Pathogenesis and treatment of gastrointestinal disease in antibody deficiency syndromes
2009; Elsevier BV; Volume: 124; Issue: 4 Linguagem: Inglês
10.1016/j.jaci.2009.06.018
ISSN1097-6825
Autores Tópico(s)Chronic Lymphocytic Leukemia Research
ResumoPrimary humoral immune deficiencies are characterized by limited antibody responses secondary to either impaired B-lymphocyte development or B-cell responses to T-lymphocyte signals. Given that the gastrointestinal tract is the largest lymphoid organ in the body, it is not surprising that intestinal diseases are common in immunodeficiency. These gastrointestinal diseases can be classified into one of 4 groups, infection, malignancy, inflammatory, and autoimmune, and can mimic other known disease processes, such as inflammatory bowel disease and celiac sprue. The exact pathogenesis of these gastrointestinal disorders in the setting of systemic immunodeficiency is still under investigation. However, studies suggest that defects in antibody deficiency alone do not result in gastrointestinal disease but rather that defects in cellular immunity are also involved. Treatment is difficult given an already immunocompromised state, and often therapy with immunomodulators is required for more severe processes. Primary humoral immune deficiencies are characterized by limited antibody responses secondary to either impaired B-lymphocyte development or B-cell responses to T-lymphocyte signals. Given that the gastrointestinal tract is the largest lymphoid organ in the body, it is not surprising that intestinal diseases are common in immunodeficiency. These gastrointestinal diseases can be classified into one of 4 groups, infection, malignancy, inflammatory, and autoimmune, and can mimic other known disease processes, such as inflammatory bowel disease and celiac sprue. The exact pathogenesis of these gastrointestinal disorders in the setting of systemic immunodeficiency is still under investigation. However, studies suggest that defects in antibody deficiency alone do not result in gastrointestinal disease but rather that defects in cellular immunity are also involved. Treatment is difficult given an already immunocompromised state, and often therapy with immunomodulators is required for more severe processes. The mucosal immune system of the gastrointestinal tract faces distinct challenges in the form of commensal bacteria and dietary antigens daily. However, the system must maintain its integrity and be able to distinguish between harmful pathogens and normal intestinal flora. The intestine is the largest lymphoid organ in the body, housing more cells and being the site of greatest production of antibody (secretory IgA) in the body for protection against foreign antigens. T lymphocytes function to regulate the immune response toward viruses, intracellular bacteria, and parasites, whereas B lymphocytes function to protect against bacterial organisms and produce immunoglobulins. In addition, secreted factors, such as gastric acid, lysozyme, lactoferrin, and mucin, serve as innate defenses and further contribute to antimicrobial activities. Unlike the systemic immune system, where foreign proteins, carbohydrates, and lipids are viewed as potential pathogens and eventually destroyed, the microenvironment and macroenvironment of the gastrointestinal tract is continuously exposed to bacteria, viruses, and parasites but maintains a balance between active immunity, tolerance, and immune suppression. Dysregulation of this controlled/physiologic inflammation in the gut can lead to mucosal injury and diseases such as inflammatory bowel disease (IBD), food allergy, or celiac sprue. Therefore it is not surprising that