Clinical features, epidemiology, and therapy of lymphangioleiomyomatosis

Clinical Epidemiology

Volumn 7, Issue , 2015, Pages 249-257

  Taveira DaSilva, Angelo M ^a   Moss, Joel ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Lymphangioleiomyomatosis; Mammalian target of rapamycin signaling pathway; TSC1 and TSC2 mutations; Tuberous sclerosis

Indexed keywords

AROMATASE INHIBITOR; ESTROGEN RECEPTOR ANTAGONIST; EVEROLIMUS; HYDROXYCHLOROQUINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PROTEIN INHIBITOR; RAPAMYCIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SIMVASTATIN; VASCULOTROPIN INHIBITOR;

ANGIOMYOLIPOMA; ARTICLE; ASCITES; CARDIOPULMONARY EXERCISE TEST; CHYLOTHORAX; CLINICAL FEATURE; COMPUTER ASSISTED TOMOGRAPHY; DIFFERENTIAL DIAGNOSIS; DISEASE ASSOCIATION; DYSPNEA; EPIDEMIOLOGICAL DATA; FORCED EXPIRATORY VOLUME; GENE; GENE MUTATION; GENETIC ASSOCIATION; HEMOPTYSIS; HISTOPATHOLOGY; HUMAN; LEIOMYOMA; LUNG DIFFUSION CAPACITY; LUNG FUNCTION TEST; LUNG GAS EXCHANGE; LYMPHANGIOLEIOMYOMA; LYMPHANGIOLEIOMYOMATOSIS; NONHUMAN; PATHOGENESIS; PATIENT CARE; PLEURA EFFUSION; PNEUMOTHORAX; PREVALENCE; PROGNOSIS; PROTEIN FUNCTION; PROTEIN TARGETING; RECURRENT DISEASE; SIGNAL TRANSDUCTION; THORAX RADIOGRAPHY; TREATMENT INDICATION; TSC1 GENE; TSC2 GENE;

EID: 84936999277     PISSN: None     EISSN: 11791349     Source Type: Journal    
DOI: 10.2147/CLEP.S50780     Document Type: Article

References (93)

1. Ryu JH, Moss J, Beck GJ, et al. The NHLBI Lymphangioleiomyomatosis Registry. Characteristics of 230 patients at enrollment. Am J Respir Crit Care Med. 2006; 173(1): 105-111.
2. McCormack FX. Lymphangioleiomyomatosis: a clinical update. Chest. 2008; 133(2): 507-516.
3. Urban T, Lazor R, Lacronique J, et al. Pulmonary lymphangioleiomyomatosis. A study of 69 patients. Groupe d'Etudes et de Recherche sur les Maladies "Orphelines" Pulmonaires (GERM"O"P). Medicine. 1999; 78(5): 321-327.
4. Matsui K, Tatsuguchi A, Valencia J, et al. Extrapulmonary lymphangioleiomyomatosis (LAM): clinicopathologic features in 22 cases. Hum Pathol. 2000; 31(10): 12421248.
5. Abbott GF, Rosado-de-Christenson ML, Frazier AA, Franks TJ, Pugatch RD, Galvin JR. From the archives of the AFIP: lymphangioleiomyomatosis: radiologic-pathologic correlation. Radiographics. 2005; 25(3): 803-828.
6. Ferrans VJ, Yu ZX, Nelson WK, et al. Lymphangioleiomyomatosis (LAM). A review of clinical and morphological features. J Nippon Med Sch. 2000; 67(5): 311-329.
7. Curatolo P, Bombardieri R, Jozwiak S. Tuberous sclerosis. Lancet. 2008; 372(9639): 657-668.
8. Smolarek TA, Wessner LL, McCormack FX, Mylet JC, Menon AG, Henske EP. Evidence that lymphangiomyomatosis is caused by TSC2 mutations, chromosome 16p13 loss of heterozygosity in angiomyolipomas and lymph nodes from women with lymphangiomyomatosis. Am J Hum Genet. 1998; 62(4): 810-815.
