Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T18:19:29.413Z Has data issue: false hasContentIssue false
  • English
  • Français

Bone turnover and nutritional status in Crohn's disease: relationship to circulating mononuclear cell function and response to fish oil and antioxidants

Published online by Cambridge University Press:  07 March 2007

T. M. Trebble
T. M. Trebble*
Affiliation:
Institute of Human Nutrition, School of Medicine, University of Southampton, Tremona Road, Southampton, SO16 6YD, UK
*
Corresponding author: Dr Timothy Trebble, fax +44 23 80794945, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Crohn's disease is associated with osteoporosis, malnutrition and altered function of peripheral blood mononuclear cells (PBMC). The responses of circulating immune cells and extra-intestinal manifestations to increased inflammatory activity and to modulation by dietary supplementation are uncertain. The relationships between disease status, bone turnover and body mass and composition, PBMC function and fatty acid availability have been investigated in patients with Crohn's disease. The availability of n-3 and n-6 PUFA is altered in adult patients and interferon (IFN)-γ production by PBMC is lower. Increased inflammatory activity is associated with increased bone resorption in adult patients and decreased body mass in paediatric patients. In healthy male subjects there is a proportionate relationship between supplementary intake of EPA and DHA (0.3–2.0 g as fish oil/d) in combination with antioxidants (vitamins A, C and E and Se) and incorporation into plasma phospholipids and PBMC, and a non-linear relationship with PBMC synthesis of TNF-α, IL-6 and prostaglandin E2 (decrease) and IFN-γ (increase). In adults with Crohn's disease high-dose fish oil (2.7 g EPA+DHA/d) in combination with antioxidants (vitamins A, C and E and Se) increases the EPA and DHA content of PBMC and decreases the production of IFN-γ by PBMC, but is not associated with effects on bone turnover or nutritional status.

Keywords

Crohn's diseaseMononuclear cellFish oil and antioxidantsBone turnover
Type
Postgraduate Symposium
Information
Proceedings of the Nutrition Society , Volume 64 , Issue 2 , May 2005 , pp. 183 - 191
Copyright
Copyright © The Nutrition Society 2005

References

Aghdassi, E, Wendland, BE, Steinhart, AH, Wolman, SL, Jeejeebhoy, K & Allard, JP (2003) Antioxidant vitamin supplementation in Crohn's disease decreases oxidative stress. A randomized controlled trial. American Journal of Gastroenterology 98, 348–353.Google Scholar
Andreassen, H, Rungby, J, Dahlerup, JF & Mosekilde, L (1997) Inflammatory bowel disease and osteoporosis. Scandinavian Journal of Gastroenterology 32, 1247–1255.CrossRefGoogle ScholarPubMed
Arron, JR & Choi, Y (2000) Bone versus immune system. Nature 408, 535–536.Google Scholar
Barland, P & Lipstein, E (1996) Selection and use of laboratory tests in the rheumatic diseases. American Journal of Medicine 100 16S – 23SCrossRefGoogle ScholarPubMed
Baumann, H & Gauldie, J (1994) The acute phase response. Immunology Today 15, 74–80.Google Scholar
Beisel, WR (1995) Infection-induced malnutrition – from cholera to cytokines. American Journal of Clinical Nutrition 62, 813–819.CrossRefGoogle ScholarPubMed
Belluzzi, A, Brignola, C, Campieri, M, Pera, A, Boschi, S & Miglioli, M (1996) Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. New England Journal of Medicine 334, 1557–1560.Google Scholar
