The stomach as the target organ of celiac disease

Cover Page

Abstract


The aim of this study was to observe the features of chronic gastritis in children with celiac disease (СD).

Materials and methods. 176 children with chronic gastritis (CG) aged from 3 to 16 years were examined. Group I consisted 58 child ren with CG and newly diagnosed CD not adherent to the gluten-free diet (GFD), group II consisted 49 children with CG and CD, adherent to the GFD. In the group III of comparisons were 69 children with CG and excluded CD. The exa mination included serological, morphological methods to confirm or exclude CD. The histological examination of the biopsy specimens of the gastric mucosa, the determination of antiparietal antibodies by the method of iIFR and ELISA (antibodies to Castle’s intrinsic factor and Anti-H+/K+ ATPase antibodies) were carried out.

Results. Helicobacter pylori infection was diagnosed in vast majority of patients in all groups. Autoantibodies to the gastric mucosa were found in every tenth patient in groups I and III, and did not occur in group II. In group II statistically significant the etiology of gastritis remained not determined. Endoscopically the gastric mucosa in groups I and II often remained intact. Accor ding to the morphological study in groups I and II, the pathological process was more often localized in the body of the stomach, and in group III in the antrum. Autoimmune gastritis is presented in groups without a statistically significant difference.

Conclusion. Chronic gastritis is a frequent co-morbid pathology in СD, and it is also not uncommon in these patients. Data of endoscopy in children, regardless of diet, does not reflect the complete picture of CG. All children with CD, regardless of compliance with GFD, are recommended to take biopsy specimens of the gastric mucosa for histological examination in order to exclude CG, and in case of detecting atrophic changes in the gastric mucosa to define the antiparietal antibodies.


Full Text

INTRODUCTION

Celiac disease (CD) is a systemic autoimmune disease induced by impaired gluten tolerance and develops in genetically predisposed people [4, 8]. The prevalence is approximately 1:100 among the Western population and is one of the most common autoimmune diseases [16]. Currently, CD is not considered a pathology affecting only the small intestine and is reflected in modern definitions.

The range of clinical manifestation is extensive and includes both the classic form with malabsorption and the atypical form with extraintestinal symptoms. It has been demonstrated that the atypical and “silent” forms are much more common than the typical ones [5]. In addition, many organs and systems are involved in the autoimmune process because of both the common genetic mechanisms of development of other autoimmune diseases and extraintestinal deposits of its own antibodies to tissue transglutaminase (tTG) in the lymph nodes, liver, muscles, and other organs [10, 15]. The combination of celiac disease with type 1 diabetes mellitus and autoimmune thyroiditis [4] with impaired reproductive function in women has been well-described [2].

Considerably less attention has been paid to the association of CD with other autoimmune diseases of the gastrointestinal tract. Primary biliary cirrhosis occurs in 3% of celiac disease cases [6, 9], which exceeds the population risk by 20 fold [11, 12]. The prevalence of CD among patients with autoimmune hepatitis reaches 6% [20], and hepatitis among patients with CD is observed in approximately 2% cases [19]. Primary sclerosing cholangitis (PSC) shows an association with CD in 3% of cases [17], and a four-fold increased risk of CD compared with population risk in PSC patients persists despite the exclusion of inflammatory intestinal disease [12]. Furthermore, up to 15% of patients with microscopic (lymphocytic) colitis (MC) suffer from CD [14], and the prevalence of MC among patients with celiac disease reaches 4%, which exceeds the population risk by 70 times [7, 18].

Currently, researchers have focused on chronic gastritis as comorbid pathology in CD [1, 3]; however, there is no evidence of increased prevalence of autoimmune gastritis (AIG) among patients with CD

The study aimed to analyze the aspects of chronic gastritis in pediatric patients with CD.

MATERIALS AND METHODS

We examined 176 pediatric patients with chronic gastritis (CG), aged 3–16 years. Group I consisted of 58 pediatric patients with CG and newly diagnosed CD who did not adhere to gluten-free diet (GFD), while Group II included 49 pediatric patients with CG and CD who adhered to GFD. The control group (group III) consisted of 69 pediatric patients with CG and excluded celiac disease.

