Expanding the Borders: the Evolution of Neurosurgical Approaches

Neurosurg Focus 36 (4):E11, 2014 ©AANS, 2014

Expanding the borders: the evolution of neurosurgical approaches

Malte Ottenhausen, M.D., Imithri Bodhinayake, M.D., Alexander I. Evins, M.D., Matei Banu, M.D., John A. Boockvar, M.D., and Antonio Bernardo, M.D. Department of Neurological Surgery, Weill Medical College of Cornell University, New York, New York

In this article the authors discuss the development of neurosurgical approaches and the advances in science and technology that influenced this development throughout history. They provide a broad overview of this interesting topic from the first attempts of trephination by ancient cultures to the work of the pioneers of neurosurgery and the introduction of microsurgery. (http://thejns.org/doi/abs/10.3171/2014.2.FOCUS13547)

Key Words • approaches • history • skull base • overview • craniotomy • neurosurgery

hy and how men first opened the skull remains beliefs and techniques of early skull surgery. The Corpus a matter of speculation. It cannot be determined Hippocraticum, a collection of more than 60 medical texts for certain whether they were attempting to originating from between 500 bce and 200 ce, contains treatW medical conditions, as postulated by the English the first description of trephination and provides detailed surgeon Sir Victor Horsley (1857–1916),10 or perform- instructions in the chapter “On Head Wounds.”18 The ing religious and cultural rituals, as suggested by the Greek physician Galen of Pergamon (129–200 ce) further French physician Pierrre Paul Broca (1824–1880).2,7 developed and described the technique and contributed Archaeological findings from 3000 bce25 and earlier tremendously to the understanding of neuroanatomy. In show that various cultures practiced opening the skull. particular, he stressed the importance of maintaining the Early evidence of trephination comes from the famous integrity of the dura mater.27 Evidence of the practice of discovery of the Incan skull by Ephraim George Squier trephination has also been found in many cultures outside (1821–1888) in the 1860s,11 which dated to 1530 ce, as of Greece and Rome. From ancient times through antiq- well as from several other skulls showing evidence of uity and the Middle Ages, trephination and removal of premortem trephination found across Europe,29 Asia,25,28 bone fragments were established as treatments for head and the Americas.23 Examination of these skulls suggest trauma. Subsequently, cranioplasty using metal plates1,31 that most of the individuals survived the operation—sug- or even xenografts33 was developed and described. gesting that these procedures were actually attempted as After the fall of the Roman Empire, education was medical treatments rather than religious rituals.2 largely based in religious institutions, and it was not until Archeological evidence from such skulls suggests the 11th century ce that the first universities (University the existence of different techniques for trephination. As of Bologna, est. 1088) and medical schools were estab- explained in detail by Charles Gross,15 a technique used lished. However, cadaveric dissections were forbidden, across various regions such as Peru, France, Israel, and inhibiting complete understanding of cranial anatomy. It Africa involved the use of rectangular intersecting cuts. was not until the Renaissance in the 16th century and the Initially these cuts were made using hard stone tools and cadaveric dissections of Leonardo Da Vinci (1452–1519) later using metal tools. Other techniques for trephination and Andreas Vesalius (1514–1564) that the contents of included abrasion with a rough tool until the dura was the cranial vault including the cranial nerves became exposed, carving out a circular piece of bone using sharp known.14 Several detailed illustrations of neuroanatomy stone tools, and the creation of multiple small holes in a were subsequently printed for the first time, and the first circumferential manner to facilitate the cutting of a small public dissections of the cranium were performed.17 disk of bone with sharp instruments (Fig. 1). This growing knowledge of cranial anatomy was com- More detailed information about early operations on municated through organized societies, including the Aca- the skull can be found in documents providing insight on démie des Sciences in Paris, the Royal Society of London,

