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Arthritis and Other Chronic Inflammatory Diseases

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Arthritis and Other Chronic Inflammatory Diseases J. Clip. Biochem. Nutr., 20, 1-26, 1996 Review Diet and Nutrition in Rheumatoid Arthritis and Other Chronic Inflammatory Diseases Ann L. PARKE,1 Dennis V. PARKE ,2,* and Francis Avery JONES2 1 Division of Rheumatology, Department of Medicine, University of Connecticut School of Medicine, Farmington, CT, U.S.A. 2School of Biological Sciences, University of Surrey, Guildford, Surrey, GU2 5XH, U.K. (Received October 25, 1995) Summary A greater understanding of the etiology of rheumatoid and other inflammatory diseases, their association with reactive oxygen species (ROS), and the role of environmental chemicals as antigens , has opened the way to new approaches in disease prevention and treatment by dietary modulation. Normal protection against the inflammatory effects of ROS (antioxidant defense) and environmental chemicals (detox- ication) requires constant dietary replenishment to provide the redox buffer, glutathione (GSH), the antioxidant vitamins, E, C, and A, and other essential components such as selenium for the GSH peroxidase enzymes. Fasting and some environmental chemicals (haloalkanes) induce the ROS-generating enzyme cytochrome P4502E, as also does inorganic iron; and the various dietary lipids provide prostanoids of different inflammatory potentials. Adequate calories (NADPH) are essen- tial for maintaining the two defense systems, but caloric excess may lead to changes in membrane composition, electron leakage, ROS generation , and exacerbation of the inflammatory condition. Key Words. rheumatoid arthritis, inflammatory disease , food, antiox- idants, reactive oxygen Rheumatoid arthritis (RA) and chronic inflammatory disease have long been associated with food and nutrition, both in disease causation and in treatment [1, 2]; and because of the known relationships between polyunsaturated fatty acids * To whom correspondence should be addressed . 1 2 AL. PARKE, D.V. PARKE, and F.A, JONES (PUFAs), prostanoids, cytokines, and inflammation [3, 4] there appeared to be some scientific rationale for this. Lay advocates of dietary treatment considered that "rheumatic diseases are caused by chemical poisoning from the additives put into our food" [5, 6], and prescribed a diet low in red meat, saturated fat, alcohol, food additives, and preservatives, but rich in seafood, vegetables , and rice-the Dong diet. However, in 1981, an Arthritis Foundation pamphlet advised RA patients that "no food has anything to do with causing arthritis and no food is effective in treating or curing it" [7] ; and later a 10-week scientific study of 25 RA subjects fed the popular Dong diet found only limited benefit among a small sub- group of patients [8]. Obviously, with so many dietary variants studied simultane- ously in the treatment of a multifactorial disease, one would expect an equivocal, largely negative response; and against a previous background of lay enthusiasm it would be wrong to summarily dismiss a possible association of RA with diet on the strength of a single study of some 25 patients. The difficulties in conducting such studies were further considered by Ziff, who advocated that the choice of diet for future investigations "should be based on a concept that links intermediary metabolism with immunity and chronic inflammation" [9]. Recent advances in our understanding of the molecular pathology of RA and autoimmunity [10-12] and of the role of oxygen radicals (reactive oxygen species, ROS) in the manifestation of inflammatory disease [13, 14], together with recent views on the role of nutrition in biological defense against ROS and toxic chemicals [15, 16], have brought into sharp focus the possible role of nutrition in the prevention and treatment of inflammatory disease. Hence, the objective of this paper is to review these recent developments, and to identify any association of food and nutrition with intermediary metabolism and chronic inflammation that might lead to the prevention and/or exacerbation of RA and other chronic inflammatory disease states. MOLECULAR PATHOLOGY OF CHRONIC INFLAMMATORY DISEASE The various manifestations of chronic inflammatory disease, e.g., RA, systemic lupus erythematosus (SLE), and inflammatory bowel disease (IBD), all involve ROS-mediated tissue damage [11, 13, 14]. It is uncertain whether ROS are the cause or effect, or both [17], but oxidative stress resulting in tissue injury is due to excess ROS production and/or defective biological antioxidant/detoxication defense systems. Oxygen radicals are produced by various mechanisms including: (i) the simple interaction of water, molecular 02, and inorganic iron; (ii) activation of leucocytes by cytokines; (iii) induction of cytochrome P4502E; (iv) prostanoid