gastrointestinal disease is a common manifestation in patients with an underlying immunodeficiency in whom there is dysregulation in humoral immunity, cell-mediated immunity, or both. Primary antibody deficiencies are the most common form of primary immunodeficiency diseases. The spectrum of immune deficiency is wide, ranging from a complete lack of B cells and absent serum immunoglobulins in X-linked agammaglobulinemia (XLA) to a reduction in only specific immunoglobulin isotypes, such as in selective IgA deficiency. Despite this broad difference in immunity, the antibody deficiency syndromes share clinical manifestations, such as recurrent sinopulmonary infections, autoimmunity, and gastrointestinal disease. There are 4 major types of gastrointestinal manifestations associated with humoral immunodeficiencies: infection, malignancy, inflammatory, and autoimmunity (Table I). Treatment for antibody deficiency syndromes is the administration of immunoglobulin (intravenous or subcutaneous), which may reduce the frequency of infections and autoimmune disease, such as immune thrombocytopenic purpura. However, gastrointestinal diseases are not treated with immunoglobulin because preparations contain IgG, which cannot reach the lumen of the intact gut, and very little IgA or IgM. Treatment with oral immunoglobulin has not been successful because IgG is rapidly destroyed before reaching the small intestine. Currently, treatment for gastrointestinal manifestations in antibody deficiency syndromes is guided by successful therapy used for similar disorders in immunocompetent patients, with additional caution when immunosuppressive agents are administered. In this review we will discuss 3 major primary immunodeficiencies and highlight the gastrointestinal manifestations associated with these disorders. The incidence of these manifestations ranged from 20% to 60% in past reviews.1Ammann A.J. Hong R. Selective IgA deficiency: presentation of 30 cases and a review of the literature.Medicine (Baltimore). 1971; 50: 223-236Crossref PubMed Google Scholar, 2Cunningham-Rundles C. Clinical and immunologic analyses of 103 patients with common variable immunodeficiency.J Clin Immunol. 1989; 9: 22-33Crossref PubMed Scopus (272) Google Scholar, 3Cunningham-Rundles C. Bodian C. Common variable immunodeficiency: clinical and immunological features of 248 patients.Clin Immunol. 1999; 92: 34-48Crossref PubMed Scopus (872) Google Scholar, 4Hermaszewski R.A. Webster A.D. Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications.QJM. 1993; 86: 31-42PubMed Google Scholar, 5Khodadad A. Aghamohammadi A. Parvaneh N. Rezaei N. Mahjoob F. Bashashati M. et al.Gastrointestinal manifestations in patients with common variable immunodeficiency.Dig Dis Sci. 2007; 52: 2977-2983Crossref PubMed Scopus (54) Google Scholar, 6Lederman H.M. Winkelstein J.A. X-linked agammaglobulinemia: an analysis of 96 patients.Medicine (Baltimore). 1985; 64: 145-156Crossref PubMed Google Scholar, 7Lai Ping So A. Mayer L. Gastrointestinal manifestations of primary immunodeficiency disorders.Semin Gastrointest Dis. 1997; 8: 22-32PubMed Google Scholar Our discussion is limited to antibody deficiency syndromes, although patients with combined T- and B-cell immunodeficiencies, such as severe combined immunodeficiency, or defects in innate immunity, such as chronic granulomatous disease, also have gastrointestinal disease. These immunodeficiency syndromes can be further reviewed in the literature; however, we have included them and their associated gastrointestinal manifestations in Table II1Ammann A.J. Hong R. Selective IgA deficiency: presentation of 30 cases and a review of the literature.Medicine (Baltimore). 