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Diffusion tensor MR fiber tractography in assessment of inflammatory processes and neoplasms of the cervical cord
The Egyptian Journal of Radiology and Nuclear Medicine xxx (2017) xxx–xxx
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The Egyptian Journal of Radiology and Nuclear Medicine journal homepage: www.sciencedirect.com/locate/ejrnm
Original Article
Diffusion tensor MR fiber tractography in assessment of inflammatory processes and neoplasms of the cervical cord Mohamed Saeid Abdelgawad a,⇑, Mohamed Ihab Samy Reda b, Nermeen Abd El-Monsef Abd El-Maaboud b a b
Radiodiagnosis Department National Liver Institute, El-Menoufia University, Egypt Radiodiagnosis Department, Alexandria Faculty of Medicine, Egypt
a r t i c l e
i n f o
Article history: Received 25 November 2016 Accepted 7 March 2017 Available online xxxx Keywords: MR tractography Cervical cord neoplastic lesions Cervical cord neoplastic inflammatory lesions
a b s t r a c t Our goal of this research is to assess the value of MR fiber tractography in assessment of inflammatory process and neoplasms of the cervical cord. Patients: We included 40 patients diagnosed as inflammatory diseases and neoplasm of the cervical cord in our research. 17 patients with pathologically proved cervical cord neoplasms, including three patients with anaplastic astrocytoma, five patients with cellular ependymoma, two patients with anaplastic ependymoma, two patients with fibrillary astrocytoma, one glioblastoma multiforme (GBM), one with cervicomedullary glioma, two with metastasis and one hemangioblastoma. The remaining 23 patients were finally diagnosed as inflammatory processes of the cervical cord, through clinical examination, laboratory results and serial follow up. The latter category include ten patients with myelitis, eight with multiple sclerosis, three patients with post irradiation myelitis and two patients with neuromyelitis optica. Methods: MRI sequences including T2W (sagittal and axial), pre and post contrast T1 (Sagittal and axial) and diffusion tensor MR fiber tractography. Results: All the 17 patients with neoplasm of the cervical cord show more or less displacement of the cervical tract fibers, ten without fibers disruption and seven with fibers disruption. In all patients with inflammatory processes (23 patients) of the cervical cord no fibers displacement identified, but different grades of fibers disruption or sparse fibers. Conclusion: MR fibers tractography is a very promising tool in assessment of inflammatory processes and neoplasms of the cervical cord. Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/ 4.0/).
1. Introduction The most important differential diagnosis for spinal cord mass lesions includes spinal cord tumors and inflammatory disease processes. In many cases making the distinction among these pathologic entities can be difficult only by routine Magnetic resonance imaging (MRI) and clinical symptoms. In many cases, final diagnosis is reached by surgical biopsy for indeterminate lesions [1]. Multiple sclerosis is a diseased affecting the white matter of the brain and spinal cord. It is characterized by multiple white matter lesions associated with manifestations changing in place and time [2]. Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine. ⇑ Corresponding author. E-mail address: [email protected] (M.S. Abdelgawad).
Magnetic resonance imaging (MRI) has an important role in the diagnosis of MS [3]. Awareness of the imaging features of MS affecting the cord is very crucial as there is high association between cord lesions and incapability more than those with brain manifestation of MS [4]. T2W sequence is the most widely used sequence for assessment of MS plaques either in cord or in the brain [5,6]. About 90% of patients with cord MS will have high T2W hyperintense foci [6]. The most common site of cord affection in cases of MS is the cervical cord with high rate of occurrence at the posterior and lateral aspects of the cord [4]. The maximum extent of MS plaques in the cord may reach up to 6 cm average, while its short axis less than 50% of the cord diameter [7]. In acute stage, MS plaques are usually associated with edema and expansion of the cord at the level of the affection, with less
http://dx.doi.org/10.1016/j.ejrnm.2017.03.007 0378-603X/Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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degree of enhancement as compared with MS plaques of the brain [6]. In equivocal cases with questionable T2 hyperintense foci in the brain, sometime MRI of the cord may be helpful in demonstrating lesions in the cord, which may help to make the diagnosis of multiple sclerosis [6,8]. Early phase of neuromyelitis optica NMO usually spare the brain with high tendency to involve the optic nerves and cord. The length of the lesion can reach up to 3 contiguous vertebrae, and usually inclined to be centrally located within the cord substance [9,10]. Cases with acute transverse myelitis ATM, usually presented by sphincteric incontinence and paraplegia, regarding that secondary causes, of these manifestation have been ruled out, as cord infiltration by neoplasms, compression, infection, vascular malformation or trauma [11–14]. The usual MRI appearance of ATM is T2W high signal within the central part of the cord, usually with length exceeding 3 vertebral bodies and width exceeding more than 70% of the transverse diameter of the cord [15]. In some cases abnormal T2 hyperintense signal lesions may be associated with central isointensity; distinguishing ATM from other hyperintense cord lesions such as multiple sclerosis. Following intravenous contrast injection nodular or patchy enhancement may be seen at the outermost cord aspect [15,16]. Primary and secondary tumors usually presented on MRI as an ill defined T2W high intensity expanding the cord with heterogeneous post contrast enhancement [17,18]. Most ependymomas show T2W hyperintense signal. Ependymomas usually shows intense and homogeneous enhancement with well defined borders. Cap sign is a hypointense area around tumor margins limits and these caps represents haemosiderin from old hemorrhage [19]. Up to 75% of astrocytoma seen involving the cervicothoracic region, and usually of large size [17]. The lesions usually displays hyperintense signal; which represent a combination of tumor itself and the associated cord edema. Astrocytomas are usually located eccentrically in the cord. It shows heterogeneous partial post contrast enhancement. The borders of the lesions are frequently ill defined. Lesions with cystic components are typically intratumoral; however, it is sometimes associated with satellite cysts and secondary hydromyelia [20]. Haemangioblastomas are highly vascular tumors. These lesions are usually solitary, but with Von Hippel-Lindau disease multiple may be seen [21]. The typical MRI appearance of haemangioblastomas is a well defined T2 hyperintense cystic lesion, with ovoid or rounded appearance and with an intensity enhancing mural nodule. Many cases are associated with extensive hydrosyringomyelia. Large tumors frequently have signal defect due to vascular nature of the lesions [22]. It is not common for metastasis to involve the spinal cord. The highest percentage of cord metastasis seen in the cervical region next is the dorsal spine and finally the lumbar spine. Cord metastasis from lung cancer has the highest incidence; breast, kidney, colon and lymphoma are other site that can send metastasis to the cord [23]. On MR imaging the lesions typically produce long segment of mild cord expansion. The lesion usually shows central area of T1W hypointense signal, T2W hyperinensity with intense homogeneous enhancement, and disproportionate extensive amounts of perilesion edema [24,25]. Cases with myelitis after radiotherapy can either acute or chronic. The criteria for myelitis post radiotherapy includes, 1past history of exposure to radiotherapy, 2-the involved cord must be included in the radiation port, 3-finally causes of cord indentation are kept out [26].