All patients underwent the same examination. The diagnosis of CD was established on the Federal Clinical guidelines for the provision of medical care for pediatric patients with celiac disease1 and the Celiac Disease Guidelines of European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPHAN) from 2012 [8], We analyzed clinical and anamnestic data that tested the presence of positive specific antibodies (IgG, IgA) against deamidated gliadine peptides and tissue transglutami­nase-2. If it was necessary anti- endomysium antibodies and the level of total IgA were also determined. A morphometric study of the duodenal mucosa was performed in all patients. Detection of atrophy to a degree of no less than Marsh 3a was considered evidence in favor of CD. HLA genotyping was performed in all patients to detect DQ2 and DQ8 genes associated with CD.

The diagnosis of CG was verified morphologically for all studied participants. Biopsy samples of the mucous membrane of the gastric antrum and fundus were obtained by esophagogastroduodenoscopy performed using an Evis Exera 2 OLYMPUS device of the HGi 180 type (Japan) using the standard procedure. Endoscopic and histological evaluation of the gastric mucosa was performed according to the Sydney system. The test for H.pylori was performed for all patients using the rapid urease test (AMA LLC, St. Petersburg, Russia).

In order to diagnose autoimmune gastritis, in 45 pediatric patients anti-parietal PCA IgG antibodies were determined by indirect immunofluorescence (iIF) using the EUROIMMUN IIFT EUROPLUS™ Stomach (Monkey) reagent kit manufactured by EUROIMMUN Medizinische Labordiagnostika AG (Germany). The normal value was <40u/ml. The study was performed on a specialized microscope for immunofluorescence studies EUROStar II of EUROIMMUN AG (Germany). Antibodies (IgG) to Н+/К+-ATPase of the parietal cells of the gastric mucosa (GM) were detected in 58 pediatric patients in the blood plasma by enzyme-linked immunosorbent assay (ELISA) using standard kits ORGENTEC Anti-Parietal Cell (H+/K+-ATPase), ORGenTec Diagnostika (Germany) (negative result was 0–10 U/ml, and a positive result was more than 10 U/ml). Antibodies (IgG) to Castle intrinsic factor were determined in blood plasma by ELISA on a standard photometer using kits manufactured by EUROIMMUN Medizinische Labordiagnostika AG (Germany) from 140 pediatric patients. According to the instructions, the negative result was 0–20 RU/ml, and the positive one was greater than 20 RU/ml.

Statistical analysis was performed using IBM SPSS Statistics 23 software. The average antibody level was calculated with a 95% confidence interval, indication of the upper and lower limits, median, and mean squared deviation. For comparison of means, the Student’s t-test was used for independent samples (two-sided significance, p < 0.05). The Livin’s dispersion test and the normal distribution test of Kolmogorov–Smirnov and Shapiro–Wilk were taken into account. To analyze endoscopic and morphological studies in groups, the Fisher’s exact test was used (significance p < 0.05).

RESULTS

The etiology of CG in the studied groups is presented in Table 1.

 

Table 1. Etiology of chronic gastritis in the studied groups

(Таблица 1). Этиология хронического гастрита в исследуемых группах

Groups/

Группы

n (%)

I group / I группа

(n = 58)

II group / II группа

(n = 49)

III group / III группа

(n = 69)

p

Fisher’s exact test / Точный критерий Фишера

р1

р2

р3

Helicobacter infection / Хеликобактерная инфекция

37

63.8%

26

53.1%

47

68.1%

p1,2 = 0.00

p1,3 = 0.00

p2,3 = 0.35

Autoantibodies to the stomach mucous membrane / Аутоантитела к слизистой оболочке желудка

7

12.1%

0

0%

7

10.1%

p1,2 = 0.01

p1,3 = 0.8

p2,3 = 0.01

НР+ Autoantibodies to the stomach mucous membrane / НР+-аутоантитела к слизистой оболочке желудка

