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DOI 10.1007/s10143-011-0345-2
ORIGINAL ARTICLE
Received: 12 September 2010 / Revised: 26 March 2011 / Accepted: 1 May 2011 / Published online: 6 August 2011
# Springer-Verlag 2011
Abstract Multisegment intramedullary spinal cord tumors difference in initial symptoms of patients (Z=−2.08, P=0.04)
(MSICT) are a special type of spinal cord tumor. Up to now, no was statistically significant between the two groups. Pain
comparative clinical study of MSICT has been performed with motor weakness and gait deterioration predominated in
according to different age groups. Seventy-seven patients adolescents and decreased in frequency into adulthood where
underwent microsurgery for MSICT. As grouped with two sensory disturbances became more predominant.
different methods, the parametric and nonparametric data of
MSICT and patients were comparatively analyzed using Keywords Spinal cord . Intramedullary tumor .
statistically correlative methods. Forty-eight patients were Multisegments . Years . Initial symptoms . Histological
males and 29 were females, ranging in age from 4 to 64 years classification
(mean, 32.9 years). Among the six groups, being divided
with intervals of 10 years, the whole difference in the initial
symptoms of patients (Z=17.4, P=0.004) and in the Introduction
histological classification of tumors (Z=12.5, P=0.03) was
statistically significant, respectively. Neurodevelopmental Multisegment intramedullary spinal cord tumors (MSICT)
tumor and benign glioma predominated in adolescents and are a special type of spinal cord tumor. Intramedullary
decreased in frequency into adulthood where ependymoma tumor length occupying more than two vertebral bodies is
became more predominant. In the 25 years old grouping considered as a MSICT [18]. Recently, numerous clinical
method, there were 27 adolescent and 50 adult patients. The researches were performed in this field. Many scholars
emphasized that it is necessary for the early surgical
removal of the tumor and the removal must be as complete
as possible [17–19].
All of our clinical studies were permitted by the patients and the In our previous studies, many cases were analyzed and
Ethics Committee of Peking University Third Hospital.
discussed including multisegment intramedullary benign
Electronic supplementary material The online version of this article spinal cord tumors and multisegment intramedullary astro-
(doi:10.1007/s10143-011-0345-2) contains supplementary material, cytomas [18, 19]. It is thought that the growth of the spinal
which is available to authorized users.
column is finalized once people reach adulthood or an age
Z.-y. Wang : J.-j. Sun (*) : J.-c. Xie : Z.-d. Li : C.-c. Ma : of 25 years old and older, which is around the age of bone
B. Liu : X.-d. Chen : T. Yu : J. Zhang
ossification [4]. Up to now, no comparative clinical study of
Department of Neurosurgery, Peking University Third Hospital,
No. 49 Huayuan North RoadHaidian District Beijing 100191, MSICT has been performed in different age groups. Our
People’s Republic of China effort is to find differences in the histological classification,
e-mail: sunjj2008@gmail.com location, long diameter, extent of MSICT removal, initial
symptoms, gender, neurological function, and prognosis of
H.-I. Liao
Department of Orthopedics, Peking University Third Hospital, patients in different age groups. This comparative analysis
Beijing, People’s Republic of China was performed on 77 consecutive cases with MSICT who
86 Neurosurg Rev (2012) 35:85–93
underwent microsurgery in the neurosurgery inpatient monitoring was used. The pia mater was not normally
department of Peking University Third Hospital. reattached at the end of the resection [18].
The extent of tumor removal was categorized into four
different classes according to intraoperative observations
Materials and methods and postoperative enhanced MRI. Cases with total resection
and without residual tumors on postoperative MRI were
This was an analytical study using clinical records. Ethics classified as class 1, resection of around 80% to 90% of
approval was obtained from the Research Ethics Board of tumors was defined as class 2, and resection of around 60%
Peking University Third Hospital to conduct this study. All to 80% of tumors was defined as class 3. All other
subjects were unrelated individuals, and patients or guard- procedures, including decompression and biopsy of the
ians provided written informed consent. tumors, were classified as class 4. The cross section with
the longest diameter of tumor was measured under
Patients microscope intraoperatively. Diameters less than 5.0 cm
were classified as class 1, between 5.1 and 10.0 cm as class
A consecutive series of 78 patients diagnosed with MSICT 2, between 10.1 and 15.0 cm as class 3, and more than
occupying three or more vertebral bodies were admitted in 15.0 cm as class 4.
