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Reduction in Serum Leptin and IGF-1 but Preserved T-Lymphocyte Numbers and Activation After a Ketogenic Diet in Rheumatoid Arthritis Patients

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Reduction in Serum Leptin and IGF-1 but Preserved T-Lymphocyte Numbers and Activation After a Ketogenic Diet in Rheumatoid Arthritis Patients Reduction in serum leptin and IGF-1 but preserved T-lymphocyte numbers and activation after a ketogenic diet in rheumatoid arthritis patients D.A. Fraser1,4, J. Thoen1, S. Bondhus1, M. Haugen1, J.E. Reseland2, O. Djøseland3, Ø. Førre1, J. Kjeldsen-Kragh4 1Centre for Rheumatic Diseases, The National Hospital; 2Institute for Nutrition Research, University of Oslo; 3Department of Endocrinology, The National Hospital; 4Department of Immunology and Transfusion Medicine, Ullevaal University Hospital, Oslo, Norway. Abstract Objective To assess the clinical, immunological and hormonal effects of carbohydrate restriction in rheumatoid arthritis (RA) patients via the provision of a ketogenic diet. Methods Thirteen RA patients with active disease consumed a ketogenic diet for 7 days, providing the estimated require- ments for energy and protein whilst restricting their carbohydrate intake to < 40 g/day. This was followed by a 2- week re-feeding period. Clinical and laboratory evaluations were carried out on days 0, 7 and 21. Changes in serum glucose, -hydroxybutyrate ( -HB), leptin, insulin-like growth factor-1 (IGF-1) and cortisol were also measured at these time points. To study CD4+ and CD8+ lymphocyte responses, mitogen stimulated T-cell activation was assessed in heparinised whole blood via flow-cytometric analysis of CD69 expression. Results After the 7-day ketogenic diet, there were significant increases in serum -HB and cortisol, and significant decreases in body weight, the total lymphocyte count, serum leptin, IGF-1 and glucose. However, with the exception of morning stiffness, there were no significant changes in any of the clinical or laboratory measures of disease activity, or in early T-lymphocyte activation and the absolute numbers of CD4+ and CD8+ cells. Conclusion In RA patients several of the metabolic and hormonal responses to a ketogenic diet, such as a fall in serum IGF-1 and leptin, resemble those which occur in response to acute starvation. However, the clinical and immunological changes which occur in response to acute starvation do not take place with a ketogenic diet and thus may be dependent upon energy and/or protein restriction. Key words Rheumatoid arthritis, ketogenic diet, leptin, IGF-1, fasting, immune. Clinical and Experimental Rheumatology 2000; 18: 209-214. Ketogenic diet and rheumatoid arthritis / D.A. Fraser et al. David A. Fraser, MSc; Jørn Thoen, MD, Introduction levels, suggesting that the reduced im- PhD; Sissel Bondhus, BSc; Margaretha Beneficial effects of acute starvation mune function associated with starvation Haugen, PhD; Janne E. Reseland, PhD; upon both clinical and laboratory vari- may be leptin-mediated (18). We found Ole Djøseland, PhD; Øystein Førre, MD, ables reflecting disease activity in rheu- that serum leptin concentrations were PhD; Jens Kjeldsen-Kragh, MD, PhD. matoid arthritis (RA) have been docu- reduced by 67% after fasting in RA pa- Please address correspondence and reprint mented (1-3). We have recently shown tients (4). As leptin enhances both naive requests to: David A. Fraser, Department in RA patients that a 7-day fast, in addi- CD4+ lymphocyte proliferative respon- of Immunology and Transfusion Medicine, tion to causing significant decreases in ses and Th1 cytokine production (18), a Ullevaal University Hospital, N-0407, Oslo, Norway. ESR, CRP, the tender joint count and fall in serum leptin might explain both E-mail: [email protected] morning stiffness, also decreases CD4+ the increase in IL-4 production and the lymphocyte activation and numbers decrease in CD4+ T-cell activation pro- © Copyright CLINICAL AND whilst increasing IL-4 production from duction in mitogen stimulated peripheral EXPERIMENTAL RHEUMATOLOGY 2000. peripheral blood cells (4). Fasting has blood cells we recently observed (4). also been shown to decrease mitogen- We speculated that the immunosuppres- and antigen-induced lymphocyte prolif- sive and clinical effects of acute starva- erative responses (5) and to suppress tion in RA patients might be dependent interleukin-2 production in healthy sub- upon hormonal adaptations to dietary jects (6). carbohydrate restriction rather than upon Although it is well established that chro- energy and/or protein deprivation. We nic sub-optimal protein and calorie in- have therefore assessed the effects of a takes have a negative effect upon cell- 7-day ketogenic diet (2000-2500 kcal/ mediated immune function (7, 8), the day primarily as lipids, 0.8 g protein/kg mechanisms underlying immunological body weight/day, < 40 g carbohydrate/ changes associated with acute starvation day) upon laboratory and clinical indi- in both healthy subjects and RA patients ces of disease activity in a group of 13 are unclear. The lack of any clinical or RA patients. We simultaneously assessed laboratory effects of an elemental diet changes in T-cell number and function does not support the idea that the avoid- along with serum glucose, leptin, IGF- ance of specific food items is responsi- 1, b-hydroxybutyrate (b-HB) and corti- ble for the clinical effects of fasting in sol levels. RA patients (9, 10). Interestingly, it is known that carbohy- Patients and methods drate restriction mediates many of the Patients metabolic and hormonal responses to Thirteen RA patients attending the out- fasting (11, 12). Thus, the substitution of patient department at the Centre for dietary carbohydrates with lipids results Rheumatic Diseases, The National Hos- in similar decreases in blood glucose and pital, who satisfied the American Col- insulin and increases in free fatty acids, lege of Rheumatology criteria for RA ketone bodies and whole body lipolysis (19) were recruited. All had active dis- as would be observed during total fast- ease, as defined by the presence of 3 of ing. Other hormonal adaptations to car- the 4 following criteria; more than 3 bohydrate restriction may have impor- swollen joints (28-joint score), more than tant immunomodulatory effects. For ex- 6 tender joints (28-joint score), duration ample cortisol, which has well estab- of morning stiffness > 45 mins, erythro- lished anti-inflammatory effects, plays cyte sedimentation rate (ESR) > 28 mm a counter-regulatory role in response to in the 1st hour. All patients had radio- hypoglycaemia (13) and is increased by logical erosions of grade 3 or less, a body an isoenergetic carbohydrate restricted mass index (BMI) between 22 kg/m2 and diet (14). 28 kg/m2 and had not previously partici- A reduction in blood glucose concentra- pated in any dietary regime incorporat- tions may also mediate acute changes in ing fasting, and were not on any self- or serum concentrations of leptin, the pro- medically-prescribed diets which could tein product of the ob gene (15-17). Re- influence the results. Patients with other cently it has been shown that the immu- serious medical conditions were not in- nosuppressive effects of acute starvation cluded in the trial. There were 12 women in mice can be abolished by preventing and 1 man, with a median age of 37 years the fasting-induced fall in plasma leptin (range 25-69 years) and a median dis- 210 Hypothalamus-pituitary-adrenocortical and -gonadal axis in RA / M. CutoloKetogenic diet and rheumatoid arthritis / D.A.EDITORIAL Fraser et al. ease duration of 4 years (range 0.2 - 20 instructed to consume a normal break- temperature the erythrocytes were lysed years). Twelve patients were in func- fast before the evaluation. Two further by a Multi-Q-Prep (Coulter, Hialeah, FL, tional class II and 1 was in functional clinical examinations were carried out on USA). The samples were then analysed class III (20). Eleven patients were rheu- the last morning of the diet (day 7) and by a FACScan or FACSCalibur (Becton matoid factor positive (IgM). Four pa- 2 weeks later on the completion of the Dickinson) flow cytometer. tients were taking second-line drugs, 4 re-feeding period (day 21). The follow- The lymphocytes were identified on the were taking corticosteroids, 3 were tak- ing clinical variables were measured at forward light scatter versus side light ing cytostatic drugs, 13 were taking baseline, on day 7 and on day 21 by the scatter plot. The percentage of CD69- NSAIDS and 4 were taking painkillers. same examining physician: body weight, positive cells was obtained by subtract- The corticosteroid dosage did not exceed morning stiffness (min), the number of ing the percentage of positive events in 5 mg/day and this dose was stable for at tender joints (28 joint score), and the the isotype control sample from the per- least 4 weeks before study entry and number of swollen joints (28 joint score). centage of positive events in the anti- during the trial. Patients using slow-act- At baseline, on day 7 and on day 21 pe- CD69 antibody-stained sample. Lym- ing anti-rheumatic or cytostatic drugs ripheral blood samples were taken by phocyte subset numbers were quantified were on a stable dosage for at least 3 venipuncture between 9:00 and 10:00 using FlowCount fluorospheres (Coul- months prior to study entry. The dosage am. The ESR, CRP, platelet count and ter) by adding a known amount of fluor- of NSAIDs was stable for 2 weeks prior differential white blood cell count ospheres to each tube immediately prior to inclusion. Patients were instructed to (WBC) were measured immediately at to sample analysis on the flow cytom- maintain a stable dosage of their current the Department of Clinical Chemistry, eter. The fluorospheres were gated on the drugs and no changes in drug type were National Hospital, Oslo. Samples of FL1 and FL2 channels and their num- permitted during the trial. heparinised blood (preservative-free so- bers obtained, and the numbers of CD4+ dium heparin 150 U.S.P. units) were also and CD8+ lymphocytes were similarly Study design collected at all time points for analysis gated and counted on the FL1 and FL3 The study was approved by the regional of lymphocyte activation.
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