Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Clinical Reviews in Allergy & Immunology
Published in: Clinical Reviews in Allergy & Immunology 2/2019

01-10-2019

Gastrointestinal Disorders Associated with Primary Immunodeficiency Diseases

Authors: Stella Hartono, Michelina Rosa Ippoliti, Maria Mastroianni, Ricardo Torres, Nicholas L. Rider

Published in: Clinical Reviews in Allergy & Immunology | Issue 2/2019

Login to get access

Abstract

There are now 354 inborn errors of immunity (primary immunodeficiency diseases (PIDDs)) with 344 distinct molecular etiologies reported according to the International Union of Immunological Sciences (IUIS) (Clin Gastroenterol Hepatol 11: p. 1050-63, 2013, Semin Gastrointest Dis 8: p. 22-32, 1997, J Clin Immunol 38: p. 96-128, 2018). Using the IUIS document as a reference and cross-checking PubMed (www.​ncbi.​nlm.​nih.​pubmed.​gov), we found that approximately one third of the 354 diseases of impaired immunity have a gastrointestinal component [J Clin Immunol 38: p. 96-128, 2018]. Often, the gastrointestinal symptomatology and pathology is the heralding sign of a PIDD; therefore, it is important to recognize patterns of disease which may manifest along the gastrointestinal tract as a more global derangement of immune function. As such, holistic consideration of immunity is warranted in patients with clinically significant gastrointestinal disease. Here, we discuss the manifold presentations and GI-specific complications of PIDDs which could lead patients to seek advice from a variety of clinician specialists. Often, patients with these medical problems will engage general pediatricians, surgeons, gastroenterologists, rheumatologists, and clinical immunologists among others. Following delineation of the presenting concern, accurate and often molecular diagnosis is imperative and a multi-disciplinary approach warranted for optimal management. In this review, we will summarize the current state of understanding of PIDD gastrointestinal disease involvement. We will do so by focusing upon gastrointestinal disease categories (i.e., inflammatory, diarrhea, nodular lymphoid hyperplasia, liver/biliary tract, structural disease, and oncologic disease) with an intent to aid the healthcare provider who may encounter a patient with an as-yet undiagnosed PIDD who presents initially with a gastrointestinal symptom, sign, or problem.
Literature
1.
Petersen BS, August D, Abt R, Alddafari M, Atarod L, Baris S, Bhavsar H, Brinkert F, Buchta M, Bulashevska A, Chee R, Cordeiro AI, Dara N, Dückers G, Elmarsafy A, Frede N, Galal N, Gerner P, Glocker EO, Goldacker S, Hammermann J, Hasselblatt P, Havlicekova Z, Hübscher K, Jesenak M, Karaca NE, Karakoc-Aydiner E, Kharaghani MM, Kilic SS, Kiykim A, Klein C, Klemann C, Kobbe R, Kotlarz D, Laass MW, Leahy TR, Mesdaghi M, Mitton S, Neves JF, Öztürk B, Pereira LF, Rohr J, Restrepo JLR, Ruzaike G, Saleh N, Seneviratne S, Senol E, Speckmann C, Tegtmeyer D, Thankam P, van der Werff ten Bosch J, von Bernuth H, Zeissig S, Zeissig Y, Franke A, Grimbacher B (2017) Targeted gene panel sequencing for early-onset inflammatory bowel disease and chronic diarrhea. Inflamm Bowel Dis 23(12):2109–2120PubMedCrossRef
2.
Glocker EO, Kotlarz D, Boztug K, Gertz EM, Schäffer AA, Noyan F, Perro M, Diestelhorst J, Allroth A, Murugan D, Hätscher N, Pfeifer D, Sykora KW, Sauer M, Kreipe H, Lacher M, Nustede R, Woellner C, Baumann U, Salzer U, Koletzko S, Shah N, Segal AW, Sauerbrey A, Buderus S, Snapper SB, Grimbacher B, Klein C (2009) Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med 361(21):2033–2045PubMedPubMedCentralCrossRef
3.
Atarod L et al (2003) A review of gastrointestinal disorders in patients with primary antibody immunodeficiencies during a 10-year period (1990–2000), in children hospital medical center. Iran J Allergy Asthma Immunol 2(2):75–79PubMed
4.
Glocker E, Grimbacher B (2012) Inflammatory bowel disease: is it a primary immunodeficiency? Cell Mol Life Sci 69(1):41–48PubMedCrossRef
5.
Henderson P, Hansen R, Cameron FL, Gerasimidis K, Rogers P, Bisset MW, Reynish EL, Drummond HE, Anderson NH, van Limbergen J, Russell RK, Satsangi J, Wilson DC (2012) Rising incidence of pediatric inflammatory bowel disease in Scotland. Inflamm Bowel Dis 18:999–1005PubMedCrossRef
6.
Benchimol E et al (2014) Incidence, outcomes and health services burden of children with very early onset inflammatory bowel disease. Gastroenterology 147:803–813.e7PubMedCrossRef
7.
Silverberg M et al (2005) Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol 19(suppl A):5A–36APubMedCrossRef
8.
Uhlig HH et al (2014) The Diagnostic Approach to Monogenic Very Early Onset Inflammatory Bowel Disease. Gastroenterology 147:990–1007PubMedCrossRef
9.
Levine A, Griffiths A, Markowitz J, Wilson DC, Turner D, Russell RK, Fell J, Ruemmele FM, Walters T, Sherlock M, Dubinsky M, Hyams JS (2011) Pediatric modification of the Montreal classification for inflammatory bowel disease: the Paris classification. Inflamm Bowel Dis 17:1314–1321PubMedCrossRef
10.
Agarwal S, Mayer L (2013) Diagnosis and treatment of gastrointestinal disorders in patients with primary immunodeficiency. Clin Gastroenterol Hepatol 11(9):1050–1063PubMedCrossRefPubMedCentral
11.
12.
13.
Bonilla FA, Barlan I, Chapel H, Costa-Carvalho BT, Cunningham-Rundles C, de la Morena MT, Espinosa-Rosales FJ, Hammarström L, Nonoyama S, Quinti I, Routes JM, Tang MLK, Warnatz K (2016) International consensus document (ICON): common variable immunodeficiency disorders. J Allergy Clin Immunol 4(1):38–59CrossRef
14.
Pecoraro A, Nappi L, Crescenzi L, D’Armiento FP, Genovese A, Spadaro G (2018) Chronic diarrhea in common variable immunodeficiency: a case series and review of the literature. J Clin Immunol 38:67–76PubMedCrossRef
15.
