Neurosurg Focus / Volume 36 / April 2014

Neurosurg Focus 36 (4):E11, 2014

1

©AANS, 2014

Why and how men first opened the skull remains a matter of speculation. It cannot be determined for certain whether they were attempting to

treat medical conditions, as postulated by the English surgeon Sir Victor Horsley (1857–1916),10 or perform-ing religious and cultural rituals, as suggested by the French physician Pierrre Paul Broca (1824–1880).2,7 Archaeological findings from 3000 bce25 and earlier show that various cultures practiced opening the skull. Early evidence of trephination comes from the famous discovery of the Incan skull by Ephraim George Squier (1821–1888) in the 1860s,11 which dated to 1530 ce, as well as from several other skulls showing evidence of premortem trephination found across Europe,29 Asia,25,28 and the Americas.23 Examination of these skulls suggest that most of the individuals survived the operation—sug-gesting that these procedures were actually attempted as medical treatments rather than religious rituals.2

Archeological evidence from such skulls suggests the existence of different techniques for trephination. As explained in detail by Charles Gross,15 a technique used across various regions such as Peru, France, Israel, and Africa involved the use of rectangular intersecting cuts. Initially these cuts were made using hard stone tools and later using metal tools. Other techniques for trephination included abrasion with a rough tool until the dura was exposed, carving out a circular piece of bone using sharp stone tools, and the creation of multiple small holes in a circumferential manner to facilitate the cutting of a small disk of bone with sharp instruments (Fig. 1).

More detailed information about early operations on the skull can be found in documents providing insight on

beliefs and techniques of early skull surgery. The Corpus Hippocraticum, a collection of more than 60 medical texts originating from between 500 bce and 200 ce, contains the first description of trephination and provides detailed instructions in the chapter “On Head Wounds.”18 The Greek physician Galen of Pergamon (129–200 ce) further developed and described the technique and contributed tremendously to the understanding of neuroanatomy. In particular, he stressed the importance of maintaining the integrity of the dura mater.27 Evidence of the practice of trephination has also been found in many cultures outside of Greece and Rome. From ancient times through antiq-uity and the Middle Ages, trephination and removal of bone fragments were established as treatments for head trauma. Subsequently, cranioplasty using metal plates1,31 or even xenografts33 was developed and described.

After the fall of the Roman Empire, education was largely based in religious institutions, and it was not until the 11th century ce that the first universities (University of Bologna, est. 1088) and medical schools were estab-lished. However, cadaveric dissections were forbidden, inhibiting complete understanding of cranial anatomy. It was not until the Renaissance in the 16th century and the cadaveric dissections of Leonardo Da Vinci (1452–1519) and Andreas Vesalius (1514–1564) that the contents of the cranial vault including the cranial nerves became known.14 Several detailed illustrations of neuroanatomy were subsequently printed for the first time, and the first public dissections of the cranium were performed.17

This growing knowledge of cranial anatomy was com-municated through organized societies, including the Aca-démie des Sciences in Paris, the Royal Society of London,

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

1

Unauthenticated | Downloaded 02/15/21 09:12 PM UTC

M. Ottenhausen et al.

2 Neurosurg Focus / Volume 36 / April 2014

and others that formed around the 17th century.14 These societies, which originated from small scientific circles and grew in the Age of Enlightenment, were dedicated to ex-panding knowledge and making it publicly available.

Throughout the 17th and 18th centuries, surgeons with extensive practical experience from the battlefields helped advanced surgical technique.14 One well-known example is the surgeon Antoine Louis (1723–1792), who became secretary of the Académie Royale de Chirurgie in Paris. Louis introduced the use of ligatures to amputate a tumor at its base and successfully removed an extra-axial brain tumor (meningioma) in as early as 1774.14

From Cranial Surgery to Brain SurgeryIn the period that followed, anatomical and medical

knowledge continued to grow, but the practice of cranial surgery remained largely unchanged. It was not until the 19th century that more sophisticated approaches through the skull were developed. This period was marked by sci-entific advancement in many fields, which allowed sur-geons to perform more extensive skull openings, including openings that extended beyond the dura. The development of anesthesia, antisepsis, radiography, hemostasis, and new operating instruments enabled a deeper understanding of neuroanatomy, pathology, and physiology that laid the ground for the evolution of modern neurosurgery.

After several failures and unacknowledged initial successes, William Thomas Green Morton (1819–1868) publicly demonstrated the successful use of ether as an anesthetic on October 16, 1846.35 This so-called “Ether Day” marks the birth of modern anesthesia and the start of longer, more complex procedures.