biosynthesis in the cyclooxygenase and lipoxygenase pathways [18]; (v) futile cycling of microsomal cytochromes P450 (CYP); (vi) redox cycling of quinone drug metabolites; (vii) xanthine oxidase functioning as an oxygenase; and (viii) electron leakage from mitochondrial and microsomal membranes; and although the first two mechanisms are probably the major ones involved in chronic J. Clin. Biochem. Nutr. DIET AND NUTRITION IN RHEUMATOID ARTHRITIS 3 inflammatory disease, the other sources of ROS are also likely to contribute [11]. Iron This plays a major role in the pathology of RA and chronic inflammatory disease [11], since iron mobilized from ferritin or microsomal iron protein [19] effects the following: (i) the formation of highly toxic hydroxyl radicals (' OH) from the superoxide anion (O2-.) and peroxide; (ii) the production of ROS directly from 02 and water; (iii) membrane lipid peroxidation [16]; and (iv) chemotaxis for neutrophils (PMN) [20], which then generate ROS, thus perpetuating inflam- matory tissue damage [21] (Fig. 1). RA patients with chronic anemia have high plasma ferritin levels, and low plasma B12 and folate levels [22], as would be expected from a high turnover of erythrocytes, hemoglobin, and other heme proteins resulting from lipid peroxidation. Further evidence of the critical role of iron in RA is that oral administration of iron produces a flare of rheumatoid synovitis [21], infusion of iron dextran promotes synovitis in previously inflamed joints [23], and the ferritin content of synovial fluid of RA patients is some 10- fold greater than that of healthy controls or osteoarthritic patients [24] . From the observations, Blake has proposed that in RA, inflamed joints result from iron- mediated generation of ROS, arising from intermittent intra-articular microhem- orrhage and hypoxic reperfusion injury [21]. Excessive absorption of dietary iron is normally prevented by its binding to gastrointestinal mucus [25] , but absorp- tion of aluminum increases iron-mediated lipid peroxidation [26] possibly by displacing iron from natural silicic acid complexes in the body [27]. Silicic acid, present in cereals, is considered to be an essential nutrient for some species and protects against aluminum toxicity; deficiency may result in changes in col- lagenous connective tissue, and in osteomalacia, anemia, and dementia [27] . Fig. 1. Iron toxicity. •0H, Hydroxyl radical; OZ'-, superoxy anion; PMN , polymorphonu- clear leucocytes. Vol. 20, No. 1, 1996 4 AL. PARKE, D.V. PARKE, and F.A. JONES Table 1. Some of the families of the cytochromes P450. TCDD, 2,3,7,8-Tetrachlorodibenzo-p-dioxin; PAH, polycylic aromatic hydrocarbons; EETEs, epoxyeicosatetraenoic acids; HETEs, hydroxyeicosatetraenoic acids . Cytochrome P4502E1 (CYP2E) In recent studies into the molecular pathology of ROS-mediated tissue dam- age, surgical trauma, and multiple system organ failure, we identified a role for CYP-mediated ROS production. CYP2E, a unique member of the GYP super- family, is a potent generator of ROS, and is activated by fasting (acetone), ethanol, ether, certain halogenated anesthetics and solvents, and many other low molecular weight chemicals (Table 1). Exposure of experimental animals to fasting and ether/halothane anesthesia resulted in extensive lipid peroxidation in liver and kidney, with loss of other isoforms of GYP [28, 29]. Furthermore, in a hepatic ischemia-reperfusion model for hemorrhage and hypovolemic shock, the initial phase of xanthine oxidase-mediated ROS production was followed by PMN infiltration and a second greater burst of ROS production, mediated by PMN leucocytes [30], PMNs also infiltrated the lungs although reperfusion was limited to the liver, indicating that iron, cytokines or prostanoids produced by inflammation in one organ or tissue can mediate leucotaxis in another tissue [30]. Food as a cause of chronic inflammatory disease Sensitivity to particular foods has long been considered to be a possible cause of RA and other chronic inflammatory disease, but there is little evidence to support this. In only a small percentage (less than 5%) of patients with RA can this disease be attributed to "allergy" to food [2]. A few RA patients have im- munological hypersensitivity to milk and dairy products [2], and in some rheumatoid patients, exclusion of dairy products from the diet has been associated with a clinical improvement in inflammatory synovitis [31]. Food antigens are J. Clin. Biochem. Nutr. DIET AND NUTRITION IN RHEUMATOID ARTHRITIS 5 predominantly proteins, but lipids and food additives (sulphites, tartrazine, monosodium glutamate) may also precipitate food hypersensitivity [32] . The gastrointestinal barrier is permeable, and food proteins may cross this and circu- late as antigens or as immune complexes. All subjects may absorb food antigens from the
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