Fatal systemic (paradoxical) air embolism diagnosed by postmortem funduscopy
Lucy M. Bradley MD
Department of Pathology, Wake Forest Baptist Medical Center, Winston-Salem, NC, USA
Search for more papers by this authorAnna G. McDonald MD
Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, NC, USA
Search for more papers by this authorCorresponding Author
Patrick E. Lantz MD
Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, NC, USA
Correspondence
Patrick E. Lantz MD, Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, NC, USA.
Email: [email protected]
Search for more papers by this authorLucy M. Bradley MD
Department of Pathology, Wake Forest Baptist Medical Center, Winston-Salem, NC, USA
Search for more papers by this authorAnna G. McDonald MD
Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, NC, USA
Search for more papers by this authorCorresponding Author
Patrick E. Lantz MD
Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, NC, USA
Correspondence
Patrick E. Lantz MD, Department of Pathology, Wake Forest University School of Medicine, Winston-Salem, NC, USA.
Email: [email protected]
Search for more papers by this authorPresented at the 72nd Annual Scientific Meeting of the American Academy of Forensic Sciences, February 15–19, 2021, held virtually.
Abstract
Air embolism is often unrecognized and underreported. Published case reports or case series describe only rare fundal examinations of retinal air emboli (RAE)—a distinctive sign of systemic air embolism. We report an infant, found unresponsive at home, who died in the emergency department after unsuccessful resuscitative efforts. Before the autopsy, diagnostic RAE were recognized and imaged during postmortem funduscopy. Postmortem radiography and an autopsy confirmed systemic (paradoxical) air embolism due to inflicted abdominal and thoracic blunt force injuries. While a few descriptions and illustrations of RAE occur in case reports, we found no published photographic images of RAE in infants, children, or adults. This case report describes and photographically documents classic RAE associated with fatal systemic (paradoxical) air embolism. Complementing postmortem radiography and judicious autopsy techniques, the detection of RAE can aid pathologists in diagnosing systemic air embolism.
REFERENCES
- 1Liebermeister G. Das anämische zungenphänomen, ein wichtiges frühsymptom der arteriellen luftembolie [The anemic tongue phenomenon, an important early symptom of arterial air embolism]. Klin Wochenschr. 1929; 8(1): 21–3.
10.1007/BF01738313 Google Scholar
- 2Zaugg M, Kaplan V, Widmer U, Baumann PC, Russi EW. Fatal air embolism in an airplane passenger with a giant intrapulmonary bronchogenic cyst. Am J Respir Crit Care Med. 1998; 157(5 Pt 1): 1686–9. https://doi.org/10.1164/ajrccm.157.5.9706040.
- 3Barkan H. Air embolism of the retinal vessels. Trans Am Ophthalmol Soc. 1927; 25: 225–36.
- 4Wong RT. Air emboli in the retinal arteries: report of a case. Arch Ophthalmol. 1941; 25(1): 149–50. https://doi.org/10.1001/archopht.1941.00870070163017.
10.1001/archopht.1941.00870070163017 Google Scholar
- 5Ho AM, Ling E. Systemic air embolism after lung trauma [see comments]. Anesthesiology. 1999; 90(2): 564–75. https://doi.org/10.1097/00000542-199902000-00033. Comments. In: Anesthesiology. 1999;91(6):1962. doi: 10.1097/00000542-199912000-00058; Anesthesiology. 1999;91(6):1963. doi: 10.1097/00000542-199912000-00059.
- 6Neuman TS. Arterial gas embolism and decompression sickness. News Physiol Sci. 2002; 17: 77–81. https://doi.org/10.1152/nips.01370.2001.
- 7Reyer GW, Kohl HW. Air embolism complicating thoracic surgery: Report of ten cases. JAMA. 1926; 87(20): 1626–30. https://doi.org/10.1001/jama.1926.02680200026008.
10.1001/jama.1926.02680200026008 Google Scholar
- 8Cory RA. Death from air embolism following bronchoscopy: Case report. J Thorac Surg. 1944; 13(1): 30–1.
10.1016/S0096-5588(20)31922-X Google Scholar
- 9Hirsch C. Luftembolie in die arteria centralis retinae nach kieferhöhlenspülung. [Air embolism in the central retinal artery after irrigation of the maxillary sinus] Klin Monbl Augenheilkd. 1920; 65: 625–36.
- 10Peachey T, Eason J, Moxham J, Jarvis D, Driver M. Systemic air embolism during laser bronchoscopy. Anaesthesia. 1988; 43(10): 872–5. https://doi.org/10.1111/j.1365-2044.1988.tb05604.x.
- 11Sachsenweger R. Luftembolie und auge [Air embolism and eye]. Klin Monbl Augenheilkd Augenarztl Fortbild. 1957; 130(6): 813–23.
- 12Sachsenweger R. Zur differentialdiagnose der luftembolie des netzhautkreislaufes [Differential diagnosis of air embolism in retinal circulation]. Klin Monbl Augenheilkd Augenarztl Fortbild. 1958; 133(6): 788–97.
- 13Wever E. Cerebrale luftembolie [Cerebral air embolism]. Beitr Klin Tuberk Spezif Tuberkuloseforsch. 1914; 31(2): 159–230.
10.1007/BF01866062 Google Scholar
- 14Peirce EC. Cerebral gas embolism (arterial) with special reference to iatrogenic accidents. Hyperb Oxyg Rev. 1980; 1(3): 161–84.
- 15Schlaepfer K. Air embolism following various diagnostic or therapeutic procedures in diseases of the pleura and the lung. Bull Johns Hopkins Hosp. 1922; 33: 321–30.
- 16Rukstinat GJ, LeCount ER. Air in the coronary arteries. JAMA. 1928; 91(23): 1776–9. https://doi.org/10.1001/jama.1928.02700230016005.
10.1001/jama.1928.02700230016005 Google Scholar
- 17Capps JA. Air embolism versus pleural reflex as the cause of pleural shock. JAMA. 1937; 109(11): 852–4. https://doi.org/10.1001/jama.1937.02780370018008.
10.1001/jama.1937.02780370018008 Google Scholar
- 18Durant TM, Long J, Oppenheimer MJ. Pulmonary (venous) air embolism. Am Heart J. 1947; 33(3): 269–81. https://doi.org/10.1016/0002-8703(47)90656-x.
- 19Van Allen CM, Hrdina LS, Clark J. Air embolism from the pulmonary vein: a clinical and experimental study. Arch Surg. 1929; 19(4): 567–99. https://doi.org/10.1001/archsurg.1929.01150040003001.
10.1001/archsurg.1929.01150040003001 Google Scholar
- 20Schattenberg JH, Ziskind J. Air embolism as a complication of artificial pneumothorax. Am J Clin Pathol. 1939; 9(4): 477–82. https://doi.org/10.1093/ajcp/9.4.477.
10.1093/ajcp/9.4.477 Google Scholar
- 21Palmon SC, Moore LE, Lundberg J, Toung T. Venous air embolism: a review. J Clin Anesth. 1997; 9(3): 251–7. https://doi.org/10.1016/s0952-8180(97)00024-x.
- 22Chuang DY, Sundararajan S, Sundararajan VA, Feldman DI, Xiong W. Accidental air embolism. Stroke. 2019; 50(7): e183–e186. https://doi.org/10.1161/STROKEAHA.119.025340.
- 23Hagen PT, Scholz DG, Edwards WD. Incidence and size of patent foramen ovale during the first 10 decades of life: an autopsy study of 965 normal hearts. Mayo Clin Proc. 1984; 59(1): 17–20. https://doi.org/10.1016/s0025-6196(12)60336-x.
- 24Aberle DR, Gamsu G, Golden JA. Fatal systemic arterial air embolism following lung needle aspiration. Radiology. 1987; 165(2): 351–3. https://doi.org/10.1148/radiology.165.2.3659355.
- 25Ali Z, Bolster F, Goldberg E, Fowler D, Li L. Systemic air embolism complicating upper gastrointestinal endoscopy: a case report with post-mortem CT scan findings and review of literature. Forensic Sci Res. 2017; 1(1): 52–7. https://doi.org/10.1080/20961790.2016.1252898.
- 26Almas ET, Casserly B. Air embolism following bronchoscopy with fine-needle aspiration: an unexpected complication. Respir Med Case Rep. 2018; 25: 228–32. https://doi.org/10.1016/j.rmcr.2018.09.012.
- 27Bou-Assaly W, Pernicano P, Hoeffner E. Systemic air embolism after transthoracic lung biopsy: a case report and review of literature. World J Radiol. 2010; 2(5): 193–6. https://doi.org/10.4329/wjr.v2.i5.193.
- 28Deadman WJ. Fatal air embolism–Case reports. Can Med Assoc J. 1937; 37(2): 157–60.
- 29Jensen ME, Lipper MH. CT in iatrogenic cerebral air embolism. AJNR Am J Neuroradiol. 1986; 7(5): 823–7.
- 30Katzgraber F, Glenewinkel F, Fischler S, Rittner C. Mechanism of fatal air embolism after gastrointestinal endoscopy. Int J Legal Med. 1998; 111(3): 154–6. https://doi.org/10.1007/s004140050137.
- 31Levy I, Mosseri R, Garty B. Peripheral intravenous infusion–Another cause of air embolism. Acta Paediatr. 1996; 85(3): 385–6. https://doi.org/10.1111/j.1651-2227.1996.tb14042.x.
- 32Linden JV, Kaplan HS, Murphy MT. Fatal air embolism due to perioperative blood recovery. Anesth Analg. 1997; 84(2): 422–6. https://doi.org/10.1097/00000539-199702000-00034.
- 33Morris RE, Sapp MR, Oltmanns MH, Kuhn F. Presumed air by vitrectomy embolisation (PAVE) a potentially fatal syndrome. Br J Ophthalmol. 2014; 98(6): 765–8. https://doi.org/10.1136/bjophthalmol-2013-303367.
- 34Muth CM, Shank ES. Gas embolism [see comments]. N Engl J Med. 2000; 342(7): 476–82. https://doi.org/10.1056/NEJM200002173420706. Comments. In: N Engl J Med. 2000;342(26):2000; author reply 2001-2. doi: 10.1056/NEJM200006293422617; N Engl J Med. 2000;342(26):2000-1; author reply 2001-2; N Engl J Med. 2000;342(26):2001; author reply 2001-2.
- 35Nayagam J, Ho KM, Liang J. Fatal systemic air embolism during endoscopic retrograde cholangio-pancreatography. Anaesth Intensive Care. 2004; 32(2): 260–4. https://doi.org/10.1177/0310057X0403200217.
- 36Ohashi S, Endoh H, Honda T, Komura N, Satoh K. Cerebral air embolism complicating percutaneous thin-needle biopsy of the lung: Complete neurological recovery after hyperbaric oxygen therapy. J Anesth. 2001; 15(4): 233–6. https://doi.org/10.1007/s005400170008.
- 37van Rijn RR, Knoester H, Maes A, van der Wal AC, Kubat B. Cerebral arterial air embolism in a child after intraosseous infusion. Emerg Radiol. 2008; 15(4): 259–62. https://doi.org/10.1007/s10140-007-0681-2.
- 38Yang MS, Yang TH, Ou CH, Chan SW, Chen TI, Tu CW, et al. Iatrogenic and fatal arterial air embolism during the CT scan. J Chin Med Assoc. 2011; 74(4): 188–91. https://doi.org/10.1016/j.jcma.2011.01.042.
- 39Flanagan JP, Gradisar IA, Gross RJ, Kelly TR. Air embolism—A lethal complication of subclavian venipuncture. N Engl J Med. 1969; 281(9): 488–9. https://doi.org/10.1056/NEJM196908282810907.
- 40Lew TW, Tay DH, Thomas E. Venous air embolism during cesarean section: more common than previously thought. Anesth Analg. 1993; 77(3): 448–52. https://doi.org/10.1213/00000539-199309000-00005.
- 41Mishra R, Reddy P, Khaja M. Fatal cerebral air embolism: a case series and literature review. Case Rep Crit Care. 2016; 2016: 3425321. https://doi.org/10.1155/2016/3425321.
- 42Yu AS, Levy E. Paradoxical cerebral air embolism from a hemodialysis catheter. Am J Kidney Dis. 1997; 29(3): 453–5. https://doi.org/10.1016/s0272-6386(97)90209-2.
- 43Fyke FE 3rd, Kazmier FJ, Harms RW. Venous air embolism. Life-threatening complication of orogenital sex during pregnancy. Am J Med. 1985; 78(2): 333–6. https://doi.org/10.1016/0002-9343(85)90445-0.
- 44Perkins J. Air-embolism, with report of cases, clinical and experimental. Boston Med Surg J. 1897; 136(8): 179–81. https://doi.org/10.1056/NEJM189702251360803.
10.1056/NEJM189702251360803 Google Scholar
- 45Finn WF. Air embolism in obstetrics and gynecology. Am J Surg. 1945; 68(1): 100–2.
- 46Mushkat Y, Luxman D, Nachum Z, David MP, Melamed Y. Gas embolism complicating obstetric or gynecologic procedures. Case reports and review of the literature. Eur J Obstet Gynecol Reprod Biol. 1995; 63(1): 97–103. https://doi.org/10.1016/0301-2115(95)02221-r.
- 47Brune JE, Kaech DL, Wyler D, Jeker R. Delayed lethal pulmonary air embolism after a gunshot head injury. BMJ Case Rep. 2018; 2018: bcr2017223545. https://doi.org/10.1136/bcr-2017-223545.
10.1136/bcr-2017-223545 Google Scholar
- 48Adams VI, Hirsch CS. Venous air embolism from head and neck wounds. Arch Pathol Lab Med. 1989; 113(5): 498–502.
- 49King MW, Aitchison JM, Nel JP. Fatal air embolism following penetrating lung trauma: an autopsy study. J Trauma. 1984; 24(8): 753–5. https://doi.org/10.1097/00005373-198408000-00012.
- 50Martland HS. Air embolism: fatal air embolism due to powder insufflators used in gynecological treatments. Am J Surg. 1945; 68(2): 164–9. https://doi.org/10.1016/0002-9610(45)90100-0.
- 51Reith G, Bouillon B, Sakka SG, Defosse JM, Gossmann A, Probst C. Massive cerebral air embolism after blunt chest trauma with full neurological recovery. CJEM. 2016; 18(1): 62–5. https://doi.org/10.1017/cem.2014.78.
- 52Tellides G, Ugurlu BS, Kim RW, Hammond GL. Pathogenesis of systemic air embolism during bronchoscopic Nd:YAG laser operations [see comment]. Ann Thorac Surg. 1998; 65(4): 930–4. https://doi.org/10.1016/s0003-4975(98)00109-x. Comment. In: Ann Thorac Surg. 1998;66(1):308.
- 53Segal AJ, Wasserman M. Arterial air embolism: a cause of sudden death in status asthmaticus. Radiology. 1971; 99(2): 271–2. https://doi.org/10.1148/99.2.271.
- 54Westcott JL. Air embolism complicating percutaneous needle biopsy of the lung. Chest. 1973; 63(1): 108–10. https://doi.org/10.1378/chest.63.1.108.
- 55Orebaugh SL. Venous air embolism: clinical and experimental considerations. Crit Care Med. 1992; 20(8): 1169–77. https://doi.org/10.1097/00003246-199208000-00017.
- 56Yeakel AE. Lethal air embolism from plastic blood-storage container. JAMA. 1968; 204(3): 267–9. https://doi.org/10.1001/jama.1968.03140160077026.
- 57Mirski MA, Lele AV, Fitzsimmons L, Toung TJ. Diagnosis and treatment of vascular air embolism [see comments]. Anesthesiology. 2007; 106(1): 164–77. https://doi.org/10.1097/00000542-200701000-00026. Comments. In: Anesthesiology. 2007;107(5):850-1; author reply 853-4. doi: 10.1097/01.anes.0000287348.70351.a2; Anesthesiology. 2007;107(5):850; author reply 853-4. doi: 10.1097/01.anes.0000287347.49179.ee; Anesthesiology. 2007;107(5):851; author reply 853-4. doi: 10.1097/01.anes.0000287349.87497.4d; Anesthesiology. 2007;107(5):852; author reply 853-4. doi: 10.1097/01.anes.0000287531.35507.89; Anesthesiology. 2007;107(5):853; author reply 853-4. doi: 10.1097/01.anes.0000287350.01937.9e.
- 58Butler BD, Hills BA. Transpulmonary passage of venous air emboli. J Appl Physiol (1985). 1985; 59(2): 543–7. https://doi.org/10.1152/jappl.1985.59.2.543.
- 59O'Quin RJ, Lakshminarayan S. Venous air embolism. Arch Intern Med. 1982; 142(12): 2173–6. https://doi.org/10.1001/archinte.1982.00340250139020.
- 60Khan MA, Alkalay I, Suetsugu S, Stein M. Acute changes in lung mechanics following pulmonary emboli of various gases in dogs. J Appl Physiol. 1972; 33(6): 774–7. https://doi.org/10.1152/jappl.1972.33.6.774.
- 61Warren BA, Philp RB, Inwood MJ. The ultrastructural morphology of air embolism: platelet adhesion to the interface and endothelial damage. Br J Exp Pathol. 1973; 54(2): 163–72.
- 62Fries CC, Levowitz B, Adler S, Cook AW, Karlson KE, Dennis C. Experimental cerebral gas embolism. Ann Surg. 1957; 145(4): 461–70. https://doi.org/10.1097/00000658-195704000-00002.
- 63Gomes OM, Pereira SN, Castagña RC, Bittencourt D, Amaral RV, Zerbini EJ. The importance of the different sites of air injection in the tolerance of arterial air embolism. J Thorac Cardiovasc Surg. 1973; 65(4): 563–8.
- 64Kent EM, Blades B. Experimental observations upon certain intracranial complications of particular interest to the thoracic surgeon. J Thorac Surg. 1942; 11(4): 434–45.
10.1016/S0096-5588(20)31993-0 Google Scholar
- 65Goldfarb D, Bahnson HT. Early and late effects on the heart of small amounts of air in the coronary circulation. J Thorac Cardiovasc Surg. 1963; 46: 368–78.
- 66Stegmann T, Daniel W, Bellmann L, Trenkler G, Oelert H, Borst HG. Experimental coronary air embolism. Assessment of time course of myocardial ischemia and the protective effect of cardiopulmonary bypass. Thorac Cardiovasc Surg. 1980; 28(2): 141–9. https://doi.org/10.1055/s-2007-1022065.
- 67Groell R, Schaffler GJ, Rienmueller R, Kern R. Vascular air embolism: Location, frequency, and cause on electron-beam CT studies of the chest. Radiology. 1997; 202(2): 459–62. https://doi.org/10.1148/radiology.202.2.9015074.
- 68Griese H, Seifert D, Koerfer R. Cortical infarction following cardiosurgical procedures –Air embolism as a probable cause. Eur Neurol. 2009; 61(6): 343–9. https://doi.org/10.1159/000210546.
