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1 Legal Medicine 15 (2013) Contents lists available at SciVerse ScienceDirect Legal Medicine journal homepage: Case Report Respiratory complications of Ehlers Danlos syndrome type IV Katsuhiko Hatake a,, Yoshifumi Morimura a, Risa Kudo a, Wataru Kawashima a, Shogo Kasuda a, Hiroki Kuniyasu b a Department of Legal Medicine, Nara Medical University, Kashihara , Japan b Department of Molecular Pathology, Nara Medical University, Kashihara , Japan article info abstract Article history: Received 11 August 2011 Received in revised form 4 July 2012 Accepted 25 July 2012 Available online 30 August 2012 Keywords: Sudden death Ehlers Danlos syndrome Fibrous pseudotumors Hemoptysis We describe a case of Ehlers Danlos syndrome (EDS) type IV in a male in early half in his twenties, who experienced recurrent and eventually fatal pulmonary hemorrhage. EDS type IV is a rare disorder of type III collagen synthesis that is characterized by unusual facies, thin translucent skin with a venous vascular pattern, easy bruising, and hypermobility of the small joints. Autopsy findings showed hypermobility of the joints and distensibility of the skin. Microscopically, the abdominal skin showed substantially decreased dermal thickness. Moreover, the reticular dermis showed fine collagen bundles and large interstitial spaces compared with the skin from a normal control that showed large collagen bundles. Individual elastic fibers were also thicker than those observed in the skin of a normal control. The thoracic aorta showed thin adventitia and a relative increase in elastic fibers. The parenchyma of both the lungs showed markedly diffuse hemorrhage with hemosiderin-laden alveolar macrophages or old thrombi and organized thrombi in the small bronchi. Furthermore, both sections of the lung showed multiple fibrous nodules containing benign metaplastic bone. Vascular wall disruption and tearing of the vessel walls in the lung parenchyma were also observed. We concluded that EDS type IV led to the patient s death because of pulmonary hemorrhage. Because this syndrome resulted in the patient s death from arterial and bowel rupture, it is important to consider EDS as a potential cause of sudden death. Ó 2012 Elsevier Ireland Ltd. All rights reserved. 1. Introduction Ehlers Danlos syndrome (EDS) is a group of inherited disorders involving abnormal production or secretion of collagen. EDS has three major clinical manifestations: hyperextensibility of the skin, hypermobility of the joints, and a bleeding tendency. EDS is classified into six types: classical, hypermobile, vascular, kyphoscoliosis, arthrochalasia, and dermatosparaxis [1]. EDS was originally reported to have an incidence rate of 1 in 150,000 individuals [2]. However, with the discovery of additional subtypes or variants of EDS, the frequency has now been reported to be 1 in ,000 [3]. Type IV is one of the rarest and clinically most serious EDS variants, because it is the only form of the disease with lethal complications. EDS type IV is characterized by thin transparent skin, easy bruising, and rupture of large arteries as well as bowel rupture, followed by death, which usually occurs in patients second decade of life [4 8]. Because patients with EDS mimic signs of abusive injuries and/ or present with sudden infant death, forensic pathologists must be aware of this rare, autosomal-dominant connective tissue disorder. Corresponding author. Tel.: ; fax: address: khatake@naramed-u.ac.jp (K. Hatake). Here, we describe the case of a male in early half in his twenties with EDS, who died suddenly while expectorating blood. We concluded that the decedent had EDS type IV. 2. Case report 2.1. Case history A male in early half in his twenties experienced a severe cough and sneezing with repeated hemoptysis in the morning in his own room. His younger brother, who was in a nearby room, took notice of the strange circumstances and found his older brother in an unconscious state. The patient was brought to the emergency department by paramedics who responded to an emergency call for unresponsiveness. The patient arrived in a state of cardiopulmonary arrest, and despite medical treatment, he could not be resuscitated. The patient had been in good health until he was years of age, after which he began experiencing episodes of repeated intermittent hemoptysis. After consulting the hospital of the Medical University, his condition was diagnosed as EDS after checking the clinical characteristics such as joint hypermobility and characteristic facial appearance. However, his genetic profile and the type of EDS were not determined. The patient had /$ - see front matter Ó 2012 Elsevier Ireland Ltd. All rights reserved.