9. Carsillo T, Astrinidis A, Henske EP. Mutations in the tuberous sclerosis complex gene TSC2 are a cause of sporadic pulmonary lymphangioleiomyomatosis. Proc Natl Acad Sci U S A. 2000; 97(11): 6085-6090.
10. Yu J, Astrinidis A, Henske EP. Chromosome 16 loss of heterozygosity in tuberous sclerosis and sporadic lymphangiomyomatosis. Am J Respir Crit Care Med. 2001; 164(8): 1537-1540.
11. Harknett EC, Chang WY, Byrnes S, et al. Use of variability in national and regional data to estimate the prevalence of lymphangioleiomyomatosis. Q J Med. 2011; 104(11): 971-979.
12. Silversteen EF, Ellis K, Wolff M, Jaretzki A. Pulmonary lymphangiomyomatosis. Am J Roentgenol. 1974; 120(4): 832-850.
13. Corrin B, Liebow AA, Friedman PJ. Pulmonary lymphangioleiomyomatosis: a review. Am J Pathol. 1975; 79(2): 348-382.
14. Taylor JR, Ryu J, Colby TV, Raffin TA. Lymphangioleiomyomatosis: clinical course in 32 patients. N Engl J Med. 1990; 323(18): 1254-1260.
15. Cohen MM, Pollock-BarZiv S, Johnson SR. Emerging clinical picture of lymphangioleiomyomatosis. Thorax. 2005; 60(10): 875-879.
16. Oprescu N, McCormack FX, Byrnes S, Kinder BW. Clinical predictors of mortality and cause of death in lymphangioleiomyomatosis: a population-based registry. Lung. 2013; 191(1): 35-42.
17. Dwyer JM, Hickie JB, Garvan J. Pulmonary tuberous sclerosis. Q J Med. 1971; 40(157): 115-125.
18. Shepherd CW, Gomez MR, Lie JT, Crowson CS. Causes of death in tuberous sclerosis. Mayo Clin Proc. 1991; 66(8): 792-796.
19. Castro M, Shepherd CW, Gomez MR, Lie JT, Ryu JH. Pulmonary tuberous sclerosis. Chest. 1995; 107(1): 189-195.
20. Hancock E, Tomkins S, Sampson J, Osborne J. Lymphangioleiomyomatosis and tuberous sclerosis. Respir Med. 2002; 96(1): 7-13.
21. Costello LC, Hartman TE, Ryu JH. High frequency of pulmonary lymphangioleiomyomatosis in women with tuberous sclerosis complex. Mayo Clin Proc. 2000; 75(6): 591-594.
22. Moss J, Avila N, Barnes PM, et al. Prevalence and clinical characteristics of lymphangioleiomyomatosis (LAM) in patients with tuberous sclerosis complex. Am J Respir Crit Care Med. 2001; 164(4): 669-471.
23. Franz DN, Brody A, Meyer C, et al. Mutational and radiographic analysis of pulmonary disease consistent with lymphangioleiomyomatosis and micronodular pneumocyte hyperplasia in women with tuberous sclerosis. Am J Respir Crit Care Med. 2001; 164(4): 661-668.
24. Cudzilo CJ, Szczesniak RD, Brody AS, et al. Lymphangioleiomyomatosis screening in women with tuberous sclerosis. Chest. 2013; 144(2): 578-585.
25. Adriaensen ME, Schaefer-Prokop CM, Duyndam DAC, Zonnenberg BA, Prokop M. Radiological evidence of lymphangioleiomyomatosis in female and male patients with tuberous sclerosis complex. Clin Radiol. 2011; 66(7): 625-628.
26. Avila NA, Kelly JA, Chu SC, Dwyer AJ, Moss J. Lymphangioleiomyomatosis: abdominopelvic CT and US findings. Radiology. 2000; 216(1): 147-153.
27. Steagall WK, Glasgow CG, Hathaway OM, et al. Genetic and morphologic determinants of pneumothorax in lymphangioleiomyomatosis. Am J Physiol Lung Cell Mol Physiol. 2007; 293(3): L800-L808.
