Airway ciliary dysfunction and sinopulmonary symptoms in patients with congenital heart disease

Annals of the American Thoracic Society

Volumn 11, Issue 9, 2014, Pages 1426-1432

  Garrod, Andrea S ^a   Zahid, Maliha ^b   Tian, Xin ^c   Francis, Richard J ^b   Khalifa, Omar ^b   Devine, William ^a   Gabriel, George C ^b   Leatherbury, Linda ^d   Lo, Cecilia W ^b  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

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

^d CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

Ciliary dyskinesia; Heterotaxy; Nasal nitric oxide

Indexed keywords

NITRIC OXIDE;

ADULT; ARTICLE; CHILD; CILIARY DYSKINESIA; CILIARY MOTILITY; CONGENITAL HEART DISEASE; FEMALE; HETEROTAXY SYNDROME; HUMAN; MAJOR CLINICAL STUDY; MALE; NASAL BIOPSY; PHENOTYPE; PREVALENCE; QUESTIONNAIRE; VIDEO MICROSCOPY; ADOLESCENT; BREATH ANALYSIS; CILIARY MOTILITY DISORDERS; COMPLICATION; CONGENITAL HEART MALFORMATION; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; OTITIS MEDIA; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT DISEASE; YOUNG ADULT;

ADOLESCENT; ADULT; BREATH TESTS; CHILD; CILIARY MOTILITY DISORDERS; FEMALE; HEART DEFECTS, CONGENITAL; HETEROTAXY SYNDROME; HUMANS; MALE; MICROSCOPY, VIDEO; MIDDLE AGED; MULTIVARIATE ANALYSIS; NITRIC OXIDE; OTITIS MEDIA; RESPIRATORY HYPERSENSITIVITY; RESPIRATORY TRACT DISEASES; YOUNG ADULT;

EID: 84914708622     PISSN: 23296933     EISSN: 23256621     Source Type: Journal    
DOI: 10.1513/AnnalsATS.201405-222OC     Document Type: Article

References (37)