Infection was the most common cause of mortality related to trephination during the 18th century.13 The idea of antisepsis was first described by the Hungarian physi-cian Ignaz Philipp Semmelweis (1818–1865) in 1847 and

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 ra-diography, 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 strontium bromide and sodium iodide into patients before x-ray examination in order to visualize cranial vessels. Moniz is also known as the father of the controversial field of psychosurgery, and in 1949 he was awarded the Nobel Prize in Physiology or Medicine for his contribu-tions in that area.24

Removal of the first brain tumor using electrocautery in 1926 marked an important step in the evolution of neu-rosurgery.34 In the late 1920s the American neurosurgeon Harvey Cushing (1869–1939) was looking for a more ef-ficient way to ensure hemostasis than the clamp-and-tie methods, which were of limited use in neurosurgery. He found his solution in the “electro-surgical apparatus” de-veloped by Dr. William T. Bovie (1882–1958), a biophysi-cist working in a nearby hospital. This device used high-frequency electricity to heat-seal or cut tissue on contact. This technique was patented in 1931 and has been used for dissection and hemostasis ever since.5

The bipolar electrocautery also paved the way for mi-crosurgery.4 Previously, hemostasis was achieved through a combination of packing, suture ligation, and surgical clips. From the mid-19th century onward, bone wax was used for calvarial hemostasis.16

In 1898 the Italian obstetrician Leonardo Gigli (1863–1908) introduced into neurosurgery a wire saw (“Drahtsäge”), which he initially developed in 1894 dur-ing obstetrics training in Germany.3 The wire saw made craniotomies safer and faster and is still used by neuro-surgeons today. Previously, when larger parts of bone needed to be removed, multiple bur holes were enlarged using forceps or a mallet and chisel, a technique that often resulted in concussions.

The endoscope, first developed in 1853 as a cysto-scope, was used to perform the first endoscopic third ven-triculostomy by Dandy in 1922. The endoscope continued to be developed for use in endonasal and other skull base approaches.36 Another important tool, the surgical micro-scope, based on the microscopes invented during the late 16th century, was introduced in 1921. However, it was not used by neurosurgeons until the late 1950s. Alongside these technical advances, surgical technique also improved, al-lowing for the first successful removal of a brain tumor in 1887 by William W. Keen Jr. (1837–1932).30

The evolution of surgery from a risky endeavor to an

Fig. 1. A cranium from the Andahualyas province, Peru (~ 1000–1200 ad) demonstrating trepanations made by scraping (upper left inset shows evidence of healing) and by drilling multiple small holes (likely postmortem to practice and optimize technique). Reproduced from Kurin DS: Trepanation in South-Central Peru during the early late in-termediate period (ca. AD 1000-1250). Am J Phys Anthropol 152:484–494, 2013. Used with permission from John Wiley & Sons.

Unauthenticated | Downloaded 02/15/21 09:12 PM UTC

Neurosurg Focus / Volume 36 / April 2014

The evolution of neurosurgical approaches

3

evidence-based profession was acknowledged by the sci-entific 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 ap-proaches 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 cranioto-mies 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 not always be the ones who first described or establish these approaches. In the following paragraphs, we de-scribe the development of some of the many neurosurgi-cal approaches (Fig. 3). Although we only mention some of their pioneers, many neurosurgeons have contributed and continue to contribute to the development of our field.

Microsurgery was first propagated by plastic sur-geons and otolaryngologists and was introduced to neu-rosurgery by Theodore Kurze (1922–2002) in 1957. In the 1960s, fellow neurosurgeons, including Raymond M. P. Donaghy (1910–1991) and Mahmut Gazi Yaşargil (b. 1925), actively established microneurosurgery.22 The use of the microscope allowed for surgical access to regions with complex anatomy such as the skull base with its tight networks of vessels and nerves. Use of the microscope led to the development of new approaches and sophisticated modifications.26

The gradual development and subsequent modifi-cations of surgical approaches is well illustrated by the pterional approach. Popularized by Yaşargil in 1969 for

intracranial aneurysms, it soon became one of the most widely used approaches in neurosurgery because of the access it provides not only to the anterior circulation but also to lesions of the sellar region, cavernous sinus, and anterior and middle cranial fossae. This approach had its origins in the frontotemporal craniotomy described by George J. Heuer (1882–1950), Krause, and Dandy in the beginning of the 20th century. As more tools became available tools and surgical skills improved, the pterional approach was modified to include removal of the supra-orbital rim (Charles Frazier, 1870–1936),12 removal of the zygomatic arch (Cushing), or combined with the orbitozy-gomatic approach.

Similar progression can be seen in the lateral and posterior approaches. While Krause described the sub-temporal craniotomy as early as 1911, it was Charles Drake (1920–1998) who popularized the approach and described new variations and modifications. The operat-ing 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) became the first to use a transsphenoidal approach32 to re-move a pituitary tumor. This technique was adapted and modified by Cushing8 and others who laid the important

Fig. 2. Intraoperative photograph illustrating a translabyrinthine ap-proach facilitated by power tools, including the hand-held drill, allowing for the fast and precise removal of compact bone.

Fig. 3. Schematic illustration showing examples of typical neurosur-gical approaches. From left to right: orbitozygomatic approach, transpe-trosal approach, far-lateral approach.

Unauthenticated | Downloaded 02/15/21 09:12 PM UTC

M. Ottenhausen et al.

4 Neurosurg Focus / Volume 36 / April 2014

groundwork for further development. Austrian otorhino-laryngologist Oskar Hirsch (1877–1965) was the first to describe an endonasal approach in 1910.19 While this ap-proach was nearly abandoned in the following decades due to high morbidity from infection, the introduction of the microscope and improved imaging techniques led to its renaissance in the late 1960s. Since then, this has been one of the most dynamic areas of neurosurgery. Today, the endonasal route is used for extended approaches to reach lesions even beyond the sellar region.20 While the microscope led to the reemergence of this approach, the endoscope extended its limits.

Although the time of revolutions may appear to be over, the constantly increasing knowledge and techno-logical progression continue to influence neurosurgical approaches to the brain and skull base. Intraoperative MRI and neuronavigation are only a few of many recent advances that have enhanced the practice of standardized neurosurgical approaches. The presence of microsurgical and skull base laboratories (Fig. 4) in neurosurgical edu-cation and research enable surgeons to push the frontiers of neurosurgery.

ConclusionsThe development of cranial approaches is driven

and influenced by new scientific discoveries. Although most approaches have been around for nearly a century, their widespread use and efficacy is only possible due to advances in technological advancement and scientific knowledge. Simple bur holes and extradural approaches have developed into an extensive intradural technique and into minimally invasive and microneurosurgery.

Acknowledgment

We thank Danielle S. Kurin, Ph.D., visiting assistant professor at the Department of Anthropology, University of California Santa Barbara, for providing the photograph of a trepanned skull from the Andahuaylas province, Peru.

Disclosure

The authors report no conflict of interest concerning the mate-rials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Ottenhausen. Drafting the article: Ottenhausen, Bodhinayake. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Bernardo. Study supervision: Bernardo.

References

1. Aciduman A, Belen D: The earliest document regarding the history of cranioplasty from the Ottoman era. Surg Neurol 68:349–353, 2007

2. Arnott R, Finger S, Smith CUM: Trepanation: History, Dis-covery, Theory. Lisse, The Netherlands: Swets & Zeitlinger, 2003

3. Brunori A, Bruni P, Greco R, Giuffré R, Chiappetta F: Cel-ebrating the centennial (1894-1994): Leonardo Gigli and his wire saw. J Neurosurg 82:1086–1090, 1995

4. Bulsara KR, Sukhla S, Nimjee SM: History of bipolar coagu-lation. Neurosurg Rev 29:93–96, 2006

5. Carter PL: The life and legacy of William T. Bovie. Am J Surg 205:488–491, 2013

6. Choong C, Kaye AH: Emil Theodor Kocher (1841-1917). J Clin Neurosci 16:1552–1554, 2009

7. Clower WT, Finger S: Discovering trepanation: the contribu-tion of Paul Broca. Neurosurgery 49:1417–1426, 2001

8. Cohen-Gadol AA, Liu JK, Laws ER Jr: Cushing’s first case of transsphenoidal surgery: the launch of the pituitary surgery era. J Neurosurg 103:570–574, 2005

9. Elhadi AM, Kalb S, Martirosyan NL, Agrawal A, Preul MC: Fedor Krause: the first systematic use of X-rays in neurosur-gery. Neurosurg Focus 33(2):E4, 2012

10. Finger S, Clower WT: Victor Horsley on “trephining in pre-historic times.” Neurosurgery 48:911–918, 2001

11. Finger S, Fernando HR: E. George Squier and the discovery of cranial trepanation: a landmark in the history of surgery and ancient medicine. J Hist Med Allied Sci 56:353–381, 2001

12. Frazier CH: I. An approach to the hypophysis through the an-terior cranial fossa. Ann Surg 57:145–150, 1913

13. Ganz JC: Trepanation and surgical infection in the 18th cen-tury. Acta Neurochir (Wien) 156:615–623, 2013

14. Goodrich JT: A millennium review of skull base surgery. Childs Nerv Syst 16:669–685, 2000

15. Gross CG: A Hole in the Head: More Tales in the History of Neuroscience. Cambridge, MA: MIT Press, 2009

16. Gupta G, Prestigiacomo CJ: From sealing wax to bone wax: predecessors to Horsley’s development. Neurosurg Focus 23(1):E16, 2007

17. Hanigan WC, Ragen W, Foster R: Dryander of Marburg and

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.

Unauthenticated | Downloaded 02/15/21 09:12 PM UTC

Neurosurg Focus / Volume 36 / April 2014

The evolution of neurosurgical approaches

5

the first textbook of neuroanatomy. Neurosurgery 26:489–498, 1990

18. Hippocrates: On Head Wounds. Maury Hanson, trans. Ber-lin: Akademie Verlag, 1999

19. Hirsch O: Endonasal method of removal of hypophyseal tu-mors with report of two successful cases. JAMA 55:772–774, 1910

20. Kanter AS, Dumont AS, Asthagiri AR, Oskouian RJ, Jane JA Jr, Laws ER Jr: The transsphenoidal approach. A historical perspective. Neurosurg Focus 18(4):E6, 2005

21. Kawase T, Shiobara R, Toya S: Anterior transpetrosal-trans-tentorial approach for sphenopetroclival meningiomas: surgi-cal method and results in 10 patients. Neurosurgery 28:869–876, 1991

22. Kriss TC, Kriss VM: History of the operating microscope: from magnifying glass to microneurosurgery. Neurosurgery 42:899–908, 1998

23. Kurin DS: Trepanation in South-Central Peru during the early late intermediate period (ca. AD 1000-1250). Am J Phys An-thropol 152:484–494, 2013

24. Ligon BL: Biography: history of developments in imaging techniques: Egas Moniz and angiography. Semin Pediatr In-fect Dis 14:173–181, 2003

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-tory of acoustic neurinoma surgery. Neurosurg Focus 18(4): E9, 2005

27. Missios S: Hippocrates, Galen, and the uses of trepanation in the ancient classical world. Neurosurg Focus 23(1):E11, 2007

28. Mogliazza S: An example of cranial trepanation dating to the Middle Bronze Age from Ebla, Syria. J Anthropol Sci 87:187–192, 2009

29. Papagrigorakis MJ, Toulas P, Tsilivakos MG, Kousoulis AA, Skorda D, Orfanidis G, et al: Neurosurgery during the Bronze Age: a skull trepanation in 1900 BC Greece. World Neuro-surg [epub ahead of print], 2013

30. Ray BS: The development of neurosurgery in New York City. Bull N Y Acad Med 55:916–938, 1979

31. Sanan A, Haines SJ: Repairing holes in the head: a history of cranioplasty. Neurosurgery 40:588–603, 1997

32. Schmidt RF, Choudhry OJ, Takkellapati R, Eloy JA, Couldwell WT, Liu JK: Hermann Schloffer and the origin of transsphe-noidal pituitary surgery. Neurosurg Focus 33(2):E5, 2012

33. Shoja MM, Agutter PS, Loukas M, Shokouhi G, Khalili M, Farhoudi M, et al: Cranioplasty in medieval Persia and the potential spread of this knowledge to Europe. Childs Nerv Syst 28:1993–1996, 2012

34. Voorhees JR, Cohen-Gadol AA, Laws ER, Spencer DD: Bat-tling blood loss in neurosurgery: Harvey Cushing’s embrace of electrosurgery. J Neurosurg 102:745–752, 2005

35. Westhorpe R: William Morton and the first successful demon-stration of anaesthesia. Anaesth Intensive Care 24:529, 1996

36. Zada G, Liu C, Apuzzo ML: “Through the looking glass”: optical physics, issues, and the evolution of neuroendoscopy. World Neurosurg 77:92–102, 2012

Manuscript submitted December 3, 2013.Accepted February 21, 2014.Please include this information when citing this paper: DOI:

10.3171/2014.2.FOCUS13547. Address correspondence to: Antonio Bernardo, M.D., Microneu-

rosurgery Skull Base Laboratory, Weill Cornell Medical College, NewYork-Presbyterian Hospital, 525 E. 68th St., New York, NY 10065. email: anb2029@med.cornell.edu.

Unauthenticated | Downloaded 02/15/21 09:12 PM UTC