Picard C, Bobby Gaspar H, al-Herz W, Bousfiha A, Casanova JL, Chatila T, Crow YJ, Cunningham-Rundles C, Etzioni A, Franco JL, Holland SM, Klein C, Morio T, Ochs HD, Oksenhendler E, Puck J, Tang MLK, Tangye SG, Torgerson TR, Sullivan KE (2018) International Union of Immunological Societies: 2017 Primary Immunodeficiency Diseases Committee report on inborn errors of immunity. J Clin Immunol 38(1):96–128PubMedCrossRef
16.
Kammermeier J, Dziubak R, Pescarin M, Drury S, Godwin H, Reeve K, Chadokufa S, Huggett B, Sider S, James C, Acton N, Cernat E, Gasparetto M, Noble-Jamieson G, Kiparissi F, Elawad M, Beales PL, Sebire NJ, Gilmour K, Uhlig HH, Bacchelli C, Shah N (2017) Phenotypic and genotypic characterisation of inflammatory bowel disease presenting before the age of 2 years. J Crohn’s Colitis 11:60–69CrossRef
17.
Quigley E, Carmichael H, Watkinson G (1986) Case report and review of the relationships between vitamin B12 deficiency, small intestinal mucosal disease and immunoglobulin deficiency. J Clin Gastroenterol 8:277–281PubMedCrossRef
18.
Spector J (1974) Juvenile achlorhydric pernicious anemia with IgA deficiency. A family study. JAMA 228:334–336PubMedCrossRef
19.
Barzaghi F, Passerini L, Bacchetta R (2012) Immune dysregulation, polyendocrinopathy, enteropathy, x-linked syndrome: a paradigm of immunodeficiency with autoimmunity. Front Immunol 3:211PubMedCrossRefPubMedCentral
20.
Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L, Kelly TE, Saulsbury FT, Chance PF, Ochs HD (2001) The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 27(1):20–21PubMedCrossRef
21.
Gambineri E et al (2008) Clinical and molecular profile of a new series of patients with immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome: inconsistent correlation between forkhead box protein 3 expression and disease severity. J Allergy Clin Immunol 122(6):1105–1112 e1PubMedCrossRef
22.
Duclaux-Loras R, Collardeau-Frachon S, Nancey S, Fabien N, Kaiserlian D, Lachaux A (2015) Long-term disease course in a patient with severe neonatal IPEX syndrome. Clin Res Hepatol Gastroenterol 39(4):e43–e47PubMedCrossRef
23.
Guerrerio AL, Frischmeyer-Guerrerio PA, Lederman HM, Oliva-Hemker M (2010) Recognizing gastrointestinal and hepatic manifestations of primary immunodeficiency diseases. J Pediatr Gastroenterol Nutr 51(5):548–555PubMedCrossRef
24.
Scaillon M, van Biervliet S, Bontems P, Dorchy H, Hanssens L, Ferster A, Segers V, Cadranel S (2009) Severe gastritis in an insulin-dependent child with an IPEX syndrome. J Pediatr Gastroenterol Nutr 49(3):368–370PubMedCrossRef
25.
D’Hennezel E et al (2009) FOXP3 forkhead domain mutation and regulatory T cells in the IPEX sydrome. NEJM 17(Oct 22 361):1710–1713CrossRef
26.
de Serre Patey-Mariaud N et al (2009) Digestive histopathological presentation of IPEX syndrome. Mod Pathol 22(1):95–102CrossRef
27.
Torgerson TR, Linane A, Moes N, Anover S, Mateo V, Rieux–Laucat F, Hermine O, Vijay S, Gambineri E, Cerf–Bensussan N, Fischer A, Ochs HD, Goulet O, Ruemmele FM (2007) Severe food allergy as a variant of IPEX syndrome caused by a deletion in a noncoding region of the FOXP3 gene. Gastroenterology 132(5):1705–1717PubMedCrossRef
28.
Barzaghi F et al (2017) Long-term follow up of IPEX syndrome patients after different therapeutic strategies: an international multicenter retrospective study. J Allergy Clin Immunol 17(Epub ahead of print):31893–31896
29.
Caudy AA, Reddy ST, Chatila T, Atkinson JP, Verbsky JW (2007) CD25 deficiency causes an immune dysregulation, polyendocrinopathy, enteropathy, X-linked-like syndrome, and defective IL-10 expression from CD4 lymphocytes. J Allergy Clin Immunol 119(2):482–487PubMedCrossRef
30.
31.
Ozgur T et al (2008) Hematopoietic stem cell transplantation in a CD3 gamma-deficient infant with inflammatory bowel disease. Pediatr Transplant 12(8):910–913PubMedCrossRef
32.
Alroqui F et al (2017) DOCK8 deficiency presenting as an IPEX-like disorder. J Clin Immunol 37(8):811–819CrossRef
33.
Stray-Pedersen A, Sorte HS, Samarakoon P, Gambin T, Chinn IK, Coban Akdemir ZH, Erichsen HC, Forbes LR, Gu S, Yuan B, Jhangiani SN, Muzny DM, Rødningen OK, Sheng Y, Nicholas SK, Noroski LM, Seeborg FO, Davis CM, Canter DL, Mace EM, Vece TJ, Allen CE, Abhyankar HA, Boone PM, Beck CR, Wiszniewski W, Fevang B, Aukrust P, Tjønnfjord GE, Gedde-Dahl T, Hjorth-Hansen H, Dybedal I, Nordøy I, Jørgensen SF, Abrahamsen TG, Øverland T, Bechensteen AG, Skogen V, Osnes LTN, Kulseth MA, Prescott TE, Rustad CF, Heimdal KR, Belmont JW, Rider NL, Chinen J, Cao TN, Smith EA, Caldirola MS, Bezrodnik L, Lugo Reyes SO, Espinosa Rosales FJ, Guerrero-Cursaru ND, Pedroza LA, Poli CM, Franco JL, Trujillo Vargas CM, Aldave Becerra JC, Wright N, Issekutz TB, Issekutz AC, Abbott J, Caldwell JW, Bayer DK, Chan AY, Aiuti A, Cancrini C, Holmberg E, West C, Burstedt M, Karaca E, Yesil G, Artac H, Bayram Y, Atik MM, Eldomery MK, Ehlayel MS, Jolles S, Flatø B, Bertuch AA, Hanson IC, Zhang VW, Wong LJ, Hu J, Walkiewicz M, Yang Y, Eng CM, Boerwinkle E, Gibbs RA, Shearer WT, Lyle R, Orange JS, Lupski JR (2017) Primary immunodeficiency diseases: genomic approaches delineate heterogeneous Mendelian disorders. J Allergy Clin Immunol 139(1):232–245PubMedCrossRef
34.
Vlantis K et al (2016) NEMO prevents RIP kinase 1-mediated epithelial cell death and chronic intestinal inflammation by NK-kB-dependent and -independent functions. Immunity 33(3):553–567CrossRef
35.
Nenci A et al (2007) Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446(7135):557–561PubMedCrossRef
36.
Tegtmeyer D et al (2017) Inflammatory bowel disease caused by primary immunodeficiencies—clinical presentations, review of literature and proposal of a rational diagnostic algorithm. Pediatr Allergy Immunol 28(5):412–429PubMedCrossRef
37.
Klemann C, Pannicke U, Morris-Rosendahl DJ, Vlantis K, Rizzi M, Uhlig H, Vraetz T, Speckmann C, Strahm B, Pasparakis M, Schwarz K, Ehl S, Rohr JC (2016) Transplantation from a symptomatic carrier sister restores host defenses but does not prevent colitis in NEMO deficiency. Clin Immunol 164(Mar):52–56PubMedCrossRefPubMedCentral
