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10.02.2020 | Original Article

Genetic, Immunological, and Clinical Features of the First Mexican Cohort of Patients with Chronic Granulomatous Disease

verfasst von: Lizbeth Blancas-Galicia, Eros Santos-Chávez, Caroline Deswarte, Quentin Mignac, Isabel Medina-Vera, Ximena León-Lara, Manon Roynard, Selma C Scheffler-Mendoza, Ricardo Rioja-Valencia, Alexandra Alvirde-Ayala, Saul O Lugo Reyes, Tamara Staines-Boone, Jorge García-Campos, Omar J Saucedo-Ramírez, Blanca E Del-Río_Navarro, Antonio Zamora-Chávez, Arturo López-Larios, Susana García-Pavón-Osorio, Eugenia Melgoza-Arcos, María R Canseco-Raymundo, Dolores Mogica-Martínez, Marco Venancio-Hernández, Daniel Pacheco-Rosas, Sigifredo Pedraza-Sánchez, Martha Guevara-Cruz, Federico Saracho-Weber, Berenise Gámez-González, Guillermo Wakida-Kuzunoki, Ana R Morán-Mendoza, Ana P Macías-Robles, Roselia Ramírez-Rivera, Eugenia Vargas-Camaño, Carmen Zarate-Hernández, Héctor Gómez-Tello, Emmanuel Ramírez-Sánchez, Fredy Ruíz-Hernández, Domingo Ramos-López, Héctor Acuña-Martínez, María L García-Cruz, María G Román-Jiménez, Marina G González-Villarreal, Aristóteles Álvarez-Cardona, Beatriz A Llamas-Guillén, Jennifer Cuellar-Rodríguez, Alberto Olaya-Vargas, Nideshda Ramírez-Uribe, Stéphanie Boisson-Dupuis, Jean-Laurent Casanova, Francisco J Espinosa-Rosales, Jeanet Serafín-López, Marco Yamazaki-Nakashimada, Sara Espinosa-Padilla, Jacinta Bustamante

Erschienen in: Journal of Clinical Immunology | Ausgabe 3/2020

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Abstract

Purpose

Chronic granulomatous disease (CGD) is a primary immunodeficiency characterized by an inability of phagocytes to produce reactive oxygen species, impairing their killing of various bacteria and fungi. We summarize here the 93 cases of CGD diagnosed in Mexico from 2011 to 2019.

Methods

Thirteen Mexican hospitals participated in this study. We describe the genetic, immunological, and clinical features of the 93 CGD patients from 78 unrelated kindreds.

Results

Eighty-two of the patients (88%) were male. All patients developed bacterial infections and 30% suffered from some kind of fungal infection. Fifty-four BCG-vaccinated patients (58%) presented infectious complications of BCG vaccine. Tuberculosis occurred in 29%. Granulomas were found in 56% of the patients. Autoimmune and inflammatory diseases were present in 15% of patients. A biological diagnosis of CGD was made in 89/93 patients, on the basis of NBT assay (n = 6), DHR (n = 27), and NBT plus DHR (n = 56). The deficiency was complete in all patients. The median age of biological diagnosis was 17 months (range, 0–186 months). A genetic diagnosis was made in 83/93 patients (when material was available), corresponding to CYBB (n = 64), NCF1 (n = 7), NCF2 (n = 7), and CYBA (n = 5) mutations.

Conclusions

The clinical manifestations in these Mexican CGD patients were similar to those in patients elsewhere. This cohort is the largest in Latin America. Mycobacterial infections are an important cause of morbidity in Mexico, as in other countries in which tuberculosis is endemic and infants are vaccinated with BCG. X-linked CGD accounted for most of the cases in Mexico, as in other Latin American countries. However, a significant number of CYBA and NCF2 mutations were identified, expanding the spectrum of known causal mutations.

