Historical Vignette

Ancient Observation of Spinal Cord Injury: The Case of the Assyrian Lion

Gustavo J. Luvizutto1, Emerson G.M. Siqueira2, Pedro Tadao Hamamoto Filho2, Viviane H.F. Ze´tola3, Marcos C. Lange3, He´ lio A.G. Teive3, Luiz A.L. Resende2, Rodrigo Bazan2

Key words The description of paraplegia is considered a milestone in the history of - Dermatomes neurology. The Egyptians provided excellent descriptions of spinal cord injuries, - History of neurology - Paraplegia the Bible has several references to paraplegia, and, more recently, the pioneers - Spinal cord injury of neurology described the classic syndromes related to spinal injuries and paraplegia. Here, we describe an ancient observation by the Assyrian people of 1 â From the Univ. Federal do Tri ngulo Mineiro, Uberaba; paraplegia in an animal. In ancient Assyria, lion hunting was a ritualized activity 2Department of Neurology, Psychology, and Psychiatry, Univ. Estadual Paulista/Botucatu Medical School, Botucatu; and conducted for political and religious purposes. The Lion Hunt of Ashurbanipal, a 3Univ. Federal do Paraná, Curitiba, Brazil series of Assyrian palace reliefs from the North Palace at Nineveh dating from To whom correspondence should be addressed: approximately 645 BCE, which is now in the British Museum in London, UK, Pedro Tadao Hamamoto Filho, M.D., M.Sc. shows King Ashurbanipal hunting lions. Applying modern knowledge of [E-mail: [email protected]] mammalian dermatomes to the images, we reveal a detailed and precise Citation: World Neurosurg. (2018) 116:149-151. observation of paraplegia after spinal cord injury. https://doi.org/10.1016/j.wneu.2018.05.083 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com arrow or spear. Sometimes, the king animal’s back. There was no neurologic 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved. would kill it on foot with a sword. He involvement, because the forelimbs sup- would do this by holding the lion by the ported the animal’s weight on the ground; INTRODUCTION mane and then thrusting the sword into there was good tropism and muscular the lion’s throat. Then, when the lion was strength. This region of cervicothoracic Paraplegia is paralysis of the legs or the dead, the king would pour a liquid over it intumescence is seen in both domestic lower parts of the body. The International and give a speech to the city’s god and wild animals of the family Felidae. Standards for Neurological Classification ’ fi thanking him, so the lion s evil spirit Lesions in this region may generate signs of Spinal Cord Injury updated this de ni- would not come back and haunt him. of inferior motor neuron dysfunction in tion to include the impairment or loss of Expert spearmen and archers would pro- the thorax, with normal or spastic motor or sensory function in the thoracic, tect the king. Sometimes the king would hindlimbs. lumbar, or sacral segments of the spinal invite nobles to accompany him.3 cord secondary to damaged neural ele- 1,2 The Lion Hunt of Ashurbanipal, a series Arrow 2 ments within the spinal canal. The of Assyrian palace reliefs from the North description of paraplegia is considered a The arrow traversed the spine, with prob- Palace at Nineveh dating from approxi- able involvement of the spinal cord in the milestone in the history of neurology; mately 645 BCE, which is now in the here, we present 1 of the oldest observa- lumbar segment, identified by the loss of British Museum in London, UK, shows support by the hindlimbs. This involve- tions of spinal cord injury, which was King Ashurbanipal hunting lions made by the Assyrian people. ment can be observed by the possible (Figure 1). In fact, the royal lion hunt was decrease in muscle tone when forelimbs the staged and ritualized killing by the and hindlimbs are compared, with the THE ASSYRIAN PARAPLEGIC LION king of lions that had been captured and hindlimbs oriented in the caudal direc- In ancient Assyria, lion hunting was a released into an arena. The realism of tion. The most likely lesion is in the ritualized activity reserved for kings. These the lions in the reliefs has always been lumbar region, with involvement of the hunts were symbolic of the ruling mon- praised, although the pathos modern lumbar medullar portion of the spinal arch’s duty to protect and fight for his viewers tend to feel was perhaps not part cord. Therefore, the resulting posture is people. The Assyrian kings hunted lions of the Assyrian response. what would be expected according to the Applying modern knowledge of for political and religious purposes and to 4,5 analysis of the insertion site of the arrow demonstrate their power. To encourage mammalian dermatomes to the images and the apparent loss of muscle tone. In the lion out of his cage and onto the (Figure 2), we can describe the 3 arrows in this type of injury, we may have a victim Assyrian plains, a servant would raise the the following manner: with sphincter hypotonia, and also muscle cage door and start running. The lion was hypotonia, including the bladder detrusor. beaten by dogs and beaters, forcing the Arrow 1 In addition, hyporeflexia would be ex- lion to go to the king. The king would kill The arrow did not cross the spine and was pected in the hindlimbs, particularly in the the lion from a chariot with his bow and inserted into the muscular region of the patellar reflex.

WORLD NEUROSURGERY 116: 149-151, AUGUST 2018 www.WORLDNEUROSURGERY.org 149 HISTORICAL VIGNETTE GUSTAVO J. LUVIZUTTO ET AL. THE ASSYRIAN LION

Seti I (1290e1279 BCE) built the Temple of Amun in Karnak, and on the north wall of the Hypostyle Hall there are the Battle Reliefs, which present graphic representa- tions of neurologic injuries, including spine lesions, observed in battles.9 The Old Testament of the Bible also has several references to paraplegia, such as the mention of Mephibosheth (1000 BCE), grandson of King Saul.10 In the fourth century BCE, Hippo- fi Figure 1. (A) Sculpted reliefs depicting Ashurbanipal, the last great Assyrian king, hunting lions. crates, a leading gure in the history of Gypsum Hall relief from the North Palace of Nineveh (Iraq), c. 645e635 BCE, British Museum. (B) medicine, also provided detailed de- The image of the hunted lion, showing 3 arrows in his back; the arrow traversing the spine in the scriptions of spine lesions, such as lower back probably injured the spinal cord. tuberculous spondylitis and traumatic injuries. Additionally, he created some Arrow 3 The first clinical report of spinal cord principles for spine management that The arrow traversed the spine, with prob- lesions was registered in the Edwin Smith were observed for centuries, including able involvement of the spinal cord in the papyrus. In 1930, the Egyptologist James the concept that some maneuvers could sacral segment. There was neurologic Henry Breasted translated a papyrus, the worsen the prognosis.11-13 involvement, but there was an overlap with original content of which was probably Galen (129e200 AD) was the first to the arrow that affected the lumbar region. written during the seventeenth century perform several anatomic experiments, BCE. This papyrus contains the de- including early studies on the effects of scriptions of 48 traumatic cases, 6 involving transection of the spinal cord. Combining DISCUSSION the cervical spine, with 2 of those 6 clearly the medical heritage of the Hippocratic, Paraplegia is a well-established condition describing injuries to the spinal cord. The Alexandrian, and ancient medical schools that occurs with complete or incomplete anatomy of the lesions is described, as are in his studies, he was able to describe the spinal cord lesions. Thorough de- strategies for how to manage each case. specific loss of function below the level of scriptions of spinal cord lesions have Some have suggested that the author of the transection.14,15 made it possible to understand the history papyrus was Imhotep, but the original Other authors provided significant ad- of neurologic knowledge. authorship is controversial.6-8 Later, King vances in the understanding of the anat- omy and physiology of the spine. Leonardo da Vinci (1452e1519) made the first attempts to describe spinal stability, Andreas Vesalius (1514e1564) made a very precise description of spinal anatomy, and Giovanni Alfonso Borelli (1608e1679) introduced the concept of spinal biome- chanics.16 Gerard Blaes (Blasius) (1627e 1682) described the anterior and posterior spinal roots and also the white matter surrounding the H-shaped formation of the gray matter.17 Domenico Cotugno (1736e18) described cerebrospinal fluid and formulated the hypothesis of nerve sheath involvement in the origin of sciatica.18,19 In 1746, William Hunter founded a medical school, the Great Windmill Street School of Anatomy, where several outstanding physicians, such as Percival Pott (1714e 1788), Astley Cooper (1768e1841), John Abernethy (1764e1831), and Everard Home (1756e1832) studied spinal disorders.20 In 1849, Charles-Edouard Figure 2. The hunted lion image overlapped by a schematic of the Brown-Séquard (1817e1894) published dermatomes in mammals. Arrows 1, 2, and 3 are identified as described in the first description of medullary syn- the text. drome, a lateral hemisection causing