38.
Permaul P, Narla A, Hornick JL, Pai SY (2009) Allogeneic hematopoietic stem cell transplantation for X-linked ectodermal dysplasia and immunodeficiency: case report and review of outcomes. Immunol Res 44(1–3):89–98PubMedCrossRef
39.
Cheng LE, Kanwar B, Tcheurekdjian H, Grenert JP, Muskat M, Heyman MB, McCune JM, Wara DW (2009) Persistent systemic inflammation and atypical enterocolitis in patients with NEMO syndrome. Clin Immunol 132(1):124–131PubMedCrossRefPubMedCentral
40.
Mizukami T, Obara M, Nishikomori R, Kawai T, Tahara Y, Sameshima N, Marutsuka K, Nakase H, Kimura N, Heike T, Nunoi H (2012) Successful treatment with infliximab for inflammatory colitis in a patient with X-linked anhidrotic ectodermal dysplasia with immunodeficiency. J Clin Immunol 32(1):39–49PubMedCrossRef
41.
Barmettler S, Otani IM, Minhas J, Abraham RS, Chang Y, Dorsey MJ, Ballas ZK, Bonilla FA, Ochs HD, Walter JE (2017) Gastrointestinal manifestations in X-linked agammaglobulinemia. J Clin Immunol 37(3):287–294PubMedCrossRefPubMedCentral
42.
Washington K, Stenzel TT, Buckley RH, Gottfried MR (1996) Gastrointestinal pathology in patients with common variable immunodeficiency and X-linked agammaglobulinemia. Am J Surg Pathol 20(10):1240–1252CrossRefPubMed
43.
Shera IA, Khurshid SM, Bhat MS (2017) Inflammatory duodenal polyposis associated with primary immunodeficiency disease: a novel case report. Case Rep Med 2017:6206085PubMedCrossRefPubMedCentral
44.
45.
Kalha I, Sellin JH (2004) Common variable immunodeficiency and the gastrointestinal tract. Curr Gastroenterol Rep 6(5):377–383PubMedCrossRef
46.
47.
Cunningham-Rundles C, Bodian C (1999) Common variable immunodeficiency: clinical and immunological features of 248 patients. Clin Immunol 92(1):34–48PubMedCrossRef
48.
Hermaszewski R, Webster A (1993) Primary hypogammaglobulinemia: a survey of clinical manifestations and complications. Q J Med 86(1):31–42PubMed
49.
Oksenhendler E et al (2008) Infections in 252 patients with common variable immunodeficiency. Clin Infect Dis 46(10):1547–1554PubMedCrossRef
50.
Wood P, Stanworth S, Burton J, Jones A, Peckham DG, Green T, Hyde C, Chapel H, the UK Primary Immunodeficiency Network (2007) Recognition, clinical diagnosis and management of patients with primary antibody deficiencies: a systematic review. Clin Exp Immunol 149(3):410–423PubMedCrossRefPubMedCentral
51.
Khodadad A, Aghamohammadi A, Parvaneh N, Rezaei N, Mahjoob F, Bashashati M, Movahedi M, Fazlollahi MR, Zandieh F, Roohi Z, Abdollahzade S, Salavati A, Kouhi A, Talebpour B, Daryani NE (2007) Gastrointestinal manifestations in patients with common variable immunodeficiency. Dig Dis Sci 52(11):2977–2983PubMedCrossRef
52.
Mannon PJ, Fuss IJ, Dill S, Friend J, Groden C, Hornung R, Yang Z, Yi C, Quezado M, Brown M, Strober W (2006) Excess IL-12 but not IL-23 accompanies the inflammatory bowel disease associated with common variable immunodeficiency. Gastroenterology 131(3):748–756PubMedCrossRef
53.
Luzi G, Zullo A, Iebba F, Rinaldi V, Mete LS, Muscaritoli M, Aiuti F (2003) Duodenal pathology and clinical-immunological implications in common variable immunodeficiency patients. Am J Gastroenterol 98(1):118–121PubMedCrossRef
54.
Daniels JA, Lederman HM, Maitra A, Montgomery EA (2007) Gastrointestinal tract pathology in patients with common variable immunodeficiency (CVID): a clinicopathologic study and review. Am J Surg Pathol 31(12):1800–1812CrossRefPubMed
55.
Hermans PE, Diaz-Buxo JA, Stobo JD (1976) Idiopathic late-onset immunoglobulin deficiency. Clinical observations in 50 patients. Am J Med 61(2):221–237PubMedCrossRef
56.
Twomey JJ, Jordan PH, Jarrold T, Trubowitz S, Ritz ND, Conn HO (1969) The syndrome of immunoglobulin deficiency and pernicious anemia. A study of ten cases. Am J Med 47(3):340–350PubMedCrossRef
57.
Quinti I et al (2007) Long-term follow up and outcome of a large cohort of patients with common variable immunodeficiency. J Clin Immunol 27(3):308–316PubMedCrossRef
58.
Agarwal S, Smereka P, Harpaz N, Cunningham-Rundles C, Mayer L (2011) Characterization of immunologic defects in patients with common variable immunodeficiency (CVID) with intestinal disease. Inflamm Bowel Dis 17(1):251–259PubMedCrossRef
59.
Dhalla F, da Silva SP, Lucas M, Travis S, Chapel H (2011) Review of gastric cancer risk factors in patients with common variable immunodeficiency disorders, resulting in a proposal for a surveillance programme. Clin Exp Immunol 165(1):1–7PubMedCrossRefPubMedCentral
60.
Comunoglu, N., S.Kara, and N.Kepil, (2015) Inflammatory bowel disease-like colitis pathology in a patient with common variable immune deficiency. BMJ Case Rep 2015
61.
Bosworth BP, Sanders A, Maltz C (2006) Common variable immunodeficiency masquerading as Crohn’s ileocolitis. Inflamm Bowel Dis 12(2):151–152PubMedCrossRef
62.
Mudter J, Wirtz S, Weigmann B, Tiede I, Tubbe I, Kiesslich R, Galle PR, Lehr HA, Neurath MF (2006) Crohn’s-like colitis in a patient with immunodeficiency associated with a defect in expression of inducible costimulator. Dig Dis Sci 51(4):711–717PubMedCrossRef
63.
Baehner RL, Karnovsky ML (1968. Dec 13) Deficiency of reduced nicotinamide-adenine dinucleotide oxidase in chronic granulomatous disease. Science 162(3859):1277–1279PubMedCrossRef
64.
McPhail LC et al (1977) Deficiency of NADPH oxidase activity in chronic granulomatous disease. J Pediatr 90(2):213–217PubMedCrossRef
65.
Abo A et al (1994) Activation of NADPH oxidase involves the dissociation of p21rac from its inhibitory GDP/GTP exchange protein (rhoGDI) followed by its translocation to the plasma membrane. Biochem J 298(Pt3):585–591PubMedPubMedCentralCrossRef
66.
Hampton MB, Kettle AJ, Winterbourn CC (1996) Involvement of superoxide and myeloperoxidase in oxygen-dependent killing of Staphylococcus aureus by neutrophils. Infect Immun 64(9):3512–3517PubMedPubMedCentralCrossRef
67.