Roos D, Kuhns DB, Maddalena A, Roesler J, Lopez JA, Ariga T, et al. Hematologically important mutations: X-linked chronic granulomatous disease (third update). Blood Cells Mol Dis. 2010;45(3):246–65.PubMedPubMedCentral

Roos D, Kuhns DB, Maddalena A, Bustamante J, Kannengiesser C, de Boer M, et al. Hematologically important mutations: the autosomal recessive forms of chronic granulomatous disease (second update). Blood Cells Mol Dis. 2010;44(4):291–9.PubMedPubMedCentral

Arnadottir GA, Norddahl GL, Gudmundsdottir S, Agustsdottir AB, Sigurdsson S, Jensson BO, et al. A homozygous loss-of-function mutation leading to CYBC1 deficiency causes chronic granulomatous disease. Nat Commun. 2018;9(1):4447.PubMedPubMedCentral

Thomas DC, Charbonnier LM, Schejtman A, Aldhekri H, Coomber EL, Dufficy ER, et al. EROS/CYBC1 mutations: decreased NADPH oxidase function and chronic granulomatous disease. J Allergy Clin Immunol. 2019;143(2):782–5 e1.PubMed

van de Geer A, Nieto-Patlan A, Kuhns DB, Tool AT, Arias AA, Bouaziz M, et al. Inherited p40phox deficiency differs from classic chronic granulomatous disease. J Clin Invest. 2018;128(9):3957–75.PubMedPubMedCentral

Segal BH, Grimm MJ, Khan AN, Han W, Blackwell TS. Regulation of innate immunity by NADPH oxidase. Free Radic Biol Med. 2012;53(1):72–80.PubMedPubMedCentral

Chiriaco M, Salfa I, Di Matteo G, Rossi P, Finocchi A. Chronic granulomatous disease: clinical, molecular, and therapeutic aspects. Pediatr Allergy Immunol. 2016;27(3):242–53.PubMed

Roos D, de Boer M. Molecular diagnosis of chronic granulomatous disease. Clin Exp Immunol. 2014;175(2):139–49.PubMedPubMedCentral

Kovacs I, Horvath M, Lanyi A, Petheo GL, Geiszt M. Reactive oxygen species-mediated bacterial killing by B lymphocytes. J Leukoc Biol. 2015;97(6):1133–7.PubMed

10.

Baba LA, Ailal F, El Hafidi N, Hubeau M, Jabot-Hanin F, Benajiba N, et al. Chronic granulomatous disease in Morocco: genetic, immunological, and clinical features of 12 patients from 10 kindreds. J Clin Immunol. 2014;34(4):452–8.PubMed

11.

Bustamante J, Aksu G, Vogt G, de Beaucoudrey L, Genel F, Chapgier A, et al. BCG-osis and tuberculosis in a child with chronic granulomatous disease. J Allergy Clin Immunol. 2007;120(1):32–8.PubMed

12.

van den Berg JM, van Koppen E, Ahlin A, Belohradsky BH, Bernatowska E, Corbeel L, et al. Chronic granulomatous disease: the European experience. PLoS One. 2009;4(4):e5234.PubMedPubMedCentral

13.

Zhou Q, Hui X, Ying W, Hou J, Wang W, Liu D, et al. A cohort of 169 chronic granulomatous disease patients exposed to BCG vaccination: a retrospective study from a single center in Shanghai, China (2004-2017). J Clin Immunol. 2018;38(3):260–72.PubMed

14.

Ben-Ari J, Wolach O, Gavrieli R, Wolach B. Infections associated with chronic granulomatous disease: linking genetics to phenotypic expression. Expert Rev Anti-Infect Ther. 2012;10(8):881–94.PubMed

15.

Conti F, Lugo-Reyes SO, Blancas-Galicia L, He J, Aksu G, Borges de Oliveira E Jr, et al. Mycobacterial disease in patients with chronic granulomatous disease: a retrospective analysis of 71 cases. J Allergy Clin Immunol. 2016;138(1):241–8 e3.PubMed

16.

Lee PP, Chan KW, Jiang L, Chen T, Li C, Lee TL, et al. Susceptibility to mycobacterial infections in children with X-linked chronic granulomatous disease: a review of 17 patients living in a region endemic for tuberculosis. Pediatr Infect Dis J. 2008;27(3):224–30.PubMed

17.