the neurosurgery inpatient department and 77 patients
underwent microsurgical treatment between Jan. 2002 and Location and histological classification of tumors
Dec. 2009 [18, 19]. Basic demographic data, clinical and
radiological presentation, and intraoperative observations The location of intramedullary spinal cord tumors was
were evaluated. Preoperative neuroimaging including mag- determined based on enhanced MRI scans. The locations
netic resonance imaging (MRI) was performed in all cases. were classified as medulla–cervical, cervical, cervicothora-
Spinal angiography was performed if the MRI suggested a cic, thoracic, thoracolumbar, and lumbar (including lumbo-
possible vascular lesion. sacral) regions. Affected segments of the spinal cord were
recorded. Based on the postoperative hematoxylin and
Group eosin and immunohistochemical stainings, MSICT were
classified as ependymoma, benign gliomas (including
The patients with MSICT were divided into six groups with astrocytoma I–II and oligodendrocytoma), vascular tumors
intervals of 10 years. The parametric and nonparametric (including hemangioblastomas and cavernous angioma),
data in different patient groups were collected prospectively. neurodevelopmental tumors (including lipoma, epidermoid
In addition, when 25 years old and older were considered as cyst, and teratoma), malignant glioma, and neurogenic
an adult standard, 77 patients were divided into adolescent tumors (including neurinoma and cyst).
and adult groups. The parametric and nonparametric data of
MSICT and patients were comparative analyzed using Evaluation of neurological functions
statistically correlative methods within the two different
grouping methods. The improved Japanese Orthopaedic Association (IJOA)
scoring system was used to evaluate preoperative and
Surgical techniques postoperative neurological function of patients. IJOA was
based on the JOA scoring system with the addition of
Seventy-seven patients underwent operation at our institu- scoring stool function as either normal, slightly dysfunction-
tion with an exception of one 13-year-old patient who al, severely dysfunctional, or incontinence. Short-term
refused to accept an open surgery. The operation followed prognosis was assessed by IJOA difference values equal to
the standard procedures for intramedullary spinal cord the postoperative IJOA score minus the preoperative IJOA
tumors. Laminectomy, laminoplasty, and laminectomy with score. Postoperative IJOA scores were evaluated 2 weeks
reinsertion of lamina were performed as exposure methods after the operation. The short-term prognosis of patients was
over the region of the tumor on the basis of preoperative classified into five grades (<−4, −1 to −3, 0, 1–3, and >4)
neurodiagnostic testing. After a midline dural incision, the based on the IJOA difference values. The clinical outcomes
operating microscope was brought into view. A midline were independently analyzed by a blind observer.
myelotomy was then performed and pia traction was
obtained using sutures to the dura. The resection was then Postoperative management
modified based on the tumor dissection plane and the
severity of the infiltration seen on the preoperative MRI and Postoperatively, all patients received a routine flushing dose
intraoperative microscopy. Intraoperative neurophysiologic of methylprednisolone (around 10mg/kg/day depending on
Neurosurg Rev (2012) 35:85–93 87
Table 1 Differences of parametric data in the different age group (x SD; one-way ANOVA test)
Classification 1–9 years 10–19 years 20–29 years 30–39 years 40–49 years 50 ~ years F value P value
Hospitalized days 21±4.08 21.7±3.32 23±5.12 20.2±4.89 20.9±5.12 21.9±7.49 0.54 0.75
Preoperative IJOA scores 15.3±2.36 13.7±3.57 14.8±3.97 12.4±4.87 14.6±3.01 13.1±4.76 0.97 0.44
Postoperative IJOA scores 16.7±2.50 14.7±2.78 15.9±3.51 13.2±4.97 15.0±2.34 13.1±5.0 1.73 0.14
Affected tumor segments 4.3±0.95 4.8±1.79 4.2±1.3 4.6±1.82 4±1.29 3.9±0.54 0.67 0.65
Tumor’s long diameter 11.6±3.92 9.4±3.8 10.8±6.56 12.1±7.22 8.6±5.94 7.4±2.59 1.38 0.24
IJOA difference values 1.4±2.88 1±1.58 1.1±2.39 0.7±1.36 0.4±1.76 −0.1±3.17 0.67 0.65
88 Neurosurg Rev (2012) 35:85–93
Class 1 resection for tumor was obtained in 36 (46.8%) difference in the extent of tumor removal was statistically
cases, class 2 resection in 14 (18.2%) cases, class 3 in 11 insignificant in the different age groups within the two
(14.2%) cases, and class 4 in 16 (20.8%) cases. The different grouping methods.