Rosen H, Klebanoff SJ (1979) Bactericidal activity of a superoxide anion-generating system. A model for the polymorphonuclear leukocyte. J Exp Med 149(1):27–39PubMedCrossRef
68.
Kaplan EL, Laxdal T, Quie PG (1968) Studies of polymorphonuclear leukocytes from patients with chronic granulomatous disease of childhood; bactericidal capacity for streptococci. Pediatrics 41(3):591–599PubMedCrossRef
69.
Magnani A et al (2014) Inflammatory manifestations in a single-center cohort of patients with chronic granulomatous disease. J Allergy Clin Immunol 134(3):655–662 e8PubMedCrossRef
70.
van den Berg JM, van Koppen E, Åhlin A, Belohradsky BH, Bernatowska E, Corbeel L, Español T, Fischer A, Kurenko-Deptuch M, Mouy R, Petropoulou T, Roesler J, Seger R, Stasia MJ, Valerius NH, Weening RS, Wolach B, Roos D, Kuijpers TW (2009) Chronic granulomatous disease: the European experience. PLoS One 4(4):e5234PubMedPubMedCentralCrossRef
71.
Raptaki M, Varela I, Spanou K, Tzanoudaki M, Tantou S, Liatsis M, Constantinidou N, Bakoula C, Roos D, Kanariou M (2013) Chronic granulomatous disease: a 25-year patient registry based on a multistep diagnostic procedure, from the referral center for primary immunodeficiencies in Greece. J Clin Immunol 33(8):1302–1309PubMedCrossRef
72.
Marciano BE, Rosenzweig SD, Kleiner DE, Anderson VL, Darnell DN, Anaya-O'Brien S, Hilligoss DM, Malech HL, Gallin JI, Holland SM (2004) Gastrointestinal involvement in chronic granulomatous disease. Pediatrics 114(2):462–468PubMedCrossRef
73.
Winkelstein JA, Marino MC, Johnston RB Jr, Boyle J, Curnutte J, Gallin JI, Malech HL, Holland SM, Ochs H, Quie P, Buckley RH, Foster CB, Chanock SJ, Dickler H (2000) Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 79(3):155–169CrossRef
74.
Huang A, Abbasakoor F, Vaizey CJ (2006) Gastrointestinal manifestations of chronic granulomatous disease. Color Dis 8(8):637–644CrossRef
75.
Barton LL, Moussa SL, Villar RG, Hulett RL (1998) Gastrointestinal complications of chronic granulomatous disease: case report and literature review. Clin Pediatr (Phila) 37(4):231–236CrossRef
76.
Marks DJ et al (2009) Inflammatory bowel disease in CGD reproduces the clinicopathological features of Crohn’s disease. Am J Gastroenterol 104(1):117–124PubMedCrossRef
77.
Mulholland MW, Delaney JP, Simmons RL (1983) Gastrointestinal complications of chronic granulomatous disease: surgical implications. Surgery 94(4):569–575PubMed
78.
Alimchandani M, Lai JP, Aung PP, Khangura S, Kamal N, Gallin JI, Holland SM, Malech HL, Heller T, Miettinen M, Quezado MM (2013) Gastrointestinal histopathology in chronic granulomatous disease: a study of 87 patients. Am J Surg Pathol 37(9):1365–1372PubMedPubMedCentralCrossRef
79.
Yu JE, de Ravin SS, Uzel G, Landers C, Targan S, Malech HL, Holland SM, Cao W, Harpaz N, Mayer L, Cunningham-Rundles C (2011) High levels of Crohn’s disease-associated anti-microbial antibodies are present and independent of colitis in chronic granulomatous disease. Clin Immunol 138(1):14–22PubMedCrossRef
80.
Uzzan M, Ko HM, Mehandru S, Cunningham-Rundles C (2016) Gastrointestinal disorders associated with common variable immune deficiency (CVID) and chronic granulomatous disease (CGD). Curr Gastroenterol Rep 18(4):17PubMedPubMedCentralCrossRef
81.
Rieber N et al (2012) Current concepts of hyperinflammation in chronic granulomatous disease. Clin Dev Immunol 2012:252460PubMedCrossRef
82.
Meissner F, Seger RA, Moshous D, Fischer A, Reichenbach J, Zychlinsky A (2010) Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 116(9):1570–1573PubMedPubMedCentralCrossRef
83.
Kuijpers T, Lutter R (2012) Inflammation and repeated infections in CGD: two sides of a coin. Cell Mol Life Sci 69(1):7–15PubMedCrossRef
84.
Crowley CA, Curnutte JT, Rosin RE, André-Schwartz J, Gallin JI, Klempner M, Snyderman R, Southwick FS, Stossel TP, Babior BM (1980) An inherited abnormality of neutrophil adhesion. Its genetic transmission and its association with a missing protein. N Engl J Med 302(21):1163–1168PubMedCrossRef
85.
Arnaout MA (1990) Leukocyte adhesion molecules deficiency: its structural basis, pathophysiology and implications for modulating the inflammatory response. Immunol Rev 114:145–180PubMedCrossRef
86.
87.
Movahedi M, Entezari N, Pourpak Z, Mamishi S, Chavoshzadeh Z, Gharagozlou M, Mir-Saeeid-Ghazi B, Fazlollahi MR, Zandieh F, Bemanian MH, Farhoudi A, Aghamohammadi A (2007) Clinical and laboratory findings in Iranian patients with leukocyte adhesion deficiency (study of 15 cases). J Clin Immunol 27(3):302–307PubMedCrossRef
88.
Jain S, Gozdziak P, Morgan A, Burt RK (2013) Remission of Crohn’s disease after cord blood transplantation for leukocyte adhesion deficiency type 1. Bone Marrow Transplant 48(7):1006–1007PubMedCrossRef
89.
Jain AK, Motil KJ, Abramson SL, Han YS, Tatevian N (2010) Rectal ulcer with an elusive diagnosis: all that ulcers is not Crohn disease. J Pediatr Gastroenterol Nutr 51(3):367–369PubMedCrossRef
90.
91.
Uzel G, Kleiner DE, Kuhns DB, Holland SM (2001) Dysfunctional LAD-1 neutrophils and colitis. Gastroenterology 121(4):958–964PubMedCrossRef
92.
Boztug K, Appaswamy G, Ashikov A, Schäffer AA, Salzer U, Diestelhorst J, Germeshausen M, Brandes G, Lee-Gossler J, Noyan F, Gatzke AK, Minkov M, Greil J, Kratz C, Petropoulou T, Pellier I, Bellanné-Chantelot C, Rezaei N, Mönkemöller K, Irani-Hakimeh N, Bakker H, Gerardy-Schahn R, Zeidler C, Grimbacher B, Welte K, Klein C (2009) A novel syndrome with congenital neutropenia caused by mutations in G6PC3. N Engl J Med 360(1):32–43PubMedPubMedCentralCrossRef
93.
Kaya Z et al (2014) Resolution of inflammatory colitis with pegfilgrastim treatment in a case of severe congenital neutropenia due to glucose 6 phosphatase catalytic subunit-3 deficiency. J pediatr Hem Onc 36(5):e316-e318
94.
Desplantes C et al (2014) Clinic spectrum and long-term follow-up of 14 cases with G6PC3 mutations from the French severe congenital neutropenia registry. Orphanet J Rare Dis 183(9):1–15