2

3.4%

0

0%

2

2.9%

p1,2 = 0.14

p1,3 = 0.91

p2,3 = 0.18

НР-reflux / Рефлюкс HP–

3

5.17%

3

6.1%

4

5.8%

p1,2 = 0.94

p1,3 = 0.91

p2,3 = 0.96

Not determined / Этиология хронического гастрита не установлена

9

15.6%

20

40.8%

9

13.1%

p1,2 = 0.03

p1,3 = 0.78

p2,3 = 0.01

 

The primary etiological factor of CG in pediatric patients in all groups was Helicobacter pylori infection. Duodenogastric reflux was rarely observed as an independent cause of CG. An increased level of autoantibodies to GM was equally common in the group of pediatric patients with newly diagnosed CD and CG but did not occur in any patient in the CD on GFD. For patients adhering to GFD, the etiology of gastritis was more often was undetermined.

The main endoscopic characteristic among patients with СВ (groups I and II) was intact GM in contrast to the comparison group. In group 3, superficial antral gastritis was most often observed. These data are presented in Table 2.

 

Table 2. Endoscopic characteristics of the gastric mucosa in the studied groups

(Таблица 2). Эндоскопическая характеристика слизистой оболочки желудка в исследуемых группах

Groups/

Группы

n (%)

I group / I группа

(n = 58)

II group / II группа

(n = 49)

III group / III группа

(n = 69)

p

Fisher’s exact test / Точный критерий Фишера

р1

р2

р3

Normal / Норма

23

39.7%

26

53.1%

0

0%

p1,2 = 0.00

p1,3 = 0.00

p2,3 = 0.35

Superficial fundal gastritis / Поверхностный фундальный гастрит

2

3.4%

2

4.1%

4

5.8%

p1,2 = 1.000

p1,3 = 0.687

p2,3 = 1.000

Superficial antral gastritis / Поверхностный антральный гастрит

23

39.7%

6

12.2%

37

53.6%

p1,2 = 0.002

p1,3 = 0.153

p2,3 = 0.000

Nodular antral gastritis / Нодулярный антральный гастрит

3

5.2%

4

8.2%

6

8.7%

p1,2 = 0.700

p1,3 = 0.507

p2,3 = 1.000

Superficial pangastritis /
Поверхностный пангастрит

6

10.3%

9

18.4%

18

26.1%

p1,2 = 0.272

p1,3 = 0.039

p2,3 = 0.379

Atrophic gastritis /
Атрофический гастрит

0

0.0%

0

0.0%

2

2.9%

p1,3 = 0.500

p2,3 = 0.510

Erosive gastritis /
Эрозивный гастрит

1

1.7%

1

2.0%

1

1.4%

p1,2 = 1.000

p1,3 = 1.000

p2,3 = 1.000

Polyp of the stomach /
Полип желудка

0

0.0%

1

2.0%

1

1.4%

p1,2 = 0.458

p1,3 = 1.000

p2,3 = 1.000

 

Motor disorders, such as insufficiency of cardia, gastroesophageal reflux, and duodenogastric reflux, were not different between the groups. These data are presented in Table 3.

 

Table 3. Endoscopic characteristic of gastric motor function in the studied groups

(Таблица 3). Эндоскопическая характеристика моторной функции желудка в исследуемых группах

Groups/

Группы

n (%)

I group / I группа

(n = 58)

II group / II группа

(n = 49)

III group / III группа

(n = 69)

p

Fisher’s exact test / Точный критерий Фишера

р1

р2

р3

Insufficiency of cardia /

Недостаточность кардии

1

1.7%

4

8.2%

7

10.1%

p1,2 = 0.177

p1,3 = 0.070

p2,3 = 1.000

Gastroesophageal reflux / Гастроэзофагеальный рефлюкс

4

6.9%

5

10.2%

8

11.6%

p1,2 = 0.729

p1,3 = 0.544

p2,3 = 1.000

Duodenogastric reflux / Дуоденогастральный рефлюкс

6

10.3%

2

4.1%

12

17.4%

p1,2 = 0.285

p1,3 = 0.313

p2,3 = 0.041

Normal motor function /
Нормальная моторика

48

82.8%

42

85.7%

50

72.5%

p1,2 = 0.793

p1,3 = 0.205

p2,3 = 0.115

 

According to the morphological study, the pathological process in the mucous membrane of the gastric body was more often registered in groups I and II with celiac disease, and an antral lesion was more characteristic of isolated CG. Chronic active pangastritis was common in all groups. Chronic inactive gastritis was more often detected in group I than in group III. These data are presented in Table 4.