2 24 K. Hatake et al. / Legal Medicine 15 (2013) Microscopically, the abdominal skin showed a substantial decrease in dermal thickness. In addition, a reticular dermis with fine and irregular collagen bundles as well as large interstitial spaces was seen, which was in contrast to skin of a normal control, which contained large collagen bundles (Fig. 2a d). Individual elastic fibers were thicker than those in the control skin (Fig. 2e and f). The thoracic aorta between the aortic arch and descending aorta showed thin adventitia and a relative increase in elastic fibers (Fig. 3a and b). The parenchyma of both the lungs showed diffuse alveolar hemorrhage with hemosiderin-laden alveolar macrophages or old thrombi and organized thrombi in the small bronchi (Fig. 4a c). Furthermore, sections of both lungs showed multiple fibrous nodules containing benign metaplastic bone (Fig. 4d). Vascular wall disruption was observed in the area of lung hemorrhage (Fig. 4e). The thickness of the vascular wall was not uniform, and Azan staining revealed a tear in the vessel wall that was stained blue (Fig. 4f). The central nervous system did not reveal any significant findings except calcification in the thalamus. The liver showed mild fatty degeneration. The heart, pancreas, and kidneys did not reveal any significant findings, except a mild to moderate congestion. 3. Discussion Fig. 1. Joint hypermobility in our patient with Ehlers Danlos syndrome. experienced pneumothorax of the left lung 2 years before his death, and he was being followed up every 3 months. The decedent s younger brother had also been diagnosed with EDS at the same hospital; however, the type of EDS had not been determined. He underwent surgery for a dissecting aneurysm of the thoracic aorta at 17 years of age. The decedent s father had died suddenly of unknown causes. Moreover, the decedent s paternal grandmother had translucent skin through which the venous vasculature was visible Autopsy findings Autopsy was performed 6 h after death. Postmortem examination revealed an externally normal man, with a height of 170 cm and weight of 76 kg. Examination of the skin revealed moderate distensibility. All joints were hyperextensible, but the abnormality was most marked at the metacarpal phalangeal and interphalangeal joints (Fig. 1). No deformation of the nails was observed. Cardiac blood was fluidity and no arterial aneurysms were found. The weights of the left and right lungs was 360 g and 334 g, respectively. Many coin-sized, dark reddish parts were found on the surface of both the lungs, with the color occupying approximately 50% of the entire surface area. Parenchymal hemorrhage was seen on the cut surface of the foci. The dark reddish parts on the surface of both the lungs were not wedge-shaped pleural-based hemorrhagic foci. Thus, pulmonary infarcts were not observed. Pulmonary thromboembolism was also not observed. Hemorrhage was absent in the trachea or large bronchi. The liver, spleen, and lungs were markedly friable, allowing them to be easily toned during autopsy. Other organs did not show any significant findings, except a mild to moderate congestion Histopathological findings The sudden death of the decedent as well as his family and clinical history, including repeated hemoptysis, skin laxity, and joint hypermobility, strongly suggested that he had EDS type IV. Furthermore, autopsy findings were consistent with those of patients with EDS type IV as described below. EDS type IV is inherited in an autosomal-dominant fashion. The disorder is caused by a mutation of the Col 3A1 gene, which results in abnormal type III collagen synthesis [9 11]. Thus, because of abnormal collagen synthesis, hyperextensibility of the skin, joint hypermobility, and increased tissue fragility are observed in patients with EDS type IV, as in our case. Histological examination of the present decedent revealed abdominal skin with an irregular and fine collagen pattern. In addition, the thoracic aorta showed thin adventitia and a relative increase in elastic fibers. These findings were considered to be because of an increase in abnormal collagen fibers as described previously [12 14]. Although uncommon, respiratory manifestations of EDS have also been described [15 17] and include recurrent hemoptysis, bulla formation, spontaneous pneumothorax, and repeated episodes of pneumonia. In this case, the patient had recurrent hemoptysis and pneumothorax. Furthermore, histological examination of the parenchyma of both lungs revealed fibrous nodules with osseous metaplasia, diffuse