Dmitrieva YuA, Zakharova IN, Zaplatnikov AL, Radchenko ER, Epifanova EI, Abdurakhmanova LS, Pokhvashcheva PYu. Collagenous enteritis as a rare cause of exudative enteropathy in a child. Case report. Pediatrics. Consilium Medicum. 2024;2:138–144. DOI: 10.26442/26586630.2024.2.202925
Коллагеновый энтерит как редкая причина экссудативной энтеропатии у ребенка
Дмитриева Ю.А., Захарова И.Н., Заплатников А.Л., Радченко Е.Р., Епифанова Е.И., Абдурахманова Л.С., Похващева П.Ю. Коллагеновый энтерит как редкая причина экссудативной энтеропатии у ребенка. Педиатрия. Consilium Medicum. 2024;2:138–144. DOI: 10.26442/26586630.2024.2.202925
Dmitrieva YuA, Zakharova IN, Zaplatnikov AL, Radchenko ER, Epifanova EI, Abdurakhmanova LS, Pokhvashcheva PYu. Collagenous enteritis as a rare cause of exudative enteropathy in a child. Case report. Pediatrics. Consilium Medicum. 2024;2:138–144. DOI: 10.26442/26586630.2024.2.202925
Синдром экссудативной энтеропатии (ЭЭ) может сопровождать различные заболевания желудочно-кишечного тракта (ЖКТ) и проявляется отечным синдромом, гипопротеинемией, гипоальбуминемией, лимфопенией, гипогаммаглобулинемией и повышением концентрации α-1-антитрипсина в кале. Потеря белка через ЖКТ может отмечаться при более чем 60 патологических состояниях, включая эрозивно-язвенные заболевания ЖКТ, неэрозивные поражения слизистой оболочки, приводящие к увеличению проницаемости кишечной стенки, а также заболевания, сопровождающиеся повышением давления в лимфатической системе. Корректная диагностика и своевременная заместительная и патогенетическая терапия лежат в основе быстрого прекращения патологических потерь, восстановления протеинограммы и предотвращения жизнеугрожающих осложнений. Одним из редких заболеваний тонкой кишки, сопровождающимся синдромом ЭЭ, является коллагеновый энтерит. В статье представлена клиническая демонстрация ребенка раннего возраста с ЭЭ на фоне течения коллагенового энтерита. Обсуждены этапы диагностического поиска при выявлении у ребенка синдрома ЭЭ, рассмотрены патогенетические факторы, определившие развитие данного патологического состояния.
Exudative enteropathy (EE) syndrome can be associated with various diseases of the gastrointestinal tract (GIT) and is manifested by edematous syndrome, hypoproteinemia, hypoalbuminemia, lymphocytopenia, hypogammaglobulinemia, and an increase in the level of α-1-antitrypsin in the feces. More than 60 medical conditions are associated with loss of protein through the gastrointestinal tract, including erosive-ulcerative diseases of the gastrointestinal tract, non-erosive lesions of the mucous membrane causing an increase in the permeability of the intestinal wall, as well as disorders with an increase in pressure in the lymphatic system. Correct diagnosis and timely replacement and pathogenetic therapy are essential for the rapid cessation of pathological losses, the recovery of the proteinogram, and the prevention of life-threatening complications. Collagenous enteritis is one of the rare diseases of the small intestine associated with EE syndrome. The article presents a clinical case of a young child with EE and collagenous enteritis. The stages of the diagnostic workup in detecting EE syndrome in the child are discussed, and the pathogenetic factors that determined the development of this disorder are considered.
Keywords: children, early age, proteinogram, total protein, albumin, hypoproteinemia, hypoalbuminemia, hypogammaglobulinemia, α-1-antitrypsin, exudative enteropathy, collagenous enteropathy, atrophic enteropathy, celiac disease
1. Elli L, Topa M, Rimondi A. Protein-losing enteropathy. Curr Opin Gastroenterol. 2020;36(3):238-44. DOI:10.1097/MOG.0000000000000629
2. Umar SB, Dibaise JK. Protein-losing enteropathy: case illustrations and clinical review. Am J Gastroenterol. 2010;105:43-9. DOI:10.1038/ajg.2009.561
3. Strygler B, Nicar MJ, Santangelo WC, et al. a1-antitrypsin excretion in stool in normal subjects and in patients with gastrointestinal disorders. Gastroenterology. 1990;99:1380-7. DOI:10.1016/0016-5085(90)91165-3
4. Levitt DG, Levitt MD. Protein losing enteropathy: comprehensive review of the mechanistic association with clinical and subclinical disease states. Clin Exp Gastroenterol. 2017;10:147-68. DOI:10.2147/CEG.S136803
5. Levitt DG, Levitt MD. Human serum albumin homeostasis: a new look at the roles of synthesis, catabolism, renal and gastrointestinal excretion, and the clinical value of serum albumin measurements. Int J Gen Med. 2016;9:229-55. DOI:10.2147/IJGM.S102819
6. Nagra N, Dang S. Protein-Losing Enteropathy. 2023 Jun 12. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2024 Jan.
