Nutritional status of newly diagnosed celiac disease patients before and after the institution of a celiac disease diet-association with the ...
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Nutritional status of newly diagnosed celiac disease patients before and after the institution of a celiac disease diet— association with the grade of mucosal villous atrophy1–3 Tarja A Kemppainen, Veli-Matti Kosma, Esko K Janatuinen, Risto J Julkunen, Pekka H Pikkarainen, and Matti I Uusitupa ABSTRACT No systematic studies have been carried out on SUBJECTS AND METHODS the association of nutritional status with the severity of mucosal villous atrophy in newly diagnosed celiac disease patients. We Patients examined the nutritional status of 40 adult patients with newly All newly diagnosed celiac disease patients from Kuopio Uni- diagnosed celiac disease classified according to the grade of vil- versity Hospital were recruited for an intervention study (6, 12) lous atrophy: partial, subtotal, and total. Nutritional status was from November 1988 to December 1990. The study population determined by food records as well as by anthropometric and bio- consisted of 40 newly diagnosed celiac disease patients chemical measurements. Anthropometric results did not differ (Table 1). They had suffered from abdominal symptoms for among the three atrophy groups, but serum ferritin and erythrocyte 1–57 y, but the diagnosis of celiac disease was made at the out- folate were lower in patients with total villous atrophy than in the set of the study. The diagnosis was based on the presence of par- other groups. Most of the abnormal biochemical values were nor- tial, subtotal, or total villous atrophy of the duodenal mucosa malized during 1 y of a gluten-free diet; villous atrophy healed before the introduction of a gluten-free diet (13). One newly concomitantly. To conclude, patients with total mucosal villous diagnosed celiac disease patient was excluded from the analysis atrophy at diagnosis had low erythrocyte folate and serum ferritin of dietary intakes because of incomplete food records. The values, but no other major differences were found in nutritional patients were also participants of a randomized trial examining status among celiac disease patients with different grades of vil- the use of oats as part of a celiac disease diet (12). The study was lous atrophy. Am J Clin Nutr 1998;67:482–7. conducted according to the guidelines of the Ethics Committee of Kuopio University Hospital and the University of Kuopio. KEY WORDS Celiac disease, nutritional status, villous Methods atrophy, adults, gluten-free diet, Finland A screening gastroscopy was performed with an Olympus GIF Q20 end-viewing gastroscope (Tokyo). Endoscopic biopsy speci- INTRODUCTION mens were obtained at the duodenal bulb and the duodenal mucosa Low concentrations of blood hemoglobin and serum albumin, at 5-cm intervals thereafter as far as possible; two specimens at calcium, potassium, magnesium, and iron are frequently encoun- each level were taken by using jumbo forceps (Olympus FB-13K; tered in adult celiac disease patients (1). Patients with untreated Tokyo). Specimens were fixed in 10% buffered formalin and celiac sprue and even those with subclinical disease have been fre- processed by standard methods. The staining method used was van quently reported to suffer from anemia because of deficiencies of Gieson’s (14). Specimens were oriented with the aid of a dissect- iron and folate (2–5). Recent studies indicate that 11–38% of ing microscope to get well-oriented villi in the histologic sections. untreated celiac disease patients have concentrations of hemoglo- The pathologist conducted the histopathologic examinations with- bin, serum ferritin, iron, vitamin B-12, or erythrocyte folate below out knowledge of the clinical state of the patient. The degree of reference values (6, 7). At present, celiac disease is commonly crypt hyperplastic villous atrophy was graded as normal (0), par- diagnosed early enough so that marked abnormalities in labora- tory values of untreated patients do not occur as frequently as seen 1 From the Departments of Clinical Nutrition and Pathology and Forensic previously (4, 8, 9). It has also been suggested