28. Avila NA, Dwyer AJ, Rabel A, Moss J. Sporadic lymphangioleiomyomatosis and tuberous sclerosis complex with lymphangioleiomyomatosis, comparison of CT features. Radiology. 2007; 242(1): 277-285.
29. Meraj R, Wikenheiser-Brokamp KA, Young LR, McCormack FX. Lymphangioleiomyomatosis: new concepts in pathogenesis, diagnosis, and treatment. Semin Respir Crit Care Med. 2012; 33(5): 486-497.
30. Crooks DM, Pacheco-Rodriguez G, DeCastro RM, et al. Molecular and genetic analysis of disseminated neoplastic cells in lymphangioleiomyomatosis. Proc Natl Acad Sci U S A. 2004; 101(50): 17462-17467.
31. Cai X, Pacheco-Rodriguez G, Fan QY, et al. Phenotypic characterization of disseminated cells with TSC2 loss of heterozygosity in patients with lymphangioleiomyomatosis. Am J Respir Crit Care Med. 2010; 182(11): 1410-1418.
32. Mitani K, Kumasaka T, Takemura H, et al. Cytologic, immunocytochemical and ultrastructural characterization of lymphangioleiomyomatosis cell clusters in chylous effusions of patients with lymphangioleiomyomatosis. Acta Cytol. 2009; 53(4): 402-409.
33. Bittmann I, Rolf B, Amann G, Löhrs U. Recurrence of lymphangioleiomyomatosis after single lung transplantation, new insights into pathogenesis. Human Pathol. 2003; 34(1): 95-98.
34. Karbowniczek M, Astrinidis A, Balsara BR, et al. Recurrent lymphangioleiomyomatosis after transplantation. Am J Respir Crit Care Med. 2003; 167(7): 976-982.
35. Hayashi T, Kumasaka T, Mitani K, et al. Prevalence of uterine and adnexal involvement in pulmonary lymphangioleiomyomatosis: a clinicopathologic study of 10 patients. Am J Surg Pathol. 2011; 35(12): 1776-1785.
36. Rosner M, Hanneder M, Siegel N, Valli A, Hengstschläger M. The tuberous sclerosis gene products hamartin and tuberin are multifunctional proteins with a wide spectrum of interacting partners. Mutat Res. 2008; 658(3): 234-246.
37. Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cel. 2010; 40(2): 310-322.
38. Sarbassov DD, Ali SM, Kim DH, et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cystoskeleton. Curr Biol. 2004; 14(14): 1296-1302.
39. Huang J, Manning BD. A complex interplay between Akt, TSC2 and the mTOR complexes. Bioch Soc Trans. 2009; 37(P1): 217-222.
40. Berger U, Khaghani A, Pomerance A, Yacoub MH, Coombes RC. Pulmonary lymphangioleiomyomatosis and steroid receptors. Am J Clin Pathol. 1990; 93(5): 609-614.
41. Ohori NP, Yousem SA, Sonmez-Alpan E, Colby TV. Estrogen and progesterone receptors in lymphangioleiomyomatosis, epithelioid hemangioendothelioma, and sclerosing hemangioma of the lung. Am J Clin Pathol. 1991; 96(4): 529-535.
42. Logginidou H, Ao X, Russo I, Henske EP. Frequent estrogen and progesterone receptor immunoreactivity in renal angiomyolipomas from women with pulmonary lymphangioleiomyomatosis. Chest. 2000; 117(1): 25-30.
43. Brunelli A, Catalini G, Fianchini A. Pregnancy exacerbating unsuspected mediastinal lymphangioleiomyomatosis and chylothorax. Int J Gynaecol Obstet. 1996; 52(3): 289-290.
44. Yano S. Exacerbation of pulmonary lymphangioleiomyomatosis by exogenous oestrogen used for infertility treatment. Thorax. 2002; 57(12): 1085-1086.
