Eosinophilic Esophagitis: From the Bench to the Bedside
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1 Summary of presentation Eosinophilic Esophagitis: From the Bench to the Bedside at the North American Society of Pediatric Gastroenterology, Hepatology and Nutrition, October 22, 2005 Glenn T. Furuta, M.D. Assistant Professor of Pediatrics Harvard Medical School Attending Physician Children s Hospital, Boston 300 Longwood Avenue Hunnewell Ground Floor Boston, MA Telephone Fax Chris A. Liacouras, M.D. Associate Professor of Pediatrics University of Pennsylvania School of Medicine Pediatric Gastroenterologist The Children s Hospital of Philadelphia Philadelphia, PA Telephone Fax
2 Eosinophilic Esophagitis: From the Bench to the Bedside Clinical Features of Eosinophilic Gastrointestinal Diseases (EGIDs) An increasing body of evidence suggests that the eosinophil plays a role in gastrointestinal (GI) diseases. A number of different diseases are associated with eosinophilic inflammation of the gastrointestinal tract, including gastroesophageal reflux disease; eosinophilic gastrointestinal diseases (eosinophilic esophagitis, eosinophilic gastroenteritis, eosinophilic colitis, and eosinophilic ganglionitis); intestinal infections (parasites and fungus); celiac disease; hypereosinophilic syndrome; food or drug hypersensitivity reactions; inflammatory bowel diseases; and transplant-associated eosinophilic enteritis [1]. Since symptoms associated with these diseases are overlapping and common, a mucosal biopsy and other ancillary testing are required to complete a diagnostic evaluation. When diseases such as the more common GERD (abnormal ph monitoring, response to proton pump inhibition), infections (stool cultures, serological testing) and inflammatory bowel diseases (radiographic studies and histological assessment) are ruled out, the diagnosis of EGID can be made. Incumbent on the physician is the task of determining which part of the GI tract is involved, as this will impact treatment and potentially long-term management. For instance, if the patient is found to have eosinophilic esophagitis (EoE), current experience suggests that esophageal strictures are a potential long-term complication of ongoing inflammation, a risk not typically observed with the mucosal form of eosinophilic gastroenteritis. During the last 5 years, clinical observations declared the emergence of eosinophilic esophagitis (EoE) as a cause of upper intestinal symptoms that are unresponsive to maximal acid suppression [2]. While the exact diagnostic criteria are still undergoing definition, it is safe to say that EoE is a clinicopathological diagnosis requiring upper intestinal symptoms and an esophageal biopsy that contains large numbers (>20 eosinophils/hpf), both of which are unresponsive to proton pump inhibition. Symptoms associated with EoE include feeding difficulties, vomiting, and abdominal pain in young children and dysphagia and food impaction in adults. The classic patient is a young male with a history of atopic disease, peripheral eosinophilia and a family history of atopic disease. At endoscopy, the esophageal mucosa can appear normal but usually displays features of acute or chronic inflammation such as longitudinal furrowing, whitish exudates and circular rings [3]. The exudates can be confused with Candida infection or swallowed topical anesthetic spray. The rings can be fixed or transient. The one endoscopic finding that is likely unique to EoE is longitudinal shearing or splitting of the esophageal mucosa following minor trauma such as the passage of the endoscope. Radiographic features include proximal strictures and a small caliber esophagus that represents long segment narrowing. Histological specimens reveal increased numbers of eosinophils, -2-