 

Table 4. Morphological characteristics of the gastric mucosa in the studied groups

(Таблица 4). Морфологическая характеристика слизистой оболочки желудка в исследуемых группах

Groups/

Группы

n (%)

I group / I группа

(n = 58)

II group / II группа

(n = 49)

III group / III группа

(n = 69)

p

Fisher’s exact test / Точный критерий Фишера

р1

р2

р3

Chronic inactive pangastritis /
Хронический неактивный пангастрит

36

62.1%

28

57.1%

25

36.2%

p1,2 = 0.68

p1,3 = 0.04

p2,3 = 0.1

Chronic active pangastritis /
Хронический активный пангастрит

12

21.1%

7

14.3%

19

27.5%

p1,2 = 0.48

p1,3 = 0.55

p2,3 = 0.19

Chronic active gastritis in the body of stomach / Хронический активный гастрит тела желудка

1

1.7%

0

0%

0

0%

p1,2 = 0.3

p1,3 = 0.3

Chronic inactive gastritis in the body of stomach / Хронический неактивный гастрит тела желудка

0

0%

4

8.7%

0

0%

p1,2 = 0.02

p2,3 = 0.02

Chronic inactive antral gastritis / Хронический неактивный антральный гастрит

4

6.9%

3

6.1%

1

1.4%

p1,2 = 0.9

p1,3 = 0.24

p2,3 = 0.3

Chronic active antral gastritis / Хронический активный антральный гастрит

4

6.9%

3

6.1%

20

29%

p1,2 = 0.9

p1,3 = 0.02

p2,3 = 0.01

Chronic active antral gastritis and chronic inactive gastritis in the body of stomach / Хронический активный антральный гастрит и хронический неактивный гастрит тела желудка

0

0%

0

0%

4

5.8%

p1,3 = 0.06

p2,3 = 0.06

Chronic active gastritis in the body of stomach and chronic inactive antral gastritis / Хронический активный гастрит тела желудка и хронический неактивный антральный гастрит

1

1.7%

4

8.2%

0

0%

p1,2 = 0.21

p1,3 = 0.3

p2,3 = 0.002

 

The average level of anti-parietal autoantibodies for the ELISA method in all groups was the same. These data are presented in Table 5.

 

Table 5. The average level of antiparietal autoantibodies in the studied groups

(Таблица 5). Средний уровень антипариетальных аутоантител в исследуемых группах

Groups /

Группы

I group /
I группа

II group /

II группа

III group /

III группа

p

Student’s t-test /

t-критерий Стьюдента

Antibodies to Castle’s intrinsic factor / Антитела к фактору Кастла

Average value / Среднее значение

4.0353

3.1215

8.0258

p1,2 = 0.347

p1,3 = 0.464

p2,3 = 0.368

Lower bound / Нижняя граница

2.5298

1.8327

–1.3677

Upper bound / Верхняя граница

5.5409

4.4102

17.4193

Median / Медиана

2.4485

2.3700

2.3880

Standard deviation / Среднеквадратичное отклонение

3.72735

3.19066

27.34546

Anti-H+/K+-ATPase antibodies / Антитела к Н+/К+-АТФазе

Average value / Среднее значение

16.2538

1.4625

4.7470

p1,2 = 0.352

p1,3 = 0.213

p2,3 = 0.655

Lower bound / Нижняя граница

–2.6066

0.4039

1.1093

Upper bound / Верхняя граница

35.1141

3.3289

8.3846

Median / Медиана

1.9300

1.0150

1.4600

Standard deviation / Среднеквадратичное отклонение

35.39445

1.17296

10.25888

 

The frequency of detection of increased levels of anti-parietal autoantibodies were significantly different between the groups. The data are presented in Table 6.