that there might be Medicine University of Kuopio, Kuopio, Finland; the Departments of Clini- a new type of disease, clinically silent celiac disease, in which no cal Nutrition and Clinical Pathology and Unit of Gastroenterology, Depart- marked clinical abnormalities are observed (10, 11). The severity ment of Medicine, Kuopio University Hospital, Kuopio, Finland; and the Unit of mucosal villous atrophy may in part explain the differences in of Gastroenterology, Department of Medicine, Tampere University Hospital, Tampere, Finland. nutritional status found earlier. However, to our knowledge the 2 Supported by grants from the Olvi Foundation, the Finnish Association association between biochemical measurements and the grade of of Academic Agronomist and Finnish Cultural Foundation. villous atrophy in newly diagnosed celiac disease patients has not 3 Address reprint requests to TA Kemppainen, Department of Clinical been reported before. Therefore, we set up a study to examine the Nutrition, PO Box 1627, 70211 Kuopio, Finland. association of the grade of villous atrophy with the nutritional sta- Received May 14, 1997. tus in newly diagnosed celiac disease patients. Accepted for publication October 13, 1997. 482 Am J Clin Nutr 1998;67:482–7. Printed in USA. © 1998 American Society for Clinical Nutrition
KEMPPAINEN ET AL 483 TABLE 1 millimeter at four sites (biceps, triceps, subscapular, and suprail- Age, anthropometric characteristics, and duration of symptoms related to iac) and the mean of six measurements at each site was calcu- celiac disease in newly diagnosed celiac disease patients1 lated. Body density and fat-free mass (FFM) were calculated Men Women according to the method of Durnin and Womersley (18) and the Variables (n = 12) (n = 28) body fat content from the body density by using Siri’s 1956 Age (y) 47 ± 12 (24–65) 44 ± 13 (18–62) equation as described by Durnin and Womersley (18). BMI (kg/m2) 25 ± 12 (20–32) 24 ± 5 (17–46) Blood samples were taken from the subjects after they had Fat-free mass (kg) 57 ± 8 (47–70) 43 ± 4 (35–49) fasted overnight. The following analyses were made by using Fat mass (%) 22 ± 7 (8–34) 32 ± 4 (23–40) routine clinical laboratory methods: blood hemoglobin, serum Weight loss (kg) 1.2 ± 2.2 (0–6.0) 2.1 ± 3.7 (0–13.0) total protein, serum albumin, iron, ferritin (immunoluminometric Duration of celiac disease– 5.0 ± 2.6 (2.0–7.0) 14.1 ± 11.0 (6.0–36.0) assay), transferrin, vitamin B-12 (radioisotope dilution assay), related weight loss (mo) calcium, magnesium, alkaline phosphatase, and folic acid in ery- Duration of celiac disease– 15.8 ± 19.2 (0–51) 13.1 ± 18.4 (0–57) throcytes (saturation analysis). Serum zinc was determined by related symptoms (y) using atomic-absorption spectrophotometry. All specimens were 1 – x ± SD; range in parentheses. analyzed in a single run and the within-run CV was 3.6%. Serum vitamin D metabolite (calcidiol) was assayed as described by Parviainen et al (19). Vitamins A and E were determined by using HPLC with ultraviolet detection by the method of De tial (I), subtotal (II), and total (III) (12, 13). In partial atrophy, villi Leenheer (1979) as modified by Parviainen and Koskinen (20). were broadened and shortened. In subtotal atrophy, villi were Antigliadin antibodies (AGAs) of immunoglobulin class A (IgA) more damaged and almost completely absent. No villous projec- were measured by an enzyme immunoassay as described by tions from the surface were seen in total atrophy. Ascher et al (21). Antireticulin antibodies (ARAs) of IgA was One investigator also measured histomorphometrically the determined by indirect immunofluorescence (22). ratio of the perimeter area to lamina propria area of the same Statistics biopsy specimens without knowledge of the patient’s clinical state, according to the procedure of Corazza et al (15). In brief, Statistical analyses were performed by using the SPSS statis- the Quantimet 570 image analyzer (Leica, Cambridge, United tical program (23). The results for continuous variables are given Kingdom), operated in an interactive mode with a cursor used to as the arithmetic mean ± SD and the range. The results for non- draw on a digitizing table at an objective magnification of 325 continuous