limiting the performance of growing pigs in commercial environments. ‘Manipulating pig production VIII’. (Ed. PD Cranwell)
pp. 9–36. (Australasian Pig Science Association: Werribee, Vic.)
Bontempo V,
Sciannimanico D,
Pastorelli G,
Rossi R,
Rosi F, Corino C
(2004) Dietary conjugated linoleic acid positively affects immunologic variables in lactating sows and piglets. Journal of Nutrition 134, 817–824.
| PubMed |
Cesano A,
Visonneau S,
Scimeca JA,
Kritchevsky D, Santoli D
(1998) Opposite effects of linoleic acid and conjugated linoleic acid on human prostatic cancer in SCID mice. Anticancer Research 18, 1429–1434.
| PubMed |
Chew BP,
Wong TS,
Shultz TD, Magnuson NS
(1997) Effects of conjugated dienoic derivatives of linoleic acid and beta-carotene in modulating lymphocyte and macrophage function. Anticancer Research 17, 1099–1106.
| PubMed |
Chin SF,
Storkson JM,
Albright KJ,
Cook ME, Pariza MW
(1994) Conjugated linoleic acid is a growth factor for rats as shown by enhanced weight gain and improved feed efficiency. Journal of Nutrition 124, 2344–2349.
Coffman RL,
Seymour BW,
Hudak S,
Jackson J, Rennick D
(1989) Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 245, 308–310.
| PubMed |
Cook ME, Jerome DE, Pariza MW, Schmidt JKG
(1998) The pathology, hematology and blood chemistry of pigs fed conjugated linoleic acid synthesized from sunflower oil. ‘Proceedings of the American Association of Oil Chemistry’. (American Association of Oil Chemistry: Chicago, IL)
Cook ME,
Miller CC,
Park Y, Pariza M
(1993) Immune modulation by altered nutrient metabolism, nutritional control of immune-induced growth depression. Poultry Science 72, 1301–1305.
| PubMed |
Cross RF,
Ostrowska E,
Muralitharan M, Dunshea FR
(2000) Mixed mode retention and the use of competing acid for the Ag-HPLC analysis of underivatized conjugated linoleic acids. Journal of High Resolution Chromatography 23, 317–323.
| Crossref | GoogleScholarGoogle Scholar |
Cunningham DC,
Harrison LY, Shultz TD
(1997) Proliferative responses of normal human mammary and MCF-7 breast cancer cells to linoleic acid, conjugated linoleic acid and eicosanoid synthesis inhibitors in culture. Anticancer Research 17, 197–203.
| PubMed |
Dunshea FR,
King RH,
Campbell RG,
Sainz RD, Kim YS
(1993) Interrelationships between sex and ractopamine on protein and lipid deposition in rapidly growing pigs. Journal of Animal Science 71, 2919–2930.
| PubMed |
Dunshea FR,
Ostrowska E,
Luxford B,
Smits RJ,
Campbell RG,
D’Souza DN, Mullan BP
(2002) Dietary conjugated linoleic acid can decrease backfat in pigs housed under commercial conditions. Asian-Australasian Journal of Animal Sciences 15, 1011–1017.
Dhurandhar NR, Zorrilla O
(1988) Special stains in cytology: a technique using one half of a previously stained slide Diagnostic Cytopathology 4, 347–351.
| PubMed |
Ha YL,
Grimm NK, Pariza MW
(1987) Anticarcinogens from fried ground beef, heat-altered derivatives of linoleic acid. Carcinogenesis 8, 1881–1887.
| PubMed |
Ha YL,
Storkson J, Pariza MW
(1990) Inhibition of benzo(a)pyrene-induced mouse forestomach neoplasia by conjugated dienoic derivatives of linoleic acid. Cancer Research 50, 1097–1101.
| PubMed |
Ip C,
Banni S,
Angioni E,
Carta G,
McGinley J,
Thompson HJ,
Barbano D, Bauman D
(1999b) Conjugated linoleic acid-enriched butter fat alters mammary gland morphogenesis and reduces cancer risk in rats. Journal of Nutrition 129, 2135–2142.
| PubMed |
Ip C,
Chin SF,
Scimeca JA, Pariza MW
(1991) Mammary cancer prevention by conjugated dienoic derivative of linoleic acid. Cancer Research 51, 6118–6124.
| PubMed |
Ip C,
Singh M,
Thompson HJ, Scimeca JA
(1994) Conjugated linoleic acid suppresses mammary carcinogenesis and proliferative activity of the mammary gland in the rat. Cancer Research 54, 1212–1215.
| PubMed |
Ip MM,
Masso-Welch PA,
Shoemaker SF,
Shea-Eaton WK, Ip C
(1999a) Conjugated linoleic acid inhibits proliferation and induces apoptosis of normal rat mammary epithelial cells in primary culture. Experimental Cell Research 250, 22–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jelinek DF
(2000) Regulation of B lymphocyte differentiation. Annals of Allergy, Asthma and Immunololgy 84, 375–385.
Klasing KC, Korver DR
(1997) Leukocytic cytokines regulate growth rate and composition following activation of the immune system. Journal of Animal Science 75, 58–67.
