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GENERAL

Legacy

THE EVOLUTION OF INTRAMEDULLARY


SPINAL CORD TUMOR SURGERY
Daniel M. Sciubba, M.D. OBJECTIVE: Resections of intramedullary spinal cord tumors were attempted as early
Department of Neurosurgery, as 1890. More than a century after these primitive efforts, profound advancements in
The Johns Hopkins University,
Baltimore, Maryland
imaging, instrumentation, and operative techniques have greatly improved the mod-
ern surgeon’s ability to treat such lesions successfully, often with curative results.
Daniel Liang, M.D. METHODS: We review the history of intramedullary spinal cord tumor surgery, as well
Department of Neurosurgery, as the evolution and advancement of technologies and surgical techniques that have
University of Maryland, defined the procedure over the past 100 years.
Baltimore, Maryland
RESULTS: Surgery to remove intramedullary spinal cord tumors has evolved to include
Karl F. Kothbauer, M.D. sophisticated imaging equipment to pinpoint tumor location, laser scalpel systems to
Division of Neurosurgery, provide precise incisions with minimal damage to surrounding tissue, and physiolog-
Kantonsspital Luzern, ical monitoring to detect and prevent intraoperative motor deficits.
Lucerne, Switzerland
CONCLUSION: Modern surgical devices and techniques have developed dramatically
Joseph C. Noggle, B.S.
with the availability of new technologies. As a result, continual advancements have
Department of Neurosurgery,
been achieved in intramedullary spinal cord tumor surgery, thus increasing the safety
The Johns Hopkins University, and effectiveness of tumor resection, and progressively improving the overall outcomes
Baltimore, Maryland in patients undergoing such procedures.
KEY WORDS: History, Intramedullary, Spinal cord, Surgery, Tumor
George I. Jallo, M.D.
Department of Neurosurgery, Neurosurgery 65[ONS Suppl 1]:ons84–ons92, 2009 DOI: 10.1227/01.NEU.0000345628.39796.40
The Johns Hopkins University,
Baltimore, Maryland