variables are given as the frequency and the percent- (Olympus Vanox T light microscope; Tokyo), was used for these age. Parametric tests were used when applicable, otherwise non- measurements. Length of perimeter is given by tracing along sur- parametric tests were used. The association between the face epithelium, sides of the field, and the superficial aspect of nutritional status of the newly diagnosed celiac disease patients muscularis mucosae. Area of lamina propria was measured by and their grade of villous atrophy was tested by using analysis of tracing around the basement membrane of the epithelium, cut variance or the Kruskall-Wallis test between the three groups. margins, and muscular mucosae and editing out any cross-sec- Also, the analysis of variance standardized for sex was used to tioned crypts. These measurements were done on three random test the association between nutritional status and the grade of fields from each biopsy specimen. As a sensitive indicator for the villous atrophy. Multiple comparison tests (multiple classifica- changes in villous architecture, the ratio of perimeter to lamina tion analysis) and distribution-free multiple comparisons based propria area was calculated for each specimen: the final index at on previous rank sums test were used after analysis of variance each level was the mean of all three measurements, and the mean and Kruskall-Wallis tests, respectively, as secondary analyses. histomorphometric index was the mean of all level indexes. The differences in the frequency or proportion of the categorized A structured questionnaire was used to collect data on symp- variables were analyzed by chi-square test, and the distribution toms and signs possibly related to celiac disease and their dura- of abnormal laboratory values by the grade of villous atrophy tion. Nutritional status was determined on the basis of food was checked by the nonparametric chi-square test. The associa- records and anthropometric and biochemical measurements. Four- tions between the variables of interest were assessed by non- day food records were kept by all subjects with amounts deter- parametric (Spearman) correlations. The Wilcoxon test was used mined by using household measures. Nutrient intake was calcu- in comparisons of continuous variables between the time points lated by using the NUTRICA computer program (Social Insurance (before and after the celiac disease diet). Institution, Helsinki), which uses the Food and Nutrient Data Base of the Social Insurance Institution (16). The nutrient content data on the gluten-free products used were collected from the manu- RESULTS facturers and added into the database before calculations. At the time of diagnosis the mean histomorphometric index of Body weight was determined with the subject standing bare- the patients was 0.018 ± 0.003 in patients with partial villous atro- foot on a digital scale (Seca 770; Dayton, Hamburg, Germany) phy, 0.015 ± 0.002 in patients with subtotal villous atrophy, and and wearing light clothing. Height of subjects without shoes was 0.013 ± 0.002 in patients with total villous atrophy (P = 0.004 for measured with a wall-mounted stadiometer. Body mass index trend). IgA ARA values were abnormal in five of eight patients (BMI) was calculated as body weight (kg)/height 2 (m). Skinfold with partial villous atrophy, 12 of 17 patients with subtotal villous thicknesses were measured on the nondominant side of the body atrophy, and 13 of 15 patients with total villous atrophy (P = 0.53). as described by Weiner and Lourie (17) by using Harpenden IgA AGA values were abnormal in five of eight patients with par- skinfold calipers (John Bull, British Indicators, St Albans, tial villous atrophy, 13 of 17 patients with subtotal villous atrophy, United Kingdom). The measurements were taken to the nearest and 12 of 15 patients with total villous atrophy (P = 0.27).