7. Braamskamp MJ, Dolman KM, Tabbers MM. Clinical practice. Protein-losing enteropathy in children. Eur J Pediatr. 2010;169(10):1179-85. DOI:10.1007/s00431-010-1235-2
8. Vignes S, Bellanger J. Primary intestinal lymphangiectasia (Waldmann’s disease). Orphanet J Rare Dis. 2008;3:5-1172-3-5. DOI:10.1038/ajg.2009.561
9. Ellia L, Topaa T, Rimondia A. Protein-losing enteropathy. Curr Opin Gastroenterol. 2020;36:238-44. DOI:10.1097/MOG.0000000000000629
10. Perrineau S, Cazals-Hatem D, Zarrouk V, et al. Cytomegalovirus-associated protein-losing enteropathy in a healthy man. Med Mal Infect.
2017;47(8):562-5. DOI:10.1016/j.medmal.2017.07.003
11. Lopez RN, Day AS. Primary intestinal lymphangiectasia in children: A review. J Paediatr Child Health. 2020;56(11):1719-23. DOI:10.1111/jpc.14837
12. Fritscher-Ravens A, Scherbakov P, Bufler P, et al. The feasibility of wireless capsule endoscopy in detecting small intestinal pathology in children under the age of 8 years: a multicentre European study. Gut. 2009;58(11):1467-72. DOI:10.1136/gut.2009.177774
13. Desai AP, Guvenc BH, Carachi R. Evidence for medium chain triglycerides in the treatment of primary intestinal lymphangiectasia. Eur J Pediatr Surg.
2009;19(4):241-5. DOI:10.1055/s-0029-1216389
14. Lee HL, Han DS, Kim JB, et al. Successful treatment of protein-losing enteropathy induced by intestinal lymphangiectasia in a liver cirrhosis patient with octreotide: a case report. J Korean Med Sci. 2004;19(3):466-9. DOI:10.3346/jkms.2004.19.3.466
15. Hoashi T, Ichikawa H, Ueno T, et al. Steroid pulse therapy for protein-losing enteropathy after the Fontan operation. Congenit Heart Dis. 2009;4(4):284-7.
DOI:10.1111/j.1747-0803.2009.00274.x
16. Martins CR, Gagnaire A, Rostain F, et al. Waldmann’s disease: a rare cause of protein losing enteropathy in an adult patient. Rev Esp Enferm Dig.
2017;109(5):385-8. DOI:10.17235/reed.2017.4593/2016
17. Vignes S, Bellanger J. Primary intestinal lymphangiectasia (Waldmann’s disease). Orphanet J Rare Dis. 2008;3:5. DOI:10.1186/1750-1172-3-5
18. Ingle SB, Hinge Ingle CR. Primary intestinal lymphangiectasia: Minireview. World J Clin Cases. 2014;2(10):528-33. DOI:10.12998/wjcc.v2.i10.528
19. Schein J. Syndrome on non tropical sprue with hitherto undescribed lesions of the intestine. Gastroenterology. 1947;8:438-60.
20. Weinstein WM, Saunders DR, Tytgat GN, et al. Collagenous sprue – an unrecognized type of malabsorption. N Engl J Med.
