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Original Research |

Heterogeneous pulmonary phenotypes associated with mutations in the thyroid transcription factor gene NKX2-1

Aaron Hamvas, MD*; Robin R. Deterding*; Susan E. Wert, PhD; Frances V. White; Megan K. Dishop; Danielle N. Alfano; Ann C. Halbower; Benjamin Planer; Mark J. Stephan; Derek A. Uchida; Lee D. Williames; Jill A. Rosenfeld, MS; Robert Roger Lebel; Lisa R. Young; F. Sessions Cole; Lawrence M. Nogee
Author and Funding Information

Edward Mallinckrodt Department of Pediatrics, Washington University, St. Louis, MO (Hamvas, Alfano, Cole); Department of Pediatrics, University of Colorado School of Medicine, Aurora, CO (Deterding, Halbower); The Perinatal Institute, Divisions of Neonatology, Perinatal and Pulmonary Biology, Cincinnati Children's Hospital Medical Center and the Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH (Wert); Lauren Ackerman Department of Pathology and Immunology, Washington University, St. Louis, MO (White); Department of Pathology and Laboratory Medicine, University of Colorado School of Medicine, Aurora, CO (Dishop); Department of Pediatrics, Hackensack University Medical Center, Hackensack, NJ (Planer); Department of Pediatrics, University of Washington, Seattle, WA (Stephan); Department of Pediatrics, University of Utah School of Medicine, Salt Lake City, UT (Uchida); Department of Pediatrics, Madigan Healthcare System, Tacoma, WA (Williames); Signature Genomic Laboratories, PerkinElmer, Inc., Spokane, WA (Rosenfeld); Section of Medical Genetics, Department of Pediatrics, SUNY Upstate Medical University, Syracuse, NY (Lebel); Department of Pediatrics, Vanderbilt University, Nashville, TN (Young); Department of Pediatrics, Johns Hopkins University, Baltimore, MD (Nogee)

Corresponding authors: Aaron Hamvas, MD, Division of Newborn Medicine, Washington University School of Medicine, Campus Box 8116, 660 S. Euclid Ave., St. Louis, MO 63110 e-mail: hamvas@kids.wustl.edu, Robin R. Deterding, MD, Department of Pediatrics, Pulmonary Section, University of Colorado School of Medicine, 13123 East 16th Ave., B-395, Aurora CO 80045 e-mail: robin.deterding@childrenscolorado.org

*These authors contributed equally to this work.
Funding: Supported by NIH HL065174,HL082747 (AH, FSC), and HL54703 (LMN)


Chest. 2013. doi:10.1378/chest.12-2502
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Abstract

Background:  Mutations in the gene encoding thyroid transcription factor (NKX2-1) result in neurologic abnormalities, hypothyroidism, and neonatal respiratory distress (RDS) known as the “Brain-Thyroid-Lung syndrome.” We identified individuals with mutations in NKX2-1 whose primary manifestation was respiratory disease in order to characterize the spectrum of associated pulmonary phenotypes.

Methods:  Retrospective and prospective approaches identified infants and children with unexplained diffuse lung disease for NKX2-1 sequencing. Histopathology, electron microscopy and immunohistochemical analysis for surfactant associated proteins were assessed in a subset of 10 children for whom lung tissue was available.

Results:  We identified 16 individuals with heterozygous missense, nonsense and frameshift mutations and 5 individuals with heterozygous whole gene deletions of NKX2-1. Neonatal RDS was the presenting pulmonary phenotype in 16 (76%), interstitial lung disease in 4 (19%), and pulmonary fibrosis in 1 adult family member. Altogether, 12 individuals (57%) had the full triad of neurologic, thyroid, and respiratory manifestations, but 5 (24%) had only pulmonary symptoms at the time of presentation. Recurrent respiratory infections were a prominent feature in 9 subjects. Lung histopathology demonstrated evidence of disrupted surfactant homeostasis in the majority of cases and at least 5 cases had evidence of disrupted lung growth.

Conclusions:  Patients with mutations in NKX2-1 may present with pulmonary manifestations in the newborn period or during childhood when thyroid or neurologic abnormalities are not apparent. Surfactant dysfunction and, in more severe cases, disrupted lung development, are likely mechanisms for the respiratory disease.


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