- 69Fujioka M, Niino D, Ito M, Matsuoka Y. Fatal paradoxical air embolism diagnosed by postmortem imaging and autopsy. J Forensic Sci. 2012; 57(4): 1118–9. https://doi.org/10.1111/j.1556-4029.2012.02094.x.
- 70Mercurio I, Capano D, Torre R, Taddei A, Troiano G, Scialpi M, et al. A case of fatal cerebral air embolism after blunt lung trauma: Postmortem computed tomography and autopsy findings [see comment]. Am J Forensic Med Pathol. 2018; 39(1): 61–8. https://doi.org/10.1097/PAF.0000000000000375. Comment. In: Am J Forensic Med Pathol. 2018;39(3):284. doi: 10.1097/PAF.0000000000000413.
- 71Taylor JD. Post-mortem diagnosis of air embolism by radiography. Br Med J. 1952; 1(4764): 890–3. https://doi.org/10.1136/bmj.1.4764.890.
- 72Edler C, Klein A, Püschel K, Schröder AS. Fatal air embolism in hospital confirmed by autopsy and postmortem computed tomography [see comment]. Forensic Sci Med Pathol. 2018; 14(2): 251–4. https://doi.org/10.1007/s12024-018-9961-2. Comment. In: Forensic Sci Med Pathol. 2018;14(4):579. doi: 10.1007/s12024-018-9976-8. Epub 2018 Apr 17.
- 73Emby DJ, Ho K. Air embolus revisited – A diagnostic and interventional radiological perspective (bubble trouble and the dynamic Mercedes Benz sign). SA J Radiol. 2006; 10(1): 3–7. https://doi.org/10.4102/sajr.v10i1.186.
10.4102/sajr.v10i1.186 Google Scholar
- 74Casadesús JM, Aguirre F, Carrera A, Boadas-Vaello P, Serrando MT, Reina F. Diagnosis of arterial gas embolism in SCUBA diving: Modification suggestion of autopsy techniques and experience in eight cases. Forensic Sci Med Pathol. 2018; 14(1): 18–25. https://doi.org/10.1007/s12024-018-9951-4.
- 75Bajanowski T, West A, Brinkmann B. Proof of fatal air embolism. Int J Legal Med. 1998; 111(4): 208–11. https://doi.org/10.1007/s004140050153.
- 76Zolotarov P, Fraser R. Venous air embolism: artefactual air entrapment and autopsy technique. Int J Legal Med. 2020; 134(3): 1033–6. https://doi.org/10.1007/s00414-019-02158-2.
- 77Bernaldo de Quirós Y, González-Díaz O, Møllerløkken A, Brubakk AO, Hjelde A, Saavedra P, et al. Differentiation at autopsy between in vivo gas embolism and putrefaction using gas composition analysis. Int J Legal Med. 2013; 127(2): 437–45. https://doi.org/10.1007/s00414-012-0783-6.
- 78Lantz PE, Adams GG. Postmortem monocular indirect ophthalmoscopy. J Forensic Sci. 2005; 50(6): 1450–2.
- 79Lantz PE, Schoppe CH, Thibault KL, Porter WT. Smartphone image acquisition during postmortem monocular indirect ophthalmoscopy. J Forensic Sci. 2016; 61(1): 238–40. https://doi.org/10.1111/1556-4029.12900.
- 80Krause D, Klein S. Tierexperimentelle untersuchungen zur postmortalen ophthalmoskopischen diagnostik der arteriellen luftembolie [Animal experiment studies of the postmortem ophthalmoscopic diagnosis of arterial air embolism]. Dtsch Z Gesamte Gerichtl Med. 1969; 65(1): 22–7. https://doi.org/10.1007/BF00584843.
- 81Klein S, Krause D, Klein A. Befunde am augenhintergrund bei arterieller luftembolie. Tierexperimentelle untersuchungen [Findings on fundus oculi in arterial air embolism. Experimental investigations in animals]. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1969; 178(3): 268–76. https://doi.org/10.1007/BF02384851.