In acute form, MRI usually negative with no appreciable signal alteration seen within the cord [27]. In the chronic form, MRI usually demonstrate an ill defined area of patchy irregular enhancement coupled with too large area of cord edema as compared to the size of the enhancing patches [28]. Focal atrophic changes of the previously irradiated portion of the cord can be seen many years latter after radiation [28]. Diffusion Tensor MR Fiber Tractography DTI has many clinical applications in brain imaging [29]. Diffusion is described as isotropic, when particles of pure material are distributed by the same degree in all ways. On the other hand when particles of certain material are oriented in certain direction as for examples the fibers of the cervical cord, diffusion is then described as anisotropic. Any causes that reduced anisotropy, will result in distorted images produced by diffusion tensor MR fiber tractography [29]. MR fiber tractography is commonly used in many applications in the brain; while in the cord there are many challenges, including the narrow area of examination contrary to that of the brain. Also the inhomogeneous area of study is another obstacle. Subsequently there are few experiments for MR fiber tractography of the cord [30].
2. Aim of the work Our goal of this research is to assess the value of MR fiber Tractography in assessment of inflammatory process and neoplasms of the cervical cord (see Figs. 1–5).
2.1. Material This study is a prospective study where patient consent was waived by the Research Ethics Board, assuring respect of the confidentiality of the medical record. We included 40 patients diagnosed as inflammatory diseases and neoplasm of the cervical cord in our research in the period from January 2014 till April 2016.
Fig. 1. 3D MR fiber tractrography; Sagittal (A) and Coronal (B); showing normal course and appearance of the cervical cord fibers tracts. No displacement. No fibers interruption.
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M.S. Abdelgawad et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2017) xxx–xxx
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Fig. 2. 45 years old male patient presented by gradual onset of bilateral lower limb weakness. Sagittal T2 (A) showing focal T2 hyperintense area opposite CV5-6 level, mildly enhancing after contrast (B); fiber tractography (C) showing neither displacement nor interruption of the fibers, (type I pattern). Follow up MRI (D–F) sagittal T2, T1 and T1 post contrast, done 1 year later revealed near total resolution of the lesion, confirming its non neoplastic nature.
The study included 22 males and 18 females, their ages ranged between 12 and 66 years. Inclusion criteria include those patients with the final diagnosis of neoplastic or inflammatory cord lesions; while those with cervical cord trauma, vascular lesions and non neoplastic syringomyelia were excluded.
examination was conducted including neurological examination to assess sensory and motor deficits. All these patients had MRI imaging that was done on 1.5 Tesla Avanto unit, Siemens system. No complications were recorded during the examinations. 2.2.1. MR examination parameters
2.2. Methods All patients were subjected to detailed clinical history was taken including personal data and neurological complaints. Clinical
T2W (axial and sagittal) TSE (turbo spin echo), Time of Repetition (TR) = 3500 ms, Echo Time (TE) = 88 ms. The time of acquisition for each sequence takes about two minutes and 35 s.
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Fig. 3. 52 years old female patient presented by neck pain, bilateral upper limb numbness, 3 months after stopping neck irradiation for oral SCC. Sagittal T2 (A) abnormal hyperintense signal extending from CV2 down to CV5 Sagittal T1 pre and post contrast (B and C) showed mildly enhancing mass like lesion. Tractography (D) showing focal fibers interruption (arrow) with no fibers displacement (type II pattern). Follow up 3 months later T1W post contrast (E) showing regression of the enhancement, confirming the diagnosis of post radiation myelitis.
T1W (axial and sagittal), (pre and post contrast), Spin Echo (SE), TR = 640 ms, TE = 10 ms, matrix (256 256), field of view (FOV) = 230 mm, 3 mm slice thickness, 0.3 mm gag, with time of acquisition 3 min and 23 s for each sequence. T1W post contrast in 3D; TR = 1650 ms, TE = 295 ms, slice thickness = 1 mm with 0.3 mm gap, matrix = (256 256), FOV = 250 mm, total time of acquisition about 5 min and 18 s. The software used for reconstruction of the Diffusion Tensor imaging (DTI), is Neruro-3D soft ware produced by Siemens Healthcare. Final diagnosis was reached by histopathology in 17 patients with neoplastic lesions, and by follow up in 23 cases with inflammatory lesions (clinically and imaging) for a period at least 3 months up to more than one year. 3. Results Neck pain was the main complaint of all patients with variable associated upper or lower limb numbness and or weakness. Twenty cases had gradual onset of symptoms, and 15 patients
had subacute onset. Three patients presented by acute onset of paraparesis. Two patients had long history of quadriplegia with muscle contractures. Two patients with subacute onset had also diminished visual acuity. 17 patients out of 40 had neoplastic lesions of the cord, five had cellular ependymoma (12.5%), two anaplastic ependymoma (5%), two Fibrillary astrocytoma (5%), three anaplastic astrocytoma (7.5%), one Glioblastoma multiforme (GBM) (2.5%), one case cervicomedullary glioma (2.5%), two cases with metastasis (5%) and one case with haemangioblastoma (2.5%) Table 1. 3.1. Fiber tractography (FT) Fiber tractography patterns of intramedullary spinal cord lesions were classified according to the morphologic fiber tractography pattern for each lesion Table 2. 1. Type I pattern (20 Cases), Normal white matter tracts detected. Neither displacement, nor interruption observed, including 9 cases with myelitis and all 8 cases of MS, 2 cases of NMO, and a case with post irradiation myelopathy.