Parvaneh N, Barlogis V, Alborzi A, Deswarte C, Boisson-Dupuis S, Migaud M, et al. Visceral leishmaniasis in two patients with IL-12p40 and IL-12Rbeta1 deficiencies. Pediatr Blood Cancer. 2017;64(6).

18.

Magnani A, Brosselin P, Beaute J, de Vergnes N, Mouy R, Debre M, et al. Inflammatory manifestations in a single-center cohort of patients with chronic granulomatous disease. J Allergy Clin Immunol. 2014;134(3):655–62 e8.PubMed

19.

Huang C, De Ravin SS, Paul AR, Heller T, Ho N, Wu Datta L, et al. Genetic risk for inflammatory bowel disease is a determinant of Crohn’s disease development in chronic granulomatous disease. Inflamm Bowel Dis. 2016;22(12):2794–801.PubMedPubMedCentral

20.

Dinauer MC. Inflammatory consequences of inherited disorders affecting neutrophil function. Blood. 2019;133(20):2130–9.PubMed

21.

De Ravin SS, Naumann N, Cowen EW, Friend J, Hilligoss D, Marquesen M, et al. Chronic granulomatous disease as a risk factor for autoimmune disease. J Allergy Clin Immunol. 2008;122(6):1097–103.PubMedPubMedCentral

22.

Ben Abdallah Chabchoub R, Turki H, Mahfoudh A. Systemic lupus erythematosus in a boy with chronic granulomatous disease: case report and review of the literature. Arch Pediatr. 2014;21(12):1364–6.PubMed

23.

Matute JD, Arias AA, Wright NA, Wrobel I, Waterhouse CC, Li XJ, et al. A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40 phox and selective defects in neutrophil NADPH oxidase activity. Blood. 2009;114(15):3309–15.PubMedPubMedCentral

24.

Winkelstein JA, Marino MC, Johnston RB Jr, Boyle J, Curnutte J, Gallin JI, et al. Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore). 2000;79(3):155–69.

25.

Wolach B, Gavrieli R, de Boer M, van Leeuwen K, Berger-Achituv S, Stauber T, et al. Chronic granulomatous disease: clinical, functional, molecular, and genetic studies. The Israeli experience with 84 patients. Am J Hematol. 2017;92(1):28–36.PubMed

26.

Kobayashi S, Murayama S, Takanashi S, Takahashi K, Miyatsuka S, Fujita T, et al. Clinical features and prognoses of 23 patients with chronic granulomatous disease followed for 21 years by a single hospital in Japan. Eur J Pediatr. 2008;167(12):1389–94.PubMed

27.

de Oliveira-Junior EB, Zurro NB, Prando C, Cabral-Marques O, Pereira PV, Schimke LF, et al. Clinical and genotypic spectrum of chronic granulomatous disease in 71 Latin American patients: first report from the LASID registry. Pediatr Blood Cancer. 2015;62(12):2101–7.PubMed

28.

Meshaal S, El Hawary R, Abd Elaziz D, Alkady R, Galal N, Boutros J, et al. Chronic granulomatous disease: review of a cohort of Egyptian patients. Allergol Immunopathol (Madr). 2015;43(3):279–85.

29.

El Hawary R, Meshaal S, Nagy D, Fikry I, Alkady R, Abd Elaziz D, et al. Study of naive and memory cells in a cohort of Egyptian chronic granulomatous disease patients. J Recept Signal Transduct Res. 2015;35(5):423–8.PubMed

30.

Fattahi F, Badalzadeh M, Sedighipour L, Movahedi M, Fazlollahi MR, Mansouri SD, et al. Inheritance pattern and clinical aspects of 93 Iranian patients with chronic granulomatous disease. J Clin Immunol. 2011;31(5):792–801.PubMed

31.

Kulkarni M, Hule G, de Boer M, van Leeuwen K, Kambli P, Aluri J, et al. Approach to molecular diagnosis of chronic granulomatous disease (CGD): an experience from a large cohort of 90 Indian patients. J Clin Immunol. 2018;38(8):898–916.PubMed

32.

Koker MY, Camcioglu Y, van Leeuwen K, Kilic SS, Barlan I, Yilmaz M, et al. Clinical, functional, and genetic characterization of chronic granulomatous disease in 89 Turkish patients. J Allergy Clin Immunol. 2013;132(5):1156–63 e5.PubMed

33.