1970;283(24):1297-301. DOI:10.1056/NEJM197012102832401
21. van Gils T, van de Donk T, Bouma G, et al. The first cases of collagenous sprue successfully treated with thioguanine. BMJ Open Gastroenterol. 2016;3(1):e000099. DOI:10.1136/bmjgast-2016-000099
22. Lan N, Shen B, Yuan L, et al. Comparison of clinical features, treatment, and outcomes of collagenous sprue, celiac disease, and collagenous colitis. J Gastroenterol Hepatol. 2017;32(1):120-7. DOI:10.1111/jgh.13592
23. Zhao X, Johnson RL. Collagenous sprue: a rare, severe small-bowel malabsorptive disorder. Arch Pathol Lab Med. 2011;135(6):803-9. DOI:10.5858/2010-0028-RS.1
24. Rustagi T, Rai M, Scholes JV. Collagenous gastroduodenitis. J Clin Gastroenterol. 2011;45:794-9. DOI:10.1097/MCG.0b013e31820c6018
25. Maguire AA, Greenson JK, Lauwers GY, et al. Collagenous sprue: a clinicopathologic study of 12 cases. Am J Surg Pathol. 2009;33:1440-9. DOI:10.1097/PAS.0b013e3181ae2545
26. Freeman HJ. Collagenous sprue. Can J Gastroenterol. 2011;25(4):189-92. DOI:10.1155/2011/821976
27. Nielsen OH, Riis LB, Danese S, et al. Proximal collagenous gastroenteritides: clinical management. A systematic review. Ann Med.
2014;46(5):311-7. DOI:10.3109/07853890.2014.899102
28. Cuoco L, Villanacci V, Salvagnini, et al. Collagenous sprue with associated features of refractory celiac disease. Rev Esp Enferm Dig. 2012;104(4):223-5.
DOI:10.4321/s1130-01082012000400015
29. Kung VL, Liu TC, Ma C. Collagenous Enteritis is Unlikely a Form of Aggressive Celiac Disease Despite Sharing HLA-DQ2/DQ8 Genotypes. Am J Surg Pathol. 2018;42(4):545-52. DOI:10.1097/PAS.0000000000001022
30. Daniels JA, Lederman HM, Maitra A, et al. Gastrointestinal tract pathology in patients with common variable immunodeficiency (CVID): a clinicopathologic study and review. Am J Surg Pathol. 2007;31(12):1800-12. DOI:10.1097/PAS.0b013e3180cab60c
31. Freeman HJ, Berean KW. Resolution of paraneoplastic collagenous enterocolitis after resection of colon cancer. Can J Gastroenterol. 2006;20(5):357-60. DOI:10.1155/2006/893928
32. Cellier C, Delabesse E, Helmer C, et al. Refractory sprue, coeliac disease, and enteropathy-associated T-cell lymphoma. French Coeliac Disease Study Group. Lancet. 2000;356(9225):203-8. DOI:10.1016/s0140-6736(00)02481-8
33. Desruisseaux C, Bensoussan M, Désilets E, et al. Adding Water to the Mill: Olmesartan-Induced Collagenous Sprue – A Case Report and Brief Literature Review. Can J Gastroenterol Hepatol. 2016;2016:4837270. DOI:10.1155/2016/4837270
34. Nielsen JA, Steephen A, Lewin M. Angiotensin-II inhibitor (olmesartan)-induced collagenous sprue with resolution following discontinuation of drug. World J Gastroenterol. 2013;19(40):6928-30. DOI:10.3748/wjg.v19.i40.6928
35. Vasant DH, Hayes S, Bucknall R, et al. Clinical and histological resolution of collagenous sprue following gluten-free diet and discontinuation of non-steroidal anti-inflammatory drugs (NSAIDs). BMJ Case Rep. 2013;2013:bcr2013200097. DOI:10.1136/bcr-2013-200097
36. Mirakhor E, Choe J, Goodman RI. Collagenous Enteritis – An Alternative Cause of Malabsorptive Enteropathy. Ann Colorectal Res.
2021;9(2):78-81. DOI:10.30476/ACRR.2021.91296.1100
________________________________________________
1. Elli L, Topa M, Rimondi A. Protein-losing enteropathy. Curr Opin Gastroenterol. 2020;36(3):238-44. DOI:10.1097/MOG.0000000000000629
2. Umar SB, Dibaise JK. Protein-losing enteropathy: case illustrations and clinical review. Am J Gastroenterol. 2010;105:43-9. DOI:10.1038/ajg.2009.561
3. Strygler B, Nicar MJ, Santangelo WC, et al. a1-antitrypsin excretion in stool in normal subjects and in patients with gastrointestinal disorders. Gastroenterology. 1990;99:1380-7. DOI:10.1016/0016-5085(90)91165-3
4. Levitt DG, Levitt MD. Protein losing enteropathy: comprehensive review of the mechanistic association with clinical and subclinical disease states. Clin Exp Gastroenterol. 2017;10:147-68. DOI:10.2147/CEG.S136803
5. Levitt DG, Levitt MD. Human serum albumin homeostasis: a new look at the roles of synthesis, catabolism, renal and gastrointestinal excretion, and the clinical value of serum albumin measurements. Int J Gen Med. 2016;9:229-55. DOI:10.2147/IJGM.S102819
6. Nagra N, Dang S. Protein-Losing Enteropathy. 2023 Jun 12. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2024 Jan.