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3. Type III pattern (10 cases), major displacement without disruption of the fibers. This group included 10 neoplastic patients. 4. Type IV pattern (7 cases), displacement with disruption of the fibers. This group included 7 neoplastic lesions. 3.2. FT in spinal cord tumors In our study, all 17 neoplastic cervical cord lesions lead to white matter tract displacement and wrapping around the tumor. The fibers were always displaced by the tumor mass as the tracts were splitted and pushed laterally. In the cases with ependymoma (n = 5), we found that the fibers are displaced nearly symmetrically around the lesion, this can be explained by origin of the tumor from the central portion of the cord. Similar findings were also seen in a case of metastasis, a case of anaplastic astrocytoma, two cases of fibrillary astrocytoma and a case of cervicomedullary glioma. We observed disruption of the fibers associated with tract displacement in 7 cases with neoplasms, six of them were high grade tumors including 1 patient with recurrent GBM, two cases with anaplastic astrocytoma, two cases with anaplastic ependymoma and one case with metastatic lesion. Interrupted tracts were also noticed in one case with haemangioblastoma.
Fig. 4. 24 years old male patient presented by bilateral upper and lower limb numbness. Sagittal T1 post contrast (A) revealed homogeneously enhancing mass within the cervical cord opposite CV3 and CV4. MR Tractography (B) shows smooth displacement of the white matter tracts around the mass with no fibers interruption (white arrow) (type III pattern). Pathologically proved neoplasm (Astrocytoma).
2. Type II pattern (3 cases), focal interruption or attenuation of the fibers, including 1 case with myelitis and 2 cases with post irradiation changes. No displacement seen.
3.3. FT in inflammatory lesions FT performed in the inflammatory lesions of spinal cord including inflammatory myelitis, post irradiation myelitis, MS and NMO patients. Type I was seen in 20 cases, with no displacement or interruption of the fibers. 9 patients with myelitis, 8 patients with MS, 1 post irradiation myelitis and 2 cases with NMO. Type II was observed in 3 cases, with focal interruption of the fibers without displacement seen; one case of myelitis and 2 cases with post irradiation myelitis.
Fig. 5. (A) sagittal T2, (B) sagittal T1 post contrast showing large mass involving the whole cervical cord, with ventral dural based meningioma seen at CV1-2 level MR tractography, (C) showing displacement with interruption of the cervical cord fibers by the enhancing lesion (black arrow) (type IV pattern). The lesion proved by biopsy to be ependymoma.
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Table 1 Distribution of the studied cases according to pathology (n = 40). Pathology
No. 40 patients
% 100%
Non neoplastic Myelitis MS Post irradiation NMO (Devic’s disease)
23 10 8 3 2
57.5 25 20 7.5 5
Neoplastic Cellular ependymoma Anaplastic ependymoma Fibrillary astrocytoma Anaplastic astrocytoma GBM Cervicomedullary glioma Metastasis Hemangioblastoma
17 5 2 2 3 1 1 2 1
42.5 12.5 5 5 7.5 2.5 2.5 5 2.5
Table 2 Distribution of the studied cases according to FT pattern (n = 40). Fiber tractography pattern
No.
%
I
20 9 with myelitis 8 with MS 2 cases NMO 1 case post irradiation myelitis
50
II
3 1 case myelitis 2 cases post irradiation myelitis
7.5
III
10 All 10 patients are neoplastic
25
IV
All 7 patients are neoplastic 40
17.5 100%
4. Discussion Patients with clinical symptoms suggesting cord etiology are usually subjected to conventional MRI examination of the cord. Although conventional MRI is sensitive in detection of inflammatory processes and cord neoplasm affecting the cervical cord, in many cases the MRI picture is similar in both categories, and reaching final diagnosis is difficult [31]. Diffusion-tensor imaging (DTI) has been clinically applied in assessment of some brain pathologies, notably after technical advances in the new MRI machines [32]. Many challenges are met during application of this new technique in the spinal region, including the narrow field of examination, the complex functional organization, magnetic susceptibility, motion artifact and CSF pulsation [33]. In recent years, methodological efforts from various groups have managed to overcome some of these technical challenges. The goal of out research is to assess the clinical application of MR fiber Tractography in assessment of inflammatory process and neoplasms of the cervical cord [34]. In our study we did fiber tracking (FT) for 40 patients with inflammatory processes and neoplasm of the cervical cord. We found displacement of the white matter fibers surrounding the mass in all neoplastic lesions as they are pushed away by the tumor, but in inflammatory lesions 3D FT showed rarefaction and spreading of the fibers in T2W hyper-intense area, due to cellular infiltration of the nerve fibers by inflammatory cells. These characteristics can be helpful in differentiating inflammatory from neoplastic processes. We classified morphologic pattern of FT into, four patterns. Type I pattern (20 Cases), with normal white matter tracts detected. Neither displacement, nor interruption observed, includ-
ing 9 cases with myelitis and all 8 cases of MS, 2 cases of NMO, and a case with post irradiation myelopathy. 2. Type II pattern (3 cases), with focal interruption or attenuation of the fibers, and no displacement. This pattern was seen in one case with myelitis and 2 cases with post irradiation changes. 3. Type III pattern (10 cases), with major displacement without disruption of the fibers. This group included 10 neoplastic patients. 