Neurosurg Rev (2012) 35:85–93 89
Initial symptoms between the different groups astrocytoma I–II, predominated in adolescents and de-
creased in frequency into adulthood, which then ependy-
The most common initial symptom was pain (39.0%, 30 out moma became more predominant (Fig. 2).
of 77), followed by sensory disturbance (36.4%, 28 out of
77), limb weakness (18.2%, 14 out of 77), gait deterioration Neurological function between the different groups
(5.2%, 4 out of 77), and sphincter dysfunction (1.2%, 1 out
of 77) (Tables 2 and 4) [18]. Age and initial symptoms have The preoperative IJOA scores of the patients were 13.9±
prognostic significance (Z=17.4, P=0.004). Children, ado- 4.06, postoperative IJOA scores were 14.6±3.99, and IJOA
lescent, and younger patients tended to present with pain. difference values were 0.7±2.20 (Tables 1, 2, 3 and 4). The
Older patients mostly presented with sensory disturbance differences of the preoperative IJOA scores, postoperative
(Fig. 1). IJOA scores, and IJOA difference values were statistically
In the 25 years old grouping method, the difference of insignificant in the different age groups within the two
initial symptoms was statistically significant between the different grouping methods.
adolescent group and the adult group (Z=−2.08, P=0.04). The difference of IJOA difference values grading was
The order of initial symptoms of adolescent patients from statistically insignificant in the different age groups within
the most common to the least common was gait deteriora- the two different grouping methods. Improvements of
tion (ratio was 1), pain (including pain with motor neurological functions and its stabilities were seen in
weakness; ratio was 0.88), motor weakness (ratio was patients younger than 40 years old. On the other hand, the
0.75), and sensory disturbances (ratio was 0.17). There patients older than 40 years old presented with deterioration
were five patients who presented with pain with motor of neurological functions and stabilities (Fig. 3).
weakness, aged 7, 15, 18, 19, and 26 years old, respective-
ly. If pain with motor weakness was singled out from pain Internal fixation and spinal stability
as a whole, then the order of initial symptoms would
change into pain with motor weakness (ratio was 4), gait Universal Spine system internal fixation (USS) was per-
deterioration (ratio was 1), motor weakness (ratio was formed in two cases following a total resection of massive
0.75), simple pain (ratio was 0.67), and sensory disturban- long diameter ependymomas (the long diameter of the tumor
ces (ratio was 0.17). was more than 20 cm) involving the thoracolumbar region
[11].
Histological classification between the different groups Two adult patients with cervical ependymomas involving
more than five spinal segments developed cervical flexion
The most frequent histological classification of MSICT was deformity 1 year after a laminectomy at both the axial
ependymomas (37.7%, 29 out of 77), followed by benign cervical spine (C1 or C2) and the cervicothoracic junction.
gliomas (including astrocytoma I–II and oligodendrocy- We believed that the deformity was probably due to the
toma; 22.1%, 17 out of 77), neurodevelopmental tumors physical requirements of their occupations. Rectification of
(including lipoma, epidermoid cyst and teratoma; 19.5%, an unhealthy posture and enhancement of the cervical
15 out of 77), malignant glioma (10.4%, 8 out of 77), hypokinesis using exercises may prevent the cervical
vascular tumors (including hemangioblastomas and cavern- vertebra from deformity in these patients [18, 19].