7. Braamskamp MJ, Dolman KM, Tabbers MM. Clinical practice. Protein-losing enteropathy in children. Eur J Pediatr. 2010;169(10):1179-85. DOI:10.1007/s00431-010-1235-2
8. Vignes S, Bellanger J. Primary intestinal lymphangiectasia (Waldmann’s disease). Orphanet J Rare Dis. 2008;3:5-1172-3-5. DOI:10.1038/ajg.2009.561
9. Ellia L, Topaa T, Rimondia A. Protein-losing enteropathy. Curr Opin Gastroenterol. 2020;36:238-44. DOI:10.1097/MOG.0000000000000629
10. Perrineau S, Cazals-Hatem D, Zarrouk V, et al. Cytomegalovirus-associated protein-losing enteropathy in a healthy man. Med Mal Infect.
2017;47(8):562-5. DOI:10.1016/j.medmal.2017.07.003
11. Lopez RN, Day AS. Primary intestinal lymphangiectasia in children: A review. J Paediatr Child Health. 2020;56(11):1719-23. DOI:10.1111/jpc.14837
12. Fritscher-Ravens A, Scherbakov P, Bufler P, et al. The feasibility of wireless capsule endoscopy in detecting small intestinal pathology in children under the age of 8 years: a multicentre European study. Gut. 2009;58(11):1467-72. DOI:10.1136/gut.2009.177774
13. Desai AP, Guvenc BH, Carachi R. Evidence for medium chain triglycerides in the treatment of primary intestinal lymphangiectasia. Eur J Pediatr Surg.
2009;19(4):241-5. DOI:10.1055/s-0029-1216389
14. Lee HL, Han DS, Kim JB, et al. Successful treatment of protein-losing enteropathy induced by intestinal lymphangiectasia in a liver cirrhosis patient with octreotide: a case report. J Korean Med Sci. 2004;19(3):466-9. DOI:10.3346/jkms.2004.19.3.466
15. Hoashi T, Ichikawa H, Ueno T, et al. Steroid pulse therapy for protein-losing enteropathy after the Fontan operation. Congenit Heart Dis. 2009;4(4):284-7.
DOI:10.1111/j.1747-0803.2009.00274.x
16. Martins CR, Gagnaire A, Rostain F, et al. Waldmann’s disease: a rare cause of protein losing enteropathy in an adult patient. Rev Esp Enferm Dig.
2017;109(5):385-8. DOI:10.17235/reed.2017.4593/2016
17. Vignes S, Bellanger J. Primary intestinal lymphangiectasia (Waldmann’s disease). Orphanet J Rare Dis. 2008;3:5. DOI:10.1186/1750-1172-3-5
18. Ingle SB, Hinge Ingle CR. Primary intestinal lymphangiectasia: Minireview. World J Clin Cases. 2014;2(10):528-33. DOI:10.12998/wjcc.v2.i10.528
19. Schein J. Syndrome on non tropical sprue with hitherto undescribed lesions of the intestine. Gastroenterology. 1947;8:438-60.
20. Weinstein WM, Saunders DR, Tytgat GN, et al. Collagenous sprue – an unrecognized type of malabsorption. N Engl J Med.