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later introduced into surgery by British surgeon Joseph Lister (1821–1888) in the 1860s. These contributions dra- matically reduced rates of perioperative infection. In 1895, the German physicist Wilhelm Conrad Röntgen (1845–1923) discovered the phenomenon of radiography, and it was introduced into surgery just 1 year later. By 1908, the German neurosurgeon Fedor Krause (1857–1937) published the first neurosurgical text con- taining a chapter on x-rays.9 The first purely neurora- diological techniques were introduced by Walter Dandy (1886–1946) in 1918 with ventriculography and in 1919 with pneumoencephalography.14 These techniques were followed by the development of angiography in 1926 by António Caetano de Abreu Freire Egas Moniz (1874–1955), a professor of neurol- ogy at the University of Lisbon. After some initial testing in cadavers, Moniz injected radioopaque agents such as Fig. 1. A cranium from the Andahualyas province, Peru (~ 1000– strontium bromide and sodium iodide into patients before 1200 ad) demonstrating trepanations made by scraping (upper left inset x-ray examination in order to visualize cranial vessels. shows evidence of healing) and by drilling multiple small holes (likely Moniz is also known as the father of the controversial postmortem to practice and optimize technique). Reproduced from Kurin DS: Trepanation in South-Central Peru during the early late in- field of psychosurgery, and in 1949 he was awarded the termediate period (ca. AD 1000-1250). Am J Phys Anthropol 152:484– Nobel Prize in Physiology or Medicine for his contribu- 494, 2013. Used with permission from John Wiley & Sons. tions in that area.24 Removal of the first brain tumor using electrocautery and others that formed around the 17th century.14 These in 1926 marked an important step in the evolution of neu- societies, which originated from small scientific circles and rosurgery.34 In the late 1920s the American neurosurgeon grew in the Age of Enlightenment, were dedicated to ex- Harvey Cushing (1869–1939) was looking for a more ef- panding knowledge and making it publicly available. ficient way to ensure hemostasis than the clamp-and-tie Throughout the 17th and 18th centuries, surgeons methods, which were of limited use in neurosurgery. He with extensive practical experience from the battlefields found his solution in the “electro-surgical apparatus” de- helped advanced surgical technique.14 One well-known veloped by Dr. William T. Bovie (1882–1958), a biophysi- example is the surgeon Antoine Louis (1723–1792), who cist working in a nearby hospital. This device used high- became secretary of the Académie Royale de Chirurgie frequency electricity to heat-seal or cut tissue on contact. in Paris. Louis introduced the use of ligatures to amputate This technique was patented in 1931 and has been used a tumor at its base and successfully removed an extra- for dissection and hemostasis ever since.5 axial brain tumor (meningioma) in as early as 1774.14 The bipolar electrocautery also paved the way for microsurgery.4 Previously, hemostasis was achieved through a combination of packing, suture ligation, and surgical From Cranial Surgery to Brain Surgery clips. From the mid-19th century onward, bone wax was In the period that followed, anatomical and medical used for calvarial hemostasis.16 knowledge continued to grow, but the practice of cranial In 1898 the Italian obstetrician Leonardo Gigli surgery remained largely unchanged. It was not until the (1863–1908) introduced into neurosurgery a wire saw 19th century that more sophisticated approaches through (“Drahtsäge”), which he initially developed in 1894 dur- the skull were developed. This period was marked by sci- ing obstetrics training in Germany.3 The wire saw made entific advancement in many fields, which allowed sur- craniotomies safer and faster and is still used by neuro- geons to perform more extensive skull openings, including surgeons today. Previously, when larger parts of bone openings that extended beyond the dura. The development needed to be removed, multiple bur holes were enlarged of anesthesia, antisepsis, radiography, hemostasis, and new using forceps or a mallet and chisel, a technique that often operating instruments enabled a deeper understanding resulted in concussions. of neuroanatomy, pathology, and physiology that laid the The endoscope, first developed in 1853 as a cysto- ground for the evolution of modern neurosurgery. scope, was used to perform the first endoscopic third ven- After several failures and unacknowledged initial triculostomy by Dandy in 1922. The endoscope continued successes, William Thomas Green Morton (1819–1868) to be developed for use in endonasal and other skull base publicly demonstrated the successful use of ether as an approaches.36 Another important tool, the surgical micro- anesthetic on October 16, 1846.35 This so-called “Ether scope, based on the microscopes invented during the late Day” marks the birth of modern anesthesia and the start 16th century, was introduced in 1921. However, it was not of longer, more complex procedures. used by neurosurgeons until the late 1950s. Alongside these Infection was the most common cause of mortality technical advances, surgical technique also improved, al- related to trephination during the 18th century.13 The idea lowing for the first successful removal of a brain tumor in of antisepsis was first described by the Hungarian physi- 1887 by William W. Keen Jr. (1837–1932).30 cian Ignaz Philipp Semmelweis (1818–1865) in 1847 and The evolution of surgery from a risky endeavor to an

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evidence-based profession was acknowledged by the scientific community in 1909 when Emil Theodor Kocher (1841–1917) became the first surgeon to receive a Nobel Prize.6 In this climate of dramatic change, Harvey Cush- ing and others established neurosurgery as a subspecial- ty and began to treat tumors and other conditions with growing success. The first standardized neurosurgical approaches were developed during this period. An important tool that enabled the development of standardized approaches was the power drill. Thierry de Martel’s (1875–1940) engineering background helped him introduce an automated drill in 1908 that was able to disengage after penetrating the skull’s inner surface. Power tools enabled surgeons to make precise craniotomies with ease and reduced operative time (Fig. 2).

The Development of Complex Approaches and the Impact of the Microscope In this dynamic field, it is sometimes difficult to cred- it surgeons who invented approaches because they may Fig. 3. Schematic illustration showing examples of typical neurosur- not always be the ones who first described or establish gical approaches. From left to right: orbitozygomatic approach, transpe- these approaches. In the following paragraphs, we de- trosal approach, far-lateral approach. scribe the development of some of the many neurosurgical approaches (Fig. 3). Although we only mention some of their pioneers, many neurosurgeons have contributed intracranial aneurysms, it soon became one of the most and continue to contribute to the development of our field. widely used approaches in neurosurgery because of the Microsurgery was first propagated by plastic sur- access it provides not only to the anterior circulation but geons and otolaryngologists and was introduced to neu- also to lesions of the sellar region, cavernous sinus, and rosurgery by Theodore Kurze (1922–2002) in 1957. In anterior and middle cranial fossae. This approach had the 1960s, fellow neurosurgeons, including Raymond M. its origins in the frontotemporal craniotomy described P. Donaghy (1910–1991) and Mahmut Gazi Yaşargil (b. by George J. Heuer (1882–1950), Krause, and Dandy in 1925), actively established microneurosurgery.22 The use the beginning of the 20th century. As more tools became of the microscope allowed for surgical access to regions available tools and surgical skills improved, the pterional with complex anatomy such as the skull base with its tight approach was modified to include removal of the supra- networks of vessels and nerves. Use of the microscope led orbital rim (Charles Frazier, 1870–1936),12 removal of the to the development of new approaches and sophisticated zygomatic arch (Cushing), or combined with the orbitozy- modifications.26 gomatic approach. The gradual development and subsequent modifi- Similar progression can be seen in the lateral and cations of surgical approaches is well illustrated by the posterior approaches. While Krause described the sub- pterional approach. Popularized by Yaşargil in 1969 for temporal craniotomy as early as 1911, it was Charles Drake (1920–1998) who popularized the approach and described new variations and modifications. The operating microscope allowed William F. House (1923–2012) to establish the subtemporal middle fossa approach in 1961 in order to treat vestibular schwannomas.26 Numerous other modifications and extensions have been described since, including removal of the petrous apex, as described by Takeshi Kawase (b. 1944).21 Another major approach was the introduction of the retrosigmoid craniotomy, which provided access to the cerebellopontine angle. This lateral suboccipital approach was first used by Sir Charles A. Balance (1856–1936) in 1894 and was further modified by many neurosurgeons and successfully used in the treatment of vestibular schwannomas and other regional pathologies.26 Similar progression is also seen with the transphenoi- dal approaches. In 1907, Herman Schloffer (1868–1937) 32 Fig. 2. Intraoperative photograph illustrating a translabyrinthine ap- became the first to use a transsphenoidal approach to re- proach facilitated by power tools, including the hand-held drill, allowing move a pituitary tumor. This technique was adapted and for the fast and precise removal of compact bone. modified by Cushing8 and others who laid the important

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Fig. 4. The Microneurosurgery Skull Base Laboratory in the Department of Neurological Surgery at Weill Cornell Medi- cal College—a state-of-the-art educational and research facility dedicated to the teaching and advancement of neurosurgery through the development of complex neurosurgical approaches. groundwork for further development. Austrian otorhino- Author contributions to the study and manuscript preparation laryngologist Oskar Hirsch (1877–1965) was the first to include the following. Conception and design: Ottenhausen. Drafting describe an endonasal approach in 1910.19 While this ap- the article: Ottenhausen, Bodhinayake. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. proach was nearly abandoned in the following decades Approved the final version of the manuscript on behalf of all authors: due to high morbidity from infection, the introduction of Bernardo. Study supervision: Bernardo. the microscope and improved imaging techniques led to its renaissance in the late 1960s. Since then, this has been References one of the most dynamic areas of neurosurgery. Today, the endonasal route is used for extended approaches to 1. Aciduman A, Belen D: The earliest document regarding the reach lesions even beyond the sellar region.20 While the history of cranioplasty from the Ottoman era. Surg Neurol microscope led to the reemergence of this approach, the 68:349–353, 2007 endoscope extended its limits. 2. Arnott R, Finger S, Smith CUM: Trepanation: History, Dis- covery, Theory. Lisse, The Netherlands: Swets & Zeitlinger, Although the time of revolutions may appear to be 2003 over, the constantly increasing knowledge and techno- 3. Brunori A, Bruni P, Greco R, Giuffré R, Chiappetta F: Cel- logical progression continue to influence neurosurgical ebrating the centennial (1894-1994): Leonardo Gigli and his approaches to the brain and skull base. Intraoperative wire saw. J Neurosurg 82:1086–1090, 1995 MRI and neuronavigation are only a few of many recent 4. Bulsara KR, Sukhla S, Nimjee SM: History of bipolar coagu- advances that have enhanced the practice of standardized lation. Neurosurg Rev 29:93–96, 2006 neurosurgical approaches. The presence of microsurgical 5. Carter PL: The life and legacy of William T. Bovie. Am J and skull base laboratories (Fig. 4) in neurosurgical edu- Surg 205:488–491, 2013 6. Choong C, Kaye AH: Emil Theodor Kocher (1841-1917). J cation and research enable surgeons to push the frontiers Clin Neurosci 16:1552–1554, 2009 of neurosurgery. 7. Clower WT, Finger S: Discovering trepanation: the contribu- tion of Paul Broca. Neurosurgery 49:1417–1426, 2001 Conclusions 8. Cohen-Gadol AA, Liu JK, Laws ER Jr: Cushing’s first case of transsphenoidal surgery: the launch of the pituitary surgery The development of cranial approaches is driven era. J Neurosurg 103:570–574, 2005 and influenced by new scientific discoveries. Although 9. Elhadi AM, Kalb S, Martirosyan NL, Agrawal A, Preul MC: most approaches have been around for nearly a century, Fedor Krause: the first systematic use of X-rays in neurosur- their widespread use and efficacy is only possible due to gery. Neurosurg Focus 33(2):E4, 2012 advances in technological advancement and scientific 10. Finger S, Clower WT: Victor Horsley on “trephining in pre- knowledge. Simple bur holes and extradural approaches historic times.” Neurosurgery 48:911–918, 2001 11. Finger S, Fernando HR: E. George Squier and the discovery of have developed into an extensive intradural technique and cranial trepanation: a landmark in the history of surgery and into minimally invasive and microneurosurgery. ancient medicine. J Hist Med Allied Sci 56:353–381, 2001 12. Frazier CH: I. An approach to the hypophysis through the an- Acknowledgment terior cranial fossa. Ann Surg 57:145–150, 1913 We thank Danielle S. Kurin, Ph.D., visiting assistant professor 13. Ganz JC: Trepanation and surgical infection in the 18th cen- at the Department of Anthropology, University of California Santa tury. Acta Neurochir (Wien) 156:615–623, 2013 Barbara, for providing the photograph of a trepanned skull from the 14. Goodrich JT: A millennium review of skull base surgery. Andahuaylas province, Peru. Childs Nerv Syst 16:669–685, 2000 15. Gross CG: A Hole in the Head: More Tales in the History of Neuroscience. Disclosure Cambridge, MA: MIT Press, 2009 16. Gupta G, Prestigiacomo CJ: From sealing wax to bone wax: The authors report no conflict of interest concerning the mate- predecessors to Horsley’s development. Neurosurg Focus rials or methods used in this study or the findings specified in this 23(1):E16, 2007 paper. 17. Hanigan WC, Ragen W, Foster R: Dryander of Marburg and

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the first textbook of neuroanatomy. Neurosurgery 26:489– 29. Papagrigorakis MJ, Toulas P, Tsilivakos MG, Kousoulis AA, 498, 1990 Skorda D, Orfanidis G, et al: Neurosurgery during the Bronze 18. Hippocrates: On Head Wounds. Maury Hanson, trans. Ber- Age: a skull trepanation in 1900 BC Greece. World Neuro- lin: Akademie Verlag, 1999 surg [epub ahead of print], 2013 19. Hirsch O: Endonasal method of removal of hypophyseal tu- 30. Ray BS: The development of neurosurgery in New York City. mors with report of two successful cases. JAMA 55:772–774, Bull N Y Acad Med 55:916–938, 1979 1910 31. Sanan A, Haines SJ: Repairing holes in the head: a history of 20. Kanter AS, Dumont AS, Asthagiri AR, Oskouian RJ, Jane JA cranioplasty. Neurosurgery 40:588–603, 1997 Jr, Laws ER Jr: The transsphenoidal approach. A historical 32. Schmidt RF, Choudhry OJ, Takkellapati R, Eloy JA, Couldwell perspective. Neurosurg Focus 18(4):E6, 2005 WT, Liu JK: Hermann Schloffer and the origin of transsphe- 21. Kawase T, Shiobara R, Toya S: Anterior transpetrosal-trans- noidal pituitary surgery. Neurosurg Focus 33(2):E5, 2012 tentorial approach for sphenopetroclival meningiomas: surgi- 33. Shoja MM, Agutter PS, Loukas M, Shokouhi G, Khalili M, cal method and results in 10 patients. Neurosurgery 28:869– Farhoudi M, et al: Cranioplasty in medieval Persia and the 876, 1991 potential spread of this knowledge to Europe. Childs Nerv 22. Kriss TC, Kriss VM: History of the operating microscope: Syst 28:1993–1996, 2012 from magnifying glass to microneurosurgery. Neurosurgery 34. Voorhees JR, Cohen-Gadol AA, Laws ER, Spencer DD: Bat- 42:899–908, 1998 tling blood loss in neurosurgery: Harvey Cushing’s embrace 23. Kurin DS: Trepanation in South-Central Peru during the early of electrosurgery. J Neurosurg 102:745–752, 2005 late intermediate period (ca. AD 1000-1250). Am J Phys An- 35. Westhorpe R: William Morton and the first successful demon- thropol 152:484–494, 2013 stration of anaesthesia. Anaesth Intensive Care 24:529, 1996 24. Ligon BL: Biography: history of developments in imaging 36. Zada G, Liu C, Apuzzo ML: “Through the looking glass”: techniques: Egas Moniz and angiography. Semin Pediatr In- optical physics, issues, and the evolution of neuroendoscopy. fect Dis 14:173–181, 2003 World Neurosurg 77:92–102, 2012 25. Lv X, Li Z, Li Y: Prehistoric skull trepanation in China. World Neurosurg 80:897–899, 2012 26. Machinis TG, Fountas KN, Dimopoulos V, Robinson JS: His- Manuscript submitted December 3, 2013. tory of acoustic neurinoma surgery. Neurosurg Focus 18(4): Accepted February 21, 2014. E9, 2005 Please include this information when citing this paper: DOI: 27. Missios S: Hippocrates, Galen, and the uses of trepanation in 10.3171/2014.2.FOCUS13547. the ancient classical world. Neurosurg Focus 23(1):E11, 2007 Address correspondence to: Antonio Bernardo, M.D., Microneu- 28. Mogliazza S: An example of cranial trepanation dating to rosurgery Skull Base Laboratory, Weill Cornell Medical College, the Middle Bronze Age from Ebla, Syria. J Anthropol Sci NewYork-Presbyterian Hospital, 525 E. 68th St., New York, NY 87:187–192, 2009 10065. email: [email protected].

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