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F
rom the rather primitive beginnings of sur- logies developed over the past 100 years,
Reprint requests:
Daniel M. Sciubba, M.D., gery on the nervous system with Victor patients harboring such lesions may benefit
600 North Wolfe Street, Horsley to the current state-of-the-art with from curative resections yielding minimal neu-
Meyer Building 8-161, sophisticated imaging, microsurgery, lasers, and rological deficits (Table 1).
Baltimore, MD 21237. intraoperative neurophysiology, spinal cord
Email: dsciubb1@jhmi.edu
tumor surgery has evolved and benefited from THE BEGINNINGS
Received, August 22, 2008.
general progress of the special field of neurolog-
Accepted, October 23, 2008.
ical surgery and the clinical and scientific contri- The first attempt to remove an intramedul-
butions of a number of bold pioneers. The “two- lary tumor from the spinal cord is thought to
Copyright © 2009 by the stage” technique of Elsberg and Beer (23), have been performed in the year 1890 by
Congress of Neurological Surgeons Greenwood’s “two-point coagulation” (29), the Chicago surgeon Christian Fenger, who oper-
operating microscope, magnetic resonance ated on a 38-year-old man with progressive
imaging (MRI), and the surgical laser are techni- paraparesis at the T4–T5 level. The patient
cal milestones in the advancement of knowl- remained paralyzed and died on postoperative
edge and practice as well as the improvement of day 5 (9). Perhaps other attempts were made,
outcomes in patients with spinal cord tumors. but never recorded. By the end of the 19th cen-
Surgical resection of intramedullary spinal tury, Vienna, the capital of what was then the
cord tumors currently remains one of the more Austro-Hungarian Empire, had become one of
demanding procedures in neurosurgery. How- the premier centers of medical excellence in
ever, because of the techniques and techno- Europe. Anton von Eiselsberg, who chaired the
Department of Surgery at the University of
ABBREVIATIONS: MEP, motor evoked potential; Vienna, was an innovative surgical generalist
MRI, magnetic resonance imaging; Nd:YAG, who ventured into procedures involving the
neodymium:yttrium-aluminum-garnet; NMR,
nervous system (Fig. 1) (20). On November 13,
nuclear magnetic resonance; US, ultrasound
1907, he performed what is believed to be the
A B
is now generally known as bipolar cautery (5, 46), an essential Janssen, Galileo Galilei, and Anton von Leeuwenhoek to its cur-
microneurosurgical dissection and hemostasis technique. It was rent form can be attributed to many pioneers who implemented
far superior to older methods, such as saline hot packs, and it it not only for laboratory work but also for surgical use (44). In
decreased damage to surrounding tissue over monopolar elec- 1848, German machinist Carl Zeiss opened his microscope
trocautery. By allowing electric current to flow between the 2 tips workshop in Jena, Germany. Ernst Abbé, a physicist working
of the forceps, there was less transmission of electricity and its with Zeiss, derived new mathematical formulas, and the two
associated heat to the surrounding tissue. This property greatly began to revolutionize lens making. For the first time, the opti-
facilitated Greenwood’s coagulation of tiny feeding vessels cal qualities of a lens could be predicted and standardized,
specifically in removing tumors from the spinal cord. allowing Zeiss to become the first mass producer of high-
Greenwood’s first series of intramedullary tumor resections quality microscopes. In 1893, he introduced the concept of stere-
was reported in 1954 (31). Not surprisingly, in the 9 of 10 cases opsis with the binocular telescope (44). By the early 1920s, oto-
involving gross total resections, 9 were found to be ependymo- laryngologists began using more advanced dissecting micro-
mas. He then reported a follow-up study in 1963 (32). Of the scope prototypes for otological dissection. Specifically, in 1921,
8 patients who were still living at the time of follow-up, all Maier and Lion published their observations of endolymph
had preserved ambulation with or without crutch assistance. movements in the ears of live pigeons (14). That same year,
From his experience, he concluded that gross total resection Swedish otolaryngologist Carl Nylén built a monocular micro-
should be attempted in tumors with clear cleavage planes, as scope and was the first to use it clinically for treating a patient
may be the case with ependymomas, because of the high with chronic otitis media (52).