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

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HISTORY OF INTRAMEDULLARY SPINE TUMOR SURGERY

first successful resection of ments, hemostasis with hot


an intramedullary tumor of saline packings, and then
the spinal cord. His patient multilevel laminectomies.
was a 27- year- old woman They found no epidural
with progressive paraparesis lesions, so they continued to
and back pain in the supine explore the intradural space.
position. Based on transla- While opening the dura, they
tion from the original report accidentally nicked the pos-
in German, he began with a terior aspect of the spinal
laminectomy of T7 and T8, cord in 2 areas. Upon closer
then extended the opening to examination, Elsberg noticed
T10, and eventually cranially abnormal-appearing tissue
to T6. Upon opening the extruding from the myelo-
dura in the upper portion of tomy incisions. He pro-
this exposure, he noted an ceeded to connect these 2
enlargement of the cord and defects and lengthen the
a blue oval tumor on the myelotomy. With an im - FIGURE 2. Portrait of Charles A.
right side covered by a thin proved view of the abnormal Elsberg. (Reprinted with permis-
translucent layer of spinal tissue, he concluded that it sion from Horwitz NH: Charles A.
cord. The tumor, measuring represented some sort of Elsberg [1871–1948]. Neurosurgery
4 ⫻ 1 cm, was removed with tumor within the cord. At 40:1315–1319, 1997.)
“blunt” dissection. The dura this point, the surgery was
was closed with catgut su- FIGURE 1. Portrait of Anton von interrupted by hemodynamic instability of the patient, so
tures and the wound closed Eiselsberg. (From the Clendening Elsberg ceased manipulating the spinal cord and closed the
with 4 drainage tubes in - Library Portrait Collection, The wound. It would be a week later before the patient would be
serted. The histology was University of Kansas Medical healthy enough to undergo reoperation.
described as “neurofibrosar- Center, Kansas City, Kansas.) During the second surgery, it turned out that Elsberg was sur-
coma.” A cerebrospinal fluid prisingly lucky. After reopening the wound and dura, he found
leak is described, but the patient apparently recovered, as it is that the tumor mass had “extruded itself.” The majority of the
noted that she was able to walk 22 months after surgery. The last tumor had pushed its way out of the cord, allowing relatively
follow-up evaluation noted, in September 1913, approximately easy separation from the cord with minimal manipulation. The
6 years after surgery, indicated that the patient was “well” and excised tumor was confirmed by pathology to be a gliosarcoma.
“able to go on long walks” (19). Thus, this has been credited as The patient did well and went on to regain most motor function
the first successful spinal cord tumor resection (21, 42). with the help of rehabilitation by 8 months postoperatively.
In the midst of various reports from the end of the first decade Elsberg’s second case with a similar history benefited from
of the 20th century (43, 63), the work of a pioneering New York the earlier experience. In this case, Elsberg did not hesitate and
City surgeon, Charles A. Elsberg (Fig. 2), stands out. He was decided to operate before the patient worsened to an even
2 years younger than Harvey Cushing and had also undergone greater degree. Using his standard approach, he noted an
the then-traditional training pattern of his American colleagues enlargement of the cord and made a midline myelotomy over
by traveling to Europe to apprentice under established general the most prominent area of spinal cord bulging. Similar to his
surgeons (33). By 1909, he had established himself as an expert other patient, he again witnessed an abnormally appearing
in cranial and spinal surgery and published several reviews mass immediately extruding itself through the myelotomy inci-
about his experiences. Then, several months later in 1910, he sion. Because the lesion appeared to be well encapsulated and
came upon 2 patients who would later become his first experi- had already delivered itself, he decided it would be amenable
ences with intramedullary spinal cord tumors. to immediate resection. He then proceeded to dissect the
These 2 patients were referred to him for evaluation because remaining attachments and removed the tumor en bloc. This
of their progressive back pain and deteriorating motor and sen- entire operation lasted less than 40 minutes. Unfortunately,
sory functioning, presumably caused by a spinal tumor. He shortly after surgery, this patient developed severe respiratory
believed the pathology was localized in or around the spinal distress and died a few hours later. Interestingly, the post-
cord and that the pathology was most likely a mass lesion, per- mortem examination revealed no wound or spinal cord
haps a tumor, which could be surgically removed to provide hematomas that could explain the rapid death of this patient.
improved clinical status.
Elsberg and his assistant, Edwin Beer, proceeded to explore THE “TWO-STAGE OPERATION”
the spinal canal and report their findings (23). They approached
the canal in their “usual fashion,” consisting of a midline incision After comparing his first 2 outcomes after intramedullary
over the spinous processes, dissection down to the bony ele- spinal cord tumor resection, Elsberg attributed the poor outcome

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SCIUBBA ET AL.

