The oesophageal string test: A novel, minimally invasive method measures mucosal inflammation in eosinophilic oesophagitis

Gut

Volumn 62, Issue 10, 2013, Pages 1395-1405

  Furuta, Glenn T ^a,b,c,d   Kagalwalla, Amir F ^e,f   Lee, James J ^g   Alumkal, Preeth ^h   Maybruck, Brian T ^h   Fillon, Sophie ^a,b,c   Masterson, Joanne C ^a,b,c   Ochkur, Sergei ^g   Protheroe, Cheryl ^g   Moore, Wendy ^a,b,c,d   Pan, Zhaoxing ^a,c   Amsden, Katie ^e   Robinson, Zachary ^a,b   Capocelli, Kelley ^a,b   Mukkada, Vince ^a,b,c   Atkins, Dan ^a,d   Fleischer, David ^a,d   Hosford, Lindsay ^a,b,c   Kwatia, Mark A ^h   Schroeder, Shauna ^a,b,c   Kelly, Caleb ^a,b   Lovell, Mark ^a,b   Melin Aldana, Hector ^e   Ackerman, Steven J ^h   more..

^a Children's Hospital Colorado   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c CHILDREN S HOSPITAL COLORADO   (United States)

^d DEPARTMENT OF MEDICINE   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

^f Jr Hospital of Cook County   (United States)

^g MAYO GRADUATE SCHOOL   (United States)

^h UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; EOSINOPHIL PEROXIDASE;

ADOLESCENT; ADULT; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGNOSTIC TEST; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; DIGESTIVE DIAGNOSTIC DEVICE; EOSINOPHIL; EOSINOPHILIC ESOPHAGITIS; ESOPHAGEAL STRING TEST; ESOPHAGUS BIOPSY; ESOPHAGUS MUCOSA; GASTROESOPHAGEAL REFLUX; HUMAN; HUMAN TISSUE; MINIMALLY INVASIVE PROCEDURE; PRIORITY JOURNAL; REMISSION; SCHOOL CHILD;

ALLERGY; BREAST MILK; CHILDHOOD NUTRITION; ENTEROTEST STRING TEST; EOSINOPHIL; EPITHELIAL BARRIER; GASTROINTESTINAL TRACT; INFLAMMATION; OESOPHAGEAL DISEASE; OESOPHAGEAL DISORDERS; OESOPHAGEAL LESIONS; OESOPHAGEAL REFLUX; OESOPHAGEAL STRICTURES; OESOPHAGITIS; PEDIATRIC;

ADOLESCENT; BIOLOGICAL MARKERS; BIOPSY; CHILD; DIAGNOSIS, DIFFERENTIAL; EOSINOPHIL GRANULE PROTEINS; EOSINOPHILIC ESOPHAGITIS; ESOPHAGUS; GASTROESOPHAGEAL REFLUX; GLYCOPROTEINS; HUMANS; LYSOPHOSPHOLIPASE; MUCOSITIS; MUCOUS MEMBRANE; SENSITIVITY AND SPECIFICITY; SPECIMEN HANDLING; YOUNG ADULT;

EID: 84884283090     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2012-303171     Document Type: Article

References (49)