150 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.05.083 HISTORICAL VIGNETTE GUSTAVO J. LUVIZUTTO ET AL. THE ASSYRIAN LION ipsilateral hyperesthesia and lost or ACKNOWLEDGMENT 18. Manni E, Petrosini L. Domenico Cotugno, a pioneer in neurosciences. JHistNeurosci.1997;6:124-132. diminished sensation in the contralateral We thank the British museum in London 21-23 e limb. Wilhelm Heinrich Erb (1840 for the authorization to use the images 19. Pearce JMS. Cotugno and cerebrospinal fluid. 1921) made early observations of tabes and we thank Mr. Cristiano de Almeida J Neurol Neurosurg Psychiatry. 2004;75:1299. dorsalis, also known as syphilitic Akama for his support on the illustration myelopathy, which was associated with a 20. Weiner MF, Silver JR. The contribution to our of the lion's dermatomes. understanding of spinal disorders by the great major epidemic of infectious diseases in Windmill Street School of Anatomy. Spinal Cord. Europe.24 William Gowers (1845e1915) REFERENCES 2011;49:323-332. was the first to identify a removable spinal tumor, and he was an enthusiastic 1. Haerer A, DeJong RN. Disorders of the spinal cord. 21. Brown-Sequard E. De la transmission croisée des In: DeJong RN, ed. DeJong’s The Neurologic Examina- impressions sensitives par la moelle epinière. CR supporter of the importance of clinical tion. Philadelphia: Lippincott; 1992:585-586. Soc Biol (Paris, France). 1850;2:33. examination for neurologic diagnoses.25 2. Haerer A, DeJong RN. Motor strength and power. This spinal tumor was successfully 22. Charcot JM. Du tabes dorsal spasmodique. Prog In: DeJong RN, ed. DeJong’s The Neurologic Exami- e Med (Paris). 1876;45:737-738. removed by Victor Horsley (1857 1916), nation. Philadelphia: Lippincott; 1992:335-339. who also made important contributions 23. Tattersall R, Turner B. Brown-Séquard and his to the surgical management of spinal 3. Radner K. Ancient Assyria: A Very Short Introduction. Oxford: Oxford University Press; 2015. syndrome. Lancet. 2000;356:61-63. lesions.26 These observations and studies contributed to the understanding of 4. Hekmatpanah J. Organization of tactile derma- 24. Mahmoudi Nezhad GS, Dalfardi B, Ghanizadeh A. spinal cord lesions, and they are part of tomes, C1 through L4, in cat. J Neurophysiol. 1961; Wilhelm Heinrich Erb (1840-1921). J Neurol. 2014; 24:129-140. 261:1846-1847. the history of neurology and neurosurgery. Currently, several conditions are recog- 5. Reid KH. Dermatomes and skin innervation 25. Mulholland RC. Sir William Gowers 1845-1915. ’ nized as causes of paraplegia, such as density in the cat s tail. Exp Neurol. 1970;26:1-16. Spine. 1996;21:1106-1110. trauma, infections, autoimmune diseases, 6. Van Middendorp JJ, Sanchez GM, Burridge AL. 26. Tan TC, Black PM. Sir Victor Horsley (1857-1916): tumors, and circulatory abnormalities. The Edwin Smith papyrus: a clinical reappraisal of pioneer of neurological surgery. Neurosurgery. the oldest known document on spinal injuries. Eur Individuals with severe fracture disloca- 2002;50:607-611. tions may be neurologically intact, Spine J. 2010;19:1815-1823. whereas some present with symptomatic 7. Breasted JH. Edwin Smith Surgical Papyrus. Chicago: 27. Zhang S, Yan TB. Severe fracture-dislocation of University of Chicago Press; 1930. the thoracic spine without any neurological spinal cord injury without any radiologic fi 27-29 de cit. World J Surg Oncol. 2017;15:3. abnormalities. 8. Hughes JT. The Edwin Smith Surgical Papyrus: an Notwithstanding the cause of the spine analysis of the first case reports of spinal cord 28. Salkov M, Tsymbaliuk V, Dzyak L, Rodinsky A, lesion, humans are highly dependent on injuries. Paraplegia. 1988;26:71-82. Cherednichenko Y, Titov G. New concept of descending pathways to maintain control of pathogenesis of impaired circulation in traumatic 9. Sanchez GM. A neurosurgeon’s view of the battle cervical spinal cord injury and its impact on dis- locomotion, and the neural networks below reliefs of King Sety I: aspects of neurological ease severity: case series of four patients. Eur Spine the level of the lesion are not as easily acti- importance. J Am Res Cent Egypt. 2000;37:143-165. J. 2016;25:11-18. 30 vated as they are in animals. Experimental 10. Bedbrook GM, Sedgley GI. The management of studies on locomotor activity and its relation e 29. Pang D, Pollack IF. Spinal cord injury without spinal injuries past and present. Int Rehab Med. radiographic abnormality in children: the SCI- to spine injuries were performed in felines 1980;2:45-61. WORA syndrome. J Trauma. 1989;29:654-664. mainly during the twentieth century. These 11. Marketos SG, Skiadas P. Hippocrates. The father experiments showed that cats can recover of spine surgery. Spine. 1999;24:1381-1387. 30. Yang JF, Gorassini M. Spinal and brain control of spontaneous hindlimb locomotion on a human walking: implications for retraining of 12. Korres DS, Mavrogenis AF, Papagelopoulos PJ. walking. Neuroscientist. 2006;12:379-389. treadmill after a complete spinal cord Hippocratic beliefs on spine and spinal cord injuries: transection, but they cannot recover new or old notions? Orthopedics.2004;27:1078-1079. 31. Rossignol S, Bouyer L. Adaptive mechanisms of spi- voluntary locomotion.31 The representation nal locomotion in cats. Integr Comp Biol. 2004;44:71-79. of the Assyrian lion is very similar to the 13. Korres D, Markatos K, Chytas D, Andreakos A, Mavrogenis A. Injuries of the spine and of the 32. Majczynski H, Sławinska U. Locomotor recovery patterns observed in cats with spine injuries, spinal cord in the hippocratic corpus of medicine. after thoracic spinal cord lesions in cats, rats and namely, the inability to support the posterior Int Orthop. 2017;41:2627-2629. humans. Acta Neurobiol Exp (Wars). 2007;67:235-257. back weight, lack of voluntary control of the 14. De G usu partium. Galen on the Usefulness of the Parts hindlimbs, absence of sustained of the Body (Peri Chreias Morion). Ithaca, NY: Cornell Conflict of interest statement: The authors declare that the coordination between the forelimbs and University Press; 1968. article content was composed in the absence of any hindlimbs during quadrupedal locomotion, commercial or financial relationships that could be construed 32 15. Marketos SG, Skiadas PK. Galen: a pioneer of as a potential conflict of interest. and loss of balance control. spine research. Spine. 1999;24:2358-2362. In this historical vignette, we show a Received 22 February 2018; accepted 12 May 2018 16. Sanan A, Rengachary SS. The history of spinal precise, accurate, and detailed ancient Citation: World Neurosurg. (2018) 116:149-151. biomechanics. Neurosurgery. 1996;39:657-668. observation of paraplegia in an animal. This https://doi.org/10.1016/j.wneu.2018.05.083 depiction may have been an involuntary 17. Markatos K, Laios K, Korres D, Tzivra A, Journal homepage: www.WORLDNEUROSURGERY.org Tsoutsos S, Androutsos G. Gerard Blaes (Blasius) contribution of the Assyrian people to the Available online: www.sciencedirect.com (1627-1682): the Dutch physician and chemist, his knowledge of comparative anatomy and work and description of the spinal cord. World 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All neurology. Neurosurg. 2017;104:148-151. rights reserved.

WORLD NEUROSURGERY 116: 149-151, AUGUST 2018 www.WORLDNEUROSURGERY.org 151