4. Type IV pattern (7 cases), displacement with disruption of the fibers. This group included 7 neoplastic lesions. It is very crucial to make difference by imaging between inflammatory processes and neoplasm of the cord to provide the correct management and to avoid invasive biopsy. Deterioration of the clinical course or increase size of the lesion on follow up MRI may give hand to reach the diagnosis, but it will lead to bad prognosis [35]. In our study, we found that inflammatory lesions showed normal course of the white matter tracts with or without mild spreading/separation of the fibers in 20 cases. Neither displacement, nor interruption observed. The remaining three cases showed focal disruption but still no fibers displacement. All neoplastic cervical cord lesions enrolled in the study, demonstrated displacement of the white matter tract. Ten cases without fibers interruption and seven cases with fibers interruption. In a study by Giussani et al., for assessment of inflammatory processes and neoplasm affecting the brainstem, there was marked reduction of the number of the visualized tracts in patients with inflammatory white matter diseases. On the other hand in cases with neoplasm, there was more or less change in directions of the fibers at the site of the neoplasm [36]. Giussani et al. attributed the reduction in the number of fibers tracts seen in inflammatory processes by tractography to the diminished anisotropy by the inflammatory edema. The diminished anisotropy will affect fibers tracing resulting in reduction of number of the visualized [36]. Giussani et al. also explained that the pattern in tumors can de due compression of the tumors upon the tract fibers with or without fibers invasion. Both will result in reduction of anisotropy with subsequent diminished fibers appearance on fibers tract mapping [36]. In our study we observed disruption of the fibers associated with tract displacement in 7 cases with neoplasms, 6 of them were high grade tumors including 1 patient with recurrent GBM, two cases with anaplastic astrocytoma, two cases with anaplastic ependymoma and one case with metastatic lesion. Interrupted tracts were also noticed in one case with haemangioblastoma. These lesions showed hemorrhage and cystic changes, both may affect anisotropy across the cord tracts. The disruption of the tract fibers can be explained by either true destruction of the fibers or the presence of the hemorrhage and or edema resulting in reduction in fibers anisotropy [37]. Diffusion tensor imaging fibers tractography gave information about special aspects of different types of neoplasms, as regards the pattern of growth as well as site of origin. Fibers invasion are commonly seen in astrocytic neoplasms and commonly has an eccentric location within the cord. On the other hand ependymoma usually located within the center of the cord as it grows from cells lining the central canal, resulting in displacement of fibers around the neoplasm [34,37]. In our study, cases with cellular ependymoma (n = 5), demonstrate deviation of fibers all around the centrally located tumor suggesting the diagnosis of ependymoma. Same findings were described in a review done by Thurner et al. they demonstrated that FT can help differentiation between ependymoma and astrocytoma which is clinically an important question, which determines whether or not this lesion is resectable. They described that spinal cord ependymoma, demonstrates
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fiber tracts being concentrically displaced outward at the level of the tumor rather than infiltrated or separated as with transverse myelitis or astrocytoma. In contrast to invasive astrocytoma, ependymoma has a line of cleavage with the surrounding sound fibers making it easy for operative excision [34]. Thurner et al. also illustrated that MR fiber tractography can be used to illustrate a road map for possible surgical plan to excise cord neoplasm with reduction of post surgical complication and improve post operative outcome [34,38]. As we mentioned earlier the cases of demyelinating/inflammatory disease, showed either, type I pattern (20 Cases), where there was normal course of the white matter tracts with or without mild spreading/separation of the fibers, neither displacement, nor interruption observed, including 9 cases with myelitis and all 8 cases of MS, two cases of NMO, and a case with post irradiation myelopathy, or type II pattern (3 cases) including one case of myelitis and two cases of post irradiation myelitis, in which there is attenuation of the fibers. Our data concerning the FT of the patient with inflammatory lesions of the cord almost matching with publication made by Renoux et al. evaluating Fiber Tracking in 15 patients with myelitis revealed that no fibers displacement seen at the affected regions. Only three patients had focal disrupted fibers at the affected regions. They explained that rarification of the fibers at 3D fiber tractography in T2W hyper-intense areas in cases of myelitis, are mostly due inflammatory edema [39]. After extended review of literature to know if we have recent approved consensus to use FT as imaging tool to differentiate neoplastic from non-neoplastic lesions, only few publications were noted and attempted to describe initial morphologic pattern of different pathologies separately. These qualitative characteristics of FT could be helpful in differentiating inflammatory from neoplastic processes, in the former we usually do not observe fiber disruption except for mild fiber spreading. Despite the limited studies with FT in spinal cord lesions, we suggest that assessment of FT may improve our understanding of nature as well as extent in many inflammatory process and neoplasms affecting the cord and narrow the differential diagnosis. 5. Conclusion Displacement of the white matter fibers surrounding the mass is a feature in all neoplastic lesions as they are pushed away by the tumor. In inflammatory conditions there is either normal course of the tracts or rarification and spreading of the fibers. These characteristics can be helpful in differentiating inflammatory from neoplastic processes. We recommend DTI, whenever there is focal abnormal signal in the cord particularly if it showed post contrast mass like enhancement. We should be careful when interpreting disruption of the white matter fibers surrounding the mass, due to the multiple factors that may affect anisotropy across the fibers. References [1] Fanous Andrew A, Olszewski Nathan P, et al. Idiopathic transverse myelitis mimicking an intramedullary spinal cord tumor. Case Reports Pathol 2016:1–8. [2] Thielen KR, Miller GM. Multiple sclerosis of the spinal cord: magnetic resonance appearance. J Comput Assist Tomogr 1996;20:434–8. [3] Pretorius PM, Quaghebeur G. The role of MRI in the diagnosis of MS. Clin Radiol 2003;58:434–48. [4] Tench CR, Morgan PS, Jaspan T, Auer DP, Constantinescu CS. Spinal cord imaging in multiple sclerosis. J Neuroimaging 2005;15:94S–102S. [5] Hittmair K, Mallek R, Prayer D, Schindler EG, Kollegger H. Spinal cord lesions in patients with multiple sclerosis: comparison of MR pulse sequences. AJNR 1996;17:1555–65.