45. Taveira-DaSilva AM, Stylianou MP, Hedin CJ, Hathaway O, Moss J. Decline in lung function in patients with lymphangioleiomyomatosis treated with or without progesterone. Chest. 2004; 126(6): 1867-1874.
46. Howe SR, Gottardis MM, Everitt JI, Walker C. Estrogen stimulation and tamoxifen inhibition of leiomyoma cell growth in vitro and in vivo. Endocrinology. 1995; 136(11): 4996-5003.
47. Yu J, Astrinidis A, Howard S, Henske EP. Estradiol and tamoxifen stimulate LAM-associated angiomyolipoma cell growth and activate both genomic and nongenomic signaling pathways. Am J Physiol Lung Cell Mol Physiol. 2004; 286(4): L694-L700.
48. Yu JJ, Robb VA, Morrison TA, et al. Estrogen promotes the survival and pulmonary metastasis of tuberin-null cells. Proc Natl Acad Sci U S A. 2009; 106(8): 2635-2640.
49. Glassberg MK, Elliot SJ, Fritz J, et al. Activation of the estrogen receptor contributes to the progression of pulmonary lymphangioleiomyomatosis via matrix metalloproteinase-induced cell invasiveness. J Clin Endocrinol Metab. 2008; 93(5): 1625-1633.
50. Henske EP, McCormack FX. Lymphangioleiomyomatosis-a wolf in sheep's clothing. J Clin Invest. 2012; 122(11): 3807-3816.
51. Matsui K, Takeda K, Yu Z-X, Travis WD, Moss J, Ferrans VJ. Role for activation of matrix metalloproteinases in the pathogenesis of pulmonary lymphangioleiomyomatosis. Arch Pathol Lab Med. 2000; 124(2): 267-275.
52. Krymskaya VP, Shipley JM. Lymphangioleiomyomatosis. A complex tale of serum response factor-mediated tissue inhibitor of metalloproteinase-3 regulation. Am J Respir Cell Mol Biol. 2003; 28(5): 546-550.
53. Papakonstantinou E, Dionyssopoulos A, Aletras AJ, Pesintzaki C, Minas A, Karakiulakis G. Expression of matrix metalloproteinases and their endogenous tissue inhibitors in skin lesions from patients with tuberous sclerosis. J Am Acad Dermatol. 2004; 51(4): 526-533.
54. Zhe X, Yang Y, Jakkaraju S, Schuger L. Tissue inhibitor of metalloproteinase-3 downregulation in lymphangioleiomyomatosis. Am J Respir Cell Mol Biol. 2003; 28(4): 504-511.
55. Odajima N, Betsuyaku T, Nasuhara Y, Inoue H, Seyama K, Nishimura M. Matrix metalloproteinases in blood from patients with LAM. Respir Med. 2009; 103(1): 124-129.
56. Goncharova EA, Goncharov DA, Fehrenbach M, et al. Prevention of alveolar destruction and airspace enlargement in a mouse model of pulmonary lymphangioleiomyomatosis (LAM). Sci Transl Med. 2012; 4(154): 154ra134.
57. Yu J, Henske EP. mTOR activation, lymphangiogenesis, and estrogen-mediated cell survival: the "perfect storm" of pro-metastatic factors in LAM pathogenesis. Lymphat Res Biol. 2010; 8(1): 43-49.
58. Seyama K, Kumasaka T, Souma S, et al. Vascular endothelial growth factor-D is increased in serum of patients with lymphangioleiomyomatosis. Lymphat Res Biol. 2006; 4(3): 143-152.
59. Glasgow CG, Avila NA, Lin JP, Stylianou MP, Moss J. Serum vascular endothelial growth factor-D levels in patients with lymphangioleiomyomatosis reflect lymphatic involvement. Chest. 2009; 135(5): 1293-1300.
60. Young L, Lee HS, Inoue Y, et al. Serum VEGF-D a concentration as a biomarker of lymphangioleiomyomatosis severity and treatment response: a prospective analysis of the Multicenter International Lymphangioleiomyomatosis Efficacy of Sirolimus (MILES) trial. Lancet Respir Med. 2013; 1(4): 445-452.