3 eosinophilic microabscesses and superficial layering of eosinophils along the esophageal lumen. These features can be seen in the proximal and distal esophagus. Importantly, the stomach and small intestine are normal, showing no evidence of increased eosinophils. The natural history of EoE is unknown but adult studies suggest the possibility of fixed strictures that are unresponsive to medical management. Pathophysiological Mechanisms of Eosinophilic Esophagitis The eosinophil is a powerhouse of a leukocyte containing a number of biologically potent mediators [4]. Not only does it store its unique pre-formed granule proteins (major basic protein, eosinophilic cationic protein, eosinophilic-derived neurotoxin and eosinophilic peroxidase), but it also has the capacity to synthesize and secrete proinflamatory cytokines and leukotrienes. Eosinophils are born in the bone marrow under the direction of interleukin-5, interleukin-3 and GM-CSF and when called by chemokines such as eotaxin, eosinophils migrate to the vascular space. When signaled, eosinophils roll, attach, and transmigrate through the endothelium into the mucosal tissues. Upon appropriate stimulation, eosinophils can synthesize and/or release mediators leading to an inflammatory nidus [5]. The pathophysiological mechanism(s) of EoE are presently unknown, but a significant body of clinical and basic evidence suggests that it is driven by a allergic stimulus. Basic studies developed a murine model in which esophageal eosinophilia develops following sensitization and challenge with an ubiquitous aeroallergen, Aspergillus fumigatus [6]. This eosinophilic inflammation is dependent on the Th2-type cytokine, interleukin-5. Further basic studies have demonstrated a role for the Th2-cytokine IL-13. For instance, exogenous IL-13 leads to eosinophilic esophageal inflammation response in mice [7]. Clinical studies show increased expression of IL-5 in affected esophageal tissues and one case report documented the utility of an anti-il-5 antibody in clinicopathological features of EoE [8,9]. Basic evidence suggests that eosinophil granule proteins induce cytokine production, histamine release, and smooth muscle contraction and alter barrier function [5,10-13]. Taken together, these studies suggest that the eosinophilic inflammation is based in a Th2-type response and begin to explain the effectiveness of anti-allergic treatments. Treatment of Eosinophilic Gastrointestinal Diseases After other causes of gastrointestinal eosinophilia have been ruled out (see above), the clinician is faced with a number of treatment options for EGIDs. Below are approaches to treatment based on the published literature and clinical experiences. Eosinophilic Colitis In the majority of cases, allergic proctocolitis occurs in infants and toddlers. The treatment revolves around the identification and removal of food antigens [14,15]. Once these foods are eliminated, clinical symptoms and tissue histology improve within 4 to 6 weeks. By 9 to 24 months of age, these foods can be reintroduced without clinical or histologic sequelae. -3-
4 Eosinophilic Gastroenteritis First, it is important to assess the severity of the patient s clinical symptoms. Many patients with this disorder are often quite ill, presenting either with severe weight loss, dehydration, GI bleeding, or ascites. It must be determined whether or not therapy needs to be conducted on an inpatient or an outpatient basis. At times, the best mode of treatment is to hospitalize these patients, make them NPO and provide central hyperalimentation. However, the majority of these patients can be treated as outpatients. In the past, the typical therapies that have been effective include the use of an elemental diet or the use of systemic corticosteroids [16,17]. Less commonly used medications include sodium chromoglycate, antihistamines, leukotriene receptor antagonists and immunosuppressive agents such as Purinethol. Eosinophilic Esophagitis Several treatment options are available to patients diagnosed with eosinophilic esophagitis. Currently, most investigators do not believe that esophageal acid exposure is the cause of EoE; however, because of the severity of mucosal and submucosal disease seen in EoE, secondary acid reflux often occurs. Additionally, because there may be some histologic overlap between patients with EoE and those with GERD, it is important to exclude acid reflux as a cause of esophageal inflammation. Therefore, most investigators believe that the initial use of proton pump inhibitors is essential in any patient who has clinical symptoms of EoE so that GERD can be excluded [18]. The diagnosis of EoE cannot be made unless a documented biopsy is performed while the patient is on aggressive acid blockade. If a severe EoE exists despite the use of an aggressive acid blockade, EoE must be considered. Patients with EoE may show partial response to aggressive acid blockade. Adult gastroenterologists have reported the use of esophageal dilatation