chance of neurological improvement and long-term control of In 1922, Holmgren attached a light source to an existing Zeiss
local recurrence. He emphasized the use of bipolar coagulation dissecting microscope, thus introducing the first binocular sur-
to minimize trauma to surrounding neural elements and gical microscope (14). For the next few decades, otolaryngolo-
stressed the importance of identifying and dissecting the cleav- gists in Europe continued to expand and refine the use of the
age plane to differentiate normal cord tissue from the tumor. surgical microscope. In the late 1950s, Howard and William
This was the first series of spinal cord tumor resections House made significant contributions to middle ear surgery
reported that showed long-term beneficial results. via highly successful microscopic temporal bone operations (6,
14, 34). After practicing dissection techniques with the micro-
THE MICROSCOPE scope in the House’s laboratory, Theodore Kurze became the
first neurosurgeon to use a microscope in the operating room
Today, the surgical microscope seems to be an essential instru- (44). In 1957, he removed a neurilemoma from the seventh
ment in the armamentarium of every neurosurgeon. However, nerve of a 5-year-old patient (16). Kurze went on to introduce
its evolution from the simple invention of Hans and Zacharias many neurosurgeons to the operating microscope, including
Robert Rand, J. Lawrence Pool, and Charles Drake. In 1965, et al. (26) proposed that intraoperative sonography had “per-
J. Lawrence Pool became the first neurosurgeon to publish an mitted more complete and better-guided radical resection of
account of aneurysm surgery using the microscope (44). In the spinal cord neoplasms, with improved postoperative quality
late 1960s and the 1970s, M. Gazi Yaşargil and Hugo Krayenbühl of neurological function,” (26, pp 732–733). This was achieved
used the operating microscope for spinal cord pathology. In by improved tumor localization, tumor and cyst characteriza-
1976, Yaşargil published a series involving 12 patients who tion, placement of myelotomy, and tumor resection monitor-
underwent “microsurgical” resection of intramedullary spinal ing, all of which were influenced by the US visualization avail-
hemangioblastomas (66). Since that time, the operating micro- able during surgery.
scope has gone through many stages of evolution, now acting as Regarding tumor localization, extensive exposure of the
an indispensable tool for spinal cord tumor surgeons. spinal cord beyond what is necessary to identify the tumor
had its drawbacks. First, a long laminectomy can potentially
ULTRASONIC ASPIRATOR increase the chance of postoperative spinal deformity. Second,
a long durotomy can increase contamination of the subdural
Ultrasonic aspiration first entered medical use in 1947, orig- or subarachnoid space with epidural debris. Conversely, if
inally developed for removal of dental plaques (35), and has either opening is too limited rostrocaudally, an incomplete
been adapted by various medical fields over the years. It was resection is possible. US has permitted tailoring of exposure
eventually modified and, 30 years after its inception, intro- before opening the dura. When MRI became available, the
duced into neurosurgical use by Flamm et al. (28) who docu- ability to compare the intraoperative echographic image with
mented successful removal of intracranial tumors. Shortly the preoperative magnetic resonance image further improved
thereafter, in 1982, Epstein and Epstein (24) published an arti- exposure planning (59).
cle on its use for spinal cord tumors. As an aid to myelotomy placement, US can be used to localize
The ultrasonic aspirator was found to be effective in localized the posterior midline via identification of spinal cord distortion,
tissue removal via a combination of suction and high-frequency the position of the dorsal root entry zone, and the location of the
vibration (28, 35). Via 2 mechanisms of tissue rupture, removal dentate ligaments. The transverse image can then be used to
of tumor could be accomplished with limited damage to neigh- localize the midline, where the tumor is bulkiest and where the
boring tissue (67). The first mechanism is based on suction. surrounding cord is most splayed, and the sagittal image can be
Aspiration of the tissue brings it to the tip of the instrument used to define the cephalocaudal extent of the myelotomy.