1. Furuta GT, Liacouras CA, Collins MH, et al. Eosinophilic esophagitis in children and adults: a systematic review and consensus recommendations for diagnosis and treatment. Gastroenterology 2007;133:1342-63.
2. Liacouras CA, Furuta GT, Hirano I, et al. Eosinophilic esophagitis: updated consensus recommendations for children and adults. J Allergy Clin Immunol 2011;128:3-20. e6.
3. Kephart GM, Alexander JA, Arora AS, et al. Marked deposition of eosinophil-derived neurotoxin in adult patients with eosinophilic esophagitis. Am J Gastroenterol 2010;105:298-307.
4. Mueller S, Aigner T, Neureiter D, et al. Eosinophil infiltration and degranulation in oesophageal mucosa from adult patients with eosinophilic oesophagitis: a Armstrong and Jo Anne Newton), research assistants (Rachel Harris, Alyson Yeckes, Joseph Ruybal, Katherine Dunne), pathology staff (Sara Garza) and endoscopy technical staff (Bill Markovich) who contributed to this work by helping to provide and collect samples and recruit subjects. We thank Shikha Sundaram, David Brumbaugh and Sean Colgan for their helpful comments on the manuscript development and Len Ross for his insights in this study. We are grateful to our patients and families who consented to be a part of this study. retrospective and comparative study on pathological biopsy. J Clin Pathol 2006;59:1175-80.
5. Mueller S, Neureiter D, Aigner T, et al. Comparison of histological parameters for the diagnosis of eosinophilic oesophagitis versus gastro-oesophageal reflux disease on oesophageal biopsy material. Histopathology 2008;53:676-84. (Pubitemid 352768719)
6. Protheroe C, Woodruff SA, De Petris G, et al. A novel histologic scoring system to evaluate mucosal biopsies from patients with eosinophilic esophagitis. Clin Gastroenterol Hepatol 2009;7:749-55. e11.
7. Ackerman SJ, Liu L, Kwatia MA, et al. Charcot-Leyden crystal protein (galectin-10) is not a dual function galectin with lysophospholipase activity but binds a lysophospholipase inhibitor in a novel structural fashion. J Biol Chem 2002;277:14859-68. (Pubitemid 34952559)
8. Dvorak AM, Letourneau L, Login GR, et al. Ultrastructural localization of the Charcot-Leyden crystal protein (lysophospholipase) to a distinct crystalloid-free granule population in mature human eosinophils. Blood 1988;72:150-8.
9. Aceves SS, Ackerman SJ. Relationships between eosinophilic inflammation, tissue remodeling, and fibrosis in eosinophilic esophagitis. Immunol Allergy Clin North Am 2009;29:197-211, xiii-xiv.
10. Aceves SS, Broide DH. Airway fibrosis and angiogenesis due to eosinophil trafficking in chronic asthma. Curr Mol Med 2008;8:350-8.
11. Kagalwalla AF, Akhtar N, Woodruff SA, et al. Eosinophilic esophagitis: epithelial mesenchymal transition contributes to esophageal remodeling and reverses with treatment. J Allergy Clin Immunol 2012;129:1387-96. e7.
12. Pegorier S, Wagner LA, Gleich GJ, et al. Eosinophil-derived cationic proteins activate the synthesis of remodeling factors by airway epithelial cells. J Immunol 2006;177:4861-9. (Pubitemid 44469822)
13. Konikoff MR, Blanchard C, Kirby C, et al. Potential of blood eosinophils, eosinophil-derived neurotoxin, and eotaxin-3 as biomarkers of eosinophilic esophagitis. Clin Gastroenterol Hepatol 2006;4:1328-36. (Pubitemid 44716743)
14. Gupta SK. Noninvasive markers of eosinophilic esophagitis. Gastrointest Endosc Clin NAm 2008;18:157-67; xi. (Pubitemid 350166937)
15. Subbarao G, Rosenman MB, Ohnuki L, et al. Exploring potential non-invasive biomarkers in eosinophilic esophagitis: a longitudinal study in children. J Pediatr Gastroenterol Nutr 2011;53:651-8.
16. Thomas GE, Goldsmid JM, Wicks AC. Use of the enterotest duodenal capsule in the diagnosis of giardiasis. A preliminary study. S Afr Med J 1974;48:2219-20.
17. Gracey M, Suharjono, Sunoto. Use of a simple duodenal capsule to study upper intestinal microflora. Arch Dis Child 1977;52:74-6. (Pubitemid 8066360)
18. Beukeveld GJ, Bijleveld CM, Kuipers F, et al. Evaluation and clinical application of the Enterotest for the determination of human biliary porphyrin composition. Eur J Clin Chem Clin Biochem 1995;33:453-62.
19. Liebman WM, Rosenthal P. The string test for gastroesophageal reflux. Am J Dis Child 1980;134:775-6. (Pubitemid 10046512)
20. Ackerman SJ, Loegering DA, Venge P, et al. Distinctive cationic proteins of the human eosinophil granule: major basic protein, eosinophil cationic protein, and eosinophil-derived neurotoxin. J Immunol 1983;131:2977-82. (Pubitemid 14207333)
21. Ackerman SJ, Corrette SE, Rosenberg HF, et al. Molecular cloning and characterization of human eosinophil Charcot-Leyden crystal protein (lysophospholipase). Similarities to IgE binding proteins and the S-type animal lectin superfamily. J Immunol 1993;150:456-68. (Pubitemid 23133621)
22. Swaminathan GJ, Weaver AJ, Loegering DA, et al. Crystal structure of the eosinophil major basic protein at 1.8 A. An atypical lectin with a paradigm shift in specificity. J Biol Chem 2001;276:26197-203.