 

Table 6. The frequency of elevated levels of antiparietal antibodies in the studied groups

(Таблица 6). Частота выявления повышенного уровня антипариетальных аутоантител в исследуемых группах

Groups /

Группы

n (%)

I group /
I группа

II group /
II группа

III group /
III группа

p

Fisher’s exact test / Точный критерий Фишера

p1

p2

p3

Antibodies to Castle’s intrinsic factor, IgG /

Антитела к фактору Кастла, IgG

n = 42

n = 30

n = 68

p1,2 = 0.08

p1,3 = 0.95

p2,3 = 0.1

2

4.76%

0

0%

3

4.4%

Anti-H+/K+-ATPase antibodies, IgG /

Антитела к Н+/К+-АТФазе, IgG

n = 18

n = 7

n = 33

p1,2 = 0.00

p1,3 = 0.28

p2,3 = 0.01

4

22.2%

0

0%

4

12.1%

PCA IgG

n = 10

n = 7

n = 28

p1,2 = 0.01

p1,3 = 0.01

1

10%

0

0%

0

0%

 

Antibodies to parietal gastric cells were more often revealed in patients with newly established celiac disease, while GFD patients had no anti-parietal autoantibodies.

Among all the examined patients, 14 were found positive for the presence of anti-parietal autoantibo­dies (APA). Among these patients, “classical” autoimmune gastritis (GM atrophy, the presence of APA, the absence of H.pylori) was found in only 5 patients. The frequency of “classical” autoimmune gastritis in the examined groups is presented in Figure 1.

 

Fig. 1. Frequency of “classical” autoimmune gastritis in the examined groups

Рис. 1. Частота «классического» аутоиммунного гастрита в обследованных группах

 

There was no significant difference in AIG between groups: p1,2 = 0.14; p1,3 = 0.85; p2,3 = 0.1.

The main endoscopic characteristic of pediatric patients with celiac disease was an intact GM, while CG was morphologically detected in all children. There were many of these pediatric patients in the GFD group. Also, according to esophagogastroduodenoscopy, cases of fundic gastritis were sporadic, while morphological inflammatory changes in the fundus were observed more often in the structure of pangastritis and in isolation. Autoimmune gastritis was diagnosed in the presence of APA and GM atrophy and was mostly not combined with Helicobacter pylori infection. Therefore, it presented in the classical form and was not differently distributed between groups. We also observed APA patients in the absence of the GM atrophy and H. pylori, which requires further examination to rule out the preatrophic stage of AIG.

Among pediatric patients with CD who adhered to GFD, APA was not observed. At present, GFD appears to have a protective effect on comorbid autoimmune diseases [9]. However, in pediatric patients with GFD, active inflammation in the gastric body was observed, and thus requires additional research.

CONCLUSION

The endoscopy data in pediatric patients with CD, regardless of adherence to GFD, does not reflect the full clinical picture of CG. Biopsy specimens of the GM are recommended when performing endoscopy for histological examination of all pediatric patients with CD, regardless of adherence to GFD in order to detect CG. Also biopsy can determine anti-parietal antibodies for verification of autoimmune gastritis when detecting atrophic and inflammatory changes in the GM. The lack of APA among pediatric patients with CD who adhere to GFD may be because of the protective effect of the diet in autoimmune gastritis. Therefore, in a large proportion of pediatric patients with CD on GFD, the etiology of gastritis remains unclear.

About the authors

Valeria P. Novikova

St. Petersburg State Pediatric Medical University

Author for correspondence.
Email: novikova-vp@mail.ru

Russian Federation, Saint Petersburg

MD, PhD, Dr Mеd Sci, Professor, Head, Research Center

Natalia S. Shapovalova

St. Petersburg State Pediatric Medical University

Email: natasunday@mail.ru

Russian Federation, Saint Petersburg

Junior Researcher, Research Center

Maria O. Revnova

St. Petersburg State Pediatric Medical University

Email: natasunday@mail.ru

Russian Federation, Saint Petersburg

MD, PhD, Dr Mеd Sci, Professor, Head, AF Tour Department of Outpatient Pediatrics

Valentina F. Melnikova

St. Petersburg State Pediatric Medical University

Email: rrmd99@mail.ru

Russian Federation, Saint Petersburg

MD, PhD, Dr Mеd Sci, Professor, Department of Pathological Anatomy at the Rate of Forensic Medicine