Condino-Neto A, Sorensen RU, Gomez Raccio AC, King A, Espinosa-Rosales FJ, Franco JL. Current state and future perspectives of the Latin American Society for Immunodeficiencies (LASID). Allergol Immunopathol (Madr). 2015;43(5):493–7.

34.

Barese C, Copelli S, Zandomeni R, Oleastro M, Zelazko M, Rivas EM. X-linked chronic granulomatous disease: first report of mutations in patients of Argentina. J Pediatr Hematol Oncol. 2004;26(10):656–60.PubMed

35.

Scheffler-Mendoza SC, Yamazaki-Nakashimada MA, Olaya-Vargas A, Morin-Contreras A, Juarez-Echenique JC, Alcantara-Ortigoza MA, et al. Successful stem cell transplantation in a child with chronic granulomatous disease associated with contiguous gene deletion syndrome and complicated by macrophage activation syndrome. Clin Immunol. 2014;154(2):112–5.PubMed

36.

Venegas-Montoya E, Sorcia-Ramirez G, Scheffler-Mendoza S, Blancas-Galicia L, Bustamante J, Espinosa-Rosales F, et al. Use of corticosteroids as an alternative to surgical treatment for liver abscesses in chronic granulomatous disease. Pediatr Blood Cancer. 2016;63(12):2254–5.PubMed

37.

Yamazaki-Nakashimada MA, Stiehm ER, Pietropaolo-Cienfuegos D, Hernandez-Bautista V, Espinosa-Rosales F. Corticosteroid therapy for refractory infections in chronic granulomatous disease: case reports and review of the literature. Ann Allergy Asthma Immunol. 2006;97(2):257–61.PubMed

38.

Yamazaki-Nakashimada MA, Ramirez-Vargas N, De Rubens-Figueroa J. Chronic granulomatous disease associated with atypical Kawasaki disease. Pediatr Cardiol. 2008;29(1):169–71.PubMed

39.

Alvarez-Cardona A, Rodriguez-Lozano AL, Blancas-Galicia L, Rivas-Larrauri FE, Yamazaki-Nakashimada MA. Intravenous immunoglobulin treatment for macrophage activation syndrome complicating chronic granulomatous disease. J Clin Immunol. 2012;32(2):207–11.PubMed

40.

Berron-Ruiz L, Morin-Contreras A, Cano-Garcia V, Yamazaki-Nakashimada MA, Gomez-Tello H, Vargas-Camano ME, et al. Detection of inheritance pattern in thirty-three Mexican males with chronic granulomatous disease through 123 dihydrorhodamine assay. Allergol Immunopathol (Madr). 2014;42(6):580–5.

41.

Bustamante-Ogando JC, Rivas-Larrauri F, Blancas-Galicia L, Otero-Mendoza F, Yamazaki-Nakashimada MA. Amphotericin B associated pulmonary complications in chronic granulomatous disease patients. Pediatr Blood Cancer. 2016;63(10):1871–2.PubMed

42.

Ramirez-Uribe N, Hernandez-Martinez C, Lopez-Hernandez G, Perez-Garcia M, Ramirez-Sanchez E, Espinosa-Padilla SE, et al. Hematopoietic progenitors transplantation in a patient with chronic granulomatous disease in Mexico. Rev Alerg Mex. 2016;63(1):95–103.PubMed

43.

Graham SM, Ahmed T, Amanullah F, Browning R, Cardenas V, Casenghi M, et al. Evaluation of tuberculosis diagnostics in children: 1. Proposed clinical case definitions for classification of intrathoracic tuberculosis disease. Consensus from an expert panel. J Infect Dis. 2012;205(Suppl 2):S199–208.PubMedPubMedCentral

44.

Gurunathan A, Boucher AA, Mark M, Prus KM, O’Brien MM, Breese EH, et al. Limitations of HLH-2004 criteria in distinguishing malignancy-associated hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer. 2018;65(12):e27400.PubMed

45.