1971; 50: 223-236Crossref PubMed Google Scholar, 3Cunningham-Rundles C. Bodian C. Common variable immunodeficiency: clinical and immunological features of 248 patients.Clin Immunol. 1999; 92: 34-48Crossref PubMed Scopus (872) Google Scholar, 4Hermaszewski R.A. Webster A.D. Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications.QJM. 1993; 86: 31-42PubMed Google Scholar, 5Khodadad A. Aghamohammadi A. Parvaneh N. Rezaei N. Mahjoob F. Bashashati M. et al.Gastrointestinal manifestations in patients with common variable immunodeficiency.Dig Dis Sci. 2007; 52: 2977-2983Crossref PubMed Scopus (54) Google Scholar, 6Lederman H.M. Winkelstein J.A. X-linked agammaglobulinemia: an analysis of 96 patients.Medicine (Baltimore). 1985; 64: 145-156Crossref PubMed Google Scholar, 8Conley M.E. Rohrer J. Minegishi Y. X-linked agammaglobulinemia.Clin Rev Allergy Immunol. 2000; 19: 183-204Crossref PubMed Google Scholar, 9Winkelstein J.A. Marino M.C. Lederman H.M. Jones S.M. Sullivan K. Burks A.W. et al.X-linked agammaglobulinemia: report on a United States registry of 201 patients.Medicine (Baltimore). 2006; 85: 193-202Crossref PubMed Scopus (184) Google Scholar, 10Atarod L. Raissi A. Aghamohammadi A. Farhoudi A. Khodadad A. Moin M. et al.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. 2003; 2: 75-79PubMed Google Scholar, 11Cellier C. Foray S. Hermine O. Regional enteritis associated with enterovirus in a patient with X-linked agammaglobulinemia.N Engl J Med. 2000; 342: 1611-1612Crossref PubMed Scopus (15) Google Scholar, 12Misbah S.A. Spickett G.P. Ryba P.C. Hockaday J.M. Kroll J.S. Sherwood C. et al.Chronic enteroviral meningoencephalitis in agammaglobulinemia: case report and literature review.J Clin Immunol. 1992; 12: 266-270Crossref PubMed Scopus (79) Google Scholar, 13Washington K. Stenzel T.T. Buckley R.H. Gottfried M.R. Gastrointestinal pathology in patients with common variable immunodeficiency and X-linked agammaglobulinemia.Am J Surg Pathol. 1996; 20: 1240-1252Crossref PubMed Scopus (165) Google Scholar, 14Collin P. Maki M. Keyrilainen O. Hallstrom O. Reunala T. Pasternack A. Selective IgA deficiency and coeliac disease.Scand J Gastroenterol. 1992; 27: 367-371Crossref PubMed Scopus (169) Google Scholar, 15Heneghan M.A. Stevens F.M. Cryan E.M. Warner R.H. McCarthy C.F. Celiac sprue and immunodeficiency states: a 25-year review.J Clin Gastroenterol. 1997; 25: 421-425Crossref PubMed Scopus (62) Google Scholar, 16Meini A. Pillan N.M. Villanacci V. Monafo V. Ugazio A.G. Plebani A. Prevalence and diagnosis of celiac disease in IgA-deficient children.Ann Allergy Asthma Immunol. 1996; 77: 333-336Abstract Full Text PDF PubMed Google Scholar, 17Cataldo F. Marino V. Ventura A. Bottaro G. Corazza G.R. Prevalence and clinical features of selective immunoglobulin A deficiency in coeliac disease: an Italian multicentre study. Italian Society of Paediatric Gastroenterology and Hepatology (SIGEP) and "Club del Tenue" Working Groups on Coeliac Disease.Gut. 1998; 42: 362-365Crossref PubMed Google Scholar, 18Jacobson K.W. deShazo R.D. Selective immunoglobulin A deficiency associated with modular lymphoid hyperplasia.J Allergy Clin Immunol. 1979; 64: 516-521Abstract Full Text PDF PubMed Scopus (9) Google Scholar, 19Piascik M. Rydzewska G. Pawlik M. Milewski J. Furmanek M.I. Wronska E. et al.Diffuse nodular lymphoid hyperplasia of the gastrointestinal tract in patient with selective immunoglobulin A deficiency and sarcoid-like syndrome—case report.Adv Med Sci. 2007; 52: 296-300PubMed Google Scholar, 20Kalha I. Sellin J.H. Common variable immunodeficiency and the gastrointestinal tract.Curr Gastroenterol Rep. 2004; 6: 377-383Crossref PubMed Google Scholar, 21Luzi G. Zullo A. Iebba F. Rinaldi V. Sanchez Mete L. Muscaritoli M. et al.Duodenal pathology and clinical-immunological implications in common variable immunodeficiency patients.Am J Gastroenterol. 