A B

FIGURE 4. Greenwood’s original setup using a monopo-


C lar unit to power coagulation forceps. (Reprinted with
permission from Malis LI: Electrosurgery and bipolar
technology. Neurosurgery 58 [1 Suppl] ONS1–12,
FIGURE 3. Illustrations of 2006.)
Elsberg’s “two-stage operation” for
removal of spinal cord tumors, in
his 1913 manuscript entitled, sure to cause grave injury to the cord. He must leave
“Experiences in Spinal Surgery, it to nature to extrude the tumor. As the normal
Observations upon 60 Laminec- intramedullary pressure will tend to readjust itself,
tomies for Spinal Disease” (23). the growth, which has caused an increased pressure,
(From World Spine Journal.)
will be gradually pushed out of its bed. Nature will
do this by a slow and gradual process, and the tumor
will be slowly extruded, with a minimum of injury of
nerve fibers. Therefore, after the small incision into
the cord has been made, the muscles and skin must be
in his second patient to manipulation of the spinal cord sub- closed and the actual removal of growth left to a sec-
stance during a more aggressive dissection. Thus, he concluded ond operation. After about one week the wound is
that this operation would be safest if done in a “two-stage” man- reopened and the tumor, which will in all probability
ner (Fig. 3). The following excerpt from an article on his initial be found outside of the cord, can be removed by
experiences summarizes “the method of extrusion” (23): dividing the few adhesions which remain. If the
manipulations are done with delicacy and care, no
The above two operations for intra medullary
injury should be done to the cord substance.
tumors of the spinal cord demonstrate that localized
growths of the cord substance must not be considered This was the very first real surgical concept for the resection
as inoperable. They should be attacked by the neuro- of intramedullary tumors. It can be regarded as a relatively
logical surgeon as readily as subcortical safe and conservative approach given the lack of specialized
equipment surgeons had at their disposal, and for today’s stan-
Based on the anatomic grounds stated above, the writers
dards, amazing diagnostic uncertainty. Elsberg’s first book,
suggest the following method of treatment for intramedullary
Diagnosis and Treatment of Surgical Diseases of the Spinal Cord and
tumors of the cord:
Its Membranes, was published in 1916. It had a widespread
If after laminectomy and incision of the dura the influence at the time and remains an impressive publication to
surgeon finds that he has to deal with a localized this day (33). The two-stage operation is still occasionally used
intramedullary growth, he should make a small inci- today under certain circumstances, such as unclear intraoper-
sion, about 1 cm long, in the posterior median col- ative pathology or poor identification of a clear surgical plane
umn a few millimeters outside of the posterior between tumor and cord (1).
median fissure, at the spot where the growth seems to
be nearest the surface of the cord. The incision should BIPOLAR CAUTERY
be deep enough to cut the pia and the substance of the
column down to the tumor. The tumor will then begin In the late 1930s, James Greenwood, Jr., began using a tech-
to bulge through the incision. No matter how nique at the Methodist Hospital in Houston that he termed the
markedly the tumor will seem to bulge, the surgeon “two-point coagulation forceps” (29, 30) (Fig. 4). This technology
must not attempt to remove the growth, for he will be was later refined by Leonard Malis, and eventually became what

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HISTORY OF INTRAMEDULLARY SPINE TUMOR SURGERY

TABLE 1. Chronology of advancements in intramedullary spinal cord tumor surgerya


Year Surgeon Advancement
1907 Anton Freiherr von Eiselsberg First to resect an intramedullary spinal tumor and confer neurological improvement
1910 Charles A. Elsberg Two-stage technique
1940 James Greenwood, Jr. Two-point coagulation forceps
1954 Greenwood’s first series of intramedullary tumor resections showing long-term success
1957 Theodore Kurze First neurosurgeon to use a microscope in the operating room
1966 Hubert L. Rosomoff First to report use of a ruby laser for surgery on a brain tumor
1977 Raymond V. Damadian Demonstrated MRI of the whole body in a human
1978 Flamm and Ransohoff Ultrasonic ablator used for brain tumors
1982 Fred Epstein Ultrasonic ablator used for spinal cord tumors
1980–1983 Chandler and Knake, Rubin and Contemporaneously pioneered intraoperative use of ultrasound (imaging) for brain
Dohrmann, and Masuzawa et al. and spinal surgery
1983 MRI used commercially for imaging intramedullary spinal cord tumors
1986–1989 MEP monitoring used for neurosurgical operations on the spinal cord
1993 Fred Epstein Reports on plated bayoneted forceps to retract normal spinal cord when resecting an
intramedullary tumor
2002 George I. Jallo First report on Nd:YAG contact laser for intramedullary spinal tumors
a
MRI, magnetic resonance imaging; MEP, motor evoked potential; Nd:YAG, neodymium:yttrium-aluminum-garnet.