484 NUTRITIONAL STATUS IN UNTREATED CELIAC DISEASE TABLE 2 Age, duration of celiac disease–related symptoms, and weight loss in newly diagnosed celiac disease patients according to grade of villous atrophy Grade of villous atrophy Partial Subtotal Total Variables (n = 8) (n = 17) (n = 15) Sex Men 1 9 2 Women 7 8 13 Age Men (y) 60 46 ± 14 (24–65)1 46 ± 2 (44–47) Women (y) 40 ± 17 (18–61) 49 ± 10 (33–62) 42 ± 13 (19–58) All (y) 42 ± 18 (18–61) 47 ± 12 (24–65) 43 ± 12 (19–58) Duration of celiac disease–related symptoms Men (y) 0 19 ± 21 (1–51) 12 ± 16 (1–24) Women (y) 14 ± 22 (0–54) 26 ± 24 (0–57) 5 ± 4 (1–13)2 All (y) 12 ± 20 (0–54) 22 ± 22 (0–57) 6 ± 7 (1–24) Weight loss (kg) 2.6 ± 5.0 (0–13.0) 1.4 ± 2.8 (0–8.0) 1.7 ± 2.5 (0–6.5) Duration of celiac disease–related weight loss 24 ± 17 (12–36) 5 ± 3 (2–7) 9 ± 3 (6–12) (mo) 1 – x ± SD; range in parentheses. 2 Significantly different from other grades of villous atrophy, P < 0.05 (Kruskall-Wallis test). Age, duration of symptoms, weight loss, and the period of ferrin (P < 0.05). Because the number of men and women was time of weight loss of the newly diagnosed celiac disease different in the different villous atrophy groups (P < 0.05), the patients according to the grade of villous atrophy before the effect of sex was standardized in analysis of variance; after this, institution of a celiac disease diet are presented in Table 2. Mean serum ferritin (P < 0.05) and erythrocyte folate concentrations duration of symptoms in subjects with subtotal villous atrophy (P < 0.05) were still lower in the patients with total villous atro- tended to be longer than that in the other groups, but this differ- phy than in the other groups (Table 5). The severity of villous ence was not significant. atrophy correlated weakly (from –0.25 to –0.43, P < 0.05) with Energy intake was higher in patients with subtotal villous serum ferritin, erythrocyte folate, and serum vitamin B-12 con- atrophy than in others, probably because most of them (9 of 17) centrations. were men. However, no significant differences were found in the The frequency of abnormally low erythrocyte folate concen- intakes of carbohydrate, protein, and fat among the groups with trations tended to be higher in the patients with total villous atro- different grades of villous atrophy (Table 3). Patients with par- phy (9 of 15) than in those with subtotal villous atrophy (4 of 17) tial villous atrophy consumed 160 ± 60 g cereals, those with or partial villous atrophy (1 of 5), but the difference was not sig- subtotal villous atrophy consumed 263 ± 86 g, and those with nificant (P = 0.07). Generally, prevalences of abnormal values of total villous atrophy consumed 213 ± 97 g (P = 0.013, compari- serum protein, vitamin A, and vitamin B-12 in the groups with son among the three groups). Patients with subtotal villous atro- different grades of villous atrophy were low (Table 6). None had phy had the highest use of cereals (P = 0.05). Severity of villous abnormal vitamin E values. atrophy had no effect on the results of anthropometric measure- In women, height (r = –0.43, P < 0.05) and serum transferrin ments in men or women (Table 4). concentration (r = –0.49, P < 0.05) had an inverse association When biochemical measurements were examined according with the duration of symptoms. In men, the duration of symptoms to the grade of villous atrophy, significant differences were had an inverse correlation with serum vitamin B-12 concentration found among the groups for serum ferritin (P < 0.01) and trans- (r = –0.84, P < 0.05). The duration of symptoms was not associ- TABLE 3 Associations between energy intake and the percentage of energy from different nutrients and grade of villous atrophy in newly diagnosed celiac disease patients1 Grade of villous atrophy Partial Subtotal Total Variables (n = 7) (n = 17) (n = 15) Energy (MJ) 7.6 ± 1.6 (4.8–9.8) 9.5 ± 2.3 (4.6–13.1)2,3 7.9 ± 1.1 (5.8–9.3) Carbohydrate (% of energy) 46 ± 7 (36–53) 48 ± 5 (41–57) 50 ± 6 (39–59) Protein (% of energy) 15 ± 2 (13–18) 17 ± 3 (9–22) 16 ± 3 (13–21) Fat (% of energy) 37 ± 5 (30–43) 35 ± 5 (23–42) 33 ± 5 (25–43) Alcohol (% of energy) 2 ± 3 (0–8) 1 ± 3 (0–10) 1 ± 1 (0–4) 1 – x ± SD; range in parentheses. 2 Significantly different from other grades of villous atrophy, P < 0.05 (Kruskall-Wallis test). 3 P = 0.05 for the distribution-free comparison based on the previous rank-sums test.
KEMPPAINEN ET AL 485 TABLE 4 Associations between anthropometric measurements and the grade of villous atrophy in newly diagnosed celiac disease patients1 Grade of villous atrophy Partial Subtotal Total Variables (n = 1M, 7W) (n = 9M, 8W) (n = 2M, 13W) Men Weight (kg) 64 76 ± 14 (58–95)2 66 ± 5 (62–69) Height (cm) 170 173 ± 5 (167–184) 166 ± 3 (164–169) BMI (kg/m2) 22 25 ± 4 (20–32) 24 ± 3 (22–26) Fat-free mass (kg) 47 59 ± 8 (47–70) 49 ± 1 (49–50) Fat mass (%) 27 21 ± 8 (9–34) 25 ± 4 (22–28) Women Weight (kg) 66 ± 5 (67–72) 68 ± 24 (46–119) 62 ± 8 (47–79) Height (cm) 164 ± 9 (155–178) 163 ± 5 (156–171) 164 ± 4 (155–169) BMI (kg/m2) 24 ± 3 (20–27) 26 ± 9 (17–46) 23 ± 3 (18–28) Fat-free mass (kg) 45 ± 4 (40–49) 42 ± 3 (39–46) 42 ± 4 (35–48) Fat mass (%) 32 ± 5 (23–40) 32 ± 3 (29–36) 32 ± 4 (25–39) 1 There were no significant differences among grades of villous atrophy (Kruskall-Wallis test). 2 –x ± SD; range in parentheses. ated with the severity of villous atrophy. Weight loss before diag- ments, and biochemical measurements did not differ between the nosis had an inverse correlation with serum total protein (r = groups with and without oats (12). –0.44, P < 0.05) and calcium (r = –0.38, P < 0.05) concentrations Most of the initially abnormal biochemical values improved in the subjects who reported weight loss. In men only, weight loss during the 1 y of follow-up concurrently with the improvement had an inverse correlation with serum protein (r = –0.64, P < of villous atrophy (Figure 1). However, one of the two patients 0.05) and serum ferritin (r = –0.75, P < 0.05) concentrations. with subtotal villous atrophy still had a low hemoglobin value. In Villous atrophy improved in all patients within 12 mo of fol- 29 patients with partial villous atrophy, low values were regis- low-up: only 2 patients had subtotal villous atrophy (mean histo- tered for erythrocyte folate (3 patients), hemoglobin morphometric index of 0.016 ± 0.003), 29 patients had partial (7 patients), serum vitamin B-12 (1 patient), serum protein villous atrophy (0.019 ± 0.002), and 3 patients had normal vil- (1 patient), serum vitamin A (5 patients), serum ferritin (5 lous architecture (0.022 ± 0.002). Six patients withdrew from the patients), serum iron (15 patients), and serum zinc (10 patients). follow-up. As reported earlier, the severity of villous atrophy did One of three patients with normal villous architecture had a low not differ between the oat and control groups (12). hemoglobin value at this stage of the follow-up. During the 1 y of gluten-free diet with or without oats, BMI increased but no changes in intakes of energy, carbohydrate, pro- tein, or fat were found in the whole group. On the other hand, DISCUSSION intakes of fiber and thiamine decreased with the gluten-free diet. The aim of the current study was to examine an association Nutrient intakes, except for thiamine, anthropometric measure- between biochemical measurements and the grade of villous TABLE 5 Associations between biochemical measurements and grades of villous atrophy in newly diagnosed celiac disease patients1 Grade of villous atrophy Partial Subtotal Total Variables (n = 5) (n = 17) (n = 15) Serum protein (g/L) 79 ± 6 (72–86) 75 ± 7 (54–84) 76 ± 5 (65–82) Serum albumin (g/L) 46 ± 6 (38–53) 46 ± 6 (37–58) 47 ± 4 (42–55) Blood hemoglobin (g/L) 134 ± 12 (128–156) 138 ± 16 (114–168) 129 ± 14 (98–154) Serum iron (mmol/L) 17 ± 9 (11–33) 15 ± 6 (7–24) 16 ± 8 (4–36) Serum ferritin (mg/L) 187 ± 361 (9–831) 49 ± 42 (7–143) 18 ± 18 (8–79)2 Serum transferrin (g/L) 3.2 ± 0.9 (2.4–4.8) 2.8 ± 0.1 (2.2–3.4) 3.3 ± 0.5 (2.5–4.4) Erythrocyte folate (nmol/L) 570 ± 357 (211–1159) 407 ± 156 (157–769) 309 ± 167 (0–582)2 Serum vitamin B-12 (pmol/L) 366 ± 134 (209–525) 332 ± 149 (95–564) 277 ± 152 (122–661) Serum calcium (mmol/L) 2.3 ± 0.2 (2.1–2.6) 2.2 ± 0.1 (1.9–2.4) 2.3 ± 0.01 (2.1–2.4) Serum magnesium (mmol/L) 0.8 ± 0.03 (0.78–0.85) 0.8 ± 0.07 (0.73–0.91) 0.8 ± 0.06 (0.70–0.95) Serum zinc (mmol/L) 11 ± 0 13 ± 2 (8–17) 12 ± 2 (10–14) Serum vitamin A (mmol/l) 1.3 ± 0.4 (0.9–1.7) 1.5 ± 0.5 (1.0–2.5) 1.4 ± 0.4 (0.8–2.2) Serum vitamin E (mmol/L) 26 ± 12 (14–41) 23 ± 5 (14–36) 24 ± 12 (12–46) Serum calcidiol (nmol/L) 51 ± 18 (27–70) 44 ± 17 (25–77) 45 ± 17 (29–97) 1 – x ± SD; range in parentheses. 2 Significantly different from other grades of villous atrophy, P < 0.05 (ANOVA standardized for sex and multiple classification analysis).