23. Ochkur SI, Kim JD, Protheroe CA, et al. The development of a sensitive and specific ELISA for mouse eosinophil peroxidase: assessment of eosinophil degranulation ex vivo and in models of human disease. J Immunol Methods 2012;375:138-47.
24. Walsh S, Antonioli D, Goldman H, et al. Allergic esophagitis in children: a clinicopathological entity. Am J Surg Pathol 1999;23:390-6. (Pubitemid 29159999)
25. Fox VL, Nurko S, Teitelbaum JE, et al. High-resolution EUS in children with eosinophilic "allergic" esophagitis. Gastrointest Endosc 2003;57:30-6. (Pubitemid 36236795)
26. Kwiatek MA, Hirano I, Kahrilas PJ, et al. Mechanical properties of the esophagus in eosinophilic esophagitis. Gastroenterology 2011;140:82-90.
27. Nurko S, Rosen R, Furuta GT. Esophageal dysmotility in children with eosinophilic esophagitis: a study using prolonged esophageal manometry. Am J Gastroenterol 2009;104:3050-7.
28. Balbi B, Pignatti P, Corradi M, et al. Bronchoalveolar lavage, sputum and exhaled clinically relevant inflammatory markers: values in healthy adults. Eur Respir J 2007;30:769-81. (Pubitemid 351194840)
29. Katial R. Biomarkers for nononcologic gastrointestinal diseases. Immunol Clin NA 2009;29:119-27; xi.
30. Leonardi A. In-vivo diagnostic measurements of ocular inflammation. Curr Opin Allergy Clin Immunol 2005;5:464-72. (Pubitemid 41345318)
31. Gleich GJ, Adolphson C. Bronchial hyperreactivity and eosinophil granule proteins. Agents Actions Suppl 1993;43:223-30. (Pubitemid 23210133)
32. Koh GC, Shek LP, Goh DY, et al. Eosinophil cationic protein: is it useful in asthma? A systematic review. Respir Med 2007;101:696-705. (Pubitemid 46335585)
33. Leonardi A, Borghesan F, Faggian D, et al. Eosinophil cationic protein in tears of normal subjects and patients affected by vernal keratoconjunctivitis. Allergy 1995;50:610-13.
34. Trocme SD, Aldave AJ. The eye and the eosinophil. Surv Ophthalmol 1994;39:241-52. (Pubitemid 24370151)
35. Udell IJ, Gleich GJ, Allansmith MR, et al. Eosinophil granule major basic protein and Charcot-Leyden crystal protein in human tears. Am J Ophthalmol 1981;92:824-8. (Pubitemid 12245757)
36. Von Ungern-Sternberg BS, Sly PD, Loh RK, et al. Value of eosinophil cationic protein and tryptase levels in bronchoalveolar lavage fluid for predicting lung function impairment in anaesthetised, asthmatic children. Anaesthesia 2006;61:1149-54. (Pubitemid 44697852)
37. Peters MS, Schroeter AL, Kephart GM, et al. Localization of eosinophil granule major basic protein in chronic urticaria. J Invest Dermatol 1983;81:39-43. (Pubitemid 13072431)
38. Leiferman KM, Ackerman SJ, Sampson HA, et al. Dermal deposition of eosinophil-granule major basic protein in atopic dermatitis. Comparison with onchocerciasis. N Engl J Med 1985;313:282-5. (Pubitemid 15044229)
39. Furuta GT, Nieuwenhuis EE, Karhausen J, et al. Eosinophils alter colonic epithelial barrier function: role for major basic protein. Am J Physiol Gastrointest Liver Physiol 2005;289:G890-7. (Pubitemid 41532582)
40. Jacobsen EA, Taranova AG, Lee NA, et al. Eosinophils: singularly destructive effector cells or purveyors of immunoregulation? J Allergy Clin Immunol 2007;119:1313-20. (Pubitemid 46855871)
41. Blanchard C, Stucke EM, Burwinkel K, et al. Coordinate interaction between IL-13 and epithelial differentiation cluster genes in eosinophilic esophagitis. J Immunol 2010;184:4033-41.
42. Abonia JP, Blanchard C, Butz BB, et al. Involvement of mast cells in eosinophilic esophagitis. J Allergy Clin Immunol 2010;126:140-9.
43. Abu-Ghazaleh RI, Dunnette SL, Loegering DA, et al. Eosinophil granule proteins in peripheral blood granulocytes. J Leukoc Biol 1992;52:611-18. (Pubitemid 23016034)
44. Aceves SS, Chen D, Newbury RO, et al. Mast cells infiltrate the esophageal smooth muscle in patients with eosinophilic esophagitis, express TGF-beta1, and increase esophageal smooth muscle contraction. J Allergy Clin Immunol 2010;126:1198-204; e4.
45. Ackerman SJ, Kephart GM, Habermann TM, et al. Localization of eosinophil granule major basic protein in human basophils. J Exp Med 1983;158:946-61. (Pubitemid 13051356)
46. Ackerman SJ, Weils GJ, Gleich GJ. Formation of Charcot-Leyden Crystals by human basophils. J Exp Med 1982;155:1597-609. (Pubitemid 12074201)
47. Butterfield JH, Weiler D, Peterson EA, et al. Sequestration of eosinophil major basic protein in human mast cells. Lab Invest 1990;62:77-86. (Pubitemid 20039526)
48. Kubach J, Lutter P, Bopp T, et al. Human CD4+CD25+ regulatory T cells: proteome analysis identifies galectin-10 as a novel marker essential for their anergy and suppressive function. Blood 2007;110:1550-8. (Pubitemid 47443971)
49. Monteseirin J, Vega A, Chacon P, et al. Neutrophils as a novel source of eosinophil cationic protein in IgE-mediated processes. J Immunol 2007;179:2634-41.