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Soluble Transferrin Receptor Level a New Marker of Iron Deficiency Anemia, a Common Manifestation of Gastric Autoimmunity in Type 1 Diabetes

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Soluble Transferrin Receptor Level a New Marker of Iron Deficiency Anemia, a Common Manifestation of Gastric Autoimmunity in Type 1 Diabetes Pathophysiology/Complications ORIGINAL ARTICLE Soluble Transferrin Receptor Level A new marker of iron deficiency anemia, a common manifestation of gastric autoimmunity in type 1 diabetes CHRISTOPHE E.M. DE BLOCK, MD MANOU MARTIN, PHD autoimmune gastritis (8–12). On the other CHRISTEL M. VAN CAMPENHOUT, PHD VIVIANE VAN HOOF, MD, PHD hand, iron deficiency anemia can also arise IVO H. DE LEEUW, MD, PHD LUC F. V AN GAAL, MD, PHD by malignant or inflammatory diseases, BEGOÑA MANUEL Y KEENOY, MD, PHD especially from the gastrointestinal tract (13,14), and atrophic gastritis predisposes patients to gastric carcinoma and carcinoid tumors (15,16). Iron plays an essential role in hemoglo- OBJECTIVE — A total of 15–20% of type 1 diabetic patients have parietal cell antibodies ϩ bin synthesis, electron transport for cellular (PCAs). PCA subjects are at increased risk for iron deficiency anemia and atrophic gastritis. respiration, DNA synthesis, and other vital Recently, soluble transferrin receptor (sTfR) levels have proven to be a sensitive indicator for iron deficiency. They are, in contrast with ferritin levels, independent of inflammation, liver and enzymatic reactions (13). Early detection hormonal status, and sex. We are the first to evaluate sTfR levels in type 1 diabetes and tested and treatment of iron deficiency and the the hypothesis of higher sTfR levels in patients with PCAs and/or autoimmune gastritis. conditions that are at its origin could signifi- cantly reduce morbidity. Recently, soluble RESEARCH DESIGN AND METHODS — We examined 148 type 1 diabetic patients transferrin receptor (sTfR) levels have been (85 men and 63 women; 50 were PCAϩ) and 59 sex- and age-matched control subjects (30 men shown to be a sensitive and highly quanti- and 29 women). The main outcome measures were sTfR levels, iron deficiency anemia, and tative indicator of early iron deficiency atrophic gastritis. Logistical regression analysis tested risk factors for iron deficiency. (17–19). Moreover, sTfR levels discriminate Ͻ Ͻ between iron deficiency anemia and anemia RESULTS — Iron deficiency was present in 38 subjects. Iron (P 0.0001) and ferritin (P of chronic disease (20,21). However, the 0.0001) levels but not sTfR levels were lower in women. sTfR levels were similar in diabetic and control subjects but were higher in PCAϩ subjects (P = 0.015). In diabetic subjects, iron use of sTfR levels to detect iron deficiency in deficiency anemia was more prevalent in PCAϩ than in PCA– patients (odds ratio 3.07, P = type 1 diabetic patients has never been 0.013) and was associated with sex (P = 0.0001), age (P = 0.046), and sTfR (P = 0.0008) lev- studied. To our knowledge, this is the first els. Atrophic gastritis was present in 15 of 28 PCAϩ and in 1 of 11 PCA– diabetic subjects (P study to evaluate whether sTfR levels are ϩ = 0.014). sTfR levels tended to be higher in patients with atrophic gastritis (P = 0.062). higher in PCA subjects or in type 1 dia- betic patients with atrophic gastritis. CONCLUSIONS — In type 1 diabetes, sTfR levels can be used to diagnose iron deficiency anemia, which is more prevalent in PCAϩ subjects. sTfR levels are higher in PCAϩ individu- als who are at risk for developing atrophic gastritis. RESEARCH DESIGN AND METHODS Diabetes Care 23:1384–1388, 2000 Patients Of a group of 497 type 1 diabetic patients attending the outpatient diabetes clinic of ype 1 diabetes results from autoim- sion can lead to atrophic gastritis (5,6). the University Hospital Antwerp, 148 mune destruction of pancreatic ␤- Moreover, PCAs target the gastric proton patients (85 men and 63 women) were cells (1). In addition, we and others pump (7), which results in decreased gas- T selected on the basis of their PCA status. A (2–4) have found that 15–20% of these tric acid secretion and decreased iron ϩ total of 50 PCA and 98 PCA– patients with patients have parietal cell antibodies absorption. This may cause iron deficiency a mean age of 40 ± 12 years, a mean dura- (PCAs), which are cytotoxic to the gastric anemia, which is a common (although fre- tion of disease of 17 ± 10 years, and a mucosa. This chronic autoimmune aggres- quently overlooked) manifestation of mean HbA1c level of 7.9 ± 1.1% were stud- ied. The diabetic patients were matched for sex and all aforementioned parameters. The From the Departments of Endocrinology-Diabetology (C.E.M.D.B., I.H.D.L., B.M.K., L.F.V.G.), Immunology nondiabetic control group consisted of 59 (C.M.V.C.), Nuclear Medicine (M.M.), and Biochemistry (V.V.H.), Faculty of Medicine, University of Antwerp, sex- and age-matched healthy individuals University Hospital Antwerp, Edegem, Belgium. (30 men and 29 women), of whom 7 sub- Address correspondence and reprint requests to Christophe E.M. De Block, MD, Department of ϩ Endocrinology-Diabetology, Faculty of Medicine, University of Antwerp, University Hospital Antwerp, jects were PCA (Table 1). Wilrijkstraat 10, B-2650 Edegem, Belgium. E-mail: [email protected]. Individuals with decreased serum vita- Received for publication 2 March 2000 and accepted in revised form 30 May 2000. min B12 concentrations, positive anti-intrin- Abbreviations: ANOVA, analysis of variance; AUCROC, area under the curve for receiver operating char- sic factor, and/or pernicious anemia were acteristics; CV, coefficient of variation; Nl, normal range; PCA, parietal cell antibody; sTfR, soluble transfer- rin receptor. excluded because, in inefficient erythro- A table elsewhere in this issue shows conventional and Système International (SI) units and conversion poiesis, sTfR levels may be elevated in the factors for many substances. absence of functional iron depletion (22). 1384 DIABETES CARE, VOLUME 23, NUMBER 9, SEPTEMBER 2000 De Block and Associates Table 1—Comparison of iron status between diabetic and control subjects Total Diabetic men Diabetic women Control men Control women P (ANOVA) n 207 85 63 30 29 — Age (years) 40 ± 12 41 ± 14 37 ± 10 41 ± 10 44 ± 13 NS (P = 0.06) Iron (µg/dl) 84 ± 41 98 ± 38 71 ± 39 92 ± 40 60 ± 26 Ͻ0.0001* Transferrin saturation (%) 33 ± 15 37 ± 15 28 ± 15 37 ± 13 29 ± 11 0.0001* Ferritin (µg/l) 78 ± 76 95 ± 81 46 ± 54 124 ± 84 48 ± 52 Ͻ0.0001* Transferrin (mg/dl) 247 ± 43 227 ± 35 254 ± 44 256 ± 31 281 ± 45 Ͻ0.0001*† sTfR (mg/l) 1.19 ± 0.32 1.17 ± 0.30 1.24 ± 0.37 1.11 ± 0.21 1.24 ± 0.36 NS (P = 0.24) sTfR/ferritin ratio 47.6 ± 90.7 21.1 ± 19.2 79.2 ± 115.3 17.1 ± 25.5 88.1 ± 148.9 Ͻ0.0001* PCAϩ (≥1/20) 57 (27.35) 23 (27.6) 27 (42.9) 4 (13.3) 3 (10.3) NS Iron deficiency‡ 38 (18.4) 8 (9.4) 19 (30.2) 5 (16.7) 6 (20.7) 0.004* Data are means ± SD or n (%). Two-way ANOVA was performed between the groups with sex and health status as fixed factors. *Statistical significance reached accord- ing to sex; †statistical significance reached according to health status; ‡iron deficiency as defined in RESEARCH DESIGN AND METHODS. Subjects with other causes of iron malab- Ͻ13 and women Ͻ12 g/dl) and microcytic The study was approved by the Ethical sorption such as anti-endomysium antibod- (mean corpuscular volume Ͻ76 fl) and Committee of the University Hospital ies and/or celiac disease were excluded (12). hypochromic indexes (mean corpuscular Antwerp. Informed consent was obtained Other exclusion criteria were reticulocytosis, hemoglobin Ͻ27 pg) accompanied by at from each person in accordance with the abnormal differential blood count, increased least 1 of the following laboratory values for Helsinki Declaration. erythrocyte sedimentation rate or C-reac- iron deficiency: a decreased serum iron level tive protein, increased serum creatinine lev- (men Ͻ50 and women Ͻ40 µg/dl), a trans- Statistical analysis els, abnormal urine sediment, abnormal ferrin saturation Յ20% (Nl 20–60%), or a All data for this cross-sectional study were liver function tests, and chronic gynecolog- decreased serum ferritin concentration analyzed using the statistical package SPSS ical blood loss. Most women, if not already (men Ͻ20 µg/dl and women Ͻ12 µg/l). Version 8.0 (SPSS, Chicago). The unpaired postmenopausal, were taking contraceptive Normal ranges, coefficients of variation t test or analysis of variance (ANOVA) with drugs. In all patients, fecal occult blood test- (CVs), and sensitivities were as follows: serum Tukey’s test as post hoc analysis was used ing was repeatedly negative. None of the iron (men 50–200 and women 40–180 µg/dl, for comparison of means. The ␹2 test or subjects was vegetarian, and none used anti- CV Ͻ3%, sensitivity 1 µg/dl), transferrin Fisher’s exact test was performed to test fre- inflammatory drugs, acid suppression ther- (men 210–340 and women 200–310 mg/dl, quency distributions. Pearson’s correlation apy, or folic acid, vitamin B12, or vitamin C CV 2.8%, sensitivity 8.4 mg/dl), ferritin (men was used where indicated. Stepwise for- supplements. All patients were euthyroid. 20–450 and women 12–250 µg/l, CV 1.5%, ward multiple logistical regression analysis sensitivity 0.48 µg/l), hemoglobin (men was used to assess the strength and inde- Study design 13–17 and women 12–16 g/dl, CV 1.2%, pendence of associations and to describe a HbA1c levels were determined by high-per- sensitivity 0.5 g/dl), and gastrin (men and predictive model. All tests were 2-tailed. A formance liquid chromatography (Variant women Ͻ110 pg/ml, CV 9.3%, sensitivity P value Յ0.05 was considered significant. Hemoglobin A1c Reorder Pack; Bio-Rad, 1.1 pg/ml).
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