1970;283(24):1297-301. DOI:10.1056/NEJM197012102832401
21. van Gils T, van de Donk T, Bouma G, et al. The first cases of collagenous sprue successfully treated with thioguanine. BMJ Open Gastroenterol. 2016;3(1):e000099. DOI:10.1136/bmjgast-2016-000099
22. Lan N, Shen B, Yuan L, et al. Comparison of clinical features, treatment, and outcomes of collagenous sprue, celiac disease, and collagenous colitis. J Gastroenterol Hepatol. 2017;32(1):120-7. DOI:10.1111/jgh.13592
23. Zhao X, Johnson RL. Collagenous sprue: a rare, severe small-bowel malabsorptive disorder. Arch Pathol Lab Med. 2011;135(6):803-9. DOI:10.5858/2010-0028-RS.1
24. Rustagi T, Rai M, Scholes JV. Collagenous gastroduodenitis. J Clin Gastroenterol. 2011;45:794-9. DOI:10.1097/MCG.0b013e31820c6018
25. Maguire AA, Greenson JK, Lauwers GY, et al. Collagenous sprue: a clinicopathologic study of 12 cases. Am J Surg Pathol. 2009;33:1440-9. DOI:10.1097/PAS.0b013e3181ae2545
26. Freeman HJ. Collagenous sprue. Can J Gastroenterol. 2011;25(4):189-92. DOI:10.1155/2011/821976
27. Nielsen OH, Riis LB, Danese S, et al. Proximal collagenous gastroenteritides: clinical management. A systematic review. Ann Med.
2014;46(5):311-7. DOI:10.3109/07853890.2014.899102
28. Cuoco L, Villanacci V, Salvagnini, et al. Collagenous sprue with associated features of refractory celiac disease. Rev Esp Enferm Dig. 2012;104(4):223-5.
DOI:10.4321/s1130-01082012000400015
29. Kung VL, Liu TC, Ma C. Collagenous Enteritis is Unlikely a Form of Aggressive Celiac Disease Despite Sharing HLA-DQ2/DQ8 Genotypes. Am J Surg Pathol. 2018;42(4):545-52. DOI:10.1097/PAS.0000000000001022
30. Daniels JA, Lederman HM, Maitra A, et al. Gastrointestinal tract pathology in patients with common variable immunodeficiency (CVID): a clinicopathologic study and review. Am J Surg Pathol. 2007;31(12):1800-12. DOI:10.1097/PAS.0b013e3180cab60c
31. Freeman HJ, Berean KW. Resolution of paraneoplastic collagenous enterocolitis after resection of colon cancer. Can J Gastroenterol. 2006;20(5):357-60. DOI:10.1155/2006/893928
32. Cellier C, Delabesse E, Helmer C, et al. Refractory sprue, coeliac disease, and enteropathy-associated T-cell lymphoma. French Coeliac Disease Study Group. Lancet. 2000;356(9225):203-8. DOI:10.1016/s0140-6736(00)02481-8
33. Desruisseaux C, Bensoussan M, Désilets E, et al. Adding Water to the Mill: Olmesartan-Induced Collagenous Sprue – A Case Report and Brief Literature Review. Can J Gastroenterol Hepatol. 2016;2016:4837270. DOI:10.1155/2016/4837270
34. Nielsen JA, Steephen A, Lewin M. Angiotensin-II inhibitor (olmesartan)-induced collagenous sprue with resolution following discontinuation of drug. World J Gastroenterol. 2013;19(40):6928-30. DOI:10.3748/wjg.v19.i40.6928
35. Vasant DH, Hayes S, Bucknall R, et al. Clinical and histological resolution of collagenous sprue following gluten-free diet and discontinuation of non-steroidal anti-inflammatory drugs (NSAIDs). BMJ Case Rep. 2013;2013:bcr2013200097. DOI:10.1136/bcr-2013-200097
36. Mirakhor E, Choe J, Goodman RI. Collagenous Enteritis – An Alternative Cause of Malabsorptive Enteropathy. Ann Colorectal Res.
2021;9(2):78-81. DOI:10.30476/ACRR.2021.91296.1100
1ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Россия; 2ГБУЗ «Детская городская клиническая больница им. З.А. Башляевой» Департамента здравоохранения г. Москвы, Москва, Россия; 3ФГБУ «Детский медицинский центр» Управления делами Президента РФ, Москва, Россия; 4ФГАОУ ВО «Российский национальный исследовательский медицинский университет им. Н.И. Пирогова» Минздрава России, Москва, Россия
*jadmitrieva@mail.ru
________________________________________________
Yulia A. Dmitrieva*1,2, Irina N. Zakharova1, Andrey L. Zaplatnikov1, Elena R. Radchenko2, Elena I. Epifanova2, Lala S. Abdurakhmanova3, Polina Yu. Pokhvashcheva4
1Russian Medical Academy of Continuous Professional Education, Moscow, Russia; 2Bashlyaeva Children’s City Clinical Hospital, Moscow, Russia; 3Children’s Medical Center, Moscow, Russia; 4Pirogov Russian National Research Medical University, Moscow, Russia
*jadmitrieva@mail.ru