ous angioma; 6.5%, 5 out of 77), and neurogenic tumors
(including neurinoma and cyst; 3.8%, 3 out of 77) (Tables 2 Long-term follow-up
and 4). Age of patients and histological classification of
MSICT have prognostic significance (Z=12.5, P=0.03). The mean follow-up period was 44.2±25.68 months (rang-
Neurodevelopmental tumor and benign glioma, mostly ing from 5 to 103 months). Compared to the preoperative
90 Neurosurg Rev (2012) 35:85–93
Discussion
to the normal spinal cord tissue. For examples, cases with
MSICT in the younger adolescent group were predomi- adipose tissue growing between normal white matter tissues
nately benign glioma, mostly astrocytoma I–II and neuro- and cases with adhesion of unyielding cyst wall with the
developmental tumor. In addition to our conclusion, Houten adjacent neurological structures or the penetrating growth
et al. [5] also presumed that astrocytomas predominated in surrounding spinal marrow. In order to avoid neurological
younger children and decreased in frequency into adulthood dysfunction, the closely adhered tumor tissues should,
where ependymomas became more predominant. therefore, not be removed by force [16]. The main purpose
Astrocytoma, mostly low-grade tumor, was the predom- of the surgery for these tumors was not a complete removal
inant histological type in the adolescent patients with but a decompression on the adjacent neurological structures
intramedullary spinal cord tumors and could be completely [17]. Hence, total or subtotal resection was obtained only in
removed with ease [3, 10]. In addition, postoperative 66.7% of patients with neurodevelopmental tumors [19].
neurological functional state was improved or stable in MSICT in the adult group were predominately ependy-
75–90% of adolescent patients [1, 13]. Sandler et al. [16] moma. Intramedullary ependymomas originated from the
considered that age was an effective influencing factor for central canal of spinal cord, which was found to be 15–
the prognosis of patients with intramedullary astrocytoma. 19.7% in all spinal cord tumors. The age of onset of
Based on the differences in color and texture between the intramedullary ependymoma was within 30–50 years old
benign gliomas and normal spinal cord intraoperatively, the [7, 18]. The boundaries between tumor body and normal
pseudoboundaries were determined. From the center of spinal cord tissue were distinct and separable. Therefore,
intramedullary tumor to the periphery, the tumor tissue was total or subtotal resection was obtained in 94.7% of
removed layer by layer until the normal white matter was in intramedullary ependymomas [9, 15, 18, 19].
view. If the measurements of intraoperative somatosensory- No matter if its benign gliomas, neurodevelopmental
evoked potential (SEP) and motor-evoked potential (MEP) tumors, or ependymomas, it was imperative that tumors
monitoring showed deteriorating neurological function or resection had been performed in time. Most scholars
pseudoboundaries could not be identified clearly, the believed that it is crucial for an early diagnosis and an
resection of tumor should be terminated [1, 13]. early open surgery for removing intramedullary tumors.
Furthermore, multisegment neurodevelopmental tumors The less severe the preoperative symptoms and signs of a
(including cystic tumors, such as epidermoid cyst, dermoid patient, the better the recovery could be obtained for the
cyst, and cystic teratoma) were also a predominant tumor in patients after an operation. Patients can even recover back
the young adolescent patients, mostly seen in males [11, 12, to normal neurological states [3, 10, 12, 13, 15, 16].
19]. In some cases, the tumor tissues were closely adhered Improvement of neurological functions and its stabilities
were seen in patients younger than 40 years old. This result
might be due to better plasticity in the spinal cord tissues of
the younger patients, which could result in a relatively
better prognosis in younger patients with MSICT [20]. New
et al. [14] thought that younger patients with traumatic or
nontraumatic spinal cord injury were more likely to regain
walking in a short-term prognosis.