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Original Article
Diffusion tensor MR fiber tractography in assessment of inflammatory processes and neoplasms of the cervical cord Mohamed Saeid Abdelgawad a,⇑, Mohamed Ihab Samy Reda b, Nermeen Abd El-Monsef Abd El-Maaboud b a b
Radiodiagnosis Department National Liver Institute, El-Menoufia University, Egypt Radiodiagnosis Department, Alexandria Faculty of Medicine, Egypt
a r t i c l e
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Article history: Received 25 November 2016 Accepted 7 March 2017 Available online xxxx Keywords: MR tractography Cervical cord neoplastic lesions Cervical cord neoplastic inflammatory lesions
a b s t r a c t Our goal of this research is to assess the value of MR fiber tractography in assessment of inflammatory process and neoplasms of the cervical cord. Patients: We included 40 patients diagnosed as inflammatory diseases and neoplasm of the cervical cord in our research. 17 patients with pathologically proved cervical cord neoplasms, including three patients with anaplastic astrocytoma, five patients with cellular ependymoma, two patients with anaplastic ependymoma, two patients with fibrillary astrocytoma, one glioblastoma multiforme (GBM), one with cervicomedullary glioma, two with metastasis and one hemangioblastoma. The remaining 23 patients were finally diagnosed as inflammatory processes of the cervical cord, through clinical examination, laboratory results and serial follow up. The latter category include ten patients with myelitis, eight with multiple sclerosis, three patients with post irradiation myelitis and two patients with neuromyelitis optica. Methods: MRI sequences including T2W (sagittal and axial), pre and post contrast T1 (Sagittal and axial) and diffusion tensor MR fiber tractography. Results: All the 17 patients with neoplasm of the cervical cord show more or less displacement of the cervical tract fibers, ten without fibers disruption and seven with fibers disruption. In all patients with inflammatory processes (23 patients) of the cervical cord no fibers displacement identified, but different grades of fibers disruption or sparse fibers. Conclusion: MR fibers tractography is a very promising tool in assessment of inflammatory processes and neoplasms of the cervical cord. Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/ 4.0/).
1. Introduction The most important differential diagnosis for spinal cord mass lesions includes spinal cord tumors and inflammatory disease processes. In many cases making the distinction among these pathologic entities can be difficult only by routine Magnetic resonance imaging (MRI) and clinical symptoms. In many cases, final diagnosis is reached by surgical biopsy for indeterminate lesions [1]. Multiple sclerosis is a diseased affecting the white matter of the brain and spinal cord. It is characterized by multiple white matter lesions associated with manifestations changing in place and time [2]. Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine. ⇑ Corresponding author. E-mail address: [email protected] (M.S. Abdelgawad).
Magnetic resonance imaging (MRI) has an important role in the diagnosis of MS [3]. Awareness of the imaging features of MS affecting the cord is very crucial as there is high association between cord lesions and incapability more than those with brain manifestation of MS [4]. T2W sequence is the most widely used sequence for assessment of MS plaques either in cord or in the brain [5,6]. About 90% of patients with cord MS will have high T2W hyperintense foci [6]. The most common site of cord affection in cases of MS is the cervical cord with high rate of occurrence at the posterior and lateral aspects of the cord [4]. The maximum extent of MS plaques in the cord may reach up to 6 cm average, while its short axis less than 50% of the cord diameter [7]. In acute stage, MS plaques are usually associated with edema and expansion of the cord at the level of the affection, with less
http://dx.doi.org/10.1016/j.ejrnm.2017.03.007 0378-603X/Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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degree of enhancement as compared with MS plaques of the brain [6]. In equivocal cases with questionable T2 hyperintense foci in the brain, sometime MRI of the cord may be helpful in demonstrating lesions in the cord, which may help to make the diagnosis of multiple sclerosis [6,8]. Early phase of neuromyelitis optica NMO usually spare the brain with high tendency to involve the optic nerves and cord. The length of the lesion can reach up to 3 contiguous vertebrae, and usually inclined to be centrally located within the cord substance [9,10]. Cases with acute transverse myelitis ATM, usually presented by sphincteric incontinence and paraplegia, regarding that secondary causes, of these manifestation have been ruled out, as cord infiltration by neoplasms, compression, infection, vascular malformation or trauma [11–14]. The usual MRI appearance of ATM is T2W high signal within the central part of the cord, usually with length exceeding 3 vertebral bodies and width exceeding more than 70% of the transverse diameter of the cord [15]. In some cases abnormal T2 hyperintense signal lesions may be associated with central isointensity; distinguishing ATM from other hyperintense cord lesions such as multiple sclerosis. Following intravenous contrast injection nodular or patchy enhancement may be seen at the outermost cord aspect [15,16]. Primary and secondary tumors usually presented on MRI as an ill defined T2W high intensity expanding the cord with heterogeneous post contrast enhancement [17,18]. Most ependymomas show T2W hyperintense signal. Ependymomas usually shows intense and homogeneous enhancement with well defined borders. Cap sign is a hypointense area around tumor margins limits and these caps represents haemosiderin from old hemorrhage [19]. Up to 75% of astrocytoma seen involving the cervicothoracic region, and usually of large size [17]. The lesions usually displays hyperintense signal; which represent a combination of tumor itself and the associated cord edema. Astrocytomas are usually located eccentrically in the cord. It shows heterogeneous partial post contrast enhancement. The borders of the lesions are frequently ill defined. Lesions with cystic components are typically intratumoral; however, it is sometimes associated with satellite cysts and secondary hydromyelia [20]. Haemangioblastomas are highly vascular tumors. These lesions are usually solitary, but with Von Hippel-Lindau disease multiple may be seen [21]. The typical MRI appearance of haemangioblastomas is a well defined T2 hyperintense cystic lesion, with ovoid or rounded appearance and with an intensity enhancing mural nodule. Many cases are associated with extensive hydrosyringomyelia. Large tumors frequently have signal defect due to vascular nature of the lesions [22]. It is not common for metastasis to involve the spinal cord. The highest percentage of cord metastasis seen in the cervical region next is the dorsal spine and finally the lumbar spine. Cord metastasis from lung cancer has the highest incidence; breast, kidney, colon and lymphoma are other site that can send metastasis to the cord [23]. On MR imaging the lesions typically produce long segment of mild cord expansion. The lesion usually shows central area of T1W hypointense signal, T2W hyperinensity with intense homogeneous enhancement, and disproportionate extensive amounts of perilesion edema [24,25]. Cases with myelitis after radiotherapy can either acute or chronic. The criteria for myelitis post radiotherapy includes, 1past history of exposure to radiotherapy, 2-the involved cord must be included in the radiation port, 3-finally causes of cord indentation are kept out [26].