for their patients who present with esophageal strictures secondary to EoE [19]. While esophageal dilatation using rigid esophageal dilators can relieve dysphagia, many of these physicians have described esophageal tearing during dilatation. In addition, there have been several reports of esophageal tearing simply with the introduction of the endoscope in patients with EoE. Thus, gastroenterologists should be extremely careful whenever performing endoscopy or dilatation on a patient with EoE as perforation is a distinct possibility. The first medical treatment that was shown to be effective in improving both symptoms and esophageal histology was systemic steroids [20]. Oral corticosteroids should be used whenever patients have severe dysphagia (with or without strictures) or other clinical symptoms that may be contributing to possible hospitalization because of a feeding disorder, poor weight gain or dehydration. While systemic steroids work rapidly, their disadvantages include that they cannot be used chronically, that they do not cure the disease, and that they often have serious side effects with prolonged use (bone, growth, and mood abnormalities). Instead of prescribing systemic steroids, topical corticosteroids can be -4-
5 utilized [21]. These medications, such as fluticasone, can be sprayed in the pharynx and swallowed. Both clinical symptoms and esophageal histology dramatically improve with the use of this therapy. The advantage of using topical steroids is that their side effects are less than that seen with systemic steroids. The disadvantage of using this medication is that it does not treat the disease fully, the disease generally recurs when the treatment is discontinued, and side effects (esophageal candidiasis) may occur with its chronic use. Recently, the use of a swallowed viscous solution containing budesonide has been reported with some effectiveness. Several other medications have also been used. Some investigators have used cromolyn sodium as an adjunct to therapy for EoE. However, no studies have been conducted to prove its effectiveness. Leukotriene receptor antagonists have also been utilized to treat EoE. Initial doses of 10 to 100 mgs per day have been prescribed with reports of symptomatic improvement; however, on repeat biopsy, there was no significant change in the patient s esophageal eosinophilia [22]. The advantage of using a leukotriene receptor antagonist is that it has minimal side effects and it may alleviate the patient s clinical symptoms. However, there have been no reports documenting improvement in the patient s histology. Additionally, in the majority of patients, both tissue inflammation as well as clinical symptoms recurred when the medication was discontinued. Dietary therapy either by removing suspected food antigens or by providing the strict use of an amino acid-based formula has been shown to significantly improve both the clinical symptoms and -5- the esophageal histology [23-25]. Two types of diets have been tried: 1) the elimination diet (removal of specific food antigens by utilizing clinical history and allergy testing); 2) strict elemental diet utilizing an amino acid-based formula. Because of the inaccuracies of present day allergy testing and the difficulties of obtaining a perfect dietary history, elimination diets are often not successful. In contrast, several investigators have demonstrated greater than a 98% clinical and histologic response with the strict use of an elemental diet. Once the diet is initiated, the patient s clinical symptoms improve within ten days and the tissue histology normalizes within one month. Finally, there have been reports of the development of other medications that will target specific chemokines and other inflammatory mediators that are involved in the activation of the eosinophil. Medications such as anti-interleukin-5, very late activating antigen, and monoclonal eotaxin antibody may benefit those patients who have severe EoE [26]. Drs. Ngo and Furuta have recently written a summary of the currently accepted medical treatments for EoE [27]. Disclaimer This document is for informational use only and not to be used directly for the care of patients. Any questions related to the care of specific patients should be directed to a health care provider.
6 References 1. Rothenberg ME: Eosinophilic gastrointestinal disorders (EGID). J Allergy Clin Immunol 2004; 113:11-28; quiz Fox VL, Nurko S, Furuta GT: Eosinophilic esophagitis: It's not just kid's stuff. Gastrointest Endosc 2002; 56: Straumann A, Spichtin HP, Bucher KA, Heer P, Simon HU: Eosinophilic esophagitis: red on microscopy, white on endoscopy. Digestion 2004; 70: Hogan SP, Rothenberg ME: Review article: The eosinophil as a therapeutic target in gastrointestinal disease. Aliment Pharmacol Ther 2004; 20: Kita H, Abu-Ghazaleh RI, Sur S, Gleich GJ: Eosinophil major basic protein induces degranulation and IL-8 production by human eosinophils. J Immunol 1995; 154: Mishra A, Hogan SP, Brandt EB, Rothenberg ME: IL-5 promotes eosinophil trafficking to the esophagus. J Immunol 2002; 168: Mishra A, Rothenberg ME: Intratracheal IL-13 induces eosinophilic esophagitis by an IL-5, eotaxin-1, and STAT6-dependent mechanism. Gastroenterology 2003; 125: Straumann A, Bauer M, Fischer B, Blaser K, Simon HU: Idiopathic eosinophilic esophagitis is associated with a T(H)2-type allergic inflammatory response. J Allergy Clin Immunol 2001; 108: Garrett JK, Jameson SC, Thomson B, Collins MH, Wagoner LE, Freese DK, Beck LA, Boyce JA, Filipovich AH, Villanueva JM, et al: Anti-interleukin-5 (mepolizumab) therapy for hypereosinophilic syndromes. J Allergy Clin Immunol 2004; 113: Furuta GT, Nieuwenhuis EE, Karhausen J, Gleich G, Blumberg RS, Lee JJ, Ackerman SJ: Eosinophils alter colonic epithelial barrier function: role for major basic protein. Am J Physiol Gastrointest Liver Physiol 2005; 289:G Lundgren JD, Davey RT, Lundgren B, Mullol J, Marom Z, Logun C, Baraniuk J, Kaliner MA, Shelhamer JH: Eosinophil cationic protein stimulates and major basic protein inhibits airway mucus secretion. J Allergy Clin Immunol 1991; 87: Thomas LL, Zheutlin LM, Gleich GJ: Pharmacological control of human basophil histamine release stimulated by eosinophil granule major basic protein. Immunology 1989; 66:
7 13. Uchida DA, Ackerman SJ, Coyle AJ, Larsen GL, Weller PF, Freed J, Irvin CG: The effect of human eosinophil granule major basic protein on airway responsiveness in the rat in vivo. A comparison with polycations. Am Rev Respir Dis 1993; 147: Kerner JA Jr: Formula allergy and intolerance. Gastroenterol Clin North Am 1995; 24: Simpser E: Gastrointestinal allergy, in Altschuler SM, Liacouras CA (eds): Clinical Pediatric Gastroenterology. Philadelphia: Churchill Livingstone, 1998; Whitington PF, Whitington GL: Eosinophilic gastroenteropathy in childhood. J Pediatr Gastroenterol Nutr 1988; 7: Justinich C, Katz A, Gurbindo C, et al: Elemental diet improves steroid-dependent eosinophilic gastroenteritis and reverses growth failure. J Pediatr Gastroenterol Nutr 1996; 23: Desai TK, Stecevic V, Chang CH, et al: Association of eosinophilic inflammation with esophageal food impaction in adults. Gastrointest Endosc 2005;61: Nostrant TT: Esophageal dilation/dilators. Curr Treat Options Gastroenterol 2005; 8: Liacouras CA, Wenner WJ, Brown K, Ruchelli E: Primary eosinophilic esophagitis in children: successful treatment with oral corticosteroids. J Pediatr Gastroenterol Nutr 1998; 26: Faubion WA Jr, Perrault J, Burgart LJ, Zein NN, Clawson M, Freese DK: Treatment of eosinophilic esophagitis with inhaled corticosteroids. J Pediatr Gastroenterol Nutr 1998; 27: Attwood SE, Lewis CJ, Bronder CS, Morris CD, Armstrong GR, Whittam J: Eosinophilic oesophagitis: a novel treatment using Montelukast. Gut 2003; 52: Kelly KJ, Lazenby AJ, Rowe PC, et al: Eosinophilic esophagitis attributed to gastroesophageal reflux: improvement with an amino acid-based formula. Gastroenterology 1995;109: Markowitz JE, Spergel JM, Ruchelli E, Liacouras CA: Elemental diet is an effective treatment for eosinophilic esophagitis in children and adolescents. Am J Gastroenterol 2003; 98: Spergel JM, Andrews T, Brown-Whitehorn TF, et al: Treatment of eosinophilic esophagitis with specific food elimination diet directed by a combination of skin prick and patch tests. Ann Allergy Asthma Immunol 2005;95:
8 26. Garrett JK, Jameson SC, Thomson B, et al: Anti-interleukin-5 (mepolizumab) therapy for hypereosinophilic syndromes. J Allergy Clin Immunol 2004;113: Ngo P, Furuta GT: Treatment of eosinophilic esophagitis in children. Curr Treat Options Gastroenterol 2005;8: A medical education project supported by Ross Products Division, Abbott Laboratories Inc /6010 LITHO IN USA
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