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

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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-

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HISTORY OF INTRAMEDULLARY SPINE TUMOR SURGERY

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

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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.

intradural spinal tumors was published (36). Among the advan-


tages of the laser scalpel over freestanding, noncontact, laser REFERENCES
beam are the following: 1) beam alignment, 2) better energy uti-
1. Benzel EC, Mirfarkhraee M, Hadden T, Fowler M: Holocord astrocytoma: A
lization with minimal loss of thermal energy, 3) tactile feedback, two-staged operative approach. Spine 12:746–749, 1987.
4) control of movements as with other microinstruments, and 5) 2. Bloch F: Nuclear induction. Phys Rev 70:460–474, 1946.
minimal to no associated smoke and carbonization of tissue 3. Bloch F, Hansen WW, Packard ME: The nuclear induction experiment. Phys
edges. Possibly the greatest advantage of the laser scalpel is Rev 70:474–485, 1946.
4. Boyd SG, Rothwell JC, Cowan JM, Webb PJ, Morley T, Asselman P, Marsden
that it can be used as regular microsurgical instrument.
CD: A method of monitoring function in corticospinal pathways during sco-
Jallo et al. (36) thought that, compared with the bipolar liosis surgery with a note on motor conduction velocities. J Neurol
cautery and arachnoid knife, the laser scalpel provided a finer Neurosurg Psychiatry 49:251–257, 1986.
and more precise incision with less bleeding when performing 5. Bulsara KR, Sukhla S, Nimjee SM: History of bipolar coagulation. Neurosurg
the myelotomy for intramedullary spinal cord tumors. Once Rev 29:93–96, 2006.
6. Buncke HJ: Microsurgery—Retrospective. Clin Plast Surg 13:315–318, 1986.
inside the spinal cord, the scalpel also afforded effective, safe,
7. Chandler WF, Knake JE: Intraoperative use of ultrasound in neurosurgery.
and precise dissection at the glial-tumor interface. During Clin Neurosurg 31:550–563, 1983.
debulking of these lesions, the laser scalpel may also poten- 8. Chandler WF, Knake JE, McGillicuddy JE, Lillehei KO, Silver TM: Intra-
tially minimize mechanical injury to normal spinal cord operative use of real-time ultrasonography in neurosurgery. J Neurosurg
parenchyma compared with the ultrasonic aspirator, which 57:157–163, 1982.
9. Church A, Eisendrath DW: A contribution to spinal cord surgery. Am J Med
relies on vibration and acoustic energy transmission. Further- Sci 103:403–405, 1892.
more, the scalpel may be particularly useful for coagulating 10. Daikuzono N, Joffe SN: Artificial sapphire probe for contact photocoagulation
and vaporizing tumors with a firm texture by minimizing the and tissue vaporization with the Nd:YAG laser. Med Instrum 19:173–178,
amount of manipulation and thermal injury to the surround- 1985.
11. Damadian R: Tumor detection by nuclear magnetic resonance. Science
ing spinal cord as typically observed with use of the bipolar
171:1151–1153, 1971.
and scissors. Finally, the laser scalpel does not produce an 12. Damadian R: Field focusing n.m.r. (FONAR) and the formation of chemical
electrical artifact when used with electrophysiological moni- images in man. Philos Trans R Soc Lond B Biol Sci 289:489–500, 1980.
toring; this benefit is especially important during the continu- 13. Dawson GD: Investigations on a patient subject to myoclonic seizures after
ous recording of MEPs used during the resection of an sensory stimulation. J Neurol Neurosurg Psychiatry 10:141–162, 1947.
14. Dohlman GF: Carl Olof Nylén and the birth of the otomicroscope and micro-
intramedullary tumor.
surgery. Arch Otolaryngol 90:813–817, 1969.
15. Dohrmann GJ, Rubin JM: Intraoperative ultrasound imaging of the spinal
CURRENT STATE OF THE ART cord: Syringomyelia, cysts, and tumors—A preliminary report. Surg Neurol
18:395–399, 1982.
Neurosurgical pioneers early in the 20th century such as von 16. Donaghy RM: The history of microsurgery in neurosurgery. Clin Neurosurg
26:619–625, 1979.
Eiselsberg and Elsberg proved that surgery within the spinal 17. Edelstein WA, Hutchison JM, Johnson G, Redpath T: Spin warp NMR imag-
cord was possible, not mere science fiction. However, the com- ing and applications to human whole- body imaging. Phys Med Biol
plication rates of early techniques worried many neurosur- 25:751–756, 1980.
geons into taking a conservative approach consisting of biopsy, 18. Edelstein WA, Hutchison JM, Smith FW, Mallard J, Johnson G, Redpath TW:
duraplasty, and adjuvant radiation therapy (65). Human whole-body NMR tomographic imaging: Normal sections. Br J
Radiol 54:149–151, 1981.
Throughout the 20th century, the advent of several key tech- 19. Eiselsberg AV: Vienna Weekly Clinics of Surgery [in German] 10:375, 1910.
nologies sparked a revival in the movement toward more 20. Eiselsberg AV: The life’s work of a surgeon [in German]. Innsbruck, Deutscher
aggressive resection of intramedullary tumors. Significant Alpenverlag, 1938.

ons90 | VOLUME 65 | OPERATIVE NEUROSURGERY 1 | DECEMBER 2009 www.neurosurgery-online.com


HISTORY OF INTRAMEDULLARY SPINE TUMOR SURGERY

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
spinal cord tumors [in German]. Arch Psychiatr Nervenkrankh 59:453–461, of motor evoked potentials during surgery for intramedullary spinal cord
1917. tumors. Neurosurgery 41:1327–1336, 1997.
22. El Negamy E, Sedgwick EM: Delayed cervical somatosensory potentials in 51. Norman D, Mills CM, Brant-Zawadzki M, Yeates A, Crooks LE, Kaufman L:
cervical spondylosis. J Neurol Neurosurg Psychiatry 42:238–241, 1979. Magnetic resonance imaging of the spinal cord and canal: Potentials and lim-
23. Elsberg CA, Beer E: The operability of intramedullary tumors of the spinal itations. AJR Am J Roentgenol 141:1147–1152, 1983.
cord. A report of two operations with remarks upon the extrusion of the 52. Nylén CO: The otomicroscope and microsurgery 1921–1971. Acta Otolaryngol
spinal cord. Am J Med Sci 142:636–647, 1911. 73:453–454, 1972.
24. Epstein F, Epstein N: Surgical treatment of spinal cord astrocytomas of child- 53. Patton HD, Amassian VE: Single and multiple-unit analysis of cortical stage
hood. A series of 19 patients. J Neurosurg 57:685–689, 1982. of pyramidal tract activation. J Neurophysiol 17:345–363, 1954.
25. Epstein FJ, Ozek M: The plated bayonet: A new instrument to facilitate sur- 54. Purcell EM, Torrey HC, Pound RV: Resonance absorption by nuclear mag-
gery for intra-axial neoplasms of the spinal cord and brain stem. Technical netic moments in solids. Phys Rev 69:37–38, 1946.
note. J Neurosurg 78:505–507, 1993. 55. Rabi II, Zacharias JR, Millman S, Kusch P: A new method of measuring
26. Epstein FJ, Farmer JP, Schneider SJ: Intraoperative ultrasonography: An nuclear magnetic moment. Phys Rev 53:318, 1938.
important surgical adjunct for intramedullary tumors. J Neurosurg 74:729– 56. Rosomoff HL, Carroll F: Reaction of neoplasm and brain to laser. Arch
733, 1991. Neurol 14:143–148, 1966.
27. Ernst RR, Anderson WA: Application of Fourier transform spectroscopy to 57. Rubin JM, Dohrmann GJ: Use of ultrasonically guided probes and catheters
magnetic resonance. Rev Sci Instrum 37:93–102, 1966. in neurosurgery. Surg Neurol 18:143–148, 1982.
28. Flamm ES, Ransohoff J, Wuchinich D, Broadwin A: Preliminary experience 58. Rubin JM, Dohrmann GJ: Work in progress: Intraoperative ultrasonography
with ultrasonic aspiration in neurosurgery. Neurosurgery 2:240–245, 1978. of the spine. Radiology 146:173–175, 1983.
29. Greenwood J Jr: Two point interpolar coagulation. A new principle and 59. Rubin JM, Aisen AM, DiPietro MA: Ambiguities in MR imaging of tumoral
instrument for applying current in neurosurgery. Am J Surg 50:267–270, 1940. cysts in the spinal cord. J Comput Assist Tomogr 10:395–398, 1986.
30. Greenwood J Jr: Two point coagulation: A follow-up report of a new tech- 60. Rubin JM, Dohrmann GJ, Greenberg M, Duda EE, Beezhold C: Intraoperative