95.
Begin P et al (2013) Inflammatory bowel disease and T cell lymphopenia in G6PC3 deficiency. J Clin Immunol 33(3):520–525PubMedCrossRef
96.
Virdis F et al (2013) Heamophagocytic lymphohistiocytosis cased by primary Epstein-Barr virus in a patient with Crohn’s disease. World J Gastrrintest Surg 5(11):306–308CrossRef
97.
Thompson, G., PepperellD., LawrenceI., McGettiganB.D. (2017) Crohn’s disease complicated by Epstein-Barr virus-driven haemophagocytic lymphohistiocytosis successfully treated with rituximab. BMJ Case Rep
98.
Li Y, Xia X, Zhang J, Song Z, Zhou L, Zhang Y, Huang Y, Shi Y, Quigley EM, Ding S (2015) Haemophagocyticlymphohistiocytosis in inflammatory bowel disease with virus infection. Prz Gastroenterol 10(2):78–82PubMedPubMedCentralCrossRef
99.
Speckmann C et al (2013) X-linked inhibitor of apoptosis (XIAP) deficiency: the spectrum of presenting manifestations beyond hemophagocytic lymphohistiocytosis. Clin Immunol 149(1):133–141PubMedCrossRef
100.
Henter JI, Elinder G, Ost A (1991) Diagnostic guidelines for hemophagocytic lymphohistiocytosis. The FHL Study Group of the Histiocyte Society. Semin. Oncol 18(1):29–33PubMed
101.
Brito-Zeron P et al (2016) Infection is the major trigger of hemophagocytic syndrome in adult patients treated with biological therapies. Semin Arthritis Rheum 45(4):391–399PubMedCrossRef
102.
Hyams J et al (2017) Infliximab is not associated with increased risk of malignancy or hemophagocytic lymphohistiocytosis in pediatric patients with inflammatory bowel disease. Gastroenterol 152(8):1901–1914CrossRef
103.
Vogel, G., et al. (2017) Disrupted apical exocytosis of cargo vesicles causes enteropathy in FHL5 patients with Munc18-2 mutations. JCI Insight. 2(Jul (14)): p. [Epub ahead of print]
104.
Speckmann C, Ehl S (2014) XIAP deficiency is a mendelian cause of late-onset IBD. Gut 63(6):1031–1032PubMedCrossRef
105.
Aguilar C, Latour S (2015) X-linked inhibitor of apoptosis protein deficiency: more than X-linked lymphoproliferative syndrome. J Clin Immunol 35(4):331–338PubMedCrossRef
106.
Pachlopnik S et al (2011) Clinical similarities and differences of patients with X-linked lymphoproliferative syndrome type 1 (XLP-1/SAP deficiency) versus type 2 (XLP-2/XIAP deficiency). Blood 117(5):1522–1529CrossRef
107.
Nielsen OH, LaCasse EC (2017) How genetic testing can lead to targeted management of XIAP deficiency-related inflammatory bowel disease. Genet Med 19(Feb 92):133–143PubMedCrossRef
108.
109.
110.
Wing K et al (2008) CTLA-4 control over Foxp3+ regulatory T cell function. Science 322(5899):271–275CrossRefPubMed
111.
Walker L, Sansom D (2011) The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nat Rev Immnol 11:852–863CrossRef
112.
Moraes-Fontes M et al (2017) Fatal CTLA-4 heterozygosity with autoimmunity and recurrent infections: a de novo mutation. Clin Case Rep 5(12):2066–2070PubMedPubMedCentralCrossRef
113.
114.
Lee S et al (2016) Abatacept alleviates severe autoimmune symptoms in a patient carrying a de novo variant in CTLA-4. J Allergy Clin Immunol 137(1):327–330PubMedCrossRef
115.
116.
Lo B et al (2015) Patients with LRBA deficiency show CTLA4 loss and immune dysregulation responsive to abatacept therapy. Science 349(6246):436–440PubMedCrossRef
117.
Gamez-Diaz L et al (2016) The extended phenotype of LPS-responsive beige-like anchor protein (LRBA) deficiency. J Allergy Clin Immunol 137(1):223–230PubMedCrossRef
118.
119.
Haapaniemi E et al (2015) Autoimmunity, hypogammaglobulinema, lymphoproliferation, and mycobacterial disease in patients with activating mutations in STAT3. Blood 125(4):639–648PubMedCrossRefPubMedCentral
120.
Holland S et al (2007) STAT3 mutations in the hyper-IgE syndrome. NEJM 357(16):1058–1062CrossRef
121.
122.
Minegishi Y et al (2007) Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 448(7157):1058–1062PubMedCrossRef
123.
Uzel G, Sampaio EP, Lawrence MG, Hsu AP, Hackett M, Dorsey MJ, Noel RJ, Verbsky JW, Freeman AF, Janssen E, Bonilla FA, Pechacek J, Chandrasekaran P, Browne SK, Agharahimi A, Gharib AM, Mannurita SC, Yim JJ, Gambineri E, Torgerson T, Tran DQ, Milner JD, Holland SM (2013) Dominant gain-of-function STAT1 mutations in FOXP3 wild-type immune dysregulation-polyendocrinopathy-enteropathy-X-linked-like syndrome. J Allergy Clin Immunol 131(6):1611–1623PubMedCrossRefPubMedCentral
124.
Engelhardt KR et al (2013) Clnical outcome in IL-10 and IL-10 receptor-deficient patients with or without hematopoietic cell transplantation. J Allergy Clin Immunol 131(3):825–830PubMedCrossRef
125.
Glocker EO, Frede N, Perro M, Sebire N, Elawad M, Shah N, Grimbacher B (2010) Infant colitis—it’s in the genes. Lancet 376(9748):1272PubMedCrossRef
126.
Kotlarz D, Beier R, Murugan D, Diestelhorst J, Jensen O, Boztug K, Pfeifer D, Kreipe H, Pfister E–D, Baumann U, Puchalka J, Bohne J, Egritas O, Dalgic B, Kolho K–L, Sauerbrey A, Buderus S, Güngör T, Enninger A, Koda YKL, Guariso G, Weiss B, Corbacioglu S, Socha P, Uslu N, Metin A, Wahbeh GT, Husain K, Ramadan D, al–Herz W, Grimbacher B, Sauer M, Sykora K–W, Koletzko S, Klein C (2012) Loss of interluken-10 signaling and infantile inflammatory bowel disease-implications for diagnosis and therapy. Gastroenterology 143:347–355PubMedCrossRef
127.
Mao H, Yang W, Lee PPW, Ho MHK, Yang J, Zeng S, Chong CY, Lee TL, Tu W, Lau YL (2012) Exome sequencing indentifies novel compound heterozygous mutations of IL-1 receptor 1 in neonatal onset Crohn’s disease. Genes Immun 13:437–442PubMedCrossRef
128.
Salzer E, Kansu A, Sic H, Májek P, Ikincioğullari A, Dogu FE, Prengemann NK, Santos-Valente E, Pickl WF, Bilic I, Ban SA, Kuloğlu Z, Demir AM, Ensari A, Colinge J, Rizzi M, Eibel H, Boztug K (2014) Early-onset inflammatory bowel disease and common variable immunodeficiency-like disease caused by IL-21 deficiency. J Allergy Clin Immunol 133(6):1651–1659PubMedCrossRef
129.
130.