2003; 98: 118-121Crossref PubMed Scopus (63) Google Scholar, 22Teahon K. Webster A.D. Price A.B. Weston J. Bjarnason I. Studies on the enteropathy associated with primary hypogammaglobulinaemia.Gut. 1994; 35: 1244-1249Crossref PubMed Google Scholar, 23Mannon P.J. Fuss I.J. Dill S. Friend J. Groden C. Hornung R. et al.Excess IL-12 but not IL-23 accompanies the inflammatory bowel disease associated with common variable immunodeficiency.Gastroenterology. 2006; 131: 748-756Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar, 24Twomey J.J. Jordan P.H. Jarrold T. Trubowitz S. Ritz N.D. Conn H.O. The syndrome of immunoglobulin deficiency and pernicious anemia. A study of ten cases.Am J Med. 1969; 47: 340-350Abstract Full Text PDF PubMed Google Scholar, 25Twomey J.J. Jordan Jr., P.H. Laughter A.H. Meuwissen H.J. Good R.A. The gastric disorder in immunoglobulin-deficient patients.Ann Intern Med. 1970; 72: 499-504Crossref PubMed Google Scholar, 26Ermis F. Akyuz F. Demir K. Besisik F. Boztas G. Mungan Z. Rapidly progressive HCV cirrhosis in a hypogammaglobulinemic patient.Intern Med. 2008; 47: 415-417Crossref PubMed Scopus (4) Google Scholar, 27Sumazaki R. Matsubara T. Aoki T. Nagai Y. Shibasaki M. Takita H. Rapidly progressive hepatitis C in a patient with common variable immunodeficiency.Eur J Pediatr. 1996; 155: 532-534Crossref PubMed Google Scholar, 28Daniels J.A. Torbenson M. Vivekanandan P. Anders R.A. Boitnott J.K. Hepatitis in common variable immunodeficiency.Hum Pathol. 2009; 40: 484-488Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar, 29Cardinale F. Friman V. Carlsson B. Bjorkander J. Armenio L. Hanson L.A. Aberrations in titer and avidity of serum IgM and IgG antibodies to microbial and food antigens in IgA deficiency.Adv Exp Med Biol. 1995; 371B: 713-716PubMed Google Scholar, 30Cunningham-Rundles C. Siegal F.P. Cunningham-Rundles S. Lieberman P. Incidence of cancer in 98 patients with common varied immunodeficiency.J Clin Immunol. 1987; 7: 294-299Crossref PubMed Scopus (149) Google Scholar, 31Daniels J.A. Lederman H.M. Maitra A. Montgomery E.A. Gastrointestinal tract pathology in patients with common variable immunodeficiency (CVID): a clinicopathologic study and review.Am J Surg Pathol. 2007; 31: 1800-1812Crossref PubMed Scopus (124) Google Scholar, 32Nos P. Bastida G. Beltran B. Aguas M. Ponce J. Crohn's disease in common variable immunodeficiency: treatment with antitumor necrosis factor alpha.Am J Gastroenterol. 2006; 101: 2165-2166Crossref PubMed Scopus (14) Google Scholar, 33Onbasi K. Gunsar F. Sin A.Z. Ardeniz O. Kokuludag A. Sebik F. Common variable immunodeficiency (CVID) presenting with malabsorption due to giardiasis.Turk J Gastroenterol. 2005; 16: 111-113PubMed Google Scholar, 34Sawatzki M. Peter S. Hess C. Therapy-resistant diarrhea due to Giardia lamblia in a patient with common variable immunodeficiency disease.Digestion. 2007; 75: 101-102Crossref PubMed Scopus (5) Google Scholar, 35Mir-Madjlessi S.H. Vafai M. Khademi J. Kamalian N. Coexisting primary malignant lymphoma and adenocarcinoma of the large intestine in an IgA-deficient boy.Dis Colon Rectum. 1984; 27: 822-824Crossref PubMed Scopus (19) Google Scholar, 36Conley M.E. Parolini O. Rohrer J. Campana D. X-linked agammaglobulinemia: new approaches to old questions based on the identification of the defective gene.Immunol Rev. 1994; 138: 5-21Crossref PubMed Google Scholar, 37Barton L.L. Moussa S.L. Villar R.G. Hulett R.L. Gastrointestinal complications of chronic granulomatous disease: case report and literature review.Clin Pediatr (Phila). 