Bjørg J. Abrahamsen, MD ; Mari Ann Kulseth, PhD ; and Benedicte Paus, MD, PhD

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1 [ Selected Reports ] A 19-Year-Old Man With Relapsing Bilateral Pneumothorax, Hemoptysis, and Intrapulmonary Cavitary Lesions Diagnosed With Vascular Ehlers-Danlos Syndrome and a Novel Missense Mutation in COL3A1 Bjørg J. Abrahamsen, MD ; Mari Ann Kulseth, PhD ; and Benedicte Paus, MD, PhD A 19-year-old sportsman experienced a right-sided pneumothorax and hemoptysis after having had an intermittent cough and blood-tinged sputum for 2 months. A chest CT scan revealed small cavitary lesions in both lungs. The relapsing pneumothorax was treated with a chest tube twice, as well as surgically after the second relapse. Two months after surgery, the patient developed a cough, fever, and high C-reactive protein levels. At that time, large consolidations had developed in the right lung, while the left lung subsequently collapsed due to pneumothorax. The patient s physical appearance and anamnestic information led us to suspect a genetic connective tissue disease. A sequencing analysis of the COL3A1 gene identified a novel, de novo missense mutation that confirmed the diagnosis of vascular Ehlers-Danlos syndrome (EDS). This atypical presentation of vascular EDS with intrathoracic complications shows that enhanced awareness is required and demonstrates the usefulness of the genetic analyses that are clinically available for several hereditary connective tissue disorders. CHEST 2015; 147 ( 5 ): e166 - e170 ABBREVIATIONS : EDS 5 Ehlers-Danlos syndrome Spontaneous pneumothorax is a well-known complication for several different pulmonary conditions; most common in young adults are rupture of subpleural blebs, cystic fibrosis, malignancy, or necrotizing pneumonia. Hemoptysis in adults may have its origin in airway diseases, such as bronchial infections or neoplasms. Pulmonary parenchymal involvement such as pneumonia and inflammatory and immune disorders may also cause hemoptysis, but it is important to consider connective tissue diseases, specifically the vascular type of Ehlers-Danlos syndrome (EDS). 1-3 Vascular EDS is a rare, autosomal dominantly inherited collagen disorder affecting the connective tissue in several organ systems. 4,5 Vascular EDS carries a serious Manuscript received December 19, 2013 ; revision accepted October 31, AFFILIATIONS: From the Department of Pulmonary Medicine (Dr Abrahamsen), Department of Medical Genetics (Drs Kulseth and Paus), and Institute of Clinical Medicine (Dr Paus), Oslo University Hospital, Oslo, Norway. CORRESPONDENCE TO: Bjørg J. Abrahamsen, MD, Department of Pulmonary Medicine, Oslo University Hospital, Ullevål Hospital, Postboks 4956 Nydalen, NO-0424 Oslo, Norway; bjjoab@ous-hf.no 2015 AMERICAN COLLEGE OF CHEST PHYSICIANS. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details. DOI: /chest e166 Selected Reports [ 147#5 CHEST MAY 2015 ]

2 prognosis because of the tendency of vital organs and blood vessels to rupture. In 90% of cases, vascular EDS presents with an extrathoracic arterial dissection or rupture. 6 Pneumothorax is the most common respiratory complication of the disorder, and the incidence of spontaneous pneumothorax in vascular EDS is reported to be 16%. 7 Here, we describe the primary findings and clinical course in a young man with vascular EDS who was diagnosed after an unusual presentation with bilateral pneumothorax and pulmonary findings. Case Report A 19-year-old sportsman experienced an acute, massive hemoptysis, shortness of breath, and dizziness after approximately 2 months of an intermittent cough with blood-tinged sputum. In the local hospital, he was diagnosed with a right-sided pneumothorax and treated with a chest tube. After 1 month, the pneumothorax relapsed, and he was readmitted to hospital and again treated conventionally with an intercostal drain. In the following month, the right-sided pneumothorax relapsed once more and chest CT scans were performed that revealed bilateral, small cavitary lesions ( Fig 1 ) of an unknown genesis. Because of the repeated relapses of pneumothorax, the patient was referred for surgery. A resection of subpleural bullae and pleural rubbing were performed by an experienced surgeon, but due to a prolonged leakage