Lee KN,
Kritchevsky D, Pariza MW
(1994) Conjugated linoleic acid and atherosclerosis in rabbits. Atherosclerosis 108, 19–25.
| PubMed |
Liu KL, Belury MA
(1998) Conjugated linoleic acid reduces arachidonic acid content and PGE2 synthesis in murine keratinocytes. Cancer Letters 127, 15–22.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miller CC,
Park Y,
Pariza MW, Cook ME
(1994) Feeding conjugated linoleic acid to animals partially overcomes catabolic responses due to endotoxin injection. Biochemical and Biophysical Research Communications 198, 1107–1112.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nicolosi RJ,
Rogers EJ,
Knichevski DD,
Scimeca HA, Huth PJ
(1997) Dietary conjugated linoleic acid reduces plasma lipoproteins and early aortic artherogenesis in hypercholestrolemic hamsters. Artery 22, 266–277.
| PubMed |
Ostrowska E,
Cross RF,
Muralitharan M,
Bauman DE, Dunshea FR
(2003a) Dietary conjugated linoleic acid differentially alters fatty acid composition and increases conjugated linoleic acid content in porcine adipose tissue. The British Journal of Nutrition 90, 915–928.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ostrowska E,
Dunshea FR,
Muralitharan M, Cross RF
(2000) Comparison of silver-ion high-performance liquid chromatographic quantification of free and methylated conjugated linoleic acids. Lipids 35, 1147–1153.
| PubMed |
Ostrowska E,
Muralitharan M,
Cross RF,
Bauman DE, Dunshea FR
(1999) Dietary conjugated linoleic acids increase lean tissue and decrease fat deposition in growing pigs. Journal of Nutrition 129, 2037–2042.
| PubMed |
Ostrowska E,
Suster D,
Muralitharan M,
Cross RF,
Leury BJ,
Bauman DE, Dunshea FR
(2003a) Conjugated linoleic acid decreases fat accretion in pigs, evaluation by dual-energy X-ray absorptiometry. The British Journal of Nutrition 89, 219–229.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Perticarari S,
Presani G,
Mangiarotti MA, Banfi E
(1991) Simultaneous flow cytometric method to measure phagocytosis and oxidative products by neutrophils. Cytometry 12, 687–693.
| PubMed |
Pescovitz MD,
Aasted B,
Canals A,
Dominguez J, Vizcaino JS , et al.
(1994) Analyses of monoclonal antibodies reacting with porcine CD3: results from the 2nd International Swine CD Workshop. Veterinary Immunology and Immunopathology 43, 233–236.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pescovitz MD,
Book BK,
Aasted B,
Dominguez J, Ezquerra A , et al.
(1998) Analyses of monoclonal antibodies reacting with porcine CD3: results from the 2nd International Swine CD Workshop. Veterinary Immunology and Immunopathology 60, 261–268.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Saalmuller A,
Aasted B,
Canals A,
Dominguez J,
Goldman T,
Lunney JK,
Maurer S,
Pescovitz MD,
Pospisil R, Salmon H
(1994) Analyses of mAb reactive with porcine CD8. Veterinary Immunology and Immunopathology 43, 249–254.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
SCA (1987).
Shultz TD,
Chew BP, Seaman WR
(1992b) Differential stimulatory and inhibitory responses of human MCF-7 breast cancer cells to linoleic acid and conjugated linoleic acid in culture. Anticancer Research 12, 2143–2145.
| PubMed |
Shultz TD,
Chew BP,
Seaman WR, Luedecke LO
(1992a) Inhibitory effect of conjugated dienoic derivatives of linoleic acid and beta-carotene on the in vitro growth of human cancer cells. Cancer Letters 63, 125–133.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stangl GI,
Muller H, Kirchgessner M
(1999) Conjugated linoleic acid effects on circulating hormones, metabolites and lipoproteins, and its proportion in fasting serum and erythrocyte membranes of swine. European Journal of Nutrition 38, 271–277.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sugano M,
Tsujita A,
Yamasaki M,
Noguchi M, Yamada K
(1998) Conjugated linoleic acid modulates tissue levels of chemical mediators and immunoglobulins in rats. Lipids 33, 521–527.
| PubMed |
Sugano M,
Tsujita A,
Yamasaki M,
Yamada K,
Ikeda I, Kritchevsky D
(1997) Lymphatic recovery, tissue distribution, and metabolic effects of conjugated linoleic acid in rats. Nutritional Biochemistry 8, 38–43.
| Crossref | GoogleScholarGoogle Scholar |
Turek JJ,
Schoenlein IA,
Clark LK, Van Alstine WG
(1994) Dietary polyunsaturated fatty acid effects on immune cells of the porcine lung. Journal of Leukocyte Biology 56, 599–604.
| PubMed |
Whigham LD,
Higbee AJ,
Pariza MW, Cook ME
(1999) Influence of dietary conjugated linoleic acid on release of PGE2 and LTB4 from guinea pig lung, trachea, and bladder. FASEB Journal 13, 4566.
Yamasaki M,
Chujo H,
Hirao A,
Koyanagi N, Okamoto T , et al.
(2003) Immunoglobulin and cytokine production from spleen lymphocytes is modulated in C57BL/6J mice by dietary cis-9, trans-11 and trans-10, cis12 conjugated linoleic acid. Journal of Nutrition 133, 784–788.
| PubMed |
Yurawecz MP,
Roach JA,
Sehat N,
Mossoba MM,
Kramer JK,
Fritsche J,
Steinhart H, Ku Y
(1998) A new conjugated linoleic acid isomer, 7 trans, 9 cis-octadecadienoic acid, in cow milk, cheese, beef and human milk and adipose tissue. Lipids 33, 803–809.
| PubMed |