nique and instrument for electrocoagulation in neurosurgery. Arch Phys Ther sonography of meningiomas. AJNR Am J Neuroradiol 3:305–308, 1982.
23:552–554, 1942. 61. Rubin JM, Mirfakhraee M, Duda EE, Dohrmann GJ, Brown F: Intraoperative
31. Greenwood J Jr: Total removal of intramedullary tumors. J Neurosurg ultrasound examination of the brain. Radiology 137:831–832, 1980.
11:616–621, 1954. 62. Saunders ML, Young HF, Becker DP, Greenberg RP, Newlon PG, Corales RL,
32. Greenwood J Jr: Intramedullary tumors of spinal cord. A follow-up study Ham WT, Povlishock JT: The use of the laser in neurological surgery. Surg
after total surgical removal. J Neurosurg 20:665–668, 1963. Neurol 14:1–10, 1980.
33. Horwitz NH: Charles A. Elsberg (1871–1948). Neurosurgery 40:1315–1319, 63. Schultze F: Further contributions for the diagnosis and operative nuances for
1997. neoplasms of the spinal cord dura and spinal cord. Successful operation of a
34. House HP, House WF, Hildyard VH: Congenital stapes footplate fixation; a spinal cord tumor [in German]. Dtsch Med Wochenschr 36:1676, 1912.
preliminary report of twenty-three operated cases. Laryngoscope 68:1389– 64. Taniguchi M, Cedzich C, Schramm J: Modification of cortical stimulation for
1402, 1958. motor evoked potentials under general anesthesia: Technical description.
35. Jallo GI: CUSA EXcel ultrasonic aspiration system. Neurosurgery 48:695–697, Neurosurgery 32:219–226, 1993.
2001. 65. Wood EH, Berne AS, Taveras JM: The value of radiation therapy in the man-
36. Jallo GI, Kothbauer KF, Epstein FJ: Contact laser microsurgery. Childs Nerv agement of intrinsic tumors of the spinal cord. Radiology 63:11–24, 1954.
Syst 18:333–336, 2002. 66. Yaşargil MG, De Preux J: Microsurgical experiments in 12 cases of intra-
37. Kim LY Jr, Day AL, Normann SJ, Abela GS, Mehta JL: The argon contact laser medullary hemangioblastomas [in French]. Neurochirurgie 21:425–434, 1975.
scalpel: A study of its effect on atherosclerosis. Neurosurgery 21:861–866, 67. Young W, Cohen AR, Hunt CD, Ransohoff J: Acute physiological effects of
1987. ultrasonic vibrations on nervous tissue. Neurosurgery 8:689–694, 1981.
38. Kim LY Jr, Roxey TE, Day AL: The argon “contact” laser scalpel: Technical 68. Zentner J: Noninvasive motor evoked potential monitoring during neurosur-
considerations. Neurosurgery 21:858–860, 1987. gical operations on the spinal cord. Neurosurgery 24:709–712, 1989.
39. Knake JE, Chandler WF, McGillicuddy JE, Gabrielsen TO, Latack JT, Gebarski
SS, Yang PJ: Intraoperative sonography of intraspinal tumors: Initial experi-
ence. AJNR Am J Neuroradiol 4:1199–1201, 1983.
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

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SCIUBBA ET AL.

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.

ons92 | VOLUME 65 | OPERATIVE NEUROSURGERY 1 | DECEMBER 2009 www.neurosurgery-online.com

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