of air on the pleural drain, the operation was carried out a second time. During the second operation, an open-lung biopsy specimen was obtained, and the surgeon observed a fragility of the lung, extensive bleeding, and an unusual texture of the pulmonary tissue. Therefore, a pleural decortication was not performed. No relapse of the right-sided pneumothorax was observed, and the patient was discharged from hospital. A histopathologic investigation of the lung biopsy specimen gave no explanation for the radiologic findings ( Fig 2 ), and because of the suspicion of an underlying Figure 2 Lung biopsy specimen was unspecific with pleural fibrosis, signs of old and new bleeding, and subpleural bullae (hematoxylin and eosin, magnification 3 4 objective lens). disease, fiber-optic bronchoscopy was performed after surgery. This revealed a diffuse and scarce bleeding. Serology tests for antinuclear antibody, antineutrophil cytoplasmic antibody, and rheumatic factor were negative. Two months after surgery, the patient developed fever, high C-reactive protein levels, anemia, a persistent productive cough, and hemoptysis. Furthermore, he experienced a left-sided pneumothorax that was not treatable with pleural tubes alone ( Fig 3 ), and was then referred to the university hospital. Upon arrival at the Department of Pulmonary Medicine, the patient was in a generally poor condition, and a chest CT scan demonstrated large, abscess-like structures in the right lung ( Figs 4, 5 ). Figure 1 CT scan of lungs before pneumothorax surgery, showing right-sided pneumothorax and small cavitary lesions (arrows). Figure 3 Chest radiography 4 mo after surgery, showing a total pneumothorax on the left side and abscess-like structures in the right lung. journal.publications.chestnet.org e167

3 Figure 4 CT scan 4 mo after surgery, showing a chest tube on the left side and a consolidation in the right upper lobe of the lung. The erythrocyte sedimentation rate was 36 mm/h (normal range, 1-12 mm/h); C-reactive protein level, 80.5 mg/l (normal range, mg/l); hemoglobin level, 9.3 g/100 ml (normal range, g/100 ml); WBC count, /L (normal range, /L), D-dimer level. 4.0 mg/l (normal range, mg/l); and platelet count, /L (normal range, /L). The patient s body temperature was 38.6 C, and oxygen saturation was 98%. Echocardiography revealed no signs of endocarditis or other valvular pathology, but the culture of a bronchial lavage demonstrated Staphylococcus aureus and Actinomyces species. Because of a suspected immuno, a broad investigation including HIV was performed, and all tests were negative. After antibiotic treatment, the productive cough and hemoptysis improved significantly, and the abnormal blood parameters became normalized. Eventually, the left-sided pneumothorax was successfully treated with chemical pleurodesis. The patient was tall and slender with slight scoliosis, an asymmetric thorax, and long fingers, with hypermobility of the small joints in his thumbs. He had pale, translucent skin and protruding eyes. Three years earlier, he had been diagnosed with keratoconus. While in the hospital, his physical appearance, bilateral pneumothorax, and intrapulmonary bleeding prompted genetic testing for vascular EDS. The testing was carried out with Sanger sequencing of the entire coding region and exon-intron boundaries of COL3A1. Heterozygosity was found for a novel variant, c.2896g.t (NM_ ), implying a missense mutation that changes a glycine to cysteine at amino acid position 966 (p.gly966cys) in the polypeptide, collagen type III alpha 1. Testing of parental samples revealed that the mutation was de novo. After 10 weeks, the patient was discharged from the Department of Pulmonary Medicine and referred for an MRI angiography of the thoracic, abdominal, and intracerebral arteries, which showed normal calibers of all arteries. Three months after discharge, a follow-up of the pulmonary complications with a chest radiograph showed no relapse of pneumothorax nor hematomas (Fig 6 ). The patient was referred for genetic counseling Figure 5 CT scan of lungs 4 mo after surgery, showing an abscesslike structure in the lower right lung and a chest tube on the left side. Figure 6 Chest radiography at 3-mo follow-up after discharge from hospital, showing no relapse of pneumothorax and clearing of the right lung. e168 Selected Reports [ 147#5 CHEST MAY 2015 ]