1998; 37: 231-236Crossref PubMed Google Scholar, 38Huang A. Abbasakoor F. Vaizey C.J. Gastrointestinal manifestations of chronic granulomatous disease.Colorectal Dis. 2006; 8: 637-644Crossref PubMed Scopus (24) Google Scholar, 39Marciano B.E. Rosenzweig S.D. Kleiner D.E. Anderson V.L. Darnell D.N. Anaya-O'Brien S. et al.Gastrointestinal involvement in chronic granulomatous disease.Pediatrics. 2004; 114: 462-468Crossref PubMed Scopus (151) Google Scholar, 40Rosh J.R. Tang H.B. Mayer L. Groisman G. Abraham S.K. Prince A. Treatment of intractable gastrointestinal manifestations of chronic granulomatous disease with cyclosporine.J Pediatr. 1995; 126: 143-145Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar, 41Wang J. Mayer L. Cunningham-Rundles C. Use of GM-CSF in the treatment of colitis associated with chronic granulomatous disease.J Allergy Clin Immunol. 2005; 115: 1092-1094Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar, 42Folwaczny C. Ruelfs C. Walther J. Konig A. Emmerich B. Ulcerative colitis in a patient with Wiskott-Aldrich syndrome.Endoscopy. 2002; 34: 840-841Crossref PubMed Scopus (15) Google Scholar, 43Hsieh K.H. Chang M.H. Lee C.Y. Wang C.Y. Wiskott-Aldrich syndrome and inflammatory bowel disease.Ann Allergy. 1988; 60: 429-431PubMed Google Scholar, 44Ochs H.D. Thrasher A.J. The Wiskott-Aldrich syndrome.J Allergy Clin Immunol. 2006; 117: 725-739Abstract Full Text Full Text PDF PubMed Scopus (197) Google Scholar, 45Buckley R.H. Primary cellular immunodeficiencies.J Allergy Clin Immunol. 2002; 109: 747-757Abstract Full Text Full Text PDF PubMed Scopus (94) Google Scholar, 46Antachopoulos C. Walsh T.J. Roilides E. Fungal infections in primary immunodeficiencies.Eur J Pediatr. 2007; 166: 1099-1117Crossref PubMed Scopus (87) Google Scholar, 47Fogarty L. Thrush and septic shock in a two-month-old.Pediatr Infect Dis J. 1996; 15 (9-60): 553-554Crossref PubMed Scopus (3) Google Scholar, 48Walcott D.W. Linehan Tt Hilman B.C. Hershfield M.S. el Dahr J. Failure to thrive, diarrhea, cough, and oral candidiasis in a three-month-old boy.Ann Allergy. 1994; 72: 408-414PubMed Google Scholar, 49Ozgur T.T. Asal G.T. Cetinkaya D. Orhan D. Kilic S.S. Usta Y. et al.Hematopoietic stem cell transplantation in a CD3 gamma-deficient infant with inflammatory bowel disease.Pediatr Transplant. 2008; 12: 910-913Crossref PubMed Scopus (8) Google Scholar, 50Reith W. Mach B. The bare lymphocyte syndrome and the regulation of MHC expression.Annu Rev Immunol. 2001; 19: 331-373Crossref PubMed Scopus (336) Google Scholar, 51Villard J. Masternak K. Lisowska-Grospierre B. Fischer A. Reith W. MHC class II deficiency: a disease of gene regulation.Medicine (Baltimore). 2001; 80: 405-418Crossref PubMed Scopus (36) Google Scholar, 52Klein C. Cavazzana-Calvo M. Le Deist F. Jabado N. Benkerrou M. Blanche S. et al.Bone marrow transplantation in major histocompatibility complex class II deficiency: a single-center study of 19 patients.Blood. 1995; 85: 580-587PubMed Google Scholar, 53Klein C. Lisowska-Grospierre B. LeDeist F. Fischer A. Griscelli C. Major histocompatibility complex class II deficiency: clinical manifestations, immunologic features, and outcome.J Pediatr. 1993; 123: 921-928Abstract Full Text PDF PubMed Scopus (125) Google Scholar, 54Winkelstein J.A. Marino M.C. Ochs H. Fuleihan R. Scholl P.R. Geha R. et al.The X-linked hyper-IgM syndrome: clinical and immunologic features of 79 patients.Medicine (Baltimore). 