Pain with motor weakness and gait deterioration pre-
dominated in adolescents and decreased in frequency into
Fig. 2 The changing figure of histological classification of MSICT adulthood where sensory disturbances became more pre-
between different age stage dominant. Houten et al. [5] concluded that pain was the
92 Neurosurg Rev (2012) 35:85–93
most frequent presenting symptom of intramedullary spinal 2. Chang UK, Choe WJ, Chung SK et al (2002) Surgical outcome
and prognostic factors of spinal intramedullary ependymomas in
cord tumors and often precedes the development of other
adults. J Neuro-oncol 57:133–139
symptoms such as weakness, gait deterioration, torticollis, 3. Crawford JR, Zaninovic A, Santi M et al (2009) Primary spinal
sensory disturbance, and sphincter dysfunction. Chang et cord tumors of childhood: effects of clinical presentation,
al. [2] found that preoperative sensory abnormality was radiographic features, and pathology on survival. J Neurooncol
95:259–269
observed in 93% of adult patients with ependymoma. As
4. Dudek RW (2001) Skeletal system. In: Nieginski E (ed) High-
easily confused with growing pains, early pain complaints yield embryology, 2nd edn. Lippincott Williams & Wilkins,
of adolescent patients may be neglected. Only if subtle Maryland, p 100
changes in gait or more frequent falls were noticed by their 5. Houten JK, Weiner HI (2000) Pediatric intramedullary spinal cord
tumors: special considerations. J Neuro-oncol 47:225–230
parents, adolescent patients will then visit the doctor. The 6. Huddart R, Traish D, Ashley S et al (1993) Management of spinal
pain from intramedullary spinal cord tumors could not have astrocytoma with conservative surgery and radiotherapy. Br J
been distinguished from growing pains by neither the Neurosurg 7:473–481
parents nor the doctors. Therefore, MRI scan screening 7. Kasim KA, Thurnher MM, Mckeever P et al (2008) Intradural
spinal tumors: current classification and MRI features. Neurora-
should be performed regularly for adolescents complaining
diology 50:301–314
of constant pain that does not dissipate. 8. Kim MS, Chung CK, Choe GY et al (2001) Intramedullary spinal
The patients who presented with benign gliomas in cord astrocytoma in adults: postoperative outcome. J Neuro-oncol
which total resection were easily performed obtained a 52:85–94
9. Lin YH, Huang CI, Wong TT et al (2005) Treatment of spinal cord
better prognosis. However, in patients who presented with
ependymomas by surgery with or without postoperative radio-
malignant gliomas, total resections were difficult to perform therapy. J Neuro-oncol 71:205–210
and suffered a relatively worse prognosis with higher 10. Makridou A, Argyriou AA, Karanasios P et al (2008) Bilateral
recurrence rates (about 50%). In the study of Kim et al. drop foot secondary to a primary tumor in the conus medullaris.
Muscle Nerve 37:778–780
[8], they reported that only 39% of benign gliomas obtained 11. McGirt MJ, Chaichana KL, Attenello F et al (2008) Spinal
a total resection, while only 20% of malignant gliomas deformity after resection of cervical intramedullary spinal cord
obtained a total resection. In addition, the study of Huddart tumors in children. Childs Nerv Syst 24:93–97
et al. [6] reported that distant metastases occurred in 50– 12. Miller DJ, McCutcheon IE (2000) Hemangioblastomas and other
uncommon intramedullary tumors. J Neuro-oncol 47:253–270
60% of patients with malignant glioma.
13. Nakamura M, Ishii K, Watanabe K et al (2008) Surgical treatment
In summary, benign glioma, mostly astrocytoma I–II, of intramedullary spinal cord tumors: prognosis and complica-
and neurodevelopmental tumor predominated in younger tions. Spinal Cord 46:282–286
adolescents and decreased in frequency into adulthood 14. New PW, Epi MC (2007) The influence of age and gender on
rehabilitation outcomes in nontraumatic spinal cord injury. J
where ependymoma became more predominant. Pain with
Spinal Cord Med 30:225–237
motor weakness and gait deterioration predominated in 15. Sandalcioglu IE, Gasser T, Asgari S et al. (2005) Functional
adolescents and decreased in frequency into adulthood outcome after surgical treatment of intramedullary spinal cord
where sensory disturbances became more predominant. tumors: experience with 78 patients. Spinal Cord 43:34–41
16. Sandler HM, Papadopoulos SM, Thornton AF et al (1992) Spinal
Due to the small sample size in our data, the results of
cord astrocytomas: results of therapy. Neurosurgery 30:490–493
the statistical correlations and analyses might have a 17. Sharma NC, Chandra T, Sharma A et al (2009) Long-segment
decrease in its statistical power. Nevertheless, the statistical intramedullary spinal dermoid. India J Radiol Imaging 19:148–150
results were sufficient to draw a conclusive statement about 18. Sun JJ, Wang ZY, Li ZD et al (2009) Microsurgical treatment and
functional outcomes of multi-segment intramedullary spinal cord
the MSICT characteristics between different age groups.