4 and to a referral center for rare connective tissue disorders. Discussion Pneumothorax, Marfanoid habitus, joint hypermobility, and keratoconus are all manifestations of several different hereditary connective tissue disorders. Tissue fragility is seen in vascular EDS and Loeys-Dietz syndrome. The facial features and transparent skin with visible veins indicated that vascular EDS was the most plausible diagnosis in this patient. While classic EDS ( Table 1 ) is characterized by generalized joint hypermobility, the hypermobility in the vascular type is usually limited to the small joints. The clinical diagnosis of vascular EDS usually relies on two or more of the following criteria: characteristic facial features with a pinched nose, narrow lips and prominent eyes; easy bruising and thin skin with visible veins; or tissue fragility with easy rupture of arteries and internal organs 5,7 (Table 1 ). The rare presentation of vascular EDS with pneumothorax, intrapulmonary hematomas, or hemothorax seems to occur more often in young adults. 1,3,8-15 The biochemical abnormality leading to vascular EDS is in type III collagen, which is a key element in the structure of arterial walls, viscous organs, and lung parenchyma. 3 Sequencing analysis of COL3A1 detects 97% of vascular EDS cases and is clinically available in many centers. 16 Numerous different mutations in COL3A1 have been shown to result in disease. The most common pathogenic mutations cause substitution of glycine in the type III collagen polypeptide, as is the case in this patient. Mutations causing a substitution of glycine in the long, triple, helical protein domain formed by glycine-x-y repeats disrupt the structural integrity of the collagen molecule. 17 The identified mutation (p.g966c) has not previously been reported, but glycine at position 966 is located in the triple-helix domain, and changes are likely to cause structural alterations. Another variant in the same codon, causing a substitution of glycine with a valine, has been described in a patient with arterial and GI complications. 5 No established correlation exists between specific mutations and particular manifestations nor between specific mutations and prognosis. The vascular cavities in this patient s preoperative CT scans ( Fig 1 ) were probably manifestations of focal lung rupture and the basis of the recurrent pneumothoraces. 15 The postoperative hematomas in the right-side lung probably created favorable conditions for bacterial growth, thus mimicking intrapulmonary abscesses. The hematomas disappeared after appropriate antibiotics. TABLE 1 ] Clinical Features and Causes of EDS OMIM No. EDS Type Mutated Gene Biochemical Defect Typical Clinical Manifestations Inheritance , Classic COL5A1, COL5A2 Deficient/defect collagen V and collagen I dysregulation Hypermobility TNXB a Tenascin-X Vascular COL3A1 Collagen III /defect Kyphoscoliotic PLOD1 Collagen lysyl hydroxylase Arthrochalasia COL1A1, COL1A2 Procollagen I peptidase inhibitor Dermatosparaxis AMTS2 Procollagen I peptidase Generalized joint hypermobility, skin hyperextensibility, abnormal scars Generalized joint and spine hypermobility with dislocations and chronic pain Facial features; thin, transparent skin; easy bruising; tissue fragility/rupture Kyphoscoliosis, hypotonia, and joint hypermobility in newborns Generalized joint hypermobility, bilateral congenital hip dislocation, contractures Severe skin fragility, redundant skin, joint hypermobility, blue sclera AR AR 5 autosomal dominant; AR 5 autosomal recessive; EDS 5 Ehlers-Danlos syndrome; OMIM 5 Online Mendelian Inheritance in Man Classification. a In a limited number of patients. journal.publications.chestnet.org e169