Sergey V. Lapin

Рavlov First Saint Petersburg State Medical University, Ministry of Healthcare of the Russian Federation

Email: svlapin@mail.ru

Russian Federation, Saint Petersburg

MD, PhD, Associate Professor, Head, Laboratory for the Diagnosis of Autoimmune Diseases

Veronika I. Guseva

Рavlov First Saint Petersburg State Medical University, Ministry of Healthcare of the Russian Federation

Email: nika_pion@mail.ru

Russian Federation, Saint Petersburg

Laboratory Doctor, Laboratory for the Diagnosis of Autoimmune Diseases

Olga P. Gurina

St. Petersburg State Pediatric Medical University

Email: ol.gurina@yandex.ru

Russian Federation, Saint Petersburg

MD, PhD, Senior Researcher, Research Center

Elena A. Dementieva

St. Petersburg State Pediatric Medical University

Email: zorra2@yandex.ru

Russian Federation, Saint Petersburg

Junior Researcher, Research Center

Ksenia A. Klikunova

St. Petersburg State Pediatric Medical University

Email: kliksa@gmail.com

Russian Federation, Saint Petersburg

PhD, Associate Professor, Department of Medical Physics

References

  1. Азанчевская С.В., Аничков Н.М., Иванова В.Ф., и др. Связь морфологических особенностей париетальных клеток желудка с концентрацией аутоантител к H+/A+-АТФазе при хроническом гастрите // Архив патологии. - 2009. - Т. 71. - № 1. - С. 18-22. [Azanchevskaya SV, Anichkov NM, Ivanova VF, et al. Svyaz’ morfologicheskikh osobennostey parietal’nykh kletok zheludka s kontsentratsiey autoantitel k H+/A+-ATFaze pri khronicheskom gastrite. Arkh Patol. 2009;71(1):18-22. (In Russ.)]
  2. Новикова В.П., Абдул-заде И.Э., Гуркин Ю.А., и др. К вопросу об аутоиммунном оофорите при целиакии у подростков и взрослых // Российский иммунологический журнал. - 2008. - Т. 2. - № 2-3. - С. 236-237. [Novikova VP, Abdul-zade IE, Gurkin YA, et al. K voprosu ob autoimmunnom ooforite pri tseliakii u podrostkov i vzroslykh. Russ J Immunol. 2008;2(2-3): 236-237. (In Russ.)]
  3. Ревнова М.О., Новикова В.П., Шаповалова Н.С., и др. Распространенность аутоиммунного гастрита у детей с целиакией по данным ИФА и реакции непрямой иммунофлюоресценции // Вопросы детской диетологии. - 2017. - Т. 15. - № 2. - С. 55-56. [Revnova MO, Novikova VP, Shapovalova NS, et al. Rasprostranennost’ autoimmunnogo gastrita u detey s tseliakiey po dannym IFA i reaktsii nepryamoy immunoflyuorestsentsii. Problems of pediatric nutritiology. 2017;15(2):55-56. (In Russ.)]
  4. Ревнова М.О., Шаповалова Н.С. Целиакия как аутоиммунное заболевание // Вопросы детской диетологии. - 2015. - Т. 13. - № 3. - С. 33-39. [Revnova MO, Shapovalova NS. Coeliac disease as an autoimmune disease. Problems of pediatric nutritiology. 2015;13(3):33-39. (In Russ.)]
  5. Bai JC, Fried M, Corazza GR, et al. World Gastroenterology Organisation global guidelines on celiac disease. J Clin Gastroenterol. 2013;47(2):121-126. doi: 10.1097/MCG.0b013e31827a6f83.
  6. Floreani A, Betterle C, Baragiotta A, et al. Prevalence of coeliac disease in primary biliary cirrhosis and of antimitochondrial antibodies in adult coeliac disease patients in Italy. Dig Liver Dis. 2002;34(4):258-261. doi: 10.1016/s1590-8658(02)80145-1.
  7. Green PH, Yang J, Cheng J, et al. An association between microscopic colitis and celiac disease. Clin Gastroenterol Hepatol. 2009;7(11):1210-1216. doi: 10.1016/j.cgh.2009.07.011.