486 NUTRITIONAL STATUS IN UNTREATED CELIAC DISEASE TABLE 6 The frequency of newly diagnosed celiac disease patients with abnormal biochemical values by grade of villous atrophy1 Grade of villous atrophy Partial Subtotal Total Biochemical variable Limit of abnormal value (n = 5) (n = 17) (n = 15) Hemoglobin Men < 135 g/L 0 3 0 Women < 125 g/L 0 (0) 4 (41) 5 (33) Serum vitamin B-12 < 150 pmol/L 0 4 (24) 2 (13) Erythrocyte folate < 300 nmol/L 1 (20) 4 (24) 9 (60) Serum ferritin Men < 25 mg/L 0 2 2 Women < 12 mg/L 2 (40) 1 (18) 6 (53) Serum iron Men < 14 mmol/L 0 2 1 Women < 13 mmol/L 2 (40) 6 (47) 4 (33) Serum protein < 64 g/L 0 1 (6) 0 Serum zinc < 13 mmol/L 1 (20) 9 (53) 9 (60) Serum vitamin A < 1 mmol/L 1 (20) 1 (6) 3 (20) Serum ferritin and erythrocyte folate 0 1 (6) 7 (47) 1 n; percentage in parentheses. There were no significant differences among grades of villous atrophy (chi-square test and nonparametric chi-square test). atrophy in newly diagnosed celiac disease patients. The grade of could explain part of the abnormal biochemical values after 1 y villous atrophy was examined with two different methods that of gluten-free diet in our study. gave consistent results regarding the severity of villous damage. Similarly to previous studies (33, 34), this study showed no Furthermore, only 75% of patients showed abnormal ARA or correlation between the duration of symptoms related to celiac AGA concentrations at the time of diagnosis. None of the disease and the grade of villous atrophy. The duration of symp- patients had IgA deficiency. toms did not correlate with the occurrence of abnormal labora- Serum ferritin and erythrocyte folate concentrations were tory values either. The reason for this may be that symptoms of lower in patients with total villous atrophy than in those with celiac disease have not been typical and there is variability in subtotal or partial atrophy, but anthropometric measurements and gluten sensitivity from patient to patient. nutrient intake did not differ among the patients with different In women, duration of symptoms related to celiac disease had grades of villous atrophy in this study. In a recent study, Bode and an inverse correlation with height. Although adult celiac disease Gudmand-Hoyer (7) reported that the percentage of patients patients are claimed to be shorter than average, the height of showing signs of malabsorption in laboratory measurements is patients with celiac disease diagnosed after reaching adulthood lower than that reported previously. Their findings agree with the does not differ significantly from that of the general population results of our study (6). Previously, weight loss has been the most (30). The fact that weight loss before diagnosis had an inverse common presenting feature in adult celiac disease patients correlation with serum protein and calcium concentrations and (24–26). Nowadays, celiac disease seems to be diagnosed suffi- that the duration of symptoms related to celiac disease had an ciently early so that marked abnormalities in laboratory and inverse correlation with serum vitamin B-12 concentrations in anthropometric measurements of untreated celiac disease are not men may reflect the possible existence of abnormal absorption expected. In contrast with many earlier studies (6, 11, 27–30), due to a delayed diagnosis of celiac disease. none of the patients in our study were clearly malnourished. Corazza et al (31) reported that patients with subclinical pre- sentation had better nutritional status than those with symptoms of malabsorption. None of the patients with subclinical presenta- tion had evidence of severe malnutrition. However, Crofton et al (32) showed that increased loss of endogenous zinc occurs even in mild untreated celiac disease. This finding suggests a possibil- ity of finding abnormal serum zinc values as well as some other abnormal biochemical measurements in celiac disease patients irrespective of the severity of the disease. In our study, serum zinc concentration was low in 18 of 37 patients at diagnosis. Celiac disease patients with classical presentation may require a longer period of gluten-free diet to achieve a significant improvement of their nutritional status than those with subclini- cal presentation, probably because of greater intestinal damage FIGURE 1. Number of celiac disease patients with values of ery- (11). In the present study, the type of presentation of celiac dis- throcyte folate, serum vitamin B-12, serum vitamin A, hemoglobin, ease was not examined, but according to the study of Corazza et serum ferritin, serum iron, and serum zinc below the reference values al (11), the variability of presentation and severity of disease before (h) and after (j) 1 y of a celiac disease diet. n = 40.
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