tumors. J Clin Neurosci 16:666–671
19. Sun JJ, Wang ZY, Xie JC et al (2010) Comparative analysis the
Acknowledgement This work was supported by the Science difference between multi-segments intramedullary spinal cord
Foundation for The Excellent Youth Scholars of Ministry of Education congenital tumors and benign ependymomas. J Pek Uni (Heal
of China (BSD-09-6-11) and Science Foundation for The Excellent Sci) 42:89–93, in Chinese
Youth Scholars of Peking University Third Hospital (74496-01). The 20. Wilson PE, Oleszek JL, Clayton GH (2007) Pediatric spinal cord
authors thank Dr. Simon Glynn (from the Department of Neurology, tumors and masses. J Spinal Cord Med 30:S15–S20
University of Pennsylvania School of Medicine) for the revision and
comments on the manuscript and Ms. Isabelle Liu (from the
Washington University in St. Louis School of Medicine) for the final
careful English-language editing. Comments
every article on these tumors emphasized the need for an early They cannot be completely removed with ease. This is in
diagnosis and an early operation as surgical morbidity was and still is opposition with the literature [2, 5]. The infiltrating nature of
directly related to the patient’s preoperative neurological function. most astrocytoma lesions makes total removal impossible without
With modern imaging techniques, we are in the fortunate position now an unacceptable loss of neurological function [6].
to diagnose patients early. With modern microsurgical techniques and – I am astonished to read that the overall postoperative status
intraoperative neurophysiological monitoring, the preservation of presented at the final follow-up review was improved in 84.4% of
function has become the rule rather than the exception if surgery is all patients (n=65), unchanged in 11.7% (n=9), and deteriorated
performed by experienced neurosurgeons. Wang et al. present their in 3.9% (n=3 with malignant gliomas). We know from the
analysis of 77 multilevel intramedullary spinal cord tumors. Apart literature that the quality of the results closely depends on the
from well-established differences in the literature concerning the preoperative neurological status. In large published series, it is
predominating tumor histologies in children and adults, the authors said that more than 50% of patients are stabilized. Furthermore,
found lower surgical morbidities in younger patients both in terms of in experienced hands, the rate of worsening runs from 5% to 20%
immediate postoperative function as well as potential recovery from a in intramedullary low-grade gliomas according to the preopera-
postoperative deterioration. These are important informations for tive neurological status (McCormick grades I to III) [7]. Here, the
preoperative patient counseling. Almost all patients experience some authors report 3.9% worsening encountered in malignant gliomas
permanent loss of sensory function after an operation on a multilevel only. It is surprising and in disagreement with classical data of the
tumor. This may have significant consequences for coordination of literature [7–10].
movements. Preservation of motor functions alone may not be enough – My last comment concerns laminoplasty. It is true that, in China,
to preserve the patient’s walking abilities. Spinal ataxia is difficult to many patients are poor and unable to cover the cost of screws and
rehabilitate in elderly patients in particular. Regarding intraoperative plates. But I wish to say that, in my practice, I have made several
neurophysiological monitoring, almost every paper focuses exclusive- laminoplasties in children with very cheap silk sutures at the time
ly on the preservation of motor-evoked potentials. Many colleagues we had not the small plates and screws in titanium. If we go back
consider attempting to preserve sensory-evoked potentials a meaning- to the original papers from pediatric neurosurgeons, laminoplasty
less undertaking. I do not agree with such a view. To try to preserve as was made with silk sutures [11].
much sensory function as possible lowers postoperative morbidity.
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