61. Crausman RS, Jennings CA, Mortensen RL, Ackerson LM, Irvin CG, King TE Jr. Lymphangioleiomyomatosis: the pathophysiology of diminished exercise capacity. Am J Respir Crit Care Med. 1996; 153(4 Pt 1): 1368-1376.
62. Taveira-DaSilva AM, Stylianou MP, Hedin CJ, et al. Maximal oxygen uptake and severity of disease in lymphangioleiomyomatosis. Am J Respir Crit Care Med. 2003; 168(12): 1427-1431.
63. Sobonya RE, Quan SF, Fleishman JS. Pulmonary lymphangioleiomyomatosis: quantitative analysis of lesions producing airflow limitation. Hum Pathol. 1985; 16(11): 1122-1228.
64. Burger CD, Hyatt RE, Stats BA. Pulmonary mechanics in lymphangioleiomyomatosis. Am Rev Respir Dis. 1991; 143(5 Pt 1): 1030-1033.
65. Baldi BG, Albuquerque AL, Pimenta SP, Salge JM, Kairalla RA, Carvalho CR. Exercise performance and dynamic hyperinflation in lymphangioleiomyomatosis. Am J Respir Crit Care Med. 2012; 186(4): 341-348.
66. Taveira-DaSilva AM, Hathaway OM, Sachdev V, Shizukuda Y, Birdsall CW, Moss J. Pulmonary artery pressure in lymphangioleiomyomatosis: an echocardiographic study. Chest. 2007; 132(5): 1573-1578.
67. Crausman RS, Lynch DA, Mortensen RL, et al. Quantitative CT predicts the severity of physiologic dysfunction in patients with lymphangiomyomatosis. Chest. 1996; 109(1): 131-137.
68. Avila NA, Chen CC, Chu SC, et al. Pulmonary lymphangioleiomyomatosis: correlation of ventilation-perfusion scintigraphy, chest radiography, and CT with pulmonary function tests. Radiology. 2000; 214(2): 441-446.
69. Avila NA, Dwyer AJ, Murphy-Johnson DV, Brooks P, Moss J. Lymphangioleiomyomatosis: correlation of qualitative and quantitative thin-section CT with pulmonary function tests and assessment of dependence on pleurodesis. Radiology. 2002; 223(1): 189-197.
70. Paciocco G, Uslenghi E, Bianchi A, et al. Diffuse cystic lung diseases. Correlation between radiologic and functional status. Chest. 2004; 125(1): 135-142.
71. Schmithorst VJ, Altes TA, Young LR, et al. Automated algorithm for quantifying the extent of cystic change on volumetric chest CT: initial results in lymphangioleiomyomatosis. AJR Am J Roentgenol. 2009; 192(4): 1037-1044.
72. Yao J, Taveira-DaSilva AM, Colby TV, Moss J. Computed tomography grading of lung disease in lymphangioleiomyomatosis. AJR Am J Roentgenol. 2012; 199(4): 787-793.
73. Bissler JJ, Kingswood JC. Renal angiomyolipomata. Kidney Int. 2004; 66(3): 924-934.
74. Avila NA, Dwyer AJ, Moss J. Imaging features of lymphangioleiomyomatosis: diagnostic pitfalls. AJR Am J Roentgenol. 2011; 196(4): 982-986.
75. Avila NA, Dwyer AJ, Murphy-Johnson DV, Brooks P, Moss J. Sonography of lymphangioleiomyoma in lymphangioleiomyomatosis: demonstration of diurnal variation in lesion size. A J R Am J Roentgenol. 2005; 184(2): 459-464.
76. Avila NA, Bechtle J, Dwyer AJ, Ferrans VJ, Moss J. Lymphangioleiomyomatosis: CT of diurnal variation of lymphangioleiomyomas. Radiology. 2001; 221(2): 415-421.