Derry J, Ochs H, Francke U (1994) Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 79(5):922
131.
Kim A et al (2000) Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404:151–158PubMedCrossRef
132.
Jin Y, Mazza C, Christie JR, Giliani S, Fiorini M, Mella P, Gandellini F, Stewart DM, Zhu Q, Nelson DL, Notarangelo LD, Ochs HD (2004) Mutations of the Wiskott-Aldrich Syndrome Protein (WASP): hotspots, effect on transcription, and translation and phenotype/genotype correlation. Blood 104(13):4010–4019PubMedCrossRef
133.
Devriendt K, Kim AS, Mathijs G, Frints SGM, Schwartz M, van den Oord JJ, Verhoef GEG, Boogaerts MA, Fryns JP, You D, Rosen MK, Vandenberghe P (2001) Constitutively activating mutation in WASP causes X-linked severe congenital neutropenia. Nat Genet 27(3):313–317PubMedCrossRef
134.
Dupuis-Girod S, Medioni J, Haddad E, Quartier P, Cavazzana-Calvo M, le Deist F, de Saint Basile G, Delaunay J, Schwarz K, Casanova JL, Blanche S, Fischer A (2003) Autoimmunity in Wiskott-Aldrich syndrome: risk factors, clinical features and outcome in a single center cohort of 55 patients. Pediatrics 111:e622–e627PubMedCrossRef
135.
Candotti F (2018) Clinical manifestations and pathophysiological mechanisms of the Wiskott-Aldrich syndrome. J Clin Immunol 38:13–27PubMedCrossRef
136.
Ngwube, A., et al. (2017) Outcomes after allogeneic transplant in patients with Wiskott-Aldrich syndrome. Biol Blood Marrow Transplant (17): p. Epub ahead of print
137.
Chen N, Zhang ZY, Liu DW, Liu W, Tang XM, Zhao XD (2015) The clinical features of autoimmunity in 53 patients with Wiskott-Aldrich syndrome in China: a single-center study. Eur J Pediatr 174:1311–1318PubMedCrossRef
138.
Afazali B et al (2017) BACH2 immunodeficiency illustrates an association between super-enhancers and haploinsufficiency. Nat Immunol 18(7):813–823CrossRef
139.
Conrad MA, Dawany N, Sullivan KE, Devoto M, Kelsen JR (2017) Novel ZBTB24 mutation associated with immunodeficiency, centromere instability, and facial anomalies type-2 syndrome identified in a patient with very early onset inflammatory bowel disease. Inflamm Bowel Dis 23(12):2252–2255PubMedCrossRef
140.
Boland BS, Widjaja CE, Banno A, Zhang B, Kim SH, Stoven S, Peterson MR, Jones MC, Su HI, Crowe SE, Bui JD, Ho SB, Okugawa Y, Goel A, Marietta EV, Khosroheidari M, Jepsen K, Aramburu J, López-Rodríguez C, Sandborn WJ, Murray JA, Harismendy O, Chang JT (2015) Immunodeficiency and autoimmune enterocolopathy linked to NFAT5 haploinsufficiency. J Immunol 194(6):2551–2560PubMedCrossRef
141.
Nagamine K, Peterson P, Scott HS, Kudoh J, Minoshima S, Heino M, Krohn KJE, Lalioti MD, Mullis PE, Antonarakis SE, Kawasaki K, Asakawa S, Ito F, Shimizu N (1997) Positional cloning of the APECED gene. Nat Genet 17:393–398PubMedCrossRef
142.
Kluger N, Jokinen M, Krohn K, Ranki A (2013) Gastrointestinal manifestations in APECED syndrome. J Clin Gastroenterol 47(2):112–120PubMedCrossRef
143.
Chida N, Kobayashi I, Takezaki S, Ueki M, Yamazaki Y, Garelli S, Scarpa R, Horikawa R, Yamada M, Betterle C, Notarangelo LD, Yawaka Y, Ariga T (2015) Disease specificity of anti-tryptophan hydroxylase-1 and anti-AIE-75 autoantibodies in APECED and IPEX syndrome. Clin Immunol 156(1):36–42PubMedCrossRef
144.
145.
Jeon M et al (2004) Essential role of the E3 ubiquitin ligase Cbl-b in T cell anergy induction. Immunity 21:167–177PubMedCrossRef
146.
Romberg N, al Moussawi K, Nelson-Williams C, Stiegler AL, Loring E, Choi M, Overton J, Meffre E, Khokha MK, Huttner AJ, West B, Podoltsev NA, Boggon TJ, Kazmierczak BI, Lifton RP (2014) Mutation of NLRC4 causes a syndrome of enterocolitis and autoinflammation. Nat Genet 46(10):1135–1139PubMedPubMedCentralCrossRef
147.
Canna SW, Girard C, Malle L, de Jesus A, Romberg N, Kelsen J, Surrey LF, Russo P, Sleight A, Schiffrin E, Gabay C, Goldbach-Mansky R, Behrens EM (2017) Life-threatening NLRC4-associated hyperinflammation successfully treated with IL-18 inhibition. J Allergy Clin Immunol 139(5):1698–1701PubMedCrossRef
148.
Jorgensen S et al (2016) Altered gut microbiota profile in common variable immunodeficiency associates with levels of lipopolysaccharide and markers of systemic immune activation. Mucossal Immunol 9(6):1455–1465CrossRef
149.
Cordova Guevara H, Guarner Aguilar L (2009) Effective treatment of common variable immunodeficiency associated diarrhea. Rev Esp Enferm Dig 101(3):215–219PubMedCrossRef
150.
Malamut G, Verkarre V, Suarez F, Viallard JF, Lascaux AS, Cosnes J, Bouhnik Y, Lambotte O, Béchade D, Ziol M, Lavergne A, Hermine O, Cerf-Bensussan N, Cellier C (2010) The enteropathy associated with common variable immunodeficiency: the delineated frontiers with celiac disease. Am J Gastroenterol 105(10):2262–2275PubMedCrossRef
151.
Kralickova P, Mala E, Vokurkova D, Krcmova I, Pliskova L, Stepanova V, Bartos V, Koblizek V, Tacheci I, Bures J, Brozik J, Litzman J (2014) Cytomegalovirus disease in patients with common variable immunodeficiency: three case reports. Int Arch Allergy Immunol 163(1):69–74PubMedCrossRef
152.
Salcedo J, Keates S, Pothoulakis C, Warny M, Castagliuolo I, LaMont JT, Kelly CP (1997) Intravenous immunoglobulin therapy for severe Clostridium difficile colitis. Gut 41(3):366–370PubMedPubMedCentralCrossRef
153.
Woodward JM, Gkrania-Klotsas E, Cordero-Ng AYK, Aravinthan A, Bandoh BN, Liu H, Davies S, Zhang H, Stevenson P, Curran MD, Kumararatne D (2015) The role of chronic norovirus infection in the enteropathy associated with common variable immunodeficiency. Am J Gastroenterol 110(2):320–327PubMedCrossRef
154.
van de Ven AA et al (2014) Increased prevalence of gastrointestinal viruses and diminished secretory immunoglobulin a levels in antibody deficiencies. J Clin Immunol 34(8):962–970PubMedCrossRef
155.
Fabre A et al (2014) Syndrome (phenotypic) diarrhoea of infancy/tricho-hepato-enteric syndrome. Arch Dis Child 99(1):35–38PubMedCrossRef
156.
Girault D et al (1994) Intractable infant diarrhea associated with phenotypic abnormalities and immunodeficiency. J Pediatr 125(1):36–42PubMedCrossRef