alveolar hemorrhage, old thrombi, and organized thrombi in the bronchi. Corrin et al. described a postmortem case of fibrous tumors with occasional inclusions of cartilage or bone that are termed fibrous pseudotumors [18]. The nodules containing metaplastic bone, as seen in the present case, were also considered fibrous pseudotumors. Fibrous pseudotumors represent an inefficient repair mechanism that occurs after rupture or injury to the pulmonary vasculature or interstitium. Repair with type I collagen (the principal collagen in bone) may be favored in patients with EDS type IV and therefore, may account for the osseous metaplasia found within these pseudotumors [15]. In our patient, vascular wall disruption was observed, the thickness of the vascular wall was not uniform, and Azan staining revealed a tear in the vessel wall that may have resulted from the attempts to repair the injured vessels. Day et al. [19] suggested that in patients with EDS type IV, the tendency to bleed results from abnormalities in the connective tissue around the capillaries and vascular wall itself. Thus, in the present case, we conclude that massive hemorrhage caused by the fragility of the vessels occurred in the parenchyma of the lungs, leading to acute respiratory insufficiency. The main causes of death among patients with EDS/EDS type IV, as reported in the autopsy reports are summarized in Table 1. Table 1 includes the cases reported in forensic literature [20 22]; it also includes cases, although rare such as the present case, showing respiratory manifestation [15] or findings of the lungs found during autopsy [16,23]. In these cases, connective tissue disorder was determined as the underlying cause of death. In particular, in the case of a quite healthy 5-month-old female infant, the initial clinical impression was of sudden infant death syndrome because of a lack of external findings [23]. This report shows that fatal complications of EDS type IV can occur even at a very young age, and are an extremely rare cause of sudden death during infancy. Fur-
3 K. Hatake et al. / Legal Medicine 15 (2013) Fig. 2. Sections of full-thickness skin from our patient with Ehlers Danlos syndrome (EDS) (a) and partial-thickness skin from a normal subject (b). Sections of skin showing fine collagen bundles (c) and thick elastic fibers (e) in our patient with EDS compared with a normal subject (d and f). ((a) and (b), hematoxylin eosin stain 40; (c) and (d), Azan stain 200; (e) and (f), Elastica van Gieson stain 200). Fig. 3. A section of the thoracic aorta showing a decrease in adventitia (arrow) and an excess of elastic fibers in our patient with Ehlers Danlos syndrome (a) compared with a normal subject (b). ((a) and (b), Elastica van Gieson stain 60).
4 26 K. Hatake et al. / Legal Medicine 15 (2013) Fig. 4. Diffuse alveolar hemorrhage with hemosiderin-laden alveolar macrophage (a and b), an old hemorrhage in the bronchus (c), a fibrous pseudotumor with osseous metaplasia (arrow) (d), vascular wall disruption in an area of lung hemorrhage (e), heterogeneity in the thickness of the vascular wall, and the vascular wall with a tear (arrow) (f) in our patient with EDS. ((a), hematoxylin eosin stain 40; (b), hematoxylin eosin stain 200; (c and d), hematoxylin eosin stain 100; (e), hematoxylin hematoxylin eosin stain 200; (f), Azan stain 400). Table 1 Summary of the causes of death in the autopsy reports of patients with EDS/EDS type IV. Age Sex Cause of death Respiratory complications/ autopsy findings References 45 Female Thoracic aortic dissection Charlier et al. [20] Myocardial tamponade 39 Male Spontaneous splenic and renal artery laceration Prahlow et al. [21] Massive blood loss 28 Male Abdominal aortic dissection and rupture Prahlow et al. [21] Massive hemoperitoneum and retroperitoneal hemorrhage 22 Female Rupture of left iliac artery Prahlow et al. [21] Massive intraperitoneal hemorrhage with associated retroperitoneal hemorrhage 30 Male Myocardial infarction Gilchrist et al. [22] Myocardial tamponade 27 Male Disruption of pulmonary capillary Recurrent hemoptysis Yost et al. [16] Diffuse alveolar hemorrhage 18 Male Thoracic aortic dissection A cyst occupying much of the Murray et al. [15] lower lobe of the right lung Massive mediastinal hemorrhage with cardiac tamponade 0 Female Spontaneous subarachnoid hemorrhage Focal periarterial hemorrhages within lung parenchyma Byard et al. [23] thermore, a patient with EDS type IV may bruise easily because of the associated skin fragility and may show voluminous hematomas despite