77. Harari S, Torre O, Cassandro R, Taveira-DaSilva AM, Moss J. Bronchoscopic diagnosis of Langerhans cell histiocytosis and lymphangioleiomyomatosis. Respir Med. 2012; 106(9): 1286-1292.
78. Meraj R, Wikenheiser-Brokamp KA, Young LR, Byrnes S, McCormack FX. Utility of transbronchial lung biopsy in the diagnosis of lymphangioleiomyomatosis. Front Med. 2012; 6(4): 395-405.
79. Johnson SR, Cordier JF, Lazor R, et al. European Respiratory Society guidelines for the diagnosis and management of lymphangioleiomyomatosis. Eur Respir J. 2010; 35(1): 14-26.
80. Johnson SR, Tattersfield AE. Decline in lung function in lymphangioleiomyomatosis: relation to menopause and progesterone treatment. Am J Respir Crit Care Med. 1999; 160(2): 628-633.
81. Hayashida M, Seyama K, Inoue Y, et al. Respiratory Failure Research Group of the Japanese Ministry of Health, Labor, and Welfare. The epidemiology of lymphangioleiomyomatosis in Japan: a nationwide cross-sectional study of presenting features and prognostic factors. Respirology. 2007; 12(4): 523-530.
82. Matsui K, Beasley MB, Nelson WK, et al. Prognostic significance of pulmonary lymphangioleiomyomatosis histologic score. Am J Surg Path. 2001; 25(4): 479-484.
83. Taveira-DaSilva AM, Hedin CJ, Stylianou MP, et al. Reversible airflow obstruction, proliferation of abnormal smooth muscle cells and impairment of gas exchange as predictors of outcome in lymphangioleiomyomatosis. Am J Respir Crit Care Med. 2001; 164(6): 1072-1076.
84. Taveira-Dasilva AM, Steagall WK, Rabel A, et al. Reversible airflow obstruction in lymphangioleiomyomatosis. Chest. 2009; 136(6): 1596-1603.
85. Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol. 2011; 12(1): 31-35.
86. McCormack FX, Inoue Y, Moss J, et al. National Institutes of Health Rare Lung Diseases Consortium; MILES Trial Group. Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N Engl J Med. 2011; 364(17): 1595-1606.
87. Taveira-DaSilva AM, Hathaway O, Stylianou M, Moss J. Changes in lung function and chylous effusions in patients with lymphangioleiomyomatosis treated with sirolimus. Ann Intern Med. 2011; 154(12): 797-805.
88. Bissler JJ, Kingswood JC, Radzikowska E, et al. Everolimus for angiomyolipoma associated with tuberous sclerosis complex or sporadic lymphangioleiomyomatosis (EXIST-2): a multicentre, randomised, double-blind, placebo-controlled trial. Lancet. 2013; 381(9869): 817-824.
89. Yu J, Parkhitko AA, Henske EP. Mammalian target of rapamycin signaling and autophagy: roles in lymphangioleiomyomatosis therapy. Proc Am Thorac Soc. 2010; 7(1): 48-53.
90. Goncharova EA, Goncharova DA, Li H, et al. mTORC2 is required for proliferation and survival of TSC2-null cells. Mol Cell Biol. 2011; 31(12): 2484-2498.
91. Hammes SR, Krymskaya VP. Targeted approaches towards understanding and treating pulmonary lymphangioleiomyomatosis. Horm Canc. 2012; 4(2): 70-77.
92. Atochina-Vasserman EN, Goncharov DA, Volgina AV, Milavec M, James ML, Krymskaya VP. Statins in lymphangioleiomyomatosis. Simvastatin and atorvastatin induce differential effects on tuberous sclerosis complex 2-null cell growth and signaling. Am J Respir Cell Mol Biol. 2013; 49(5): 704-709.
93. Lee N, Woodrum CL, Nobil AM, Rauktys AE, Messina MP, Dabora SL. Rapamycin weekly maintenance dosing and the potential efficacy of combination of sorafenib plus rapamycin but not atorvastatin or doxycycline in tuberous sclerosis preclinical models. BMC Pharmacol. 2009; 9: 8.