Bernstein, CN, Sargent, M, Rawsthorne, P & Rector, E (1997) Peripheral blood lymphocyte beta 2 integrin and ICAM expression in inflammatory bowel disease. Digestive Diseases and Sciences 42, 2338–2349.Google Scholar
Best, WR, Becktel, JM, Singleton, JW, Kern, F Jr (1976) Development of a Crohn's disease activity index. National Cooperative Crohn's Disease Study. Gastroenterology 70, 439–444.CrossRefGoogle ScholarPubMed
Bouma, G, Oudkerk, PM, Scharenberg, JG, Kolkman, JJ, Von Blomberg, BM, Scheper, RJ, Meuwissen, SG & Pena, AS (1995) Differences in the intrinsic capacity of peripheral blood mononuclear cells to produce tumor necrosis factor alpha and beta in patients with inflammatory bowel disease and healthy controls. Scandinavian Journal of Gastroenterology 30, 1095–1100.Google Scholar
Bremner, AR & Beattie, RM (2002) Therapy of Crohn's disease in childhood. Expert Opinion in Pharmacotherapy 3, 809–825.Google ScholarPubMed
Brignola, C, Campieri, M, Bazzocchi, G, Farruggia, P, Tragnone, A & Lanfranchi, GA (1986a) A laboratory index for predicting relapse in asymptomatic patients with Crohn's disease. Gastroenterology 91, 1490–1494.CrossRefGoogle ScholarPubMed
Brignola, C, Lanfranchi, GA, Campieri, M, Bazzocchi, G, Devoto, M, Boni, P, Farruggia, P, Veggetti, S & Tragnone, A (1986b) Importance of laboratory parameters in the evaluation of Crohn's disease activity. Journal of Clinical Gastroenterology 8, 245–248.CrossRefGoogle ScholarPubMed
British Nutrition Foundation(1999) n -3 Fatty Acids and Health. London: British Nutrition Foundation.Google Scholar
Buffinton, GD & Doe, WF (1995) Depleted mucosal antioxidant defences in inflammatory bowel disease. Free Radical Biology and Medicine 19, 911–918.CrossRefGoogle ScholarPubMed
Calder, PC (2001) n -3 polyunsaturated fatty acids, inflammation and immunity: pouring oil on troubled waters or another fishy tale? Nutrition Research 21, 309–341.CrossRefGoogle Scholar
Calder, PC (2003) N-3 polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids 38, 343–352.CrossRefGoogle ScholarPubMed
Calder, PC, Yaqoob, P, Thies, F, Wallace, FA & Miles, EA (2002) Fatty acids and lymphocyte functions. British Journal of Nutrition 87, S31–S48 Suppl. 1Google Scholar
Capristo, E, Mingrone, G, Addolorato, G, Greco, AV & Gasbarrini, G (1998) Metabolic features of inflammatory bowel disease in a remission phase of the disease activity. Journal of Internal Medicine 243, 339–347.CrossRefGoogle Scholar
Clowes, JA & Eastell, R (2000) The role of bone turnover markers and risk factors in the assessment of osteoporosis and fracture risk. Bailliere's Best Practice and Research Clinical Endocrinology and Metabolism 14, 213–232.Google Scholar
Colpaert, S, Vastraelen, K, Liu, Z, Maerten, P, Shen, C, Penninckx, F, Geboes, K, Rutgeerts, P & Ceuppens, JL (2002) In vitro analysis of interferon gamma (IFN-gamma) and interleukin-12 (IL-12) production and their effects in ileal Crohn's disease. European Cytokine Network 13, 431–437.Google Scholar
Department of HealthDepartment of Health (1991) Dietary Reference Values for Food Energy and Nutrients for the United Kingdom. Report on Health and Social Subjects no. 41. London: H. M. Stationery Office.Google Scholar
Endres, S, Ghorbani, R, Kelley, VE, Georgilis, K, Lonnemann, G, van der Meer, JW, Cannon, JG, Rogers, TS, Klempner, MS & Weber, PC (1989) The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. New England Journal of Medicine 320, 265–271.CrossRefGoogle ScholarPubMed
Eritsland, J (2000) Safety considerations of polyunsaturated fatty acids. American Journal of Clinical Nutrition 71 197S – 201SGoogle Scholar
Esteve-Comas, M, Nunez, MC, Fernandez-Banares, F, Abad-Lacruz, A, Gil, A, Cabre, E, Gonzalez-Huix, F, Bertran, X & Gassull, MA (1993) Abnormal plasma polyunsaturated fatty acid pattern in non-active inflammatory bowel disease. Gut 34, 1370–1373.Google Scholar
Esteve-Comas, M, Ramirez, M, Fernandez-Banares, F, Abad-Lacruz, A, Gil, A, Cabre, E, Gonzalez-Huix, F, Moreno, J, Humbert, P & Guilera, M (1992) Plasma polyunsaturated fatty acid pattern in active inflammatory bowel disease. Gut 33, 1365–1369.Google Scholar
Foulon, T, Richard, MJ, Payen, N, Bourrain, JL, Beani, JC, Laporte, F & Hadjian, A (1999) Effects of fish oil fatty acids on plasma lipids and lipoproteins and oxidant–antioxidant imbalance in healthy subjects. Scandinavian Journal of Clinical and Laboratory Investigation 59, 239–248.Google ScholarPubMed
Garnero, P (2000) Markers of bone turnover for the prediction of fracture risk. Osteoporosis International 11, S55–S65 Suppl. 6Google Scholar
Geerling, BJ, Badart-Smook, A, Stockbrugger, RW & Brummer, RJ (1998) Comprehensive nutritional status in patients with long-standing Crohn disease currently in remission. American Journal of Clinical Nutrition 67, 919–926.CrossRefGoogle ScholarPubMed
Geerling, BJ, Houwelingen, AC, Badart-Smook, A, Stockbrugger, RW & Brummer, RJ (1999a) Fat intake and fatty acid profile in plasma phospholipids and adipose tissue in patients with Crohn's disease, compared with controls. American Journal of Gastroenterology 94, 410–417.Google Scholar
Geerling, BJ, Houwelingen, AC, Badart-Smook, A, Stockbrugger, RW & Brummer, RJ (1999b) The relation between antioxidant status and alterations in fatty acid profile in patients with Crohn disease and controls. Scandinavian Journal of Gastroenterology 34, 1108–1116.CrossRefGoogle ScholarPubMed
Griffiths, AM, Nguyen, P, Smith, C, MacMillan, JH & Sherman, PM (1993) Growth and clinical course of children with Crohn's disease. Gut 34, 939–943.Google Scholar
Grisham, MB (1994) Oxidants and free radicals in inflammatory bowel disease. Lancet 344, 859–861.Google Scholar
Habtezion, A, Silverberg, MS, Parkes, R, Mikolainis, S & Steinhart, AH (2002) Risk factors for low bone density in Crohn's disease. Inflammatory Bowel Diseases 8, 87–92.CrossRefGoogle ScholarPubMed
Harries, AD & Heatley, RV (1983) Nutritional disturbances in Crohn's disease. Postgraduate Medical Journal 59, 690–697.CrossRefGoogle ScholarPubMed
Horwood, NJ, Kartsogiannis, V, Quinn, JM, Romas, E, Martin, TJ & Gillespie, MT (1999) Activated T lymphocytes support osteoclast formation in vitro. Biochemical and Biophysical Research Communications 265, 144–150.CrossRefGoogle ScholarPubMed
Hyams, JS, Ferry, GD, Mandel, FS, Gryboski, JD, Kibort, PM, Kirschner, BS, Griffiths, AM, Katz, A, Grand, RJ & Boyle, JT (1991) Development and validation of a pediatric Crohn's disease activity index. Journal of Pediatric Gastroenterology and Nutrition 12, 439–447.Google ScholarPubMed
Jordan, KM & Cooper, C (2002) Epidemiology of osteoporosis. Bailliere's Best Practice and Research Clinical Rheumatology 16, 795–806.Google Scholar
Kanof, ME, Lake, AM & Bayless, TM (1988) Decreased height velocity in children and adolescents before the diagnosis of Crohn's disease. Gastroenterology 95, 1523–1527.Google Scholar