where transmission of acoustic energy leads to fragmentation. Furthermore, if the lesion is associated with a cyst, the myelo-
The second mechanism is local cavitation. Acoustic energy tomy can be started at the cyst-tumor junction in the posterior
transmitted into neighboring tissue causes vapor pockets to midline. Epstein et al. (26) proposed that limiting the myelo-
form around cells in tissues with high water content. Bonds tomy to the extent of the neoplasm was particularly important at
between tissue cells eventually rupture with collapse of these the level of the conus, where cord segments are closely approx-
pockets. Interestingly, tissues with weak intercellular bonds, imated, because an unnecessarily long myelotomy could more
such as tumors and lipomas, have been found to be easy to easily lead to postoperative deficits. Finally, US has allowed
fragment, whereas tissues with strong bonds, such as nerves intraoperative feedback of the extent of tumor resection, espe-
and vessels, are more difficult to destroy (35). Current ultra- cially involving cases of astrocytoma in which the glial-tumor
sonic ablators confer precise localized tissue fragmentation and interface is often difficult to identify visually as the resection
aspiration to within approximately 1 mm of the tip. The small proceeds. The initial US image, which shows an echogenic
working area of intramedullary spinal cord access makes the intramedullary mass can be sequentially compared with subse-
ultrasonic ablator invaluable in seeking to minimize surround- quent images, noting the magnitude of the residual echogenic
ing parenchymal injury. signal, the amount of lateral and ventral cord remaining, and the
presence of residual intratumoral cyst of calcification.
INTRAOPERATIVE ULTRASONOGRAPHY
IMAGING DEVELOPMENT OF MRI
Intraoperative use of ultrasound (US) for brain and spinal MRI is now an indispensable tool for managing intra -
surgery was pioneered contemporaneously in the early 1980s medullary spinal cord tumors. Its early development can be
by Chandler and Knake (7), Chandler et al. (8), Knake et al. attributed to a series of Nobel Prize laureates who have helped
(39–41), Dohrmann and Rubin (15), Rubin and Dohrmann (57, to uncover the behavior of atoms in magnetic fields. Such indi-
58), Rubin et al. (59–61), and Masuzawa et al. (48). In 1980, viduals include Isidor Isaac Rabi (55), who developed the first
Rubin described intraoperative examination of the brain, and basic nuclear magnetic resonance (NMR) device in 1938, and
from 1981 to 1983, all 3 groups described use of US for intra- Felix Bloch (2, 3) and Edward Purcell (54), who conducted more
operative imaging of brain and spinal cord tumors. By the precise NMR experiments that eliminated the need to vaporize,
early 1990s, US was being used consistently by Epstein et al. and thus destroy, the sample in 1945. By 1971, Raymond V.
(26) for all intramedullary tumor resections. In the report on Damadian (11) demonstrated in vitro that an NMR tissue
their series of 186 intramedullary spinal cord tumors, Epstein parameter (T1 relaxation time) of tumor samples was signifi-
cantly higher than normal tissue; in 1973, Paul Lauterbur (45) intact axons. Thus, an amplitude decrease corresponds to a
published “Image formation by induced local interaction: similar decrease in the number of functioning axons. Using D
Examples employing magnetic resonance.” By 1975, Richard R. wave monitoring during intramedullary surgery, Morota et al.
Ernst (27) proposed a method of obtaining NMR-tomographic (50) concluded that MEP monitoring provided a reliable predic-
images using phase and frequency encoding and the Fourier tor of functional outcome intraoperatively.
transform. By changing radiosignals, Ernst succeeded in mak- The use of MEPs recorded from peripheral muscles became
ing the technology more sensitive and easier to interpret. This possible, but it was not until the 1990s, when the “multipulse”
technique formed the basis for current MRI techniques. stimulation technique was developed, that it became a reliable
Perhaps one of the more serendipitous of the technological technique (64). With this development, the blockade of spinal
developments of the 1970s was superconductors. These devices motor neurons by anesthetic mediation was overcome. The
helped to make possible the strong magnetic fields used in muscle MEPs proved particularly useful in spinal cord surgery
MRI. In 1977, Damadian (12) demonstrated MRI of the whole because they have a unique “all-or-none” interpretation profile.
body in a human. In that same year, Mansfield (47) developed D wave and muscle MEPs together are the current standard of
the echo planar imaging technique. With his novel mathemat- intraoperative monitoring for spinal cord surgery, and provide
ical analysis of NMR signals, he improved imaging techniques a safeguard for the surgeon to avoid functional deterioration in
and showed how fast imaging could be achievable. In 1980, the patient.
Edelstein et al. (17, 18) demonstrated imaging of the body using Today, this combination has even allowed surgeons to iden-
Ernst’s technique. A single image could be acquired in approx- tify a “window of warning,” i.e., a neurophysiological correla-
imately 5 minutes using this technique. Such capabilities would tion to a temporary paraparesis. The loss of muscle MEPs dur-
be further developed in later years to produce images at video ing surgery, with preservation of the D wave, correlates to a
rates (30 ms/image). temporary motor deficit. This allows the surgeon to change
By 1983, published accounts of preliminary experience with course, even to stage a tumor resection before a definite irre-
MRI of the spinal cord and intramedullary pathology were versible deficit.
becoming more widespread. Norman et al. (51) described their
results of 17 patients: “The ability to image the cord directly PLATED BAYONETED FORCEPS
rather than indirectly as in myelography, the absence of bone
artifact as in computed tomography, and the multiplanar capa- Among technological advances, even those that are seem-
bilities indicate that MRI will be the procedure of choice in the ingly small, specialized modifications to standard instruments
examination of the spinal cord,” (p 1147). can have immense value. Many intramedullary tumors leave
Since that time, the use of MRI for preoperative diagnosis, only a thin mantle of spinal cord tissue surrounding the grow-
localization, and operative planning has been of paramount ing mass. Functional tracts stretched within this mantle can be
importance in managing intramedullary spinal cord tumors. damaged with cord manipulation during surgery. In the early
1990s, surgeons began using bayoneted forceps with shovel-
INTRAOPERATIVE NEUROPHYSIOLOGICAL like plates instead of tips to retract normal spinal cord when
MONITORING resecting an intramedullary tumor. The modified “plated bay-
onet” forceps have rounded, flat tips measuring approximately
In 1947, Dawson (13) recorded the first use of somatosensory 4 mm in diameter (25). This creates a larger tip profile, and the
evoked potentials; in 1978, a description of the first use of distracting forces of the forceps are transmitted to the tissue
somatosensory evoked potentials during spinal surgery was across a larger area compared with that of traditional cylindri-
published (22). In 1980, the first successful transcranial electri- cally tapered tips, leading to a lower and less focal pressure
cal motor cortex stimulation in humans was reported (49). With transmission to tissue. Intrinsic prying action of the forceps
these achievements, a wave of work emerged during the 1980s then allows gentle opening of the myelotomy, improving the
to develop feasible techniques to continuously record motor exposure without increasing spinal cord trauma.
evoked potentials (MEPs). One of the early reports describes its
use in scoliosis surgery (4). In 1989, Zentner (68) reported on his SURGICAL LASER
series of 50 patients who had undergone MEP monitoring dur-
ing neurosurgical operations on the spinal cord. He noted that In a laser scalpel system, energy is transmitted through a
postoperative neurological complications coincided with per- flexible fiber cable to a coated sapphire crystal probe tip. The
manent reduction in amplitudes of more than 50% of the base- laser beam resides only within the sapphire tip, and the ther-
lines in every case. mal energy is delivered to the tissue only on direct contact.
Initially, motor pathway monitoring could use only one neu- Use of the contact laser scalpel in neurosurgery was initially
rophysiological modality, the D wave (53). The D wave results described in experimental studies on rabbits (38). In these stud-
from direct activation of large-diameter corticospinal axons ies, carotid endarterectomy was performed using a contact
through transcranial cortical stimulation with an electric cur- laser scalpel attached to an argon laser and the laser energy was
rent. The wave is recorded over the spinal cord distal to the sur- delivered through a sapphire crystal tip (37). This laser scalpel
gical site, and its amplitude is a measure of the number of system allowed for precise delivery of the laser energy to the
targeted tissue, producing minimal damage to adjacent healthy advancements, which are now routinely used for surgical resec-
structures. Furthermore, it provided tactile feedback on the tion, have included the development of bipolar cautery (1940s),
depth of laser penetration and the amount of pressure applied. operating microscope (1950s), the ultrasonic aspirator (1970s),
With these findings, the authors suggested that the laser intraoperative US (1980s), MRI (1980s), MEPs for intraoperative
scalpel’s ability for producing fine, precise, hemostatic inci- monitoring (1990s), plated bayoneted forceps (1990s), and the
sions made it potentially useful for making spinal cord inci- Nd:YAG contact surgical laser (2000s). These tools together
sions or removing tumors from adjacent critical structures. with ever-increasing experience in microsurgical techniques
In 1966, Rosomoff and Carroll (56) were the first to report the have enabled modern-day surgeons to provide more complete
use of a ruby laser for surgery on a brain tumor. In the 1970s, the resections while minimizing neurological damage. Patients
neodymium:yttrium-aluminum-garnet (Nd:YAG) laser was with intramedullary tumors can now receive an earlier diagno-
introduced into the medical field (62). Nd:YAG and argon lasers sis of their condition and benefit from lengthened progression-
use a fiberoptic cable to transmit light. In 1984, sapphire tips free survival with less neurological injury.
were attached to the quartz fiber of the Nd:YAG laser (10). As a
result, the laser beam resides entirely within the crystal, and Disclosure
laser energy is only delivered to tissue on direct contact. In 2002, George Jallo, M.D., has received educational grants from Codman and
the first report on the clinical use of the Nd:YAG laser scalpel in Medtronics. The other authors have no personal financial or institutional inter-
contact mode as a surgical scalpel for dysraphic conditions and est in any of the drugs, materials, or devices described in this article.
21. Eiselsberg AV, Marburg O: The question of the operability of intramedullary 50. Morota N, Deletis V, Constantini S, Kofler M, Cohen H, Epstein FJ: The role
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COMMENTS
40. Knake JE, Chandler WF, McGillicuddy JE, Silver TM, Gabrielsen TO:
Intraoperative sonography for brain tumor localization and ventricular shunt
placement. AJR Am J Roentgenol 139:733–738, 1982. T his historical vignette is of great value for all neurosurgeons inter-
ested in spinal cord tumor surgery. We should never forget or
ignore the tremendous work of the pioneers who started such difficult
41. Knake JE, Gabrielsen TO, Chandler WF, Latack JT, Gebarski SS, Yang PJ:
Real-time sonography during spinal surgery. Radiology 151:461–465, 1984. surgery without bipolar coagulation, the microscope, ultrasonic aspira-
42. Koos WT, Day JD: Neurological surgery at the University of Vienna. tion, magnetic resonance imaging, evoked potentials, laser, or ultra-
Neurosurgery 39:583–587, 1996. sound. They succeeded to remove intramedullary tumors in spite of the
43. Krauss WC: Three cases of spinal cord tumor observed within a period of ten lack of all our modern tools, and they improved several of their
days. J Nerv Ment Dis 4:222–236, 1910. patients. I am in profound admiration with our pioneers. Thanks to
44. Kriss TC, Kriss VM: History of the operating microscope: From magnifying
them, neurosurgery makes happen miracles today. But, one should not
glass to microneurosurgery. Neurosurgery 42:899–908, 1998.