  8. Husby S, Koletzko S, Korponay-Szabo IR, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guidelines for the diagnosis of coeliac disease. J Pediatr Gastroenterol Nutr. 2012;54(1):136-160. doi: 10.1097/MPG.0b013e31821a23d0.
  9. Kingham JGC, Parker DR. The association between primary biliary cirrhosis and coeliac disease: a study of relative prevalences. Gut. 1998;42(1):120-122. doi: 10.1136/gut.42.1.120.
  10. Korponay-Szabo IR. In vivo targeting of intestinal and extraintestinal transglutaminase 2 by coeliac autoantibodies. Gut. 2004;53(5):641-648. doi: 10.1136/gut.2003.024836.
  11. Lawson A, West J, Aithal GP, Logan RF. Autoimmune cholestatic liver disease in people with coeliac disease: a population-based study of their association. Aliment Pharmacol Ther. 2005;21(4):401-405. doi: 10.1111/j.1365-2036.2005.02328.x.
  12. Ludvigsson JF, Elfstrom P, Broome U, et al. Celiac disease and risk of liver disease: a general population-based study. Clin Gastroenterol Hepatol. 2007;5(1): 63-69 e61. doi: 10.1016/j.cgh.2006.09.034.
  13. Maksimović J, Djurić Z. The Association of Celiac Disease with Other Autoimmune Diseases in Children. Facta Universitatis, Series: Medicine and Biology. 2017:023. doi: 10.22190/fumb170707009m.
  14. Matteoni CA, Goldblum JR, Wang N, et al. Celiac Disease Is Highly Prevalent in Lymphocytic Colitis. J Clin Gastroenterol. 2001;32(3):225-227. doi: 10.1097/00004836-200103000-00009.
  15. Naiyer AJ, Shah J, Hernandez L, et al. Tissue transglutaminase antibodies in individuals with celiac disease bind to thyroid follicles and extracellular matrix and may contribute to thyroid dysfunction. Thyroid. 2008;18(11):1171-1178. doi: 10.1089/thy.2008.0110.
  16. Parzanese I, Qehajaj D, Patrinicola F, et al. Celiac disease: From pathophysiology to treatment. World J Gastrointest Pathophysiol. 2017;8(2):27-38. doi: 10.4291/wjgp.v8.i2.27.
  17. Schrumpf E, Abdelnoor M, Fausa O, et al. Risk factors in primary sclerosing cholangitis. J Hepatol. 1994;21(6):1061-1066. doi: 10.1016/s0168-8278(05)80618-x.
  18. Stewart M, Andrews CN, Urbanski S, et al. The association of coeliac disease and microscopic colitis: a large population-based study. Aliment Pharmacol Ther. 2011;33(12):1340-1349. doi: 10.1111/j.1365-2036.2011.04666.x.
  19. Vajro P, Paolella G, Maggiore G, Giordano G. Pediatric celiac disease, cryptogenic hypertransaminasemia, and autoimmune hepatitis. J Pediatr Gastroenterol Nutr. 2013;56(6):663-670. doi: 10.1097/MPG.0b013e31828dc5c5.
  20. Villalta D, Girolami D, Bidoli E, et al. High prevalence of celiac disease in autoimmune hepatitis detected by anti-tissue tranglutaminase autoantibodies. J Clin Lab Anal. 2005;19(1):6-10. doi: 10.1002/jcla.20047.

Supplementary files

Supplementary Files Action
1.
Fig. 1. Frequency of “classical” autoimmune gastritis in the examined groups

Download (20KB) Indexing metadata

Statistics

Views

Abstract - 340

PDF (Russian) - 126

PDF (English) - 31

Cited-By


Article Metrics

Metrics Loading ...

PlumX

Dimensions


Copyright (c) 2018 Novikova V.P., Shapovalova N.S., Revnova M.O., Melnikova V.F., Lapin S.V., Guseva V.I., Gurina O.P., Dementieva E.A., Klikunova K.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies