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Published in: Clinical and Translational Allergy 1/2014

Open Access 01-12-2014 | Research

Intestinal allergic inflammation in birch pollen allergic patients in relation to pollen season, IgE sensitization profile and gastrointestinal symptoms

Authors: Georgios Rentzos, Vanja Lundberg, Per-Ove Stotzer, Teet Pullerits, Esbjörn Telemo

Published in: Clinical and Translational Allergy | Issue 1/2014

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Abstract

Background

Birch pollen allergic patients frequently experience gastrointestinal upset accompanied by a local allergic inflammation in the small intestine especially during the pollen season. However, it is not known if the GI pathology is connected to the subjective symptoms of the patient. The objective of this study was to evaluate the immune pathology of the duodenal mucosa and the serum IgE antibody profiles in birch pollen allergic patients in relation to their gastrointestinal symptoms, during and outside the birch pollen season.

Methods

Thirty-two patients with birch pollen allergy and sixteen healthy controls were enrolled in the study. Twenty allergic patients had gastrointestinal symptoms and twelve did not. All participants underwent an allergy investigation and gastroscopy with duodenal biopsy. The duodenal biopsies were retrieved during the pollen season (May-June) and off-season (November-March). The biopsies were immunostained for mast cells (IgE and tryptase), eosinophils, T cells (CD3), and dendritic cells (CD11c). Pollen-specific IgE antibodies were determined by ImmunoCAP and component microarray (ISAC).

Results

Patients in both pollen allergic groups showed similar degree of intestinal allergic inflammation during the pollen season regardless of gastrointestinal symptoms. The eosinophils, mast cells and dendritic cells were increased in the mucosa. Patients with gastrointestinal symptoms had significantly elevated IgE antibodies to birch (rBet v 1), hazelnut (rCor a 1), and apple (rMal d1) during the pollen season.

Conclusions

Patients allergic to birch pollen have clear signs of an ongoing allergic inflammation in their intestinal mucosa, which is aggravated during the pollen season. The magnitude of the allergic intestinal inflammation is not associated with subjective gastrointestinal symptoms of the individual patient.
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Literature
1.
go back to reference Magnusson J, Lin XP, Dahlman-Hoglund A, Hanson LL, Telemo E, Magnusson O, Bengtsson U, Ahlstedt S: Seasonal intestinal inflammation in patients with birch pollen allergy. J Allergy Clin Immunol. 2003, 112 (1): 45-50. 10.1067/mai.2003.1604. Epub 2003/07/09CrossRefPubMed Magnusson J, Lin XP, Dahlman-Hoglund A, Hanson LL, Telemo E, Magnusson O, Bengtsson U, Ahlstedt S: Seasonal intestinal inflammation in patients with birch pollen allergy. J Allergy Clin Immunol. 2003, 112 (1): 45-50. 10.1067/mai.2003.1604. Epub 2003/07/09CrossRefPubMed
2.
go back to reference Caffarelli C, Romanini E, Caruana P, Street ME, de’ Angelis G: Clinical food hypersensitivity: the relevance of duodenal immunoglobulin E-positive cells. Pediatr Res. 1998, 44 (4): 485-490. 10.1203/00006450-199810000-00004. Epub 1998/10/17CrossRefPubMed Caffarelli C, Romanini E, Caruana P, Street ME, de’ Angelis G: Clinical food hypersensitivity: the relevance of duodenal immunoglobulin E-positive cells. Pediatr Res. 1998, 44 (4): 485-490. 10.1203/00006450-199810000-00004. Epub 1998/10/17CrossRefPubMed
3.
go back to reference Knutson TW, Bengtsson U, Dannaeus A, Ahlstedt S, Stalenheim G, Hallgren R, Knutson L: Intestinal reactivity in allergic and nonallergic patients: an approach to determine the complexity of the mucosal reaction. J Allergy Clin Immunol. 1993, 91 (2): 553-559. 10.1016/0091-6749(93)90261-D. Epub 1993/02/01CrossRefPubMed Knutson TW, Bengtsson U, Dannaeus A, Ahlstedt S, Stalenheim G, Hallgren R, Knutson L: Intestinal reactivity in allergic and nonallergic patients: an approach to determine the complexity of the mucosal reaction. J Allergy Clin Immunol. 1993, 91 (2): 553-559. 10.1016/0091-6749(93)90261-D. Epub 1993/02/01CrossRefPubMed
4.
go back to reference Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Muller-Lissner SA: Functional bowel disorders and functional abdominal pain. Gut. 1999, 45 (Suppl 2): II43-II47. Epub 1999/08/24PubMedCentralPubMed Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Muller-Lissner SA: Functional bowel disorders and functional abdominal pain. Gut. 1999, 45 (Suppl 2): II43-II47. Epub 1999/08/24PubMedCentralPubMed
5.
go back to reference Lillestol K, Helgeland L, Arslan Lied G, Florvaag E, Valeur J, Lind R, Berstad A: Indications of ‘atopic bowel’ in patients with self-reported food hypersensitivity. Aliment Pharmacol Ther. 31 (10): 1112-1122. Epub 2010/02/19 Lillestol K, Helgeland L, Arslan Lied G, Florvaag E, Valeur J, Lind R, Berstad A: Indications of ‘atopic bowel’ in patients with self-reported food hypersensitivity. Aliment Pharmacol Ther. 31 (10): 1112-1122. Epub 2010/02/19
6.
go back to reference Tobin MC, Keshavazian A, Farhardi A: Atopic irritable bowel syndrome: same old hat or a new entity?. Expert Rev Gastroenterol Hepatol. 2008, 2 (4): 457-459. 10.1586/17474124.2.4.457. Epub 2008/12/17CrossRefPubMed Tobin MC, Keshavazian A, Farhardi A: Atopic irritable bowel syndrome: same old hat or a new entity?. Expert Rev Gastroenterol Hepatol. 2008, 2 (4): 457-459. 10.1586/17474124.2.4.457. Epub 2008/12/17CrossRefPubMed
7.
go back to reference Tobin MC, Moparty B, Farhadi A, DeMeo MT, Bansal PJ, Keshavarzian A: Atopic irritable bowel syndrome: a novel subgroup of irritable bowel syndrome with allergic manifestations. Ann Allergy Asthma Immunol. 2008, 100 (1): 49-53. 10.1016/S1081-1206(10)60404-8. Epub 2008/02/08CrossRefPubMed Tobin MC, Moparty B, Farhadi A, DeMeo MT, Bansal PJ, Keshavarzian A: Atopic irritable bowel syndrome: a novel subgroup of irritable bowel syndrome with allergic manifestations. Ann Allergy Asthma Immunol. 2008, 100 (1): 49-53. 10.1016/S1081-1206(10)60404-8. Epub 2008/02/08CrossRefPubMed
8.
go back to reference Moawad FJ, Veerappan GR, Lake JM, Maydonovitch CL, Haymore BR, Kosisky SE, Wong RK: Correlation between eosinophilic oesophagitis and aeroallergens. Aliment Pharmacol Ther. 2010, 31 (4): 509-515. 10.1111/j.1365-2036.2009.04199.x. Epub 2009/11/21CrossRefPubMed Moawad FJ, Veerappan GR, Lake JM, Maydonovitch CL, Haymore BR, Kosisky SE, Wong RK: Correlation between eosinophilic oesophagitis and aeroallergens. Aliment Pharmacol Ther. 2010, 31 (4): 509-515. 10.1111/j.1365-2036.2009.04199.x. Epub 2009/11/21CrossRefPubMed
9.
go back to reference Liacouras CA, Ruchelli E: Eosinophilic esophagitis. Curr Opin Pediatr. 2004, 16 (5): 560-566. 10.1097/01.mop.0000141071.47572.eb. Epub 2004/09/16CrossRefPubMed Liacouras CA, Ruchelli E: Eosinophilic esophagitis. Curr Opin Pediatr. 2004, 16 (5): 560-566. 10.1097/01.mop.0000141071.47572.eb. Epub 2004/09/16CrossRefPubMed
10.
go back to reference Liacouras CA: Eosinophilic esophagitis. Gastroenterol Clin North Am. 2008, 37 (4): 989-998. 10.1016/j.gtc.2008.09.004. xi. Epub 2008/11/26CrossRefPubMed Liacouras CA: Eosinophilic esophagitis. Gastroenterol Clin North Am. 2008, 37 (4): 989-998. 10.1016/j.gtc.2008.09.004. xi. Epub 2008/11/26CrossRefPubMed
11.
go back to reference Benard A, Desreumeaux P, Huglo D, Hoorelbeke A, Tonnel AB, Wallaert B: Increased intestinal permeability in bronchial asthma. J Allergy Clin Immunol. 1996, 97 (6): 1173-1178. 10.1016/S0091-6749(96)70181-1. Epub 1996/06/01CrossRefPubMed Benard A, Desreumeaux P, Huglo D, Hoorelbeke A, Tonnel AB, Wallaert B: Increased intestinal permeability in bronchial asthma. J Allergy Clin Immunol. 1996, 97 (6): 1173-1178. 10.1016/S0091-6749(96)70181-1. Epub 1996/06/01CrossRefPubMed
12.
go back to reference Knutson TW, Bengtsson U, Dannaeus A, Ahlstedt S, Knutson L: Effects of luminal antigen on intestinal albumin and hyaluronan permeability and ion transport in atopic patients. J Allergy Clin Immunol. 1996, 97 (6): 1225-1232. 10.1016/S0091-6749(96)70189-6. Epub 1996/06/01CrossRefPubMed Knutson TW, Bengtsson U, Dannaeus A, Ahlstedt S, Knutson L: Effects of luminal antigen on intestinal albumin and hyaluronan permeability and ion transport in atopic patients. J Allergy Clin Immunol. 1996, 97 (6): 1225-1232. 10.1016/S0091-6749(96)70189-6. Epub 1996/06/01CrossRefPubMed
13.
go back to reference Wallaert B, Desreumaux P, Copin MC, Tillie I, Benard A, Colombel JF, Gosselin B, Tonnel AB, Janin A: Immunoreactivity for interleukin 3 and 5 and granulocyte/macrophage colony-stimulating factor of intestinal mucosa in bronchial asthma. J Exp Med. 1995, 182 (6): 1897-1904. 10.1084/jem.182.6.1897. Epub 1995/12/01CrossRefPubMed Wallaert B, Desreumaux P, Copin MC, Tillie I, Benard A, Colombel JF, Gosselin B, Tonnel AB, Janin A: Immunoreactivity for interleukin 3 and 5 and granulocyte/macrophage colony-stimulating factor of intestinal mucosa in bronchial asthma. J Exp Med. 1995, 182 (6): 1897-1904. 10.1084/jem.182.6.1897. Epub 1995/12/01CrossRefPubMed
14.
go back to reference Roberts G, Lack G: Food allergy and asthma–what is the link?. Paediatr Respir Rev. 2003, 4 (3): 205-212. 10.1016/S1526-0542(03)00058-7. Epub 2003/07/26CrossRefPubMed Roberts G, Lack G: Food allergy and asthma–what is the link?. Paediatr Respir Rev. 2003, 4 (3): 205-212. 10.1016/S1526-0542(03)00058-7. Epub 2003/07/26CrossRefPubMed
15.
go back to reference Roberts G, Patel N, Levi-Schaffer F, Habibi P, Lack G: Food allergy as a risk factor for life-threatening asthma in childhood: a case-controlled study. J Allergy Clin Immunol. 2003, 112 (1): 168-174. 10.1067/mai.2003.1569. Epub 2003/07/09CrossRefPubMed Roberts G, Patel N, Levi-Schaffer F, Habibi P, Lack G: Food allergy as a risk factor for life-threatening asthma in childhood: a case-controlled study. J Allergy Clin Immunol. 2003, 112 (1): 168-174. 10.1067/mai.2003.1569. Epub 2003/07/09CrossRefPubMed
16.
go back to reference Ebo DG, Bridts CH, Verweij MM, de Knop KJ, Hagendorens MM, de Clerck LS, Stevens WJ: Sensitization profiles in birch pollen-allergic patients with and without oral allergy syndrome to apple: lessons from multiplexed component-resolved allergy diagnosis. Clin Exp Allergy. 2010, 40 (2): 339-347. 10.1111/j.1365-2222.2009.03345.x. Epub 2009/08/28CrossRefPubMed Ebo DG, Bridts CH, Verweij MM, de Knop KJ, Hagendorens MM, de Clerck LS, Stevens WJ: Sensitization profiles in birch pollen-allergic patients with and without oral allergy syndrome to apple: lessons from multiplexed component-resolved allergy diagnosis. Clin Exp Allergy. 2010, 40 (2): 339-347. 10.1111/j.1365-2222.2009.03345.x. Epub 2009/08/28CrossRefPubMed
17.
go back to reference Wensing M, Akkerdaas JH, van Leeuwen WA, Stapel SO, Bruijnzeel-Koomen CA, Aalberse RC, Bast BJ, Knulst AC, van Ree R: IgE to Bet v 1 and profilin: cross-reactivity patterns and clinical relevance. J Allergy Clin Immunol. 2002, 110 (3): 435-442. 10.1067/mai.2002.126380. Epub 2002/09/05CrossRefPubMed Wensing M, Akkerdaas JH, van Leeuwen WA, Stapel SO, Bruijnzeel-Koomen CA, Aalberse RC, Bast BJ, Knulst AC, van Ree R: IgE to Bet v 1 and profilin: cross-reactivity patterns and clinical relevance. J Allergy Clin Immunol. 2002, 110 (3): 435-442. 10.1067/mai.2002.126380. Epub 2002/09/05CrossRefPubMed
18.
go back to reference Dahlman-Hoglund A, Ahlstedt S, Hanson LA, Dahlgren U, Telemo E: Different expression of IL-2 receptor alpha-chain on a lamina propria T cell population and goblet cells in rats orally tolerized or sensitized to ovalbumin (OA) after colonization with an OA-producing Escherichia coli. Clin Exp Immunol. 1996, 106 (3): 534-540. 10.1046/j.1365-2249.1996.d01-875.x. Epub 1996/12/01PubMedCentralCrossRefPubMed Dahlman-Hoglund A, Ahlstedt S, Hanson LA, Dahlgren U, Telemo E: Different expression of IL-2 receptor alpha-chain on a lamina propria T cell population and goblet cells in rats orally tolerized or sensitized to ovalbumin (OA) after colonization with an OA-producing Escherichia coli. Clin Exp Immunol. 1996, 106 (3): 534-540. 10.1046/j.1365-2249.1996.d01-875.x. Epub 1996/12/01PubMedCentralCrossRefPubMed
19.
go back to reference Lin XP, Magnusson J, Ahlstedt S, Dahlman-Hoglund A, Hanson LL, Magnusson O, Bengtsson U, Telemo E: Local allergic reaction in food-hypersensitive adults despite a lack of systemic food-specific IgE. J Allergy Clin Immunol. 2002, 109 (5): 879-887. 10.1067/mai.2002.123238. Epub 2002/05/08CrossRefPubMed Lin XP, Magnusson J, Ahlstedt S, Dahlman-Hoglund A, Hanson LL, Magnusson O, Bengtsson U, Telemo E: Local allergic reaction in food-hypersensitive adults despite a lack of systemic food-specific IgE. J Allergy Clin Immunol. 2002, 109 (5): 879-887. 10.1067/mai.2002.123238. Epub 2002/05/08CrossRefPubMed
20.
go back to reference Andrew SM, Jasani B: An improved method for the inhibition of endogenous peroxidase non-deleterious to lymphocyte surface markers. Application to immunoperoxidase studies on eosinophil-rich tissue preparations. Histochem J. 1987, 19 (8): 426-430. 10.1007/BF01675753. Epub 1987/08/01CrossRefPubMed Andrew SM, Jasani B: An improved method for the inhibition of endogenous peroxidase non-deleterious to lymphocyte surface markers. Application to immunoperoxidase studies on eosinophil-rich tissue preparations. Histochem J. 1987, 19 (8): 426-430. 10.1007/BF01675753. Epub 1987/08/01CrossRefPubMed
21.
go back to reference Skypala IJ, Calderon MA, Leeds AR, Emery P, Till SJ, Durham SR: Development and validation of a structured questionnaire for the diagnosis of oral allergy syndrome in subjects with seasonal allergic rhinitis during the UK birch pollen season. Clin Exp Allergy. 2011, 41 (7): 1001-1011. 10.1111/j.1365-2222.2011.03759.x.CrossRefPubMed Skypala IJ, Calderon MA, Leeds AR, Emery P, Till SJ, Durham SR: Development and validation of a structured questionnaire for the diagnosis of oral allergy syndrome in subjects with seasonal allergic rhinitis during the UK birch pollen season. Clin Exp Allergy. 2011, 41 (7): 1001-1011. 10.1111/j.1365-2222.2011.03759.x.CrossRefPubMed
22.
go back to reference Ebner C, Hirschwehr R, Bauer L, Breiteneder H, Valenta R, Ebner H, Kraft D, Scheiner O: Identification of allergens in fruits and vegetables: IgE cross-reactivities with the important birch pollen allergens Bet v 1 and Bet v 2 (birch profilin). J Allergy Clin Immunol. 1995, 95 (5 Pt 1): 962-969. Epub 1995/05/01CrossRefPubMed Ebner C, Hirschwehr R, Bauer L, Breiteneder H, Valenta R, Ebner H, Kraft D, Scheiner O: Identification of allergens in fruits and vegetables: IgE cross-reactivities with the important birch pollen allergens Bet v 1 and Bet v 2 (birch profilin). J Allergy Clin Immunol. 1995, 95 (5 Pt 1): 962-969. Epub 1995/05/01CrossRefPubMed
23.
go back to reference Osterballe M, Hansen TK, Mortz CG, Bindslev-Jensen C: The clinical relevance of sensitization to pollen-related fruits and vegetables in unselected pollen-sensitized adults. Allergy. 2005, 60 (2): 218-225. 10.1111/j.1398-9995.2005.00674.x. Epub 2005/01/14CrossRefPubMed Osterballe M, Hansen TK, Mortz CG, Bindslev-Jensen C: The clinical relevance of sensitization to pollen-related fruits and vegetables in unselected pollen-sensitized adults. Allergy. 2005, 60 (2): 218-225. 10.1111/j.1398-9995.2005.00674.x. Epub 2005/01/14CrossRefPubMed
24.
go back to reference Fernandez-Rivas M, Bolhaar S, Gonzalez-Mancebo E, Asero R, van Leeuwen A, Bohle B, Ma Y, Ebner C, Rigby N, Sancho AI, Miles S, Zuidmeer L, Knulst A, Breiteneder H, Mills C, Hoffmann-Sommergruber K, van Ree R: Apple allergy across Europe: how allergen sensitization profiles determine the clinical expression of allergies to plant foods. J Allergy Clin Immunol. 2006, 118 (2): 481-488. 10.1016/j.jaci.2006.05.012. Epub 2006/08/08CrossRefPubMed Fernandez-Rivas M, Bolhaar S, Gonzalez-Mancebo E, Asero R, van Leeuwen A, Bohle B, Ma Y, Ebner C, Rigby N, Sancho AI, Miles S, Zuidmeer L, Knulst A, Breiteneder H, Mills C, Hoffmann-Sommergruber K, van Ree R: Apple allergy across Europe: how allergen sensitization profiles determine the clinical expression of allergies to plant foods. J Allergy Clin Immunol. 2006, 118 (2): 481-488. 10.1016/j.jaci.2006.05.012. Epub 2006/08/08CrossRefPubMed
25.
go back to reference Powe DG, Bonnin AJ, Jones NS: ‘Entopy’: local allergy paradigm. Clin Exp Allergy. 2010, 40 (7): 987-997. 10.1111/j.1365-2222.2010.03536.x. Epub 2010/07/21CrossRefPubMed Powe DG, Bonnin AJ, Jones NS: ‘Entopy’: local allergy paradigm. Clin Exp Allergy. 2010, 40 (7): 987-997. 10.1111/j.1365-2222.2010.03536.x. Epub 2010/07/21CrossRefPubMed
26.
go back to reference Pickert CN, Lorentz A, Manns MP, Bischoff SC: Colonoscopic allergen provocation test with rBet v 1 in patients with pollen-associated food allergy. Allergy. 2012, Epub 2012/08/24 Pickert CN, Lorentz A, Manns MP, Bischoff SC: Colonoscopic allergen provocation test with rBet v 1 in patients with pollen-associated food allergy. Allergy. 2012, Epub 2012/08/24
27.
go back to reference Almansa C, Krishna M, Buchner AM, Ghabril MS, Talley N, DeVault KR, Wolfsen H, Raimondo M, Guarderas JC, Achem SR: Seasonal distribution in newly diagnosed cases of eosinophilic esophagitis in adults. Am J Gastroenterol. 2009, 104 (4): 828-833. 10.1038/ajg.2008.169. Epub 2009/02/26CrossRefPubMed Almansa C, Krishna M, Buchner AM, Ghabril MS, Talley N, DeVault KR, Wolfsen H, Raimondo M, Guarderas JC, Achem SR: Seasonal distribution in newly diagnosed cases of eosinophilic esophagitis in adults. Am J Gastroenterol. 2009, 104 (4): 828-833. 10.1038/ajg.2008.169. Epub 2009/02/26CrossRefPubMed
28.
go back to reference Onbasi K, Sin AZ, Doganavsargil B, Onder GF, Bor S, Sebik F: Eosinophil infiltration of the oesophageal mucosa in patients with pollen allergy during the season. Clin Exp Allergy. 2005, 35 (11): 1423-1431. 10.1111/j.1365-2222.2005.02351.x. Epub 2005/11/22CrossRefPubMed Onbasi K, Sin AZ, Doganavsargil B, Onder GF, Bor S, Sebik F: Eosinophil infiltration of the oesophageal mucosa in patients with pollen allergy during the season. Clin Exp Allergy. 2005, 35 (11): 1423-1431. 10.1111/j.1365-2222.2005.02351.x. Epub 2005/11/22CrossRefPubMed
29.
go back to reference Simren M, Mansson A, Langkilde AM, Svedlund J, Abrahamsson H, Bengtsson U, Bjornsson ES: Food-related gastrointestinal symptoms in the irritable bowel syndrome. Digestion. 2001, 63 (2): 108-115. 10.1159/000051878. Epub 2001/03/13CrossRefPubMed Simren M, Mansson A, Langkilde AM, Svedlund J, Abrahamsson H, Bengtsson U, Bjornsson ES: Food-related gastrointestinal symptoms in the irritable bowel syndrome. Digestion. 2001, 63 (2): 108-115. 10.1159/000051878. Epub 2001/03/13CrossRefPubMed
30.
go back to reference Zar S, Kumar D, Benson MJ: Food hypersensitivity and irritable bowel syndrome. Aliment Pharmacol Ther. 2001, 15 (4): 439-449. 10.1046/j.1365-2036.2001.00951.x. Epub 2001/04/04CrossRefPubMed Zar S, Kumar D, Benson MJ: Food hypersensitivity and irritable bowel syndrome. Aliment Pharmacol Ther. 2001, 15 (4): 439-449. 10.1046/j.1365-2036.2001.00951.x. Epub 2001/04/04CrossRefPubMed
31.
go back to reference Goral V, Kucukoner M, Buyukbayram H: Mast cells count and serum cytokine levels in patients with irritable bowel syndrome. Hepatogastroenterology. 2010, 57 (101): 751-754. Epub 2010/11/03PubMed Goral V, Kucukoner M, Buyukbayram H: Mast cells count and serum cytokine levels in patients with irritable bowel syndrome. Hepatogastroenterology. 2010, 57 (101): 751-754. Epub 2010/11/03PubMed
32.
go back to reference O’Sullivan M, Clayton N, Breslin NP, Harman I, Bountra C, McLaren A, O’Morain CA: Increased mast cells in the irritable bowel syndrome. Neurogastroenterol Motil. 2000, 12 (5): 449-457. 10.1046/j.1365-2982.2000.00221.x. Epub 2000/09/30CrossRefPubMed O’Sullivan M, Clayton N, Breslin NP, Harman I, Bountra C, McLaren A, O’Morain CA: Increased mast cells in the irritable bowel syndrome. Neurogastroenterol Motil. 2000, 12 (5): 449-457. 10.1046/j.1365-2982.2000.00221.x. Epub 2000/09/30CrossRefPubMed
33.
go back to reference Santos J, Guilarte M, Alonso C, Malagelada JR: Pathogenesis of irritable bowel syndrome: the mast cell connection. Scand J Gastroenterol. 2005, 40 (2): 129-140. 10.1080/00365520410009410. Epub 2005/03/15CrossRefPubMed Santos J, Guilarte M, Alonso C, Malagelada JR: Pathogenesis of irritable bowel syndrome: the mast cell connection. Scand J Gastroenterol. 2005, 40 (2): 129-140. 10.1080/00365520410009410. Epub 2005/03/15CrossRefPubMed
34.
go back to reference Barbara G, de Giorgio R, Stanghellini V, Cremon C, Salvioli B, Corinaldesi R: New pathophysiological mechanisms in irritable bowel syndrome. Aliment Pharmacol Ther. 2004, 20 (Suppl 2): 1-9. Epub 2004/09/01CrossRefPubMed Barbara G, de Giorgio R, Stanghellini V, Cremon C, Salvioli B, Corinaldesi R: New pathophysiological mechanisms in irritable bowel syndrome. Aliment Pharmacol Ther. 2004, 20 (Suppl 2): 1-9. Epub 2004/09/01CrossRefPubMed
Metadata
Title
Intestinal allergic inflammation in birch pollen allergic patients in relation to pollen season, IgE sensitization profile and gastrointestinal symptoms
Authors
Georgios Rentzos
Vanja Lundberg
Per-Ove Stotzer
Teet Pullerits
Esbjörn Telemo
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Clinical and Translational Allergy / Issue 1/2014
Electronic ISSN: 2045-7022
DOI
https://doi.org/10.1186/2045-7022-4-19

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Reviewer acknowledgement

Reviewer acknowledgement 2013