forget that the best tools remain of no benefit in the hands of inexperi-
45. Lauterbur PC: Image formation by induced local interactions: Examples
employing nuclear magnetic resonance. Nature 242:190–191, 1973. enced neurosurgeons and that experience remains the most important
46. Malis LI: Electrosurgery and bipolar technology. Neurosurgery 58:ONS1– condition to remove with success those tumors with preservation of
ONS12, 2006. quality of life in spinal cord tumor surgery
47. Mansfield P: Multi-planar image formation using NMR spin echoes. J Phys
Jacques Brotchi
C Solid State Phys 10:L55–L58, 1977.
Brussels, Belgium
48. Masuzawa H, Kamitani H, Sato J, Inoya H, Hachiya J, Sakai F: Intraoperative
application of sector scanning electronic ultrasound in neurosurgery [in
Japanese]. Neurol Med Chir (Tokyo) 21:277–285, 1981.
49. Merton PA, Morton HB: Stimulation of the cerebral cortex in the intact human
subject. Nature 285:227, 1980.
T he origins of modern neurosurgery date to the end of the 19th cen-
tury when some very adventurous individuals developed the nec-
essary early skills and techniques for brain surgery. Surgery on the
spine for intramedullary tumors had to wait until the beginnings of by radiation therapy, to sophisticated surgical resections that simulta-
the 20th century with the pioneering works of von Eiselberg in Vienna neously results in “cure” and in high quality neurological outcomes.
and Elsberg in New York City. The authors have provided a superb Hence, it is of paramount importance for all of us to understand how
overview of what evolved over time in both personalities and surgical we got here. We can then do a better job from where we stand and
techniques to make spine surgery safer. Not only do we have a biog- strive to achieve more; much, much, more. For the insight provided, the
raphical review of some of the key characters, but also insight into the authors are to be heartily congratulated.
various instrumentations and diagnostic techniques. As this group of Edward C. Benzel
authors have been some of the key leaders in this field of intra- Cleveland, Ohio
medullary spinal surgery, whom better to accomplish this task. The
neurosurgical resident today is most likely little aware of these impor-
tant early accomplishments, so hopefully this review will alleviate
that ignorance for those who read this elegant article. My compli-
T he authors have done a beautiful job recanting the history and evo-
lution of a classical neurosurgical operation. Because the original
documents of the early surgical procedures were not written in English,
ments are offered to the authors for taking the time to put together this this article will serve to immortalize some of those key initial observa-
important piece. tions and techniques that have since evolved into the safer methods
James T. Goodrich that we use today. Upon reading these accounts of spinal intra -
Bronx, New York medullary tumor surgery performed a century ago, one cannot help
but be in awe of the courage, tenacity, and technical skills of our surgi-
cal forefathers. I thank Sciubba et al. for providing us with this hum-
S ciubba et al. have provided a wonderful review of the history of
intramedullary spinal cord tumor surgery. The management of
intramedullary spinal cord tumors has come a long way in the past sev-
bling and enlightening document.
Michael Y. Wang
eral decades, from the biopsy (“peak and shreak”) approach followed Miami, Florida
A B C
Anteroposterior/middle cerebral artery (MCA). A, view of a left carotid angiog- tion of the same carotid angiography shown in A. Because of the superimpo-
raphy depicting an aneurysm arising proximal to the genu of the MCA, in the sition of the vessels, it is difficult to visualize the aneurysm. C, Angiography-
distal half of the M1 and pointing superiorly in this projection. B, lateral projec- computed tomographic depicting the aneurysm (arrow) shown in A.