157.
Hartley J et al (2010) Mutations in TTC37 cause tricohepatoenteric syndrome (phenotypic diarrhea of infancy). Gastroenterology 138(7):2388–2398PubMedCrossRef
158.
159.
Stepensky P et al (2013) Persistent defective membrane trafficking in epithelial cells of patients with familial hemophagocytic lymphohystiocytosis type 5 due to STXBP2/MUNC18-2 mutations. Pediatr Blood Cancer 60(7):1215–1222PubMedCrossRef
160.
Pagel J et al (2010) Distinct mutations in STXBP2 are associated with variable clinical presentations in patients with familial hemophagocytic lymphohistiocytosis type 5 (FHL5). Blood 119(25):6016–6024CrossRef
161.
de la Morena MT, Leonard D, Torgerson TR, Cabral-Marques O, Slatter M, Aghamohammadi A, Chandra S, Murguia-Favela L, Bonilla FA, Kanariou M, Damrongwatanasuk R, Kuo CY, Dvorak CC, Meyts I, Chen K, Kobrynski L, Kapoor N, Richter D, DiGiovanni D, Dhalla F, Farmaki E, Speckmann C, Español T, Shcherbina A, Hanson IC, Litzman J, Routes JM, Wong M, Fuleihan R, Seneviratne SL, Small TN, Janda A, Bezrodnik L, Seger R, Raccio AG, Edgar JDM, Chou J, Abbott JK, van Montfrans J, González-Granado LI, Bunin N, Kutukculer N, Gray P, Seminario G, Pasic S, Aquino V, Wysocki C, Abolhassani H, Dorsey M, Cunningham-Rundles C, Knutsen AP, Sleasman J, Costa Carvalho BT, Condino-Neto A, Grunebaum E, Chapel H, Ochs HD, Filipovich A, Cowan M, Gennery A, Cant A, Notarangelo LD, Roifman CM (2017) Long-term outcomes of 176 patients with X-linked hyper-IgM syndrome treated with or without hematopoietic cell transplantation. J Allergy Clin Immunol 139(4):1282–1292PubMedCrossRef
162.
Albuquerque A (2014) Nodular lymphoid hyperplasia in the gastrointestinal tract in adult patients: a review. World J Gastroenterol 6(11):534–540
163.
Ranchod M, Lewkin K, Dorfman R (1978) Lymphoid hyperplasia of the gastrointestinal tract.A study of 26 cases and review of the literature. Am J Surg Pathol 2:383–400PubMedCrossRef
164.
Colon A, DiPalma J, Leftridge C (1991) Intestinal lympho-nodular hyperplasia of childhood: patterns of presentation. J Clin Gastroenterol 13:163–166PubMedCrossRef
165.
Rambaud J et al (1982) Diffuse follicular lymphoid hyperplasia of the small intestine without primary antibody deficiency. Am J Med 73:125–132PubMedCrossRef
166.
Joo M, Shim SH, Chang SH, Kim H, Chi JG, Kim NH (2009) Nodular lymphoid hyperplasia and histologic changes mimicking celiac disease, collagenous sprue, and lymphocytic colitis in a patient with selective IgA deficiency. Pathol Res Pract 205(12):876–880PubMedCrossRef
167.
Schwartz D, Cole CE, Sun Y, Jacoby RF (2003) Diffuse nodular lymphoid hyperplasia of the colon: polyposis syndrome or normal variant? Gastrointest Endosc 58:630–632PubMed
168.
Rubio-Tapia A, Hernández-Calleros J, Trinidad-Hernández S, Uscanga L (2006) Clinical characteristics of a group of adults with nodular lymphoid hyperplasia: a single center experience. World J Gastroenterol 12:1945–1948PubMedPubMedCentralCrossRef
169.
Hermans P et al (1966) Dysgammaglobulinemia associated with nodular lymphoid hyperplasia of the small intestine. Am J Med 40:78–89PubMedCrossRef
170.
Khuroo M, Khuroo N, Khuroo M (2011) Diffuse duodenal nodular lymphoid hyperplasia: a large cohort of patients etiologically related to Helicobacter pylori infection. BMC Gastroentrol 11(36):1–11
171.
Hanich T, Majnarić L, Janković D, Šabanović Š, Včev A (2017) Nodular lymphoid hyperplasia complicated with ileal Burkitt’s lymphoma in an adult patient with selective IgA deficiency. Int J Surg Case Rep 30:69–72PubMedCrossRef
172.
Collin P, Mäki M, Keyriläinen O, Hällström O, Reunala T, Pasternack A (1992) Selective IgA deficiency and coeliac disease. Scand J Gastroenterol 27:367–371PubMedCrossRef
173.
Ouakaa-Kchaou A, Trad D, Boussourra H, Bibani N, Elloumi H, Kochlef A, Gargouri D, Kharrat J (2015) Hypogammaglobulinemia associated with nodular lymphoid hyperplasia of the intestine and pernicious anaemia. Tunis Med 93(11):662–664PubMed
174.
Webster AD, Kenwright S, Ballard J, Shiner M, Slavin G, Levi AJ, Loewi G, Asherson GL (1977) Nodular lymphoid hyperplasia of the bowel in primary hypogammaglobulinaemia: study of in vivo and in vitro lymphocyte function. Gut 18(5):364–372PubMedPubMedCentralCrossRef
175.
Bayraktar Y, Ersoy O, Sokmensuer C (2007) The findings of capsule endoscopy in patients with common variable immunodeficiency syndrome. Hepato-Gastroenterology 54(76):1034–1037PubMed
176.
Van den Brande P et al (1988) Intestinal nodular lymphoid hyperplasia in patients with common variable immunodeficiency: local accumulation of B and CD8(+) lymphocytes. J Clin Immunol 8(4):296–306PubMedCrossRef
177.
Rodrigues F, Graham Davies E, Harrison P, McLauchlin J, Karani J, Portmann B, Jones A, Veys P, Mieli-Vergani G, Hadžić N (2004) Liver disease in children with primary immunodeficiencies. J Pediatr 145(3):333–339PubMedCrossRef
178.
van den Berge J et al (2009) Chronic granulomatous disease:the European experience. PLoS One 4(4):e5234CrossRef
179.
Hussain N et al (2007) Hepatic abnormalities in patients with chronic granulomatous disease. Hepatology 45(3):675–683PubMedCrossRef
180.
Levy J, Espanol-Boren T, Thomas C, Fischer A, Tovo P, Bordigoni P, Resnick I, Fasth A, Baer M, Gomez L, Sanders EAM, Tabone MD, Plantaz D, Etzioni A, Monafo V, Abinun M, Hammarstrom L, Abrahamsen T, Jones A, Finn A, Klemola T, DeVries E, Sanal O, Peitsch MC, Notarangelo LD (1997) Clinical spectrum of X-linked hyper-IgM syndrome. J Pediatr 131(1 Pt 1):47–54PubMedCrossRef
181.
Durandy A et al (2013) Potential roles of activation-induced cytidine deaminase in promotion or prevention of autoimmunity in humans. Autoimmunity 46(2):148–156PubMedPubMedCentralCrossRef
182.
de Pontual L et al (2007) Epistatic interactions with a common hypomorphic RET allele in syndromic Hirschprung disease. Hum Mutat 28(8):790–796PubMedCrossRef
183.