In acute form, MRI usually negative with no appreciable signal alteration seen within the cord [27]. In the chronic form, MRI usually demonstrate an ill defined area of patchy irregular enhancement coupled with too large area of cord edema as compared to the size of the enhancing patches [28]. Focal atrophic changes of the previously irradiated portion of the cord can be seen many years latter after radiation [28]. Diffusion Tensor MR Fiber Tractography DTI has many clinical applications in brain imaging [29]. Diffusion is described as isotropic, when particles of pure material are distributed by the same degree in all ways. On the other hand when particles of certain material are oriented in certain direction as for examples the fibers of the cervical cord, diffusion is then described as anisotropic. Any causes that reduced anisotropy, will result in distorted images produced by diffusion tensor MR fiber tractography [29]. MR fiber tractography is commonly used in many applications in the brain; while in the cord there are many challenges, including the narrow area of examination contrary to that of the brain. Also the inhomogeneous area of study is another obstacle. Subsequently there are few experiments for MR fiber tractography of the cord [30].
2. Aim of the work Our goal of this research is to assess the value of MR fiber Tractography in assessment of inflammatory process and neoplasms of the cervical cord (see Figs. 1–5).
2.1. Material This study is a prospective study where patient consent was waived by the Research Ethics Board, assuring respect of the confidentiality of the medical record. We included 40 patients diagnosed as inflammatory diseases and neoplasm of the cervical cord in our research in the period from January 2014 till April 2016.
Fig. 1. 3D MR fiber tractrography; Sagittal (A) and Coronal (B); showing normal course and appearance of the cervical cord fibers tracts. No displacement. No fibers interruption.
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Fig. 2. 45 years old male patient presented by gradual onset of bilateral lower limb weakness. Sagittal T2 (A) showing focal T2 hyperintense area opposite CV5-6 level, mildly enhancing after contrast (B); fiber tractography (C) showing neither displacement nor interruption of the fibers, (type I pattern). Follow up MRI (D–F) sagittal T2, T1 and T1 post contrast, done 1 year later revealed near total resolution of the lesion, confirming its non neoplastic nature.
The study included 22 males and 18 females, their ages ranged between 12 and 66 years. Inclusion criteria include those patients with the final diagnosis of neoplastic or inflammatory cord lesions; while those with cervical cord trauma, vascular lesions and non neoplastic syringomyelia were excluded.
examination was conducted including neurological examination to assess sensory and motor deficits. All these patients had MRI imaging that was done on 1.5 Tesla Avanto unit, Siemens system. No complications were recorded during the examinations. 2.2.1. MR examination parameters
2.2. Methods All patients were subjected to detailed clinical history was taken including personal data and neurological complaints. Clinical
T2W (axial and sagittal) TSE (turbo spin echo), Time of Repetition (TR) = 3500 ms, Echo Time (TE) = 88 ms. The time of acquisition for each sequence takes about two minutes and 35 s.
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Fig. 3. 52 years old female patient presented by neck pain, bilateral upper limb numbness, 3 months after stopping neck irradiation for oral SCC. Sagittal T2 (A) abnormal hyperintense signal extending from CV2 down to CV5 Sagittal T1 pre and post contrast (B and C) showed mildly enhancing mass like lesion. Tractography (D) showing focal fibers interruption (arrow) with no fibers displacement (type II pattern). Follow up 3 months later T1W post contrast (E) showing regression of the enhancement, confirming the diagnosis of post radiation myelitis.
T1W (axial and sagittal), (pre and post contrast), Spin Echo (SE), TR = 640 ms, TE = 10 ms, matrix (256 256), field of view (FOV) = 230 mm, 3 mm slice thickness, 0.3 mm gag, with time of acquisition 3 min and 23 s for each sequence. T1W post contrast in 3D; TR = 1650 ms, TE = 295 ms, slice thickness = 1 mm with 0.3 mm gap, matrix = (256 256), FOV = 250 mm, total time of acquisition about 5 min and 18 s. The software used for reconstruction of the Diffusion Tensor imaging (DTI), is Neruro-3D soft ware produced by Siemens Healthcare. Final diagnosis was reached by histopathology in 17 patients with neoplastic lesions, and by follow up in 23 cases with inflammatory lesions (clinically and imaging) for a period at least 3 months up to more than one year. 3. Results Neck pain was the main complaint of all patients with variable associated upper or lower limb numbness and or weakness. Twenty cases had gradual onset of symptoms, and 15 patients
had subacute onset. Three patients presented by acute onset of paraparesis. Two patients had long history of quadriplegia with muscle contractures. Two patients with subacute onset had also diminished visual acuity. 17 patients out of 40 had neoplastic lesions of the cord, five had cellular ependymoma (12.5%), two anaplastic ependymoma (5%), two Fibrillary astrocytoma (5%), three anaplastic astrocytoma (7.5%), one Glioblastoma multiforme (GBM) (2.5%), one case cervicomedullary glioma (2.5%), two cases with metastasis (5%) and one case with haemangioblastoma (2.5%) Table 1. 3.1. Fiber tractography (FT) Fiber tractography patterns of intramedullary spinal cord lesions were classified according to the morphologic fiber tractography pattern for each lesion Table 2. 1. Type I pattern (20 Cases), Normal white matter tracts detected. Neither displacement, nor interruption observed, including 9 cases with myelitis and all 8 cases of MS, 2 cases of NMO, and a case with post irradiation myelopathy.
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3. Type III pattern (10 cases), major displacement without disruption of the fibers. This group included 10 neoplastic patients. 4. Type IV pattern (7 cases), displacement with disruption of the fibers. This group included 7 neoplastic lesions. 3.2. FT in spinal cord tumors In our study, all 17 neoplastic cervical cord lesions lead to white matter tract displacement and wrapping around the tumor. The fibers were always displaced by the tumor mass as the tracts were splitted and pushed laterally. In the cases with ependymoma (n = 5), we found that the fibers are displaced nearly symmetrically around the lesion, this can be explained by origin of the tumor from the central portion of the cord. Similar findings were also seen in a case of metastasis, a case of anaplastic astrocytoma, two cases of fibrillary astrocytoma and a case of cervicomedullary glioma. We observed disruption of the fibers associated with tract displacement in 7 cases with neoplasms, six of them were high grade tumors including 1 patient with recurrent GBM, two cases with anaplastic astrocytoma, two cases with anaplastic ependymoma and one case with metastatic lesion. Interrupted tracts were also noticed in one case with haemangioblastoma.
Fig. 4. 24 years old male patient presented by bilateral upper and lower limb numbness. Sagittal T1 post contrast (A) revealed homogeneously enhancing mass within the cervical cord opposite CV3 and CV4. MR Tractography (B) shows smooth displacement of the white matter tracts around the mass with no fibers interruption (white arrow) (type III pattern). Pathologically proved neoplasm (Astrocytoma).
2. Type II pattern (3 cases), focal interruption or attenuation of the fibers, including 1 case with myelitis and 2 cases with post irradiation changes. No displacement seen.
3.3. FT in inflammatory lesions FT performed in the inflammatory lesions of spinal cord including inflammatory myelitis, post irradiation myelitis, MS and NMO patients. Type I was seen in 20 cases, with no displacement or interruption of the fibers. 9 patients with myelitis, 8 patients with MS, 1 post irradiation myelitis and 2 cases with NMO. Type II was observed in 3 cases, with focal interruption of the fibers without displacement seen; one case of myelitis and 2 cases with post irradiation myelitis.
Fig. 5. (A) sagittal T2, (B) sagittal T1 post contrast showing large mass involving the whole cervical cord, with ventral dural based meningioma seen at CV1-2 level MR tractography, (C) showing displacement with interruption of the cervical cord fibers by the enhancing lesion (black arrow) (type IV pattern). The lesion proved by biopsy to be ependymoma.
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Table 1 Distribution of the studied cases according to pathology (n = 40). Pathology
No. 40 patients
% 100%
Non neoplastic Myelitis MS Post irradiation NMO (Devic’s disease)
23 10 8 3 2
57.5 25 20 7.5 5
Neoplastic Cellular ependymoma Anaplastic ependymoma Fibrillary astrocytoma Anaplastic astrocytoma GBM Cervicomedullary glioma Metastasis Hemangioblastoma
17 5 2 2 3 1 1 2 1
42.5 12.5 5 5 7.5 2.5 2.5 5 2.5
Table 2 Distribution of the studied cases according to FT pattern (n = 40). Fiber tractography pattern
No.
%
I
20 9 with myelitis 8 with MS 2 cases NMO 1 case post irradiation myelitis
50
II
3 1 case myelitis 2 cases post irradiation myelitis
7.5
III
10 All 10 patients are neoplastic
25
IV
All 7 patients are neoplastic 40
17.5 100%
4. Discussion Patients with clinical symptoms suggesting cord etiology are usually subjected to conventional MRI examination of the cord. Although conventional MRI is sensitive in detection of inflammatory processes and cord neoplasm affecting the cervical cord, in many cases the MRI picture is similar in both categories, and reaching final diagnosis is difficult [31]. Diffusion-tensor imaging (DTI) has been clinically applied in assessment of some brain pathologies, notably after technical advances in the new MRI machines [32]. Many challenges are met during application of this new technique in the spinal region, including the narrow field of examination, the complex functional organization, magnetic susceptibility, motion artifact and CSF pulsation [33]. In recent years, methodological efforts from various groups have managed to overcome some of these technical challenges. The goal of out research is to assess the clinical application of MR fiber Tractography in assessment of inflammatory process and neoplasms of the cervical cord [34]. In our study we did fiber tracking (FT) for 40 patients with inflammatory processes and neoplasm of the cervical cord. We found displacement of the white matter fibers surrounding the mass in all neoplastic lesions as they are pushed away by the tumor, but in inflammatory lesions 3D FT showed rarefaction and spreading of the fibers in T2W hyper-intense area, due to cellular infiltration of the nerve fibers by inflammatory cells. These characteristics can be helpful in differentiating inflammatory from neoplastic processes. We classified morphologic pattern of FT into, four patterns. Type I pattern (20 Cases), with normal white matter tracts detected. Neither displacement, nor interruption observed, includ-
ing 9 cases with myelitis and all 8 cases of MS, 2 cases of NMO, and a case with post irradiation myelopathy. 2. Type II pattern (3 cases), with focal interruption or attenuation of the fibers, and no displacement. This pattern was seen in one case with myelitis and 2 cases with post irradiation changes. 3. Type III pattern (10 cases), with major displacement without disruption of the fibers. This group included 10 neoplastic patients. 4. Type IV pattern (7 cases), displacement with disruption of the fibers. This group included 7 neoplastic lesions. It is very crucial to make difference by imaging between inflammatory processes and neoplasm of the cord to provide the correct management and to avoid invasive biopsy. Deterioration of the clinical course or increase size of the lesion on follow up MRI may give hand to reach the diagnosis, but it will lead to bad prognosis [35]. In our study, we found that inflammatory lesions showed normal course of the white matter tracts with or without mild spreading/separation of the fibers in 20 cases. Neither displacement, nor interruption observed. The remaining three cases showed focal disruption but still no fibers displacement. All neoplastic cervical cord lesions enrolled in the study, demonstrated displacement of the white matter tract. Ten cases without fibers interruption and seven cases with fibers interruption. In a study by Giussani et al., for assessment of inflammatory processes and neoplasm affecting the brainstem, there was marked reduction of the number of the visualized tracts in patients with inflammatory white matter diseases. On the other hand in cases with neoplasm, there was more or less change in directions of the fibers at the site of the neoplasm [36]. Giussani et al. attributed the reduction in the number of fibers tracts seen in inflammatory processes by tractography to the diminished anisotropy by the inflammatory edema. The diminished anisotropy will affect fibers tracing resulting in reduction of number of the visualized [36]. Giussani et al. also explained that the pattern in tumors can de due compression of the tumors upon the tract fibers with or without fibers invasion. Both will result in reduction of anisotropy with subsequent diminished fibers appearance on fibers tract mapping [36]. In our study we observed disruption of the fibers associated with tract displacement in 7 cases with neoplasms, 6 of them were high grade tumors including 1 patient with recurrent GBM, two cases with anaplastic astrocytoma, two cases with anaplastic ependymoma and one case with metastatic lesion. Interrupted tracts were also noticed in one case with haemangioblastoma. These lesions showed hemorrhage and cystic changes, both may affect anisotropy across the cord tracts. The disruption of the tract fibers can be explained by either true destruction of the fibers or the presence of the hemorrhage and or edema resulting in reduction in fibers anisotropy [37]. Diffusion tensor imaging fibers tractography gave information about special aspects of different types of neoplasms, as regards the pattern of growth as well as site of origin. Fibers invasion are commonly seen in astrocytic neoplasms and commonly has an eccentric location within the cord. On the other hand ependymoma usually located within the center of the cord as it grows from cells lining the central canal, resulting in displacement of fibers around the neoplasm [34,37]. In our study, cases with cellular ependymoma (n = 5), demonstrate deviation of fibers all around the centrally located tumor suggesting the diagnosis of ependymoma. Same findings were described in a review done by Thurner et al. they demonstrated that FT can help differentiation between ependymoma and astrocytoma which is clinically an important question, which determines whether or not this lesion is resectable. They described that spinal cord ependymoma, demonstrates
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fiber tracts being concentrically displaced outward at the level of the tumor rather than infiltrated or separated as with transverse myelitis or astrocytoma. In contrast to invasive astrocytoma, ependymoma has a line of cleavage with the surrounding sound fibers making it easy for operative excision [34]. Thurner et al. also illustrated that MR fiber tractography can be used to illustrate a road map for possible surgical plan to excise cord neoplasm with reduction of post surgical complication and improve post operative outcome [34,38]. As we mentioned earlier the cases of demyelinating/inflammatory disease, showed either, type I pattern (20 Cases), where there was normal course of the white matter tracts with or without mild spreading/separation of the fibers, neither displacement, nor interruption observed, including 9 cases with myelitis and all 8 cases of MS, two cases of NMO, and a case with post irradiation myelopathy, or type II pattern (3 cases) including one case of myelitis and two cases of post irradiation myelitis, in which there is attenuation of the fibers. Our data concerning the FT of the patient with inflammatory lesions of the cord almost matching with publication made by Renoux et al. evaluating Fiber Tracking in 15 patients with myelitis revealed that no fibers displacement seen at the affected regions. Only three patients had focal disrupted fibers at the affected regions. They explained that rarification of the fibers at 3D fiber tractography in T2W hyper-intense areas in cases of myelitis, are mostly due inflammatory edema [39]. After extended review of literature to know if we have recent approved consensus to use FT as imaging tool to differentiate neoplastic from non-neoplastic lesions, only few publications were noted and attempted to describe initial morphologic pattern of different pathologies separately. These qualitative characteristics of FT could be helpful in differentiating inflammatory from neoplastic processes, in the former we usually do not observe fiber disruption except for mild fiber spreading. Despite the limited studies with FT in spinal cord lesions, we suggest that assessment of FT may improve our understanding of nature as well as extent in many inflammatory process and neoplasms affecting the cord and narrow the differential diagnosis. 5. Conclusion Displacement of the white matter fibers surrounding the mass is a feature in all neoplastic lesions as they are pushed away by the tumor. In inflammatory conditions there is either normal course of the tracts or rarification and spreading of the fibers. These characteristics can be helpful in differentiating inflammatory from neoplastic processes. We recommend DTI, whenever there is focal abnormal signal in the cord particularly if it showed post contrast mass like enhancement. We should be careful when interpreting disruption of the white matter fibers surrounding the mass, due to the multiple factors that may affect anisotropy across the fibers. References [1] Fanous Andrew A, Olszewski Nathan P, et al. Idiopathic transverse myelitis mimicking an intramedullary spinal cord tumor. Case Reports Pathol 2016:1–8. [2] Thielen KR, Miller GM. Multiple sclerosis of the spinal cord: magnetic resonance appearance. J Comput Assist Tomogr 1996;20:434–8. [3] Pretorius PM, Quaghebeur G. The role of MRI in the diagnosis of MS. Clin Radiol 2003;58:434–48. [4] Tench CR, Morgan PS, Jaspan T, Auer DP, Constantinescu CS. Spinal cord imaging in multiple sclerosis. J Neuroimaging 2005;15:94S–102S. [5] Hittmair K, Mallek R, Prayer D, Schindler EG, Kollegger H. Spinal cord lesions in patients with multiple sclerosis: comparison of MR pulse sequences. AJNR 1996;17:1555–65.
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