Kaptoge, S, Welch, A, McTaggart, A, Mulligan, A, Dalzell, N, Day, NE, Bingham, S, Khaw, KT & Reeve, J (2003) Effects of dietary nutrients and food groups on bone loss from the proximal femur in men and women in the 7th and 8th decades of age. Osteoporosis International 14, 418–428.Google Scholar
Kotake, S, Udagawa, N, Hakoda, M, Mogi, M, Yano, K, Tsuda, E et al. (2001) Activated human T cells directly induce osteoclastogenesis from human monocytes: possible role of T cells in bone destruction in rheumatoid arthritis patients. Arthritis and Rheumatology 44, 1003–1012.3.0.CO;2-#>CrossRefGoogle Scholar
Kuroki, F, Iida, M, Matsumoto, T, Aoyagi, K, Kanamoto, K & Fujishima, M (1997) Serum n-3 polyunsaturated fatty acids are depleted in Crohn's disease. Digestive Diseases and Sciences 42, 1137–1141.CrossRefGoogle Scholar
Kuroki, F, Iida, M, Tominaga, M, Matsumoto, T, Hirakawa, K, Sugiyama, S & Fujishima, M (1993) Multiple vitamin status in Crohn's disease. Correlation with disease activity. Digestive Diseases and Sciences 38, 1614–1618.CrossRefGoogle ScholarPubMed
Lauritsen, K, Laursen, LS, Bukhave, K & Rask-Madsen, J (1988) In vivo profiles of eicosanoids in ulcerative colitis, Crohn's colitis, and Clostridium difficile colitis. Gastroenterology 95, 11–17.CrossRefGoogle ScholarPubMed
Lin, CL, Moniz, C, Chambers, TJ & Chow, JW (1996) Colitis causes bone loss in rats through suppression of bone formation. Gastroenterology 111, 1263–1271.Google Scholar
MacDonald, BR & Gowen, M (1992) Cytokines and bone. British Journal of Rheumatology 31, 149–155.CrossRefGoogle ScholarPubMed
MacDonald, TT, Monteleone, G & Pender, SL (2000) Recent developments in the immunology of inflammatory bowel disease. Scandinavian Journal of Immunology 51, 2–9.Google Scholar
Maggio, D, Barabani, M, Pierandrei, M, Polidori, MC, Catani, M, Mecocci, P, Senin, U, Pacifici, R & Cherubini, A (2003) Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study. Journal of Clinical Endocrinology and Metabolism 88, 1523–1527.Google Scholar
Manolagas, SC & Jilka, RL (1995) Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. New England Journal of Medicine 332, 305–311.Google Scholar
Mazlam, MZ & Hodgson, HJ (1992) Peripheral blood monocyte cytokine production and acute phase response in inflammatory bowel disease. Gut 33, 773–778.Google Scholar
Meydani, SN, Endres, S, Woods, MM, Goldin, BR, Soo, C, Morrill-Labrode, A, Dinarello, CA & Gorbach, SL (1991) Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women. Journal of Nutrition 121, 547–555.CrossRefGoogle Scholar
Mingrone, G, Capristo, E, Greco, AV, Benedetti, G, De Gaetano, A, Tataranni, PA & Gasbarrini, G (1999) Elevated diet-induced thermogenesis and lipid oxidation rate in Crohn disease. American Journal of Clinical Nutrition 69, 325–330.Google Scholar
Miura, M & Hiwatashi, N (1985) Cytokine production in inflammatory bowel disease. Journal of Clinical and Laboratory Immunology 18, 81–86.Google Scholar
Miyamoto, T, Ohneda, O, Arai, F, Iwamoto, K, Okada, S, Takagi, K, Anderson, DM & Suda, T (2001) Bifurcation of osteoclasts and dendritic cells from common progenitors. Blood 98, 2544–2554.Google Scholar
Moshage, H (1997) Cytokines and the hepatic acute phase response. Journal of Pathology 181, 257–266.Google Scholar
Mutchnick, MG, Lee, HH, Hollander, DI, Haynes, GD & Chua, DC (1988) Defective in vitro gamma interferon production and elevated serum immunoreactive thymosin beta 4 levels in patients with inflammatory bowel disease. Clinical Immunology and Immunopathology 47, 84–92.CrossRefGoogle ScholarPubMed
Nakamura, M, Saito, H, Kasanuki, J, Tamura, Y & Yoshida, S (1992) Cytokine production in patients with inflammatory bowel disease. Gut 33, 933–937.Google Scholar
Pallone, F, Fais, S, Squarcia, O, Biancone, L, Pozzilli, P & Boirivant, M (1987) Activation of peripheral blood and intestinal lamina propria lymphocytes in Crohn's disease. In vivo state of activation and in vitro response to stimulation as defined by the expression of early activation antigens. Gut 28, 745–753.Google Scholar
Parhami, F (2003) Possible role of oxidized lipids in osteoporosis: could hyperlipidemia be a risk factor? Prostaglandins Leukotrienes and Essential Fatty Acids 68, 373–378.Google Scholar
Pietschmann, P, Grisar, J, Thien, R, Willheim, M, Kerschan-Schindl, K, Preisinger, E & Peterlik, M (2001) Immune phenotype and intracellular cytokine production of peripheral blood mononuclear cells from postmenopausal patients with osteoporotic fractures. Experimental Gerontology 36, 1749–1759.Google Scholar
Reimund, JM, Allison, AC, Muller, CD, Dumont, S, Kenney, JS, Baumann, R, Duclos, B & Poindron, P (1998) Antioxidants inhibit the in vitro production of inflammatory cytokines in Crohn's disease and ulcerative colitis. European Journal of Clinical Investigation 28, 145–150.CrossRefGoogle ScholarPubMed
Rigaud, D, Angel, LA, Cerf, M, Carduner, MJ, Melchior, JC, Sautier, C, Rene, E, Apfelbaum, M & Mignon, M (1994) Mechanisms of decreased food intake during weight loss in adult Crohn's disease patients without obvious malabsorption. American Journal of Clinical Nutrition 60, 775–781.CrossRefGoogle ScholarPubMed
Ringstad, J, Kildebo, S & Thomassen, Y (1993) Serum selenium, copper, and zinc concentrations in Crohn's disease and ulcerative colitis. Scandinavian Journal of Gastroenterology 28, 605–608.Google Scholar
Robinson, RJ, Iqbal, SJ, Abrams, K, Al Azzawi, F, Mayberry, JF (1998) Increased bone resorption in patients with Crohn's disease. Alimentary Pharmacology and Therapeutics 12, 699–705.Google Scholar
Roux, S & Orcel, P (2000) Bone loss. Factors that regulate osteoclast differentiation: an update. Arthritis Research 2, 451–456.Google Scholar
Sanderson, P, Finnegan, YE, Williams, CM, Calder, PC, Burdge, GC, Wootton, SA, Griffin, BA, Joe, MD, Pegge, NC & Bemelmans, WJ (2002) UK Food Standards Agency Alpha-linolenic Acid Workshop Report. British Journal of Nutrition 88, 573–579.Google Scholar
Sasaki, T, Hiwatashi, N, Yamazaki, H, Noguchi, M & Toyota, T (1992) The role of interferon gamma in the pathogenesis of Crohn's disease. Gastroenterology Japan 27, 29–36.CrossRefGoogle ScholarPubMed
Savage, MO, Beattie, RM, Camacho-Hubner, C, Walker-Smith, JA & Sanderson, IR (1999) Growth in Crohn's disease. Acta Paediatrica 88, 89–92 Suppl.Google Scholar
Schoon, EJ, Geerling, BG, Van Dooren, IM, Schurgers, LJ, Vermeer, C, Brummer, RJ & Stockbrugger, RW (2001) Abnormal bone turnover in long-standing Crohn's disease in remission. Alimentary Pharmacology and Therapeutics 15, 783–792.Google Scholar
Schreiber, S, Nikolaus, S, Hampe, J, Hamling, J, Koop, I, Groessner, B, Lochs, H & Raedler, A (1999) Tumour necrosis factor alpha and interleukin 1beta in relapse of Crohn's disease. Lancet 353, 459–461.CrossRefGoogle ScholarPubMed
Simmonds, NJ & Rampton, DS (1993) Inflammatory bowel disease – a radical view. Gut 34, 865–868.Google Scholar
Starnes, HF Jr, Warren, RS, Jeevanandam, M, Gabrilove, JL, Larchian, W, Oettgen, HF, Brennan, MF (1988) Tumor necrosis factor and the acute metabolic response to tissue injury in man. Journal of Clinical Investigation 82, 1321–1325.Google Scholar
Stepan, JJ (2000) Prediction of bone loss in postmenopausal women. Osteoporosis International 11, S45–S54 Suppl. 6.Google Scholar
Takayanagi, H, Kim, S & Taniguchi, T (2002) Signaling crosstalk between RANKL and interferons in osteoclast differentiation. Arthritis Research 4, S227–S232 Suppl. 3.Google Scholar
Trebble, T, Arden, NK, Stroud, MA, Wootton, SA, Burdge, GC, Miles, EA, Ballinger, AB, Thompson, RL & Calder, PC (2003a) Inhibition of tumour necrosis factor-α and interleukin-6 production by mononuclear cells following dietary fish oil supplementation in healthy men and response to antioxidant co-supplementation. British Journal of Nutrition 90, 405–412.Google Scholar
Trebble, TM, Arden, NK, Wootton, SA, Calder, PC, Mullee, MA, Fine, DR & Stroud, MA (2004a) Fish oil and antioxidants alter composition and function of circulating mononuclear cells in Crohn's disease. American Journal of Clinical Nutrition 80, 1137–1144.Google Scholar
Trebble, TM, Arden, NK, Wootton, SA, Mullee, MA, Calder, PC, Burdge, GC, Fine, DR & Stroud, MA (2004b) Peripheral blood mononuclear cell fatty acid composition and inflammatory mediator production in adult Crohn's disease. Clinical Nutrition 23, 647–655.CrossRefGoogle ScholarPubMed
Trebble, TM, Wootton, SA, May, A, Erlewyn-Lajeunesse, MD, Chakraborty, A, Mullee, MA, Stroud, MA & Beattie, RM (2003b) Essential fatty acid status in paediatric Crohn's disease: relationship with disease activity and nutritional status. Alimentary Pharmacology and Therapeutics 18, 433–442.Google Scholar
Trebble, TM, Wootton, SA, Miles, EA, Mullee, M, Arden, NK, Ballinger, AB, Stroud, MA, Burdge, GC & Calder, PC (2003c) Prostaglandin E2 production and T cell function after fish-oil supplementation: response to antioxidant cosupplementation. American Journal of Clinical Nutrition 78, 376–382.Google Scholar
Trebble, TM, Wootton, SA, Stroud, MA, Mullee, MA, Calder, PC, Fine, DR, Moniz, C & Arden, NK (2004c) Laboratory markers predict bone loss in Crohn's disease: relationship to blood mononuclear cell function and nutritional status. Alimentary Pharmacology and Therapeutics 19, 1063–1071.Google Scholar
Warren, RS, Starnes, HF Jr, Gabrilove, JL, Oettgen, HF & Brennan, MF (1987) The acute metabolic effects of tumor necrosis factor administration in humans. Archives of Surgery 122, 1396–1400.Google Scholar
Wigmore, SJ, Fearon, KC, Maingay, JP, Garden, OJ & Ross, JA (2002) Effect of interleukin-2 on peripheral blood mononuclear cell cytokine production and the hepatic acute phase protein response. Clinical Immunology 104, 174–182.Google Scholar
Wigmore, SJ, Maingay, JP, Fearon, KC, O'Riordain, MG & Ross, JA (1998) Effect of interleukin-4 on pro-inflammatory cytokine production and the acute phase response in healthy individuals and in patients with cancer or multiple organ failure. Clinical Science 95, 347–354.Google Scholar
Zifroni, A, Treves, AJ, Sachar, DB & Rachmilewitz, D (1983) Prostanoid synthesis by cultured intestinal epithelial and mononuclear cells in inflammatory bowel disease. Gut 24, 659–664.Google Scholar