Kim HY, Kim HJ, Ki CS, Kim DW, Yoo KH, Kang ES. Rapid determination of chimerism status using dihydrorhodamine assay in a patient with X-linked chronic granulomatous disease following hematopoietic stem cell transplantation. Ann Lab Med. 2013;33(4):288–92.PubMedPubMedCentral

46.

Vowells SJ, Sekhsaria S, Malech HL, Shalit M, Fleisher TA. Flow cytometric analysis of the granulocyte respiratory burst: a comparison study of fluorescent probes. J Immunol Methods. 1995;178(1):89–97.PubMed

47.

Kutlug S, Sensoy G, Birinci A, Saraymen B, Yavuz Koker M, Yiotaldiotaran A. Seven chronic granulomatous disease cases in a single-center experience and a review of the literature. Asian Pac J Allergy Immunol. 2018;36(1):35–41.PubMed

48.

Gutierrez MJ, McSherry GD, Ishmael FT, Horwitz AA, Nino G. Residual NADPH oxidase activity and isolated lung involvement in X-linked chronic granulomatous disease. Case Rep Pediatr. 2012;2012:974561.PubMedPubMedCentral

49.

Wu J, Wang WF, Zhang YD, Chen TX. Clinical features and genetic analysis of 48 patients with chronic granulomatous disease in a single center study from Shanghai, China (2005-2015): new studies and a literature review. J Immunol Res. 2017;2017:8745254.PubMedPubMedCentral

50.

Zwerling A, Behr MA, Verma A, Brewer TF, Menzies D, Pai M. The BCG world atlas: a database of global BCG vaccination policies and practices. PLoS Med. 2011;8(3):e1001012.PubMedPubMedCentral

51.

Ohga S, Ikeuchi K, Kadoya R, Okada K, Miyazaki C, Suita S, et al. Intrapulmonary Mycobacterium avium infection as the first manifestation of chronic granulomatous disease. J Inf Secur. 1997;34(2):147–50.

52.

Chusid MJ, Parrillo JE, Fauci AS. Chronic granulomatous disease. Diagnosis in a 27-year-old man with Mycobacterium fortuitum. JAMA. 1975;233(12):1295–6.PubMed

53.

Allen DM, Chng HH. Disseminated Mycobacterium flavescens in a probable case of chronic granulomatous disease. J Inf Secur. 1993;26(1):83–6.

54.

Marciano BE, Spalding C, Fitzgerald A, Mann D, Brown T, Osgood S, et al. Common severe infections in chronic granulomatous disease. Clin Infect Dis. 2015;60(8):1176–83.PubMed

55.

El Kares R, Barbouche MR, Elloumi-Zghal H, Bejaoui M, Chemli J, Mellouli F, et al. Genetic and mutational heterogeneity of autosomal recessive chronic granulomatous disease in Tunisia. J Hum Genet. 2006;51(10):887–95.PubMed

56.

Martire B, Rondelli R, Soresina A, Pignata C, Broccoletti T, Finocchi A, et al. Clinical features, long-term follow-up and outcome of a large cohort of patients with chronic granulomatous disease: an Italian multicenter study. Clin Immunol. 2008;126(2):155–64.PubMed

57.

Patino PJ, Rae J, Noack D, Erickson R, Ding J, de Olarte DG, et al. Molecular characterization of autosomal recessive chronic granulomatous disease caused by a defect of the nicotinamide adenine dinucleotide phosphate (reduced form) oxidase component p67-phox. Blood. 1999;94(7):2505–14.PubMed

58.

Noack D, Rae J, Cross AR, Munoz J, Salmen S, Mendoza JA, et al. Autosomal recessive chronic granulomatous disease caused by novel mutations in NCF-2, the gene encoding the p67-phox component of phagocyte NADPH oxidase. Hum Genet. 1999;105(5):460–7.PubMed

59.

Beghin A, Comini M, Soresina A, Imberti L, Zucchi M, Plebani A, et al. Chronic granulomatous disease in children: a single center experience. Clin Immunol. 2018;188:12–9.PubMed

60.

Movahedi M, Aghamohammadi A, Rezaei N, Shahnavaz N, Jandaghi AB, Farhoudi A, et al. Chronic granulomatous disease: a clinical survey of 41 patients from the Iranian primary immunodeficiency registry. Int Arch Allergy Immunol. 2004;134(3):253–9.PubMed

61.

Rawat A, Vignesh P, Sharma A, Shandilya JK, Sharma M, Suri D, et al. Infection profile in chronic granulomatous disease: a 23-year experience from a tertiary care center in North India. J Clin Immunol. 2017;37(3):319–28.PubMed

62.

Bassiri-Jahromi S, Doostkam A. Actinomyces and nocardia infections in chronic granulomatous disease. J Global Infect Dis. 2011;3(4):348–52.

63.

Agudelo-Florez P, Prando-Andrade CC, Lopez JA, Costa-Carvalho BT, Quezada A, Espinosa FJ, et al. Chronic granulomatous disease in Latin American patients: clinical spectrum and molecular genetics. Pediatr Blood Cancer. 2006;46(2):243–52.PubMed

64.

Yanir AD, Hanson IC, Shearer WT, Noroski LM, Forbes LR, Seeborg FO, et al. High incidence of autoimmune disease after hematopoietic stem cell transplantation for chronic granulomatous disease. Biol Blood Marrow Transplant. 2018;24(8):1643–50.PubMed

65.

Valentine G, Thomas TA, Nguyen T, Lai YC. Chronic granulomatous disease presenting as hemophagocytic lymphohistiocytosis: a case report. Pediatrics. 2014;134(6):e1727–30.PubMed

66.

Dunogue B, Pilmis B, Mahlaoui N, Elie C, Coignard-Biehler H, Amazzough K, et al. Chronic granulomatous disease in patients reaching adulthood: a nationwide study in France. Clin Infect Dis. 2017;64(6):767–75.PubMed

Titel: Genetic, Immunological, and Clinical Features of the First Mexican Cohort of Patients with Chronic Granulomatous Disease
verfasst von: Lizbeth Blancas-Galicia
Eros Santos-Chávez
Caroline Deswarte
Quentin Mignac
Isabel Medina-Vera
Ximena León-Lara
Manon Roynard
Selma C Scheffler-Mendoza
Ricardo Rioja-Valencia
Alexandra Alvirde-Ayala
Saul O Lugo Reyes
Tamara Staines-Boone
Jorge García-Campos
Omar J Saucedo-Ramírez
Blanca E Del-Río_Navarro
Antonio Zamora-Chávez
Arturo López-Larios
Susana García-Pavón-Osorio
Eugenia Melgoza-Arcos
María R Canseco-Raymundo
Dolores Mogica-Martínez
Marco Venancio-Hernández
Daniel Pacheco-Rosas
Sigifredo Pedraza-Sánchez
Martha Guevara-Cruz
Federico Saracho-Weber
Berenise Gámez-González
Guillermo Wakida-Kuzunoki
Ana R Morán-Mendoza
Ana P Macías-Robles
Roselia Ramírez-Rivera
Eugenia Vargas-Camaño
Carmen Zarate-Hernández
Héctor Gómez-Tello
Emmanuel Ramírez-Sánchez
Fredy Ruíz-Hernández
Domingo Ramos-López
Héctor Acuña-Martínez
María L García-Cruz
María G Román-Jiménez
Marina G González-Villarreal
Aristóteles Álvarez-Cardona
Beatriz A Llamas-Guillén
Jennifer Cuellar-Rodríguez
Alberto Olaya-Vargas
Nideshda Ramírez-Uribe
Stéphanie Boisson-Dupuis
Jean-Laurent Casanova
Francisco J Espinosa-Rosales
Jeanet Serafín-López
Marco Yamazaki-Nakashimada
Sara Espinosa-Padilla
Jacinta Bustamante
Publikationsdatum: 10.02.2020
Verlag: Springer US
Erschienen in: Journal of Clinical Immunology / Ausgabe 3/2020
Print ISSN: 0271-9142
Elektronische ISSN: 1573-2592
DOI: https://doi.org/10.1007/s10875-020-00750-5

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Genetic, Immunological, and Clinical Features of the First Mexican Cohort of Patients with Chronic Granulomatous Disease