1. Knowles MR, Daniels LA, Davis SD, Zariwala MA, Leigh MW. Primary ciliary dyskinesia: recent advances in diagnostics, genetics, and characterization of clinical disease. Am J Respir Crit Care Med 2013; 188:913-922.
2. Sagel SD, Davis SD, Campisi P, Dell SD. Update of respiratory tract disease in children with primary ciliary dyskinesia. Proc Am Thorac Soc 2011;8:438-443.
3. Aylsworth AS. Clinical aspects of defects in the determination of laterality. Am J Med Genet 2001;101:345-355.
4. Shapiro AJ, Davis SD, Ferkol T, Dell SD, Rosenfeld M, Olivier KN, Sagel SD, Milla C, Zariwala MA, Wolf W, et al.; Genetic Disorders of Mucociliary Clearance Consortium. Laterality defects other than situs inversus totalis in primary ciliary dyskinesia: Insights into situs ambiguus and heterotaxy. Chest 2014;146:1176-1186.
5. Kennedy MP, Omran H, Leigh MW, Dell S, Morgan L, Molina PL, Robinson BV, Minnix SL, Olbrich H, Severin T, et al. Congenital heart disease and other heterotaxic defects in a large cohort of patients with primary ciliary dyskinesia. Circulation 2007;115:2814-2821.
6. Tan SY, Rosenthal J, Zhao XQ, Francis RJ, Chatterjee B, Sabol SL, Linask KL, Bracero L, Connelly PS, Daniels MP, et al. Heterotaxy and complex structural heart defects in a mutant mouse model of primary ciliary dyskinesia. J Clin Invest 2007;117:3742-3752.
7. Francis RJ, Christopher A, Devine WA, Ostrowski L, Lo C. Congenital heart disease and the specification of left-right asymmetry. Am J Physiol Heart Circ Physiol 2012;302:H2102-H2111.
8. Bartz PJ, Driscoll DJ, Dearani JA, Puga FJ, Danielson GK, O'Leary PW, Earing MG, Warnes CA, Hodge DO, Cetta F. Early and late results of the modified Fontan operation for heterotaxy syndrome: 30 years of experience in 142 patients. J Am Coll Cardiol 2006;48:2301-2305.
9. Swisher M, Jonas R, Tian X, Lee ES, Lo CW, Leatherbury L. Increased postoperative and respiratory complications in patients with congenital heart disease associated with heterotaxy. J Thorac Cardiovasc Surg 2011;141:637-644, 644.e631-e633.
10. American Thoracic Society; European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 2005;171: 912-930.
11. Leigh MW, Hazucha MJ, Chawla KK, Baker BR, Shapiro AJ, Brown DE, Lavange LM, Horton BJ, Qaqish B, Carson JL, et al. Standardizing nasal nitric oxide measurement as a test for primary ciliary dyskinesia. Ann Am Thorac Soc 2013;10:574-581.
12. Mateos-Corral D, Coombs R, Grasemann H, Ratjen F, Dell SD. Diagnostic value of nasal nitric oxide measured with non-velum closure techniques for children with primary ciliary dyskinesia. J Pediatr 2011;159:420-424.
13. Olin JT, Burns K, Carson JL, Metjian H, Atkinson JJ, Davis SD, Dell SD, Ferkol TW, Milla CE, Olivier KN, et al.; Genetic Disorders of Mucociliary Clearance Consortium. Diagnostic yield of nasal scrape biopsies in primary ciliary dyskinesia: A multicenter experience. Pediatr Pulmonol 2011;46:483-488.
14. Chilvers MA, Rutman A, O'Callaghan C. Ciliary beat pattern is associated with specific ultra structural defects in primary ciliary dyskinesia. J Allergy Clin Immunol 2003;112:518-524.
15. Leigh MW, O'Callaghan C, Knowles MR. The challenges of diagnosing primary ciliary dyskinesia. Proc Am Thorac Soc 2011;8:434-437.
16. Stannard WA, Chilvers MA, Rutman AR, Williams CD, O'Callaghan C. Diagnostic testing of patients suspected of primary ciliary dyskinesia. Am J Respir Crit Care Med 2010;181:307-314.
17. Nakhleh N, Francis R, Giese RA, Tian X, Li Y, Zariwala MA, Yagi H, Khalifa O, Kureshi S, Chatterjee B, et al. High prevalence of respiratory ciliary dysfunction in congenital heart disease patients with heterotaxy. Circulation 2012;125:2232-2242.
18. Harden B, Tian X, Giese R, Nakhleh N, Kureshi S, Francis R, Hanumanthaiah S, Li Y, Swisher M, Kuehl K, et al. Increased postoperative respiratory complications in heterotaxy congenital heart disease patients with respiratory ciliary dysfunction. J Thorac Cardiovasc Surg 2014;147:1291-1298.e2.
19. Leigh MW, Pittman JE, Carson JL, Ferkol TW, Dell SD, Davis SD, Knowles MR, Zariwala MA. Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 2009;11:473-487.
20. Garrod A, Zahid M, Francis R, Khalifa O, Devine W, Leatherbury L, Lo C. Airway ciliary dysfunction and increased sinopulmonary symptoms in congenital heart disease patients with and without heterotaxy [abstract]. Am J Respir Crit Care Med 2013;187:A2087.
21. Leigh MW, Zariwala MA, Knowles MR. Primary ciliary dyskinesia: Improving the diagnostic approach. Curr Opin Pediatr 2009;21: 320-325.
22. 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;169:459-467.
23. Papon JF, Bassinet L, Cariou-Patron G, Zerah-Lancner F, Vojtek AM, Blanchon S, Crestani B, Amselem S, Coste A, Housset B, et al. Quantitative analysis of ciliary beating in primary ciliary dyskinesia: A pilot study. Orphanet J Rare Dis 2012;7:78.
24. Thomas B, Rutman A, O'Callaghan C. Disrupted ciliated epithelium shows slower ciliary beat frequency and increased dyskinesia. Eur Respir J 2009;34:401-404.
25. Kharitonov SA, Rajakulasingam K, O'Connor B, Durham SR, Barnes PJ. Nasal nitric oxide is increased in patients with asthma and allergic rhinitis and may be modulated by nasal glucocorticoids. J Allergy Clin Immunol 1997;99:58-64.
26. Schwabe GC, Hoffmann K, Loges NT, Birker D, Rossier C, de Santi MM, Olbrich H, Fliegauf M, Failly M, Liebers U, et al. Primary ciliary dyskinesia associated with normal axoneme ultrastructure is caused by DNAH11 mutations. Hum Mutat 2008;29:289-298.
27. Csoma Z, Bush A, Wilson NM, Donnelly L, Balint B, Barnes PJ, Kharitonov SA. Nitric oxide metabolites are not reduced in exhaled breath condensate of patients with primary ciliary dyskinesia. Chest 2003;124:633-638.
28. Walker WT, Liew A, Harris A, Cole J, Lucas JS. Upper and lower airway nitric oxide levels in primary ciliary dyskinesia, cystic fibrosis and asthma. Respir Med 2013;107:380-386.
29. Karadag B, James AJ, Gü ltekin E, Wilson NM, Bush A. Nasal and lower airway level of nitric oxide in children with primary ciliary dyskinesia. Eur Respir J 1999;13:1402-1405.
30. Marthin JK, Nielsen KG. Choice of nasal nitric oxide technique as firstline test for primary ciliary dyskinesia. Eur Respir J 2011;37:559-565.
31. Narang I, Ersu R, Wilson NM, Bush A. Nitric oxide in chronic airway inflammation in children: diagnostic use and pathophysiological significance. Thorax 2002;57:586-589.
32. Hirst RA, Jackson CL, Coles JL, Williams G, Rutman A, Goggin PM, Adam EC, Page A, Evans HJ, Lackie PM, et al. Culture of primary ciliary dyskinesia epithelial cells at air-liquid interface can alter ciliary phenotype but remains a robust and informative diagnostic aid. PLoS One 2014;9:e89675.
33. Hirst RA, Rutman A, Williams G, O'Callaghan C. Ciliated air-liquid cultures as an aid to diagnostic testing of primary ciliary dyskinesia. Chest 2010;138:1441-1447.
34. Jorissen M, Willems T, Van der Schueren B. Ciliary function analysis for the diagnosis of primary ciliary dyskinesia: Advantages of ciliogenesis in culture. Acta Otolaryngol 2000;120:291-295.
35. Jorissen M, Willems T, Van der Schueren B, Verbeken E. Secondary ciliary dyskinesia is absent after ciliogenesis in culture. Acta Otorhinolaryngol Belg 2000;54:333-342.
36. Boon M, Smits A, Cuppens H, Jaspers M, Proesmans M, Dupont LJ, Vermeulen FL, Van Daele S, Malfroot A, Godding V, et al. Primary ciliary dyskinesia: critical evaluation of clinical symptoms and diagnosis in patients with normal and abnormal ultra structure. Orphanet J Rare Dis 2014;9:11.
37. Papon JF, Coste A, Roudot-Thoraval F, Boucherat M, Roger G, Tamalet A, Vojtek AM, Amselem S, Escudier E. A 20-year experience of electron microscopy in the diagnosis of primary ciliary dyskinesia. Eur Respir J 2010;35:1057-1063.