Makitie O et al (2002) Hirschprung’s disease in cartilage-hairhypoplasia has poor prognosis. J Pediatr Surg 37(11):1585–1588PubMedCrossRef
184.
Digilio MC, Marino B, Bagolan P, Giannotti A, Dallapiccola B (1999) Microdeletion 22q11 and oesophageal atresia. J Med Genet 36(2):137–139PubMedPubMedCentral
185.
Arora M, Bagi P, Strongin A, Heimall J, Zhao X, Lawrence MG, Trivedi A, Henderson C, Hsu A, Quezado M, Kleiner DE, Venkatesan AM, Holland SM, Freeman AF, Heller T (2017) Gastrointestinal manifestations of STAT3-deficient hyper-IgE syndrome. J Clin Immunol 37(7):695–700PubMedCrossRefPubMedCentral
186.
Chen R et al (2013) Whole-exome sequencing identifies tetratricopeptide repeat domain 7A (TTC7A) mutations for combined immunodeficiency with intestinal atresias. J Allergy Clin Immunol 132(3):656–664 e17PubMedPubMedCentralCrossRef
187.
Samuels ME, Majewski J, Alirezaie N, Fernandez I, Casals F, Patey N, Decaluwe H, Gosselin I, Haddad E, Hodgkinson A, Idaghdour Y, Marchand V, Michaud JL, Rodrigue MA, Desjardins S, Dubois S, le Deist F, Awadalla P, Raymond V, Maranda B (2013) Exome sequencing identifies mutations in the gene TTC7A in French-Canadian cases with hereditary multiple intestinal atresia. J Med Genet 50(5):324–329PubMedCrossRef
188.
Guttman FM, Braun P, Garance PH, Blanchard H, Collin PP, Dallaire L, Desjardins JG, Perreault G (1973) Multiple atresias and a new syndrome of hereditary multiple atresias involving the gastrointestinal tract from stomach to rectum. J Pediatr Surg 8(5):633–640PubMedCrossRef
189.
Mishalany HG, Der Kaloustian VM (1971) Familial multiple-level intestinal atresias: report of two siblings. J Pediatr 79(1):124–125PubMedCrossRef
190.
Moreno LA, Gottrand F, Turck D, Manouvrier-Hanu S, Mazingue F, Morisot C, le Deist F, Ricour C, Nihoul-Feketé C, Debeugny P, Griscelli C, Farriaux JP (1990) Severe combined immunodeficiency syndrome associated with autosomal recessive familial multiple gastrointestinal atresias: study of a family. Am J Med Genet 37(1):143–146PubMedCrossRef
191.
Rothenberg ME, White FV, Chilmonczyk B, Chatila T (1995) A syndrome involving immunodeficiency and multiple intestinal atresias. Immunodeficiency 5(3):171–178PubMed
192.
Ali, Y.A., et al. (2011) Hereditary multiple intestinal atresia (HMIA) with severe combined immunodeficiency (SCID): a case report of two siblings and review of the literature on MIA, HMIA and HMIA with immunodeficiency over the last 50 years. BMJ Case Rep 2011
193.
Lavilla P et al (1993) X-lined agammaglobulinemia and gastric adenocarcinoma. Cancer 72(5):1528–1531PubMedCrossRef
194.
Page A, Hansen A, Good R (1963) Occurrence of leukemia and lymphoma in patients with agammaglobulinemia. Blood 21(2):197–206PubMedCrossRef
195.
Mortaz E et al (2016) Cancers related to immunodeficiencies: update and perspectives. Front Immunol 7:1–13CrossRef
196.
Agarwal S, Mayer L (2009) Pathogenesis and treatment of gastrointestinal disese in antibody deficiency syndromes. J Allergy Clin Immunol 124(4):658–664PubMedCrossRef
197.
Conley ME, Ziegler MM, IV SB, Huff DS, Boyle JT (1988) Multifocal adenocarcinoma of the stomach in a child with common variable immunodeficiency. J Pediatr Gastroenterol Nutr 7(3):456–460PubMedCrossRef
198.
van der Meer J et al (1993) Colorectal cancer in patients with X-linked agammaglobulinemia. Lancet 341:1439–1440PubMedCrossRef
199.
Levin E et al (2016) Hyper IgM syndrome: a report from the USIDNET Registry. J Clin Immunol 36:490–501CrossRef
200.
Donaldson GP, Lee SM, Mazmanian SK (2016) Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 14(1):20–32PubMedCrossRef
201.
Lamers CB et al (1980) Jejunal lymphoma in a patient with primary adult-onset hypogammaglobulinemia and nodular lymphoid hyperplasia of the small intestine. Dig Dis Sci 25(7):553–557PubMedCrossRef
202.
Casetellano G et al (1992) Malignant lymphoma of jejunum with common variable hypogammaglobulinemia and diffuse nodular lymphoid hyperplasia of the small intestine. A case study and literature review. J Clin Gastroenterol 15(2):128–135CrossRef
203.
Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638PubMedCrossRefPubMedCentral
204.
Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28(10):1221–1227PubMedCrossRefPubMedCentral
205.
Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446–450PubMedCrossRef
206.
Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504(7480):451–455PubMedPubMedCentralCrossRef
207.
208.
Thorburn AN, McKenzie CI, Shen S, Stanley D, Macia L, Mason LJ, Roberts LK, Wong CHY, Shim R, Robert R, Chevalier N, Tan JK, Mariño E, Moore RJ, Wong L, McConville MJ, Tull DL, Wood LG, Murphy VE, Mattes J, Gibson PG, Mackay CR (2015) Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat Commun 6:7320PubMedCrossRef
209.
Rider N et al (2009) Immunologic and clinical features of 25 Amish patients with RMRP 70 A→G cartilage hair hypoplasia. Clin Immunol 131(1):119–128PubMedCrossRef
Metadata
Title
Gastrointestinal Disorders Associated with Primary Immunodeficiency Diseases
Authors
Stella Hartono
Michelina Rosa Ippoliti
Maria Mastroianni
Ricardo Torres
Nicholas L. Rider
Publication date
01-10-2019
Publisher
Springer US
Published in
Clinical Reviews in Allergy & Immunology / Issue 2/2019
Print ISSN: 1080-0549
Electronic ISSN: 1559-0267
DOI
https://doi.org/10.1007/s12016-018-8689-9

Other articles of this Issue 2/2019

Clinical Reviews in Allergy & Immunology 2/2019 Go to the issue

ReviewPaper

Gastrointestinal Manifestations of Hypereosinophilic Syndromes and Mast Cell Disorders: a Comprehensive Review

OriginalPaper

IgE-Mediated Food Allergy

ReviewPaper

Nutritional Issues in Food Allergy

ReviewPaper

Food Protein-Induced Enterocolitis Syndrome: a Comprehensive Review

ReviewPaper

Allergic and Immunologic Perspectives of Inflammatory Bowel Disease

ReviewPaper

A Comprehensive Review of Celiac Disease/Gluten-Sensitive Enteropathies
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits