Vulnerability to Nontuberculous Mycobacterial Lung Disease or Systemic Infection Due to Genetic/Heritable Disorders

  • Edward D. ChanEmail author
Part of the Respiratory Medicine book series (RM)


Nontuberculous mycobacteria (NTM) are ubiquitous in the natural and man-made environments, and yet human disease due to NTM is not widely pervasive. Presuming that human exposure to NTM is common, it suggests that NTM are relatively avirulent and that established infection resulting in disease occurs mostly in those who are innately susceptible. Most cases of NTM-LD and essentially all of extrapulmonary visceral/disseminated NTM disease occur in individuals with identifiable risk factors. While acquired disorders may predispose to either isolated NTM-LD or extrapulmonary visceral/disseminated NTM disease, this review focuses on genetic/heritable causes of these two forms of NTM disease.


Nontuberculous mycobacteria Environmental mycobacteria Bronchiectasis Genetics Lung disease 


  1. 1.
    Kim YM, Kim M, Kim SK, Park K, Jin S-H, Lee US, Kim Y, Chae GT, Lee S-B. Mycobacterial infections in coal workers’ pneumoconiosis patients in South Korea. Scand J Infect Dis. 2009;41:656–62.PubMedCrossRefGoogle Scholar
  2. 2.
    Rosenzweig DY. Pulmonary mycobacterial infections due to Mycobacterium intracellulare-avium complex. Clinical features and course in 100 consecutive cases. Chest. 1979;75:115–9.PubMedCrossRefGoogle Scholar
  3. 3.
    Sonnenberg P, Murray J, Glynn JR, Thomas RG, Godfrey-Faussett P, Shearer S. Risk factors for pulmonary disease due to culture-positive M. tuberculosis or non-tuberculous mycobacteria in South African gold miners. Eur Respir J. 2000;15:291–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Chan ED, Iseman MD. Potential association between calcified thoracic lymphadenopathy due to previous Histoplasma capsulatum infection and pulmonary Mycobacterium avium complex disease. South Med J. 1999;92:572–6.PubMedCrossRefGoogle Scholar
  5. 5.
    Dirac MA, Horan KL, Doody DR, Meschke JS, Park DR, Jackson LA, Weiss NS, Winthrop KL, Cangelosi GA. Environment or host?: a case-control study of risk factors for Mycobacterium avium complex lung disease. Am J Respir Crit Care Med. 2012;186:684–91.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Kartalija M, Ovrutsky AR, Bryan CL, Pott GB, Fantuzzi G, Thomas J, Strand MS, Bai X, Ramamoorthy R, Rothman MS, Nagabhushanam V, McDermott M, Levin AR, Frazer-Abel A, Giclas PC, Korner J, Iseman MD, Shapiro L, Chan ED. Patients with non-tuberculous mycobacterial lung disease exhibit unique body and immune phenotypes. Am J Respir Crit Care Med. 2012;187:197–205.PubMedCrossRefGoogle Scholar
  7. 7.
    Chan ED, Kaminska AM, Gill W, Chmura K, Feldman NE, Bai X, Floyd CM, Fulton KE, Huitt GA, Strand MJ, Iseman MD, Shapiro L. Alpha-1-antitrypsin (AAT) anomalies are associated with lung disease due to rapidly growing mycobacteria and AAT inhibits Mycobacterium abscessus infection of macophages. Scand J Infect Dis. 2007;39:690–6.PubMedCrossRefGoogle Scholar
  8. 8.
    Noone PG, Leigh MW, Sannuti A, Minnix SL, Carson JL, Hazucha M, Zariwala MA, Knowles MR. Primary ciliary dyskinesia: diagnostic and phenotypic features. Am J Respir Crit Care Med. 2004;169:459–67.PubMedCrossRefGoogle Scholar
  9. 9.
    Tomii K, Iwata T, Oida K, Kohri Y, Taguchi Y, Nanbu Y, Kubo Y, Yaba Y, Mino M, Kuroda Y. A probable case of adult Williams-Campbell syndrome incidentally detected by an episode of atypical mycobacterial infection. Nihon Kyobu Shikkan Gakkai Zasshi. 1989;27:518–22.PubMedGoogle Scholar
  10. 10.
    Uji M, Matsushita H, Watanabe T, Suzumura T, Yamada M. A case of primary Sjögren’s syndrome presenting with middle lobe syndrome complicated by nontuberculous mycobacteriosis. Nihon Kokyuki Gakkai Zasshi. 2008;46:55–9.PubMedGoogle Scholar
  11. 11.
    Witty LA, Tapson VF, Piantadosi CA. Isolation of mycobacteria in patients with pulmonary alveolar proteinosis. Medicine. 1994;73:103–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Damseh N, Quercia N, Rumman N, Dell SD, Kim RH. Primary ciliary dyskinesia: mechanisms and management. Appl Clin Genet. 2017;10:67–74.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Shapiro AJ, Zariwala MA, Ferkol T, Davis SD, Sagel SD, Dell SD, Rosenfeld M, Olivier KN, Milla C, Daniel SJ, Kimple AJ, Manion M, Knowles MR, Leigh MW, Genetic Disorders of Mucociliary Clearance Consortium. Diagnosis, monitoring, and treatment of primary ciliary dyskinesia: PCD foundation consensus recommendations based on state of the art review. Pediatr Pulmonol. 2016;51:115–32.PubMedCrossRefGoogle Scholar
  14. 14.
    Parr DG, Guest PG, Reynolds JH, Dowson LJ, Stockley RA. Prevalence and impact of bronchiectasis in a1-antitrypsin deficiency. Am J Respir Crit Care Med. 2007;176:1215–21.PubMedCrossRefGoogle Scholar
  15. 15.
    Chan ED, Bai A, Eichstaedt C, Hamzeh NY, Harbeck R, Honda JR, Frazer-Abel A, Kosmider B, Sandhaus RA, Bai X. Alpha-1-antitrypsin increases autophagosome number and production of host-protective cytokines in Mycobacterium Intracellulare-infected macrophages. Am J Respir Crit Care Med. 2017;195:A2906.Google Scholar
  16. 16.
    Chan ED, Iseman MD. Bronchiectasis. In: Broaddus CEJ, King TE, Lazarus SC, Mason R, Murray J, Nadel J, Slutsky AS, editors. Textbook of respiratory medicine. 6th ed: Elsevier Press; 2017. In press.Google Scholar
  17. 17.
    George J, Jain R, Tariq SM. CT bronchoscopy in the diagnosis of Williams-Campbell syndrome. Respirology. 2006;11:117–9.PubMedCrossRefGoogle Scholar
  18. 18.
    Wayne KS, Taussig LM. Probable familial congenital bronchiectasis due to cartilage deficiency (Williams-Campbell syndrome). Am Rev Respir Dis. 1976;114:15–22.PubMedGoogle Scholar
  19. 19.
    Aldave APN, Saliski DOW. The clinical manifestations, diagnosis and management of Williams-Campbell syndrome. N Am J Med Sci. 2014;6:429–32.CrossRefGoogle Scholar
  20. 20.
    Payandeh J, McGillivray B, McCauley G, Wilcox P, Swiston JR, Lehman A. A clinical classification scheme for tracheobronchomegaly (Mounier-Kuhn syndrome). Lung. 2015;193:815–22.PubMedCrossRefGoogle Scholar
  21. 21.
    Celik B, Bilgin S, Yuksel C. Mounier-Kuhn syndrome: a rare cause of bronchial dilation. Tex Heart Inst J. 2011;38:194–6.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Krustins E. Mounier-Kuhn syndrome: a systematic analysis of 128 cases published within last 25 years. Clin Respir J. 2016;10:3–10.PubMedCrossRefGoogle Scholar
  23. 23.
    Abdul-Rahman JA, Moodley YP, Phillips MJ. Pulmonary alveolar proteinosis associated with psoriasis and complicated by mycobacterial infection: successful treatment with granulocyte-macrophage colony stimulating factor after a partial response to whole lung lavage. Respirology. 2004;9:419–22.PubMedCrossRefGoogle Scholar
  24. 24.
    Bakhos R, Gattuso P, Arcot C, Reddy VB. Pulmonary alveolar proteinosis: an unusual association with Mycobacterium avium-intracellulare infection and lymphocytic interstitial pneumonia. South Med J. 1996;89:801–2.PubMedCrossRefGoogle Scholar
  25. 25.
    Bedrossian CW, Luna MA, Conklin RH, Miller WC. Alveolar proteinosis as a consequence of immunosuppression. A hypothesis based on clinical and pathologic observations. Hum Pathol. 1980;11(5 Suppl):527–35.PubMedGoogle Scholar
  26. 26.
    Carnovale R, Zornoza J, Goldman AM, Luna M. Pulmonary alveolar proteinosis: its association with hematologic malignancy and lymphoma. Radiology. 1977;122:303–6.PubMedCrossRefGoogle Scholar
  27. 27.
    Goldschmidt N, Nusair S, Gural A, Amir G, Izhar U, Laxer U. Disseminated Mycobacterium kansasii infection with pulmonary alveolar proteinosis in a patient with chronic myelogenous leukemia. Am J Hematol. 2003;74:221–3.PubMedCrossRefGoogle Scholar
  28. 28.
    Prakash UB, Barham SS, Carpenter HA, Dines DE, Marsh HM. Pulmonary alveolar phospholipoproteinosis: experience with 34 cases and a review. Mayo Clin Proc. 1987;62:499–518.PubMedCrossRefGoogle Scholar
  29. 29.
    Ramirez J. Pulmonary alveolar proteinosis. Treatment by massive bronchopulmonary lavage. Arch Intern Med. 1967;119:147–56.PubMedCrossRefGoogle Scholar
  30. 30.
    Arora R, Hagan L, Conger NG. Mycobacterium simiae infection in a patient with common variable immunodeficiency. J Allergy Clin Immunol. 2004;113:S123.CrossRefGoogle Scholar
  31. 31.
    Kralickova P, Mala E, Vokurkova D, Krcmova I, Pliskova L, Stepanova V, Bartos V, Koblizek V, Tacheci I, Bures J, Brozik J, Litzman J. Cytomegalovirus disease in patients with common variable immunodeficiency: three case reports. Int Arch Allergy Immunol. 2014;163:69–74.PubMedCrossRefGoogle Scholar
  32. 32.
    Griffith DE, Girard WM, Wallace RJ. Clinical features of pulmonary disease caused by rapidly growing mycobacteria: an analysis of 154 patients. Am Rev Respir Dis. 1993;147:1271–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Okumura M, Iwai K, Ogata H, Ueyama M, Kubota M, Aoki M, Kokuto H, Tadokoro E, Uchiyama T, Saotome M, Yoshiyama T, Yoshimori K, Yoshida N, Azuma A, Kudoh S. Clinical factors on cavitary and nodular bronchiectatic types in pulmonary Mycobacterium avium complex disease. Intern Med. 2008;47:1465–72.PubMedCrossRefGoogle Scholar
  34. 34.
    Prince DS, Peterson DD, Steiner RM, Gottlieb JE, Scott R, Israel HL, Figueroa WG, Fish JE. Infection with Mycobacterium avium complex in patients without predisposing conditions. N Engl J Med. 1989;321:863–8.PubMedCrossRefGoogle Scholar
  35. 35.
    Chan ED, Iseman MD. Slender, older women appear to be more susceptible to nontuberculous mycobacterial lung disease. Gend Med. 2010;7:5–18.PubMedCrossRefGoogle Scholar
  36. 36.
    Iseman MD, Buschman DL, Ackerson LM. Pectus excavatum and scoliosis. Thoracic anomalies associated with pulmonary disease caused by Mycobacterium avium complex. Am Rev Respir Dis. 1991;144:914–6.PubMedCrossRefGoogle Scholar
  37. 37.
    Kim RD, Greenberg DE, Ehrmantraut ME, Guide SV, Ding L, Shea Y, Brown MR, Chernick M, Steagall WK, Glasgow CG, Lin J, Jolley C, Sorbara L, Raffeld M, Hill S, Avila N, Sachdev V, Barnhart LA, Anderson VL, Claypool R, Hilligoss DM, Garofalo M, Fitzgerald A, Anaya-O'Brien S, Darnell D, DeCastro R, Menning HM, Ricklefs SM, Porcella SF, Olivier KN, Moss J, Holland SM. Pulmonary nontuberculous mycobacterial disease: prospective study of a distinct preexisting syndrome. Am J Respir Crit Care Med. 2008;178:1066–74.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Talbert J, Chan ED. The association between body shape and non-tuberculous mycobacterial lung disease. Expert Rev Respir Med. 2013;7:201–4.PubMedCrossRefGoogle Scholar
  39. 39.
    Tasaka S, Hasegawa N, Nishimura T, Yamasawa W, Kamata H, Shinoda H, Kimizuka Y, Fujiwara H, Hirose H, Ishizaka A. Elevated serum adiponectin level in patients with Mycobacterium avium-intracellulare complex pulmonary disease. Respiration. 2010;79:383–7.PubMedCrossRefGoogle Scholar
  40. 40.
    Wakamatsu K, Nagata N, Maki S, Omori H, Kumazoe H, Ueno K, Matsunaga Y, Hara M, Takakura K, Fukumoto N, Ando N, Morishige M, Akasaki T, Inoshima I, Ise S, Izumi M, Kawasaki M. Patients with MAC lung disease have a low visceral fat area and low nutrient intake. Pulm Med. 2015;2015:218253.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Hayashi M, Takayanagi N, Kanauchi T, Miyahara Y, Yanagisawa T, Sugita Y. Prognostic factors of 634 HIV-negative patients with Mycobacterium avium complex lung disease. Am J Respir Crit Care Med. 2012;185:575–83.PubMedCrossRefGoogle Scholar
  42. 42.
    Ikegame S, Maki S, Wakamatsu K, Nagata N, Kumazoe H, Fujita M, Nakanishi Y, Kawasaki M, Kajiki A. Nutritional assessment in patients with pulmonary nontuberculous mycobacteriosis. Intern Med. 2011;50:2541–6.PubMedCrossRefGoogle Scholar
  43. 43.
    Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature. 1998;394:897–901.PubMedCrossRefGoogle Scholar
  44. 44.
    Ordway D, Henao-Tamayo M, Smith E, Shanley C, Harton M, Troudt JL, Bai X, Basaraba RJ, Orme IM, Chan ED. Animal model of Mycobacterium abscessus lung infection. J Leukoc Biol. 2008;83:1502–11.PubMedCrossRefGoogle Scholar
  45. 45.
    Szymanski EP, Leung JM, Fowler CJ, Haney C, Hsu AP, Chen F, Duggal P, Oler AJ, McCormack R, Podack E, Drummond RA, Lionakis MS, Browne SK, Prevots DR, Knowles M, Cutting G, Liu X, Devine SE, Fraser CM, Tettelin H, Olivier KN, Holland SM. Pulmonary nontuberculous mycobacterial infection. A multisystem, multigenic disease. Am J Respir Crit Care Med. 2015;192:618–28.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Becker K, Arts P, Jaeger M, Plantinga T, Gilissen C, van Laarhoven A, van Ingen J, Veltman J, Joosten L, Hoischen A, Netea M, Iseman M, Chan ED, van de Veerdonk F. MST1R mutation as a genetic cause of Lady Windermere syndrome. Eur Respir J. 2017;49:1601478.PubMedCrossRefGoogle Scholar
  47. 47.
    Sakamoto O, Iwama A, Amitani R, Takehara T, Yamaguchi N, Yamamoto T, Masuyama K, Yamanaka T, Ando M, Suda T. Role of macrophage-stimulating protein and its receptor, RON tyrosine kinase, in ciliary motility. J Clin Invest. 1997;99:701–9.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Takano Y, Sakamoto O, Suga M, Suda T, Ando M. Elevated levels of macrophage-stimulating protein in induced sputum of patients with bronchiectasis. Respir Med. 2000;94:784–90.PubMedCrossRefGoogle Scholar
  49. 49.
    Fowler CJ, Olivier KN, Leung JM, Smith CC, Huth AG, Root H, Kuhns DB, Logun C, Zelazny A, Frein CA, Daub J, Haney C, Shelhamer JH, Bryant CE, Holland SM. Abnormal nasal nitric oxide production, ciliary beat frequency, and Toll-like receptor response in pulmonary nontuberculous mycobacterial disease epithelium. Am J Respir Crit Care Med. 2013;187:1374–81.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Yaacoby-Bianu K, Gur M, Toukan Y, Nir V, Hakim F, Geffen Y, Bentur L. Compassionate nitric oxide adjuvant treatment of persistent Mycobacterium infection in cystic fibrosis patients. Pediatr Infect Dis J. 2017. [Epub ahead of print].Google Scholar
  51. 51.
    Matsuyama M, Martins AJ, Shallom S, Kamenyeva O, Kashyap A, Sampaio EP, Kabat J, Olivier KN, Zelazny AM, Tsang JS, Holland SM. Transcriptional response of respiratory epithelium to nontuberculous mycobacteria. Am J Respir Cell Mol Biol. 2018;58:241–52.PubMedCrossRefGoogle Scholar
  52. 52.
    Honda JR, Bai X, Chan ED. Elucidating the pathogenesis for NTM lung disease: lesson from the six blind men and the elephant (editorial). Am J Respir Cell Mol Biol. 2017. (In press).Google Scholar
  53. 53.
    Greinert U, Schlaak M, Rüsch-Gerdes S, Flad HD, Ernst M. Low in vitro production of interferon-gamma and tumor necrosis factor-alpha in HIV-seronegative patients with pulmonary disease caused by nontuberculous mycobacteria. J Clin Immunol. 2000;20:445–52.PubMedCrossRefGoogle Scholar
  54. 54.
    Kwon YS, Kim EJ, Lee S-H, Suh GY, Chung MP, Kim H, Kwon OJ, Koh W-J. Decreased cytokine production in patients with nontuberculous mycobacterial lung disease. Lung. 2007;185:337–41.PubMedCrossRefGoogle Scholar
  55. 55.
    Safdar A, Atrmstrong D, Murray HW. A novel defect in interferon-g secretion in patients with refractory nontuberculous pulmonary mycobacteriosis. Ann Intern Med. 2003;138:521.PubMedCrossRefGoogle Scholar
  56. 56.
    Safdar A, White DA, Stover D, Armstrong D, Murray HW. Profound interferon gamma deficiency in patients with chronic pulmonary nontuberculous mycobacteriosis. Am J Med. 2002;113:756–9.PubMedCrossRefGoogle Scholar
  57. 57.
    Vankayalapati R, Wizel B, Samten B, Griffith DE, Shams H, Galland MR, Von Reyn CF, Girard WM, Wallace RJ, Barnes PF. Cytokine profiles in immunocompetent persons infected with Mycobacterium avium complex. J Infect Dis. 2001;183:478–84.PubMedCrossRefGoogle Scholar
  58. 58.
    Lim A, Allison C, Price P, Waterer G. Susceptibility to pulmonary disease due to Mycobacterium avium-intracellulare complex may reflect low IL-17 and high IL-10 responses rather than Th1 deficiency. Clin Immunol. 2010;137:296–302.PubMedCrossRefGoogle Scholar
  59. 59.
    de Jong E, Lim A, Waterer G, Price P. Monocyte-derived macrophages do not explain susceptibility to pulmonary non-tuberculous mycobacterial disease. Clin Transl Immunol. 2012;1:e2.CrossRefGoogle Scholar
  60. 60.
    Cowman SA, Jacob J, Hansell DM, Kelleher P, Wilson R, Cookson WOC, Moffatt MF, Loebinger MR. Whole blood gene expression in pulmonary non-tuberculous mycobacterial infection. Am J Respir Cell Mol Biol. 2017. [Epub ahead of print].Google Scholar
  61. 61.
    Lam PK, Griffith DE, Aksamit TR, Ruoss SJ, Garay SM, Daley CL, Catanzaro A. Factors related to response to intermittent treatment of Mycobacterium avium complex lung disease. Am J Respir Crit Care Med. 2006;173:1283–9.PubMedCrossRefGoogle Scholar
  62. 62.
    Ryu YJ, Kim EJ, Lee SH, Kim SY, Suh GY, Chung MP, Kim H, Kwon OJ, Koh WJ. Impaired expression of Toll-like receptor 2 in nontuberculous mycobacterial lung disease. Eur Respir J. 2007;30:736–42.PubMedCrossRefGoogle Scholar
  63. 63.
    Champsi J, Young LS, Bermudez LE. Production of TNF-alpha, IL-6 and TGF-beta, and expression of receptors for TNF-alpha and IL-6, during murine Mycobacterium avium infection. Immunology. 1995;84:549–54.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Denis M, Ghadirian E. Transforming growth factor beta (TGF-b1) plays a detrimental role in the progression of experimental Mycobacterium avium infection; in vivo and in vitro evidence. Microb Pathog. 1991;11:367–72.PubMedCrossRefGoogle Scholar
  65. 65.
    Judge DP, Dietz HC. Marfan’s syndrome. Lancet. 2005;366:1965–76.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Daniels ML, Birchard KR, Lowe JR, Patrone MV, Noone PG, Knowles MR. Enlarged dural sac in idiopathic bronchiectasis implicates heritable connective tissue gene variants. Ann Am Thorac Soc. 2016;13:1712–20.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Paulson ML, Olivier KN, Holland SM. Pulmonary non-tuberculous mycobacterial infection in congenital contractural arachnodactyly. Int J Tuberc Lung Dis. 2012;16:561–3.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Foster ME, Foster DR. Bronchiectasis and Marfan's syndrome. Postgrad Med J. 1980;56:718–9.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Wood JR, Bellamy D, Child AH, Citron KM. Pulmonary disease in patients with Marfan syndrome. Thorax. 1984;39:780–4.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Teoh PC. Bronchiectasis and spontaneous pneumothorax in Marfan's syndrome. Chest. 1977;72:672–3.PubMedCrossRefGoogle Scholar
  71. 71.
    Ras GJ, Van Wyk CJ. Primary ciliary dyskinesia in association with Marfan’s syndrome. A case report. S Afr Med J. 1983;64:212–4.PubMedGoogle Scholar
  72. 72.
    Saito H, Iijima K, Dambara T, Shiota J, Hirose S, Uekusa T, Saiki S, Kira S. An autopsy case of Marfan syndrome with bronchiectasis and multiple bullae. Nihon Kyobu Shikkan Gakkai Zasshi. 1992;30:1315–21.PubMedGoogle Scholar
  73. 73.
    Hwang HS, Yi CA, Yoo H, Yang JH, Kim DK, Koh WJ. The prevalence of bronchiectasis in patients with Marfan syndrome. Int J Tuberc Lung Dis. 2014;18:995–7.PubMedCrossRefGoogle Scholar
  74. 74.
    Desai U, Kalamkar S, Joshi JM. Bronchiectasis in a Marfanoid: diagnosis beyond Marfans. Indian J Chest Dis Allied Sci. 2014;56:105–7.PubMedGoogle Scholar
  75. 75.
    McCormack RM, Szymanski EP, Hsu AP, Perez E, Olivier KN, Fisher E, Goodhew EB, Podack ER. Holland SM. MPEG1/perforin-2 mutations in human pulmonary nontuberculous mycobacterial infections. JCI Insight. 2017;2:89635.PubMedCrossRefGoogle Scholar
  76. 76.
    Chen F, Szymanski EP, Olivier KN, Liu X, Tettelin H, Holland SM, Duggal P. Whole-exome sequencing identifies the 6q12-q16 linkage region and a candidate gene, TTK, for pulmonary nontuberculous mycobacterial disease. Am J Respir Crit Care Med. 2017;196:1599–604.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Colombo RE, Hill SC, Claypool RJ, Holland SM, Olivier KN. Familial clustering of pulmonary nontuberculous mycobacterial disease. Chest. 2010;137:629–34.PubMedCrossRefGoogle Scholar
  78. 78.
    Reich JM, Johnson RE. Mycobacterium avium complex pulmonary disease presenting as an isolated lingular or middle lobe pattern: the Lady Windermere syndrome. Chest. 1992;101:1605–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Tsuyuguchi K, Suzuki K, Matsumoto H, Tanaka E, Amitani R, Kuze F. Effect of oestrogen on Mycobacterium avium complex pulmonary infection in mice. Clin Exp Immunol. 2001;123:428–34.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Adjemian J, Olivier KN, Seitz AE, Holland SM, Prevots DR. Prevalence of nontuberculous mycobacterial lung disease in U.S. Medicare beneficiaries. Am J Respir Crit Care Med. 2012;185:881–6.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Chi CY, Chu CC, Liu JP, Lin CH, Ho MW, Lo WJ, Lin PC, Chen HJ, Chou CH, Feng JY, Fung CP, Sher YP, Li CY, Wang JH, Ku CL. Anti-IFN-γ autoantibodies in adults with disseminated nontuberculous mycobacterial infections are associated with HLA-DRB1*16:02 and HLA-DQB1*05:02 and the reactivation of latent varicella-zoster virus infection. Blood. 2013;121:1357–66.PubMedCrossRefGoogle Scholar
  82. 82.
    Doucette K, Fishman JA. Nontuberculous mycobacterial infection in hematopoietic stem cell and solid organ transplant recipients. Clin Infect Dis. 2004;38:1428–39.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    French AL, Benator DA, Gordin FM. Nontuberculous mycobacterial infections. Med Clin North Am. 1997;81:361–79.PubMedCrossRefGoogle Scholar
  84. 84.
    Winthrop KL, Baxter R, Liu L, Varley CD, Curtis JR, Baddley JW, McFarland B, Austin D, Radcliffe L, Suhler E, Choi D, Rosenbaum JT, Herrinton LJ. Mycobacterial diseases and antitumour necrosis factor therapy in USA. Ann Rheum Dis. 2013;72:37–42.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Altare F, Lammas D, Revy P, Jouanguy E, Döffinger R, Lamhamedi S, Drysdale P, Scheel-Toellner D, Girdlestone J, Darbyshire P, Wadhwa M, Dockrell H, Salmon M, Fischer A, Durandy A, Casanova JL, Kumararatne DS. Inherited interleukin 12 deficiency in a child with bacille Calmette-Guérin and Salmonella enteritidis disseminated infection. J Clin Invest. 1998;102:2035–40.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D, Salem S, Radovanovic I, Grant AV, Adimi P, Mansouri N, Okada S, Bryant VL, Kong XF, Kreins A, Velez MM, Boisson B, Khalilzadeh S, Ozcelik U, Darazam IA, Schoggins JW, Rice CM, Al-Muhsen S, Behr M, Vogt G, Puel A, Bustamante J, Gros P, Huibregtse JM, Abel L, Boisson-Dupuis S, Casanova JL. Mycobacterial disease and impaired IFN-γ immunity in humans with inherited ISG15 deficiency. Science. 2012;337:1684–8.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Bustamante J, Arias AA, Vogt G, Picard C, Galicia LB, Prando C, Grant AV, Marchal CC, Hubeau M, Chapgier A, de Beaucoudrey L, Puel A, Feinberg J, Valinetz E, Jannière L, Besse C, Boland A, Brisseau JM, Blanche S, Lortholary O, Fieschi C, Emile JF, Boisson-Dupuis S, Al-Muhsen S, Woda B, Newburger PE, Condino-Neto A, Dinauer MC, Abel L, Casanova JL. Germline CYBB mutations that selectively affect macrophages in kindreds with X-linked predisposition to tuberculous mycobacterial disease. Nat Immunol. 2011;12:213–21.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Döffinger R, Jouanguy E, Dupuis S, Fondanèche MC, Stephan JL, Emile JF, Lamhamedi-Cherradi S, Altare F, Pallier A, Barcenas-Morales G, Meinl E, Krause C, Pestka S, Schreiber RD, Novelli F, Casanova JL. Partial interferon-gamma receptor signaling chain deficiency in a patient with bacille Calmette-Guérin and Mycobacterium abscessus infection. J Infect Dis. 2000;181:379–84.PubMedCrossRefGoogle Scholar
  89. 89.
    Dorman SE, Picard C, Lammas D, Heyne K, van Dissel JT, Baretto R, Rosenzweig SD, Newport M, Levin M, Roesler J, Kumararatne D, Casanova JL, Holland SM. Clinical features of dominant and recessive interferon gamma receptor 1 deficiencies. Lancet. 2004;364:2113–21.PubMedCrossRefGoogle Scholar
  90. 90.
    Dupuis S, Dargemont C, Fieschi C, Thomassin N, Rosenzweig S, Harris J, Holland SM, Schreiber RD, Casanova JL. Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation. Science. 2001;293:300–3.PubMedCrossRefGoogle Scholar
  91. 91.
    Filipe-Santos O, Bustamante J, Haverkamp MH, Vinolo E, Ku CL, Puel A, Frucht DM, Christel K, von Bernuth H, Jouanguy E, Feinberg J, Durandy A, Senechal B, Chapgier A, Vogt G, de Beaucoudrey L, Fieschi C, Picard C, Garfa M, Chemli J, Bejaoui M, Tsolia MN, Kutukculer N, Plebani A, Notarangelo L, Bodemer C, Geissmann F, Israël A, Véron M, Knackstedt M, Barbouche R, Abel L, Magdorf K, Gendrel D, Agou F, Holland SM. Casanova JL. X-linked susceptibility to mycobacteria is caused by mutations in NEMO impairing CD40-dependent IL-12 production. J Exp Med. 2006;203:1745–59.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J, Fortin A, Haniffa M, Ceron-Gutierrez L, Bacon CM, Menon G, Trouillet C, McDonald D, Carey P, Ginhoux F, Alsina L, Zumwalt TJ, Kong XF, Kumararatne D, Butler K, Hubeau M, Feinberg J, Al-Muhsen S, Cant A, Abel L, Chaussabel D, Doffinger R, Talesnik E, Grumach A, Duarte A, Abarca K, Moraes-Vasconcelos D, Burk D, Berghuis A, Geissmann F, Collin M, Casanova JL, Gros P. IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med. 2011;365:127–38.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Haverkamp MH, van de Vosse E, van Dissel JT. Nontuberculous mycobacterial infections in children with inborn errors of the immune system. J Infect. 2014;68:S134–50.PubMedCrossRefGoogle Scholar
  94. 94.
    Hsu AP, Johnson KD, Falcone EL, Sanalkumar R, Sanchez L, Hickstein DD, Cuellar-Rodriguez J, Lemieux JE, Zerbe CS, Bresnick EH, Holland SM. GATA2 haploinsufficiency caused by mutations in a conserved intronic element leads to MonoMAC syndrome. Blood. 2013;121:3830–7.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Minegishi Y, Saito M, Morio T, Watanabe K, Agematsu K, Tsuchiya S, Takada H, Hara T, Kawamura N, Ariga T, Kaneko H, Kondo N, Tsuge I, Yachie A, Sakiyama Y, Iwata T, Bessho F, Ohishi T, Joh K, Imai K, Kogawa K, Shinohara M, Fujieda M, Wakiguchi H, Pasic S, Abinun M, Ochs HD, Renner ED, Jansson A, Belohradsky BH, Metin A, Shimizu N, Mizutani S, Miyawaki T, Nonoyama S, Karasuyama H. Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity. 2006;25:745–55.PubMedCrossRefGoogle Scholar
  96. 96.
    Okada S, Markle JG, Deenick EK, Mele F, Averbuch D, Lagos M, Alzahrani M, Al-Muhsen S, Halwani R, Ma CS, Wong N, Soudais C, Henderson LA, Marzouqa H, Shamma J, Gonzalez M, Martinez-Barricarte R, Okada C, Avery DT, Latorre D, Deswarte C, Jabot-Hanin F, Torrado E, Fountain J, Belkadi A, Itan Y, Boisson B, Migaud M, Arlehamn CS, Sette A, Breton S, McCluskey J, Rossjohn J, de Villartay JP, Moshous D, Hambleton S, Latour S, Arkwright PD, Picard C, Lantz O, Engelhard D, Kobayashi M, Abel L, Cooper AM, Notarangelo LD, Boisson-Dupuis S, Puel A, Sallusto F, Bustamante J, Tangye SG, Casanova JL. Impairment of immunity to Candida and Mycobacterium in humans with bi-allelic RORC mutations. Science. 2015;349:606–13.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Prando C, Samarina A, Bustamante J, Boisson-Dupuis S, Cobat A, Picard C, AlSum Z, Al-Jumaah S, Al-Hajjar S, Frayha H, Alangari A, Al-Mousa H, Mobaireek KF, Ben-Mustapha I, Adimi P, Feinberg J, de Suremain M, Jannière L, Filipe-Santos O, Mansouri N, Stephan JL, Nallusamy R, Kumararatne DS, Bloorsaz MR, Ben-Ali M, Elloumi-Zghal H, Chemli J, Bouguila J, Bejaoui M, Alaki E, AlFawaz TS, Al Idrissi E, ElGhazali G, Pollard AJ, Murugasu B, Wah-Lee B, Halwani R, Al-Zahrani M, Al Shehri MA, Al-Zahrani M, Bin-Hussain I, Mahdaviani SA, Parvaneh N, Abel L, Mansouri D, Barbouche R, Al-Muhsen S, Casanova JL. Inherited IL-12p40 deficiency: genetic, immunologic, and clinical features of 49 patients from 30 kindreds. Medicine (Baltimore). 2013;92:109–22.CrossRefGoogle Scholar
  98. 98.
    Wu UI, Holland SM. Host susceptibility to non-tuberculous mycobacterial infections. Lancet Infect Dis. 2015;15:968–80.PubMedCrossRefGoogle Scholar
  99. 99.
    Hanson EP, Monaco-Shawver L, Solt LA, Madge LA, Banerjee PP, May MJ, Orange JS. Hypomorphic nuclear factor-kappaB essential modulator mutation database and reconstitution system identifies phenotypic and immunologic diversity. J Allergy Clin Immunol. 2008;122:1169–77.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Manry J, Laval G, Patin E, Fornarino S, Tichit M, Bouchier C, Barreiro LB, Quintana-Murci L. Evolutionary genetics evidence of an essential, nonredundant role of the IFN-γ pathway in protective immunity. Hum Mutat. 2011;32:633–42.PubMedCrossRefGoogle Scholar
  101. 101.
    Vinh DC, Patel SY, Uzel G, Anderson VL, Freeman AF, Olivier KN, Spalding C, Hughes S, Pittaluga S, Raffeld M, Sorbara LR, Elloumi HZ, Kuhns DB, Turner ML, Cowen EW, Fink D, Long-Priel D, Hsu AP, Ding L, Paulson ML, Whitney AR, Sampaio EP, Frucht DM, DeLeo FR, Holland SM. Autosomal dominant and sporadic monocytopenia with susceptibility to mycobacteria, fungi, papillomaviruses, and myelodysplasia. Blood. 2010;115:1519–29.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Hsu AP, Sampaio EP, Khan J, Calvo KR, Lemieux JE, Patel SY, Frucht DM, Vinh DC, Auth RD, Freeman AF, Olivier KN, Uzel G, Zerbe CS, Spalding C, Pittaluga S, Raffeld M, Kuhns DB, Ding L, Paulson ML, Marciano BE, Gea-Banacloche JC, Orange JS, Cuellar-Rodriguez J, Hickstein DD, Holland SM. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood. 2011;118:2653–5.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Migliaccio AR, Bieker JJ. GATA2 finds its macrophage niche. Blood. 2011;118:2647–9.PubMedCrossRefGoogle Scholar
  104. 104.
    Honda JR, Knight V, Chan ED. Pathogenesis and risk factors for nontuberculous mycobacterial lung disease. Clin Chest Med. 2015;36:1–11.PubMedCrossRefGoogle Scholar
  105. 105.
    Allen DM, Chng HH. Disseminated Mycobacterium flavescens in a probable case of chronic granulomatous disease. J Infect. 1993;26:83–6.PubMedCrossRefGoogle Scholar
  106. 106.
    Chusid MJ, Parrillo JE, Fauci AS. Chronic granulomatous disease. Diagnosis in a 27-year-old man with Mycobacterium fortuitum. JAMA. 1975;233:1295–6.PubMedCrossRefGoogle Scholar
  107. 107.
    Ohga S, Ikeuchi K, Kadoya R, Okada K, Miyazaki C, Suita S, Ueda K. Intrapulmonary Mycobacterium avium infection as the first manifestation of chronic granulomatous disease. J Infect. 1997;34:147–50.PubMedCrossRefGoogle Scholar
  108. 108.
    Oberley-Deegan RE, Rebits BW, Weaver MR, Tollefson AK, Bai X, McGibney M, Ovrutsky AR, Chan ED, Crapo JD. An oxidative environment promotes growth of Mycobacterium abscessus. Free Radic Biol Med. 2010;49:1666–73.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Oberley-Deegan RE, Lee YM, Morey GE, Cook DM, Chan ED, Crapo JD. The antioxidant mimetic, MnTE-2-PyP, reduces intracellular growth of Mycobacterium abscessus. Am J Respir Cell Mol Biol. 2009;41:170–8.PubMedCrossRefGoogle Scholar
  110. 110.
    Malcolm KC, Nichols EM, Caceres SM, Kret JE, Martiniano SL, Sagel SD, Chan ED, Caverly L, Solomon GM, Reynolds P, Bratton DL, Taylor-Cousar JL, Nichols DP, Saavedra MT, Nick JA. Mycobacterium abscessus induces a limited pattern of neutrophil activation that promotes pathogen survival. PLoS One. 2013;8:e57402.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Jouanguy E, Lamhamedi-Cherradi S, Lammas D, Dorman SE, Fondanèche MC, Dupuis S, Döffinger R, Altare F, Girdlestone J, Emile JF, Ducoulombier H, Edgar D, Clarke J, Oxelius VA, Brai M, Novelli V, Heyne K, Fischer A, Holland SM, Kumararatne DS, Schreiber RD, Casanova JL. A human IFNGR1 small deletion hotspot associated with dominant susceptibility to mycobacterial infection. Nat Genet. 1999;21:370–8.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Pulmonary Section, Denver Veterans Affairs Medical CenterDenverUSA
  2. 2.Program in Cell Biology and Department of Academic Affairs, National Jewish HealthDenverUSA
  3. 3.Division of Pulmonary Sciences and Critical Care MedicineUniversity of Colorado Anschutz Medical CampusAuroraUSA

Personalised recommendations