normal findings in coagulation studies. These symptoms may easily be confused with signs of child abuse [24]. Fortunately, our patient s condition was diagnosed as EDS at the medical university during his lifetime based on his clinical characteristics, although the type of EDS was not determined at that time. In the case reported by Charlier et al. [20], a diagnosis of EDS based on autopsy findings was confirmed by genetic testing of a blood sample obtained during autopsy. Therefore, the authors emphasize that if there is a suspicion of EDS during autopsy, genetic examination is useful for the diagnosis. In summary, it is important to consider the possibility of EDS, including type IV, in any case involving bruises, thin skin, small
5 K. Hatake et al. / Legal Medicine 15 (2013) joint laxity, tissue fragility or friability, and/or arterial, uterine, or gastrointestinal rupture. References [1] Beighton P, De Paepe A, Steinmann B, Tsipouras P, Wenstrup RJ. Ehlers Danlos syndromes: revised nosology, Villefranche, Am J Med Genet 1998;77:31 7. [2] Peaceman AM, Cruikshank DP. Ehlers Danlos syndrome and pregnancy: association of type IV disease with maternal death. Obstet Gynecol 1987;69: [3] Abel MD, Carrasco LR. Ehlers Danlos syndrome: classifications, oral manifestations, and dental considerations. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102: [4] Bowen J, Boudoulas H, Wooley CF. Cardiovascular disease of connective tissue origin. Am J Med 1987;82: [5] Cikrit DF, Miles JH, Silver D. Spontaneous arterial perforation. The Ehlers Danlos spector. J Vasc Surg 1987;5: [6] Lach B, Nair SG, Russell NA, Benoit BG. Spontaneous carotid cavernous fistula and multiple arterial dissections in type IV Ehlers Danlos syndrome. J Neurosurg 1987;66: [7] Shohet I, Rosenbaum I, Frand M, Duksin D, Engelberg S, Goodman RM. Cardiovascular complications in the Ehlers Danlos syndrome with minimal external findings. Clin Genet 1987;31: [8] Pepin M, Schwarze U, Superti-Furga A, Byers PH. Clinical and genetic features of Ehlers Danlos sybdrome type IV, the vascular type. N Eng J Med 2000;342: [9] Lloyd J, Narcisi P, Richards A, Pope FM. A T+6 to C+6 mutation in the donor splice site of Col 3A1 IVS7 causes exon skipping and results in Ehlers Danlos syndrome type IV. J Med Genet 1993;30: [10] Milewicz DM, Witz AM, Smith ACM, Manchester DK, Waldstein G, Byers PH. Parental somatic and germ-line mosaicism for a multiexon deletion with unusual endpoints in a type III collagen (Col 3A1) allele produces Ehlers Danlos syndrome type IV in the heterozygous offspring. Am J Hum Genet 1993;53: [11] Superti-Furga A, Steinmann B, Ramirez F, Byers PH. Molecular defects of type III procollagen in Ehlers Danlos syndrome type IV. Hum Genet 1989;82: [12] Lees MH, Menashe VD, Sunderland CO, Morgan CL, Dawson PJ. Ehlers Danlos syndrome associated with multiple pulmonary artery stenosis and tortuous systemic arteries. J Pediatr 1969;75: [13] Smit J, Alberts C, Balk AG. Pneumothorax in the Ehlers Danlos syndrome. Consequence or coincidence. Scand J Respir Dis 1978;59: [14] Rudd NL, Nimrod C, Holbrook KA, Byers PH. Pregnancy complications in type IV Ehlers Danlos syndrome. Lancet 1983;1:50 3. [15] Murray RA, Poulton TB, Saltarelli MG, Dweik RA, Litwin DK, Kirby TJ, et al. Rare pulmonary manifestation of Ehlers Danlos syndrome. J Thorac Imaging 1995;10: [16] Yost BA, Vogelsang JP, Lie JT. Fatal hemoptysis in Ehlers Danlos Syndrome. Old Malady with a new course. Chest 1995;107: [17] Ayres JG, Pope FM, Reidy JF, Clark TJH. Abnormalities of the lungs and thoracic cage in the Ehlers Danlos syndrome. Thorax 1985;40: [18] Corrin B, Simpson CGB, Fisher C. Fibrous pseudotumors and cyst formation in the lungs in Ehlers Danlos syndrome. Histopathology 1990;17: [19] Day HJ, Zarafonetis CJ. Coagulation studies in four patients with Ehlers Danlos syndrome. Am J Med Sci 1961;242: [20] Charlier C, Germain DP, Jeunemaitre X, Delisle ST, Alvarez J-C, De la Grandmaison GL. Sudden death associated to vascular Ehlers Danlos syndrome. A case report. Leg Med 2011;13: [21] Prahlow JA, Wagner SA. Death due to Ehlers Danlos syndrome type IV. Am J Forensic Med Pathol 2005;26: [22] Gilchrist ER, Duflou JA. Incidental myocardial infarction in Ehlers Danlos syndrome type IV? J Forensic Sci 2005;50: [23] Byard RW, Keely FW, Smith CR. Type IV Ehlers Danlos syndrome presenting as sudden infant death. Am J Clin Pathol 1990;93: [24] Owen SM, Durst RD. Ehlers Danlos syndrome simulating child abuse. Arch Dermatol 1984;120:
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