2003; 82: 373-384Crossref PubMed Scopus (222) Google Scholar, 55Dimicoli S. Bensoussan D. Latger-Cannard V. Straczek J. Antunes L. Mainard L. et al.Complete recovery from Cryptosporidium parvum infection with gastroenteritis and sclerosing cholangitis after successful bone marrow transplantation in two brothers with X-linked hyper-IgM syndrome.Bone Marrow Transplant. 2003; 32: 733-737Crossref PubMed Scopus (22) Google Scholar, 56Kutukculer N. Moratto D. Aydinok Y. Lougaris V. Aksoylar S. Plebani A. et al.Disseminated cryptosporidium infection in an infant with hyper-IgM syndrome caused by CD40 deficiency.J Pediatr. 2003; 142: 194-196Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar, 57Levy J. Espanol-Boren T. Thomas C. Fischer A. Tovo P. Bordigoni P. et al.Clinical spectrum of X-linked hyper-IgM syndrome.J Pediatr. 1997; 131: 47-54Abstract Full Text Full Text PDF PubMed Scopus (394) Google Scholar, 58Malhotra R.K. Li W. Poorly differentiated gastroenteropancreatic neuroendocrine carcinoma associated with X-linked hyperimmunoglobulin M syndrome.Arch Pathol Lab Med. 2008; 132: 847-850PubMed Google Scholar, 59Zirkin H.J. Levy J. Katchko L. Small cell undifferentiated carcinoma of the colon associated with hepatocellular carcinoma in an immunodeficient patient.Hum Pathol. 1996; 27: 992-996Abstract Full Text PDF PubMed Scopus (17) Google Scholar, 60Torgerson T.R. Ochs H.D. Immune dysregulation, polyendocrinopathy, enteropathy, X-linked: forkhead box protein 3 mutations and lack of regulatory T cells.J Allergy Clin Immunol. 2007; 120: 744-752Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar as a reference.Table IGastrointestinal diseases associated with humoral immunodeficienciesInfectiousGiardia species, Campylobacter species, Salmonella species, rotavirus, enterovirus, bacterial overgrowthInflammatoryNLH, celiac disease, microscopic colitis, ulcerative colitis, Crohn disease, villous atrophyAutoimmunePernicious anemia, autoimmune hepatitis, primary biliary cirrhosis, achlorhydriaNeoplasticAdenocarcinoma of the stomach, lymphoma Open table in a new tab Table IIImmunodeficiency syndromes and associated gastrointestinal diseaseImmunodeficiencyDefectGastrointestinal manifestationCVIDMultiple defects: TACI, inducible costimulator, T cell, cytokine; failure of B cells to differentiate into plasma cellsChronic diarrhea, NLH, villous atrophy, IBD-like disease, pernicious anemia, hepatitis3Cunningham-Rundles C. Bodian C. Common variable immunodeficiency: clinical and immunological features of 248 patients.Clin Immunol. 1999; 92: 34-48Crossref PubMed Scopus (872) Google Scholar, 4Hermaszewski R.A. Webster A.D. Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications.QJM. 1993; 86: 31-42PubMed Google Scholar, 5Khodadad A. Aghamohammadi A. Parvaneh N. Rezaei N. Mahjoob F. Bashashati M. et al.Gastrointestinal manifestations in patients with common variable immunodeficiency.Dig Dis Sci. 2007; 52: 2977-2983Crossref PubMed Scopus (54) Google Scholar, 13Washington K. Stenzel T.T. Buckley R.H. Gottfried M.R. Gastrointestinal pathology in patients with common variable immunodeficiency and X-linked agammaglobulinemia.Am J Surg Pathol. 1996; 20: 1240-1252Crossref PubMed Scopus (165) Google Scholar, 20Kalha I. Sellin J.H. Common variable immunodeficiency and the gastrointestinal tract.Curr Gastroenterol Rep. 2004; 6: 377-383Crossref PubMed Google Scholar, 21Luzi G. Zullo A. Iebba F. Rinaldi V. Sanchez Mete L. Muscaritoli M. et al.Duodenal pathology and clinical-immunological implications in common variable immunodeficiency patients.Am J Gastroenterol. 2003; 98: 118-121Crossref PubMed Scopus (63) Google Scholar, 22Teahon K. Webster A.D. Price A.B. Weston J. Bjarnason I. Studies on the enteropathy associated with primary hypogammaglobulinaemia.Gut. 1994; 35: 1244-1249Crossref PubMed Google Scholar, 23Mannon P.J. Fuss I.J. Dill S. Friend J. Groden C. Hornung R. et al.Excess IL-12 but not IL-23 accompanies the inflammatory bowel disease associated with common variable immunodeficiency.Gastroenterology. 