5 Elective surgery is not recommended in patients with vascular EDS, because of the risk of fragile tissue and bleeding complications. Most patients with vascular EDS develop serious complications before the age of 50 years. Pulmonary complications have not proved to result directly in patient mortality, 18 though arterial or organ rupture may be fatal. The risk of developing aneurysms, dissection, and spontaneous rupture of arteries later in life is significant. If surgery is required, it should be performed in an institution experienced in treating this rare patient group. Intervention in patients with vascular EDS requires careful and individual assessment of risks vs benefits. 19 Because conventional angiography leads to a high risk of arterial rupture, this patient will be followed up with an MRI angiography every second year. He has been informed that he may experience hemoptysis and pneumothorax later in life and, therefore, is advised to limit physical activity. He has also been made aware of the risk of bleeding from organs other than lungs. In 50% of cases, the disease-causing mutation in COL3A1 is not inherited from a parent, as in this patient, and the diagnosis is frequently unknown to the patient and their family. It is important for patients to be aware of the risks associated with the disorder, since such information may have a profound impact on the life, including family planning, of young adults. The identification of a disease-causing mutation is a prerequisite for predictive genetic testing of the relatives, and referral for genetic counseling is strongly recommended. Acknowledgments Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article. References 1. Sareli AE, Janssen WJ, Sterman D, Saint S, Pyeritz RE. Clinical problem-solving. What s the connection? A 26-year-old white man presented to our referral hospital with a 1-month history of persistent cough productive of white sputum, which was occasionally tinged with blood. N Engl J Med ;358(6): Murphy-Ryan M, Psychogios A, Lindor NM. Hereditary disorders of connective tissue: a guide to the emerging differential diagnosis. Genet Med ;12(6): Hatake K, Morimura Y, Kudo R, Kawashima W, Kasuda S, Kuniyasu H. Respiratory complications of Ehlers-Danlos syndrome type IV. Leg Med (Tokyo) ;15 (1 ): Beighton P, De Paepe A, Steinmann B, Tsipouras P, Wenstrup RJ ; Ehlers-Danlos National Foundation (USA) and Ehlers-Danlos Support Group (UK). Ehlers-Danlos syndromes: revised nosology, Villefranche, Am J Med Genet ;77(1): D e Pa ep e A, Ma lfait F. The Ehlers-Danlos syndrome, a disorder with many faces. Clin Genet ;82(1): Pepin M, Schwarze U, Superti-Furga A, Byers PH. Clinical and genetic features of Ehlers-Danlos syndrome type IV, the vascular type. N Engl J Med ;342(10): Oderich GS, Panneton JM, Bower TC, et al. The spectrum, management and clinical outcome of Ehlers-Danlos syndrome type IV: a 30-year experience. J Vasc Surg ;42(1): D a r R A, Wa n i S H, Mu s ht a q u e M, K a s a n a R A. S p o nt a n e o u s hemo-pneumothorax in a patient with Ehlers-Danlos syndrome. Gen Thorac Cardiovasc Surg ;60(9): Ishiguro T, Takayanagi N, Kawabata Y, et al. Ehlers-Danlos syndrome with recurrent spontaneous pneumothoraces and cavitary lesion on chest X-ray as the initial complications. Intern Med ;48(9): Matsushita A, Takayanagi N, Ishiguro T, et al. A case of Ehlers-Danlos syndrome suspected from pulmonary hematoma due to disruption of the lung [in Japanese]. Nihon Kokyuki Gakkai Zasshi ;47(8): Selim B, Lane CR, Rubinowitz AN, Siner JM. Spontaneous hemothorax and recurrent hemoptysis in a 26-year-old man with skin lesions. Chest ;137(2): Shields LB, Rolf CM, Davis GJ, Hunsaker JC III. Sudden and unexpected death in three cases of Ehlers-Danlos syndrome type IV. J Forensic Sci ;55 (6 ): Watanabe A, Kawabata Y, Okada O, et al. Ehlers-Danlos syndrome type IV with few extrathoracic findings: a newly recognized point mutation in the COL3A1 gene. Eur Respir J ;19 (1 ): Yost BA, Vogelsang JP, Lie JT. Fatal hemoptysis in Ehlers-Danlos syndrome. Old malady with a new curse. Chest ;107 (5 ): Herman TE, McAlister WH. Cavitary pulmonary lesions in type IV Ehlers-Danlos syndrome. Pediatr Radiol ;24 (4 ): GTR: Genetic Testing Registry. Bethesda, MD: National Center for Biotechnology Information, US National Library of Medicine. Accessed December 1, Mizuno K, Boudko S, Engel J, Bächinger HP. Vascular Ehlers-Danlos syndrome mutations in type III collagen differently stall the triple helical folding. J Biol Chem ;288(26): Dowton SB, Pincott S, Demmer L. Respiratory complications of Ehlers-Danlos syndrome type IV. Clin Genet ;50(6): Aujayeb A, Taylor A, Doe S, Worthy S. Blood in a chest drain. Breathe ;9 (6 ): e170 Selected Reports [ 147#5 CHEST MAY 2015 ]

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