2006; 131: 748-756Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar, 24Twomey J.J. Jordan P.H. Jarrold T. Trubowitz S. Ritz N.D. Conn H.O. The syndrome of immunoglobulin deficiency and pernicious anemia. A study of ten cases.Am J Med. 1969; 47: 340-350Abstract Full Text PDF PubMed Google Scholar, 25Twomey J.J. Jordan Jr., P.H. Laughter A.H. Meuwissen H.J. Good R.A. The gastric disorder in immunoglobulin-deficient patients.Ann Intern Med. 1970; 72: 499-504Crossref PubMed Google Scholar, 26Ermis F. Akyuz F. Demir K. Besisik F. Boztas G. Mungan Z. Rapidly progressive HCV cirrhosis in a hypogammaglobulinemic patient.Intern Med. 2008; 47: 415-417Crossref PubMed Scopus (4) Google Scholar, 27Sumazaki R. Matsubara T. Aoki T. Nagai Y. Shibasaki M. Takita H. Rapidly progressive hepatitis C in a patient with common variable immunodeficiency.Eur J Pediatr. 1996; 155: 532-534Crossref PubMed Google Scholar, 28Daniels J.A. Torbenson M. Vivekanandan P. Anders R.A. Boitnott J.K. Hepatitis in common variable immunodeficiency.Hum Pathol. 2009; 40: 484-488Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar, 29Cardinale F. Friman V. Carlsson B. Bjorkander J. Armenio L. Hanson L.A. Aberrations in titer and avidity of serum IgM and IgG antibodies to microbial and food antigens in IgA deficiency.Adv Exp Med Biol. 1995; 371B: 713-716PubMed Google Scholar, 30Cunningham-Rundles C. Siegal F.P. Cunningham-Rundles S. Lieberman P. Incidence of cancer in 98 patients with common varied immunodeficiency.J Clin Immunol. 1987; 7: 294-299Crossref PubMed Scopus (149) Google Scholar, 31Daniels J.A. Lederman H.M. Maitra A. Montgomery E.A. Gastrointestinal tract pathology in patients with common variable immunodeficiency (CVID): a clinicopathologic study and review.Am J Surg Pathol. 2007; 31: 1800-1812Crossref PubMed Scopus (124) Google Scholar, 32Nos P. Bastida G. Beltran B. Aguas M. Ponce J. Crohn's disease in common variable immunodeficiency: treatment with antitumor necrosis factor alpha.Am J Gastroenterol. 2006; 101: 2165-2166Crossref PubMed Scopus (14) Google Scholar, 33Onbasi K. Gunsar F. Sin A.Z. Ardeniz O. Kokuludag A. Sebik F. Common variable immunodeficiency (CVID) presenting with malabsorption due to giardiasis.Turk J Gastroenterol. 2005; 16: 111-113PubMed Google Scholar, 34Sawatzki M. Peter S. Hess C. Therapy-resistant diarrhea due to Giardia lamblia in a patient with common variable immunodeficiency disease.Digestion. 2007; 75: 101-102Crossref PubMed Scopus (5) Google ScholarSelective IgA deficiencyGene defect unknown; defective maturation of B cells into IgA-secreting plasma cellsDiarrhea, celiac sprue, NLH1Ammann A.J. Hong R. Selective IgA deficiency: presentation of 30 cases and a review of the literature.Medicine (Baltimore). 1971; 50: 223-236Crossref PubMed Google Scholar, 14Collin P. Maki M. Keyrilainen O. Hallstrom O. Reunala T. Pasternack A. Selective IgA deficiency and coeliac disease.Scand J Gastroenterol. 1992; 27: 367-371Crossref PubMed Scopus (169) Google Scholar, 15Heneghan M.A. Stevens F.M. Cryan E.M. Warner R.H. McCarthy C.F. Celiac sprue and immunodeficiency states: a 25-year review.J Clin Gastroenterol. 1997; 25: 421-425Crossref PubMed Scopus (62) Google Scholar, 16Meini A. Pillan N.M. Villanacci V. Monafo V. Ugazio A.G. Plebani A. Prevalence and diagnosis of celiac disease in IgA-deficient children.Ann Allergy Asthma Immunol. 1996; 77: 333-336Abstract Full Text PDF PubMed Google Scholar, 17Cataldo F. Marino V. Ventura A. Bottaro G. Corazza G.R. Prevalence and clinical features of selective immunoglobulin A deficiency in coeliac disease: an Italian multicentre study. Italian Society of Paediatric Gastroenterology and Hepatology (SIGEP) and "Club del Tenue" Working Groups on Coeliac Disease.Gut. 1998; 42: 362-365Crossref PubMed Google Scholar, 18Jacobson K.W. deShazo R.D. Selective immunoglobulin A deficiency associated with modular lymphoid hyperplasia.J Allergy Clin Immunol. 1979; 64: 516-521Abstract Full Text PDF PubMed Scopus (9) Google Scholar, 19Piascik M. Rydzewska G. Pawlik M. Milewski J. Furmanek M.I. Wronska E. et al.Diffuse nodular lymphoid hyperplasia of the gastrointestinal tract in patient with selective immunoglobulin A deficiency and sarcoid-like syndrome—case report.Adv Med Sci. 2007; 52: 296-300PubMed Google Scholar, 35Mir-Madjlessi S.H. Vafai M. Khademi J. Kamalian N. Coexisting primary malignant lymphoma and adenocarcinoma of the large intestine in an IgA-deficient boy.Dis Colon Rectum. 1984; 27: 822-824Crossref PubMed Scopus (19) Google ScholarXLAX-linked; defective Bruton tyrosine kinase → no mature B cellsGastrointestinal disorders rare, chronic diarrhea, malabsorption4Hermaszewski R.A. Webster A.D. Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications.QJM. 1993; 86: 31-42PubMed Google Scholar, 6Lederman H.M. Winkelstein J.A. X-linked agammaglobulinemia: an analysis of 96 patients.Medicine (Baltimore). 1985; 64: 145-156Crossref PubMed Google Scholar, 8Conley M.E. Rohrer J. Minegishi Y. X-linked agammaglobulinemia.Clin Rev Allergy Immunol. 2000; 19: 183-204Crossref PubMed Google Scholar, 9Winkelstein J.A. Marino M.C. Lederman H.M. Jones S.M. Sullivan K. Burks A.W. et al.X-linked agammaglobulinemia: report on a United States registry of 201 patients.Medicine (Baltimore). 2006; 85: 193-202Crossref PubMed Scopus (184) Google Scholar, 10Atarod L. Raissi A. Aghamohammadi A. Farhoudi A. Khodadad A. Moin M. et al.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. 2003; 2: 75-79PubMed Google Scholar, 11Cellier C. Foray S. Hermine O. Regional enteritis associated with enterovirus in a patient with X-linked agammaglobulinemia.N Engl J Med. 2000; 342: 1611-1612Crossref PubMed Scopus (15) Google Scholar, 12Misbah S.A. Spickett G.P. Ryba P.C. Hockaday J.M. Kroll J.S. Sherwood C. et al.Chronic enteroviral meningoencephalitis in agammaglobulinemia: case report and literature review.J Clin Immunol. 1992; 12: 266-270Crossref PubMed Scopus (79) Google Scholar, 36Conley M.E. Parolini O. Rohrer J. Campana D. X-linked agammaglobulinemia: new approaches to old questions based on the identification of the defective gene.Immunol Rev. 1994; 138: 5-21Crossref PubMed Google ScholarChronic granulomatous diseaseMultiple defects: X-linked caused by defects in CYBB encoding the gp91phox component of NADPH oxidase; autosomal recessive caused by defects in NCF1, NCF2, or CYBA defects in components of NADPH oxidaseGranulomatous colitis, perianal fistulae, hepatic abscess, gastric outlet obstruction, small-bowel obstruction, granulomatous stomatitis, oral ulcers, esophageal dysmotility37Barton L.L. Moussa S.L. Villar R.G. Hulett R.L. Gastrointestinal complications of chronic granulomatous disease: case report and literature review.Clin Pediatr (Phila). 1998; 37: 231-236Crossref PubMed Google Scholar, 38Huang A. Abbasakoor F. Vaizey C.J. Gastrointestinal manifestations of chronic granulomatous disease.Colorectal Dis. 2006; 8: 637-644Crossref PubMed Scopus (24) Google Scholar, 39Marciano B.E. Rosenzweig S.D. Kleiner D.E. Anderson V.L. Darnell D.N. Anaya-O'Brien S. et al.Gastrointestinal involvement in chronic granulomatous disease.Pediatrics. 2004; 114: 462-468Crossre
Referência(s)