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MR neurography of lumbosacral nerve roots: Diagnostic value in chronic inflammatory demyelinating polyradiculoneuropathy and correlation with electrophysiological parameters
European Journal of Radiology 124 (2020) 108816
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Research article
MR neurography of lumbosacral nerve roots: Diagnostic value in chronic inflammatory demyelinating polyradiculoneuropathy and correlation with electrophysiological parameters
T
Fei Wua,1, Weiwei Wanga,1, Yanyin Zhaob, Bingyou Liub, Yin Wanga, Yang Yanga, Yan Rena,*,1, Hanqiu Liua,*,1 a b
Department of Radiology, Huashan Hospital, Fudan University, 12 Middle Wulumuqi Rd, Shanghai, 200040, China Department of Neurology, Huashan Hospital, Fudan University, 12 Middle Wulumuqi Rd, Shanghai, 200040, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Chronic inflammatory demyelinating polyneuropathy Lumbosacral plexus MR neurography Electrophysiology
Purpose: MR neurography(MRN) is an advanced imaging technique to visualize peripheral nerves. Our aim was to determine the value of morphological features of lumbosacral nerve roots on MRN in diagnosing chronic inflammatory demyelinating polyradiculoneuropathy(CIDP) and analyze their correlations with electrophysiological parameters. Methods: MRN of lumbosacral plexus was performed in 21 CIDP patients and 21 healthy volunteers. The crosssectional areas(CSAs) and signal intensities(SI) of L3 to S1 nerve roots were measured and compared between two groups. Receiver operating characteristic(ROC) curves were plotted to assess the diagnostic accuracy. All patients also underwent nerve conduction studies. Correlations between CSAs and SI of lumbosacral nerve roots and electrophysiological parameters were analyzed. Results: Compared with control group, CIDP patients showed significantly increased CSAs and SI from L3 to S1 nerve root (P < 0.001 and P < 0.05 respectively for all nerve roots). The CSAmean and SImean were 28.04 ± 8.55mm2, 1.314 ± 0.199 for patient group and 14.91 ± 2.36mm2,1.155 ± 0.094 for control group. ROC analysis revealed the best diagnostic accuracy for the CSAmean with an area under the curve of 0.968 and optimal cut-off value of 19.20 mm2. CSAs of L5 or S1 nerve root correlated positively with central latency and negatively with conduction velocity of tibial nerve. SI of L5 also had a positive correlation with latency of sural nerve. Conclusions: Evaluation of lumbosacral nerve roots on MRN in a quantitative manner may serve as an important tool to support the diagnosis of CIDP.
1. Introduction Chronic inflammatory demyelinating polyradiculoneuropathy (CIDP) is the most common immune-mediated inflammatory polyneuropathy, which is typically characterized by symmetrical involvement and proximal as well as distal muscle weakness [1,2]. The pathological hallmarks of CIDP are demyelination and remyelination [3]. Evidence from postmortem and electrophysiology studies proved that demyelinative lesions initially affected spinal nerve roots, and then
extended to nerve trunks and distal nerve segments [4–8]. Clinical treatments for CIDP include intravenous immunoglobulin, corticosteroids and plasm exchange. Timely treatment for the CIDP patients requires early and accurate diagnosis by evaluating proximal spinal nerve roots, which is crucial to rescue patients in early stages and prevent secondary axon injury [2]. However, existing examinations like nerve conduction studies and high-resolution ultrasound are unable to detect abnormalities of spinal nerve roots due to the deep anatomy. MR neurography(MRN), also known as MR imaging of peripheral
Abbreviations: CIDP, chronic inflammatory demyelinating polyradiculopathy; MRN, MR neurography; CSA, cross-sectional area; SI, signal intensity; MCV, conduction velocity of motor nerve; SCV, sensory velocity of sensory nerve; CMAP, compound muscle action potential; SNAP, sensory nerve action potential; 3D MERGE, three-dimensional multiple echo recalled gradient echo; ROC, receiver operating characteristic; AUC, area under the curve ⁎ Corresponding authors. E-mail addresses: [email protected] (F. Wu), [email protected] (W. Wang), [email protected] (Y. Zhao), [email protected] (B. Liu), [email protected] (Y. Wang), [email protected] (Y. Yang), [email protected] (Y. Ren), [email protected] (H. Liu). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.ejrad.2020.108816 Received 23 August 2019; Received in revised form 12 December 2019; Accepted 26 December 2019 0720-048X/ © 2020 Published by Elsevier B.V.
European Journal of Radiology 124 (2020) 108816
F. Wu, et al.
Fig. 1. Detailed procedures of measuring CSA and signal intensity of S1 nerve root. A: Draw a transverse line at the middle of S1/S2 intervertebral disc and this line was defined as the slice to measure CSA and signal intensity. B: Located bilateral S1 nerve roots and psoas muscle on the predefined slice of reconstructed axial images. Draw ROIs manually around the boundary of SI nerve roots. And lastly, place an ROI with the similar size as S1 nerve root in the psoas muscle.
conduction velocity of motor nerves(MCV) and F-wave minimal latency were recorded. Central latency was calculated as (F-M-1)/2, where F and M were latencies of the F wave and M wave respectively [23,24]. The latency, conduction velocity (SCV) and sensory nerve action potential (SNAP) amplitude of sensory nerves were also recorded.
Nerves, is an advanced MR technique that can help delineate deep nerves conspicuously and locate lesions accurately. First proposed by Filler in 1992, it combined fat suppression technique and T2-weighted sequence to suppress fat tissue around peripheral nerves and emphasize nerve signal [9–11]. To date, MRN has been widely applied for the diagnosis of various peripheral neuropathies, including entrapment, injury, neoplasm and inflammatory neuropathies such as CIDP [10,12–19]. Previous studies of CIDP mainly focused on the imaging of the brachial plexus and cervical nerve roots, whereas few studies have evaluated morphologic changes in the lumbosacral region [2,20,21]. To the best of our knowledge, lumbosacral nerve roots and cauda equina were reported to be more frequently involved in CIDP patients [5]. Therefore, in this study, we aimed to explore the value of lumbosacral nerve roots on MRN in the diagnosis of CIDP by quantifying cross-sectional areas (CSAs) and signal intensity(SI) of L3 to S1 nerve roots, and to analyze their correlations with electrophysiological parameters of lower extremities.
2.3. MRN and measurements
Inclusion criteria: patients who met the diagnostic criteria of CIDP by European Federation of Neurological Societies/Peripheral Nerve Society 2010 from June 2016 to April 2019 from our neuromuscular clinic (n = 34) [22]. Exclusion criteria: a) patients in combination with other peripheral neuropathies, such as Charcot-Marie-Tooth disease type 1A (n = 2) b) patients suffering from severe lumbar disc herniation (n = 7) c) patients with injury (n = 1), neoplasm (n = 0) and operation history (n = 2) in lumbosacral region d) patients with contraindications to MRI like claustrophobia (n = 1) A total of 21 CIDP patients were included in the patient group. All patients have undergone comprehensive neurological examination, nerve conduction studies and MRI scan. 21 healthy volunteers with sex and age matched were recruit in the control group. All volunteers underwent MRI scan with the same protocol as CIDP patients. This study was approved by our hospital’s ethic committee and informed consents were obtained from all subjects.
All subjects underwent MR imaging of lumbosacral plexuses with a 3.0 T MR scanner (Discovery MR750 3.0 T scanner-GE healthcare) using a spine surface array coil. In this study, we applied three-dimensional multiple echo recalled gradient echo (3D MERGE) sequence to visualize the L3 to S1 spinal nerves and the parameters of coronal 3D MERGE sequence were as follows: TR/TE: 33/11 ms; slice: 76; slice thickness: 2.0 mm; FOV: 380 × 380 mm; matrix size: 288 × 288; scanning time: 3 min and 33 s. Post-processing measurements of all images were accomplished by two radiologists independently (W-F, W-W-W; 3 and 6 years of experience in the department of neuroradiology respectively) on GE ADW 4.6 workstation who were blinded to subjects’ profiles. The CSAs and SI of lumbosacral nerve roots were measured on reconstructed axial 3D MERGE images. Detailed procedures were as follows (take S1 for example) [25]: Firstly, drew a transverse line at the middle of S1/S2 intervertebral disc and this line was defined as the slice to measure CSA and SI. Secondly, located bilateral S1 nerve roots and adjacent psoas muscle on the predefined slice of reconstructed axial images. Thirdly, drew ROIs manually around the boundary of SI nerve roots. And lastly, placed a ROI with the similar size as S1 nerve root in the psoas muscle. The signal intensity of S1 nerve root was defined as SI (S1 nerve root)/ SI (psoas muscle) [21]. The same method was used to measure the CSAs and SI of L3, L4 and L5 nerve roots. (Fig. 1) The measurements were repeated three times by each observer and the average values were used. For each subject, CSAmean and SImean were calculated by averaging over all 4 slices. To investigate the intra observer variability, one of the radiologist (W-F) repeated the post-processing and the measurements after two months. The reliability and reproducibility were investigated by calculating intraclass correlation coefficients (ICCs).
2.2. Nerve conduction studies
2.4. Statistically analysis
All CIDP patients underwent nerve conduction studies performed by a board-certified neurologist (Q-K, with more than 10 years’ experience in electrodiagnostic department) with skin temperature of lower extremities maintaining at 31 °C. The motor nerve conduction studies were carried out on bilateral tibial nerves and common peroneal nerves. The sensory nerve conduction studies were performed antidromically on bilateral sural nerves and superficial peroneal nerves. The distal latency, compound muscle action potential (CMAP) amplitude,
Statistical analysis was conducted on SPSS (version 22.0) and P < 0.05 was considered statistically significant unless stated otherwise. All values were shown as Mean ± SD. Independent -samples t-test was performed to compare the differences of size and signal in two groups. Additionally, receiver operating characteristic(ROC) curves in different slices were performed to assess the diagnostic accuracy of CSAs and SI. Pearson correlation tests were used for continuous variables satisfying normal distribution while Spearman correlation tests
2. Materials and methods 2.1. Subjects
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were used for the correlation between central latency of tibial nerve and other parameters because data of central latency showed a nonnormal distribution. 3. Results 3.1. Clinical characteristics A total of 21 subjects were enrolled in CIDP group including 8 females and 13 males. Their ages ranged from 28 to 67 years old and mean age ± SD was 51.3 ± 14.7 years old. Disease duration at the time of study varied dramatically, ranging from 2 months to 84 months and the median disease duration was 7 months. In CIDP group, one patient was diagnosed as Lewis-Sumner Syndrome and another one as distal acquired demyelinating symmetric neuropathy. All the rest patients met the diagnostic criteria of typical CIDP. By the time of this study was conducted, 14 patients had received treatments, including intravenous immunoglobulin, oral steroids or plasm exchange. Detailed patients’ profiles were summarized in supplementary Table 1. 21 healthy volunteers were enrolled in our control group, with age and sex matched. Their ages ranged from 24 to 68 years old and mean age ± SD was 51.2 ± 15.0 years old.
Fig. 3. ROC curves of L3 to S1 nerve root CSA and CSAmean.
3.2. CSAs of lumbosacral nerve roots Compared to healthy control group, patients with CIDP exhibited significantly enlarged nerve root CSA in all slices (P < 0.001 for all nerve roots, Fig. 2). The average values of four nerve roots were 28.04 ± 8.55mm2 for CIDP patients and 14.91 ± 2.36mm2 for control group. The CSAs of individual nerve root were shown in the supplementary Table 2. ROC curves of different slices showed the CSAmean had the best diagnostic value, with the area under the curve(AUC) 0.968 (Fig. 3). When the cut-off value was 19.20 mm2, it had a sensitivity of 85.7 % and a specificity of 100 %. The inter observer variability ranged from 0.732 to 0.918 and the intra observer variability ranged from 0.750 to 0.935, which indicated moderate reliability and reproducibility. (supplementary Table 3)
Fig. 4. SI of L3 to S1 nerve roots and SImean in CIDP and control group. * P < 0.05.
3.3. SI of lumbosacral nerve roots The SI of L3, L4, L5 and S1 nerve roots was significantly higher in CIDP patients than that in control group (P < 0.05 for all nerve roots, Fig. 4). The SImean was 1.314 ± 0.199 in CIDP patients and 1.155 ± 0.094 in control subject. The signal values of L3 to S1 nerve roots were shown in the supplementary Table2. ROC curves showed the diagnostic performance was best for signal intensity of L4 nerve roots with an AUC of 0.763 and cut-off value of 1.066 (Fig. 5). The SImean showed an AUC of 0.739 in ROC analysis. The inter observer variability ranged from 0.718 to 0.828 and the intra observer variability ranged from 0.736 to 0.948, which meant good reliability and reproducibility.
Fig. 5. ROC curves of L3 to S1 nerve root SI and SImean.
(supplementary Table 3)
3.4. Correlations with clinical and electrophysiological parameters F-wave of common peroneal nerve was not provoked in more than half of the patients so its central latency was not analyzed in this study. Correlations between morphological parameters of each spinal nerve root, clinical and electrophysiological indices were shown in supplementary Table 4. The CSAs of L5 and S1 nerve roots correlated positively with central
Fig. 2. CSAs of L3 to S1 nerve roots and CSAmean in CIDP and control group. **P < 0.001. 3
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Fig. 6. Correlations between morphological indices of L4, L5 and S1 nerve roots and electrophysiological parameters. A, correlation of L5 nerve root CSA with conduction velocity of tibial nerve; B, correlation of L5 nerve root CSA with central latency of tibial nerve; C, correlation of L5 nerve root CSA with CMAP amplitude of tibial nerve; D, correlation of S1 nerve root CSA with conduction velocity of tibial nerve; E, correlation of L5 nerve root SI with latency of sural nerve; F, correlation of L4 nerve root SI with SNAP amplitude of sural nerve * P < 0.05
indices were not significant either.
latency of tibial nerve (P = 0.046 and P = 0.002 respectively). L5 nerve root showed an inverse correlation between CSA and conduction velocity of tibial nerve (P = 0.027). Additionally, CSA of L5 nerve root correlated inversely with CMAP amplitude of tibial nerve (P = 0.010) (Fig. 6). No correlations were found between CSAs of lumbosacral nerve roots and electrophysiological parameters of common peroneal nerve and sensory nerves. The SI of L5 nerve root correlated positively with the latency of sural nerve (P = 0.040). L4 nerve root showed a negative correlation between the SI and SNAP amplitude of sural nerve (P = 0.040) (Fig. 6). There was no significant correlation between SI of L3 to S1 nerve roots and electrophysiological parameters of superficial peroneal nerve and motor nerves. The correlations between morphological parameters and clinical
4. Discussion In this study, we quantified the size and signal of L3 to S1 nerve roots in 21 CIDP patients and 21 volunteers with MR Neurography. Compared to healthy controls, CIDP patients exhibited significantly increased cross-sectional areas as well as signal intensity in every single nerve root, which was caused by the proliferation of Schwann cell and the edema in the endoneurium [6,26]. Up to now, few studies have systematically evaluated the morphological features of lumbosacral nerve roots of CIDP patients on MRN quantitatively. Tazawa et al. assessed only size but not signal of lumbosacral nerve roots in CIDP patients with STIR [20]. They didn’t 4
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conduction examinations.
evaluate the nerve roots of healthy subjects either, for lumbosacral plexuses of them were hard to identify in MR images. In STIR images, vessels adjacent to spinal nerves were hyperintense and could impede the delineation of spinal nerves and influence the measurement of signal intensity. We instead utilized 3D MERGE to visualize all subjects’ lumbosacral spinal nerves in this study because it had a higher SNR and cost much less time than STIR [25]. Kronlage et al. measured CSA as well as SI of two lumbosacral nerve roots whereas our study had a larger coverage. In our research, CIDP patients showed hypertrophic nerve roots with increased signal intensity in every single nerve root, which has nerve been investigated in detail before. ROC analysis demonstrated that nerve root CSA had a better diagnostic performance than the signal, which was compatible with the results of prior study [21]. When the average CSA of L3 to S1 nerve roots was 19.20 mm2, it could distinguish CIDP patients from healthy people, yielding a sensitivity of 85.7 % and specificity of 100 %. We believed this finding was valuable, since it provided an important reference value in clinical practice. Another important finding was the correlation between morphological indices of lumbosacral nerve roots and electrophysiological parameters of lower extremities. The central latency of tibial nerve prolonged while the conduction velocity decreased with the increase of L5 or S1 CSA. Here we used central latency instead of minimal latency of F-wave, for it represented the conduction time from cord to stimulus sites, reflecting demyelinative damage of proximal nerve roots more precisely [23]. The SI of nerve roots also demonstrated a good correlation with electrophysiological parameters and the latency of sural nerve prolonged with the increase of L5 nerve root signal intensity. As is known, central latency and conduction velocity of motor nerves as well as latency of sensory nerves were electrophysiological parameters in demyelinating neuropathy. Considering fibers from L5 and S1 nerve root participate in the formation of tibial and sural nerves, these results suggested that higher CSA and SI of L5 and S1 nerve roots correlated with more demyelination of tibial and sural nerves and morphological changes of lumbosacral nerve roots could reflect the impairment of nerve conduction function in both motor and sensory nerves of lower extremities [20]. Additionally, there was an interesting point that SI of L4 and CSA of L5 correlated inversely with the amplitude of tibial CMAP and sural SNAP respectively, which seemed contradictory to the above results. In severe CIDP, demyelination could trigger secondary axon loss. We speculated patients in this cohort had relatively severe conditions so that nerve axons were involved as well. Our study has some limitations. First, the sample size is relatively small. Second, due to a low prevalence, we didn’t examine other peripheral neuropathies such as multifocal motor neuropathy, which had a different distribution of nerve hypertrophy in brachial plexus [27,28]. In the future, we will further enlarge our patient cohort and assess both brachial and lumbosacral plexus to investigate the value of MRN in the differential diagnosis of peripheral nerve disorders. In conclusion, CIDP patients showed significantly hypertrophic lumbosacral nerve roots with increased signal intensity on MRN, some of which correlated well with electrophysiological parameters with regard to demyelination. ROC curves demonstrated CSAmean had the best diagnostic performance with cut-off value 19.20 mm2. Quantification of lumbosacral nerve roots on MRN may serve as an important supporting diagnostic tool in CIDP.
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.ejrad.2020.108816. References [1] H.C. Lehmann, D. Burke, S. Kuwabara, Chronic inflammatory demyelinating polyneuropathy: update on diagnosis, immunopathogenesis and treatment, J. Neurol. Neurosurg. Psychiatry (2019) 2019-320314. [2] C. Bunschoten, B.C. Jacobs, P. Van den Bergh, D.R. Cornblath, P.A. van Doorn, Progress in diagnosis and treatment of chronic inflammatory demyelinating polyradiculoneuropathy, Lancet Neurol. 18 (8) (2019) 784–794. [3] J.M. Vallat, C. Sommer, L. Magy, Chronic inflammatory demyelinating polyradiculoneuropathy: diagnostic and therapeutic challenges for a treatable condition, Lancet Neurol. 9 (4) (2010) 402–412. [4] S. Kuwabara, K. Ogawara, S. Misawa, M. Mori, T. Hattori, Distribution patterns of demyelination correlate with clinical profiles in chronic inflammatory demyelinating polyneuropathy, J. Neurol. 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[19] M. Kronlage, K. Pitarokoili, D. Schwarz, T. Godel, S. Heiland, M. Yoon, M. Bendszus, P. Bäumer, Diffusion tensor imaging in chronic inflammatory demyelinating polyneuropathy, Invest. Radiol. 52 (11) (2017) 701–707. [20] K. Tazawa, M. Matsuda, T. Yoshida, Y. Shimojima, T. Gono, H. Morita, T. Kaneko, H. Ueda, S. Ikeda, Spinal nerve root hypertrophy on MRI: clinical significance in the diagnosis of chronic inflammatory demyelinating polyradiculoneuropathy, Intern. Med. 47 (23) (2008) 2019–2024. [21] M. Kronlage, P. Bäumer, K. Pitarokoili, D. Schwarz, V. Schwehr, T. Godel, S. Heiland, R. Gold, M. Bendszus, M. Yoon, Large coverage MR neurography in CIDP: diagnostic accuracy and electrophysiological correlation, J. Neurol. 264 (7) (2017) 1434–1443. [22] P.Y. Van den Bergh, R.D. Hadden, P. Bouche, D.R. Cornblath, A. Hahn, I. Illa, C.L. Koski, J.M. Leger, E. Nobile-Orazio, J. Pollard, C. 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Declaration of Competing Interest The authors have no conflicts of interest to declare. Acknowledgments This work was supported by the National Key Research and Development Plan (Grant No. 2017YFC0112904). We are grateful to Jing Wang for her writing assistance and Kai Qiao for her job in nerve 5
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European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Research article
MR neurography of lumbosacral nerve roots: Diagnostic value in chronic inflammatory demyelinating polyradiculoneuropathy and correlation with electrophysiological parameters
T
Fei Wua,1, Weiwei Wanga,1, Yanyin Zhaob, Bingyou Liub, Yin Wanga, Yang Yanga, Yan Rena,*,1, Hanqiu Liua,*,1 a b
Department of Radiology, Huashan Hospital, Fudan University, 12 Middle Wulumuqi Rd, Shanghai, 200040, China Department of Neurology, Huashan Hospital, Fudan University, 12 Middle Wulumuqi Rd, Shanghai, 200040, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Chronic inflammatory demyelinating polyneuropathy Lumbosacral plexus MR neurography Electrophysiology
Purpose: MR neurography(MRN) is an advanced imaging technique to visualize peripheral nerves. Our aim was to determine the value of morphological features of lumbosacral nerve roots on MRN in diagnosing chronic inflammatory demyelinating polyradiculoneuropathy(CIDP) and analyze their correlations with electrophysiological parameters. Methods: MRN of lumbosacral plexus was performed in 21 CIDP patients and 21 healthy volunteers. The crosssectional areas(CSAs) and signal intensities(SI) of L3 to S1 nerve roots were measured and compared between two groups. Receiver operating characteristic(ROC) curves were plotted to assess the diagnostic accuracy. All patients also underwent nerve conduction studies. Correlations between CSAs and SI of lumbosacral nerve roots and electrophysiological parameters were analyzed. Results: Compared with control group, CIDP patients showed significantly increased CSAs and SI from L3 to S1 nerve root (P < 0.001 and P < 0.05 respectively for all nerve roots). The CSAmean and SImean were 28.04 ± 8.55mm2, 1.314 ± 0.199 for patient group and 14.91 ± 2.36mm2,1.155 ± 0.094 for control group. ROC analysis revealed the best diagnostic accuracy for the CSAmean with an area under the curve of 0.968 and optimal cut-off value of 19.20 mm2. CSAs of L5 or S1 nerve root correlated positively with central latency and negatively with conduction velocity of tibial nerve. SI of L5 also had a positive correlation with latency of sural nerve. Conclusions: Evaluation of lumbosacral nerve roots on MRN in a quantitative manner may serve as an important tool to support the diagnosis of CIDP.
1. Introduction Chronic inflammatory demyelinating polyradiculoneuropathy (CIDP) is the most common immune-mediated inflammatory polyneuropathy, which is typically characterized by symmetrical involvement and proximal as well as distal muscle weakness [1,2]. The pathological hallmarks of CIDP are demyelination and remyelination [3]. Evidence from postmortem and electrophysiology studies proved that demyelinative lesions initially affected spinal nerve roots, and then
extended to nerve trunks and distal nerve segments [4–8]. Clinical treatments for CIDP include intravenous immunoglobulin, corticosteroids and plasm exchange. Timely treatment for the CIDP patients requires early and accurate diagnosis by evaluating proximal spinal nerve roots, which is crucial to rescue patients in early stages and prevent secondary axon injury [2]. However, existing examinations like nerve conduction studies and high-resolution ultrasound are unable to detect abnormalities of spinal nerve roots due to the deep anatomy. MR neurography(MRN), also known as MR imaging of peripheral
Abbreviations: CIDP, chronic inflammatory demyelinating polyradiculopathy; MRN, MR neurography; CSA, cross-sectional area; SI, signal intensity; MCV, conduction velocity of motor nerve; SCV, sensory velocity of sensory nerve; CMAP, compound muscle action potential; SNAP, sensory nerve action potential; 3D MERGE, three-dimensional multiple echo recalled gradient echo; ROC, receiver operating characteristic; AUC, area under the curve ⁎ Corresponding authors. E-mail addresses: [email protected] (F. Wu), [email protected] (W. Wang), [email protected] (Y. Zhao), [email protected] (B. Liu), [email protected] (Y. Wang), [email protected] (Y. Yang), [email protected] (Y. Ren), [email protected] (H. Liu). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.ejrad.2020.108816 Received 23 August 2019; Received in revised form 12 December 2019; Accepted 26 December 2019 0720-048X/ © 2020 Published by Elsevier B.V.
European Journal of Radiology 124 (2020) 108816
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Fig. 1. Detailed procedures of measuring CSA and signal intensity of S1 nerve root. A: Draw a transverse line at the middle of S1/S2 intervertebral disc and this line was defined as the slice to measure CSA and signal intensity. B: Located bilateral S1 nerve roots and psoas muscle on the predefined slice of reconstructed axial images. Draw ROIs manually around the boundary of SI nerve roots. And lastly, place an ROI with the similar size as S1 nerve root in the psoas muscle.
conduction velocity of motor nerves(MCV) and F-wave minimal latency were recorded. Central latency was calculated as (F-M-1)/2, where F and M were latencies of the F wave and M wave respectively [23,24]. The latency, conduction velocity (SCV) and sensory nerve action potential (SNAP) amplitude of sensory nerves were also recorded.
Nerves, is an advanced MR technique that can help delineate deep nerves conspicuously and locate lesions accurately. First proposed by Filler in 1992, it combined fat suppression technique and T2-weighted sequence to suppress fat tissue around peripheral nerves and emphasize nerve signal [9–11]. To date, MRN has been widely applied for the diagnosis of various peripheral neuropathies, including entrapment, injury, neoplasm and inflammatory neuropathies such as CIDP [10,12–19]. Previous studies of CIDP mainly focused on the imaging of the brachial plexus and cervical nerve roots, whereas few studies have evaluated morphologic changes in the lumbosacral region [2,20,21]. To the best of our knowledge, lumbosacral nerve roots and cauda equina were reported to be more frequently involved in CIDP patients [5]. Therefore, in this study, we aimed to explore the value of lumbosacral nerve roots on MRN in the diagnosis of CIDP by quantifying cross-sectional areas (CSAs) and signal intensity(SI) of L3 to S1 nerve roots, and to analyze their correlations with electrophysiological parameters of lower extremities.
2.3. MRN and measurements
Inclusion criteria: patients who met the diagnostic criteria of CIDP by European Federation of Neurological Societies/Peripheral Nerve Society 2010 from June 2016 to April 2019 from our neuromuscular clinic (n = 34) [22]. Exclusion criteria: a) patients in combination with other peripheral neuropathies, such as Charcot-Marie-Tooth disease type 1A (n = 2) b) patients suffering from severe lumbar disc herniation (n = 7) c) patients with injury (n = 1), neoplasm (n = 0) and operation history (n = 2) in lumbosacral region d) patients with contraindications to MRI like claustrophobia (n = 1) A total of 21 CIDP patients were included in the patient group. All patients have undergone comprehensive neurological examination, nerve conduction studies and MRI scan. 21 healthy volunteers with sex and age matched were recruit in the control group. All volunteers underwent MRI scan with the same protocol as CIDP patients. This study was approved by our hospital’s ethic committee and informed consents were obtained from all subjects.
All subjects underwent MR imaging of lumbosacral plexuses with a 3.0 T MR scanner (Discovery MR750 3.0 T scanner-GE healthcare) using a spine surface array coil. In this study, we applied three-dimensional multiple echo recalled gradient echo (3D MERGE) sequence to visualize the L3 to S1 spinal nerves and the parameters of coronal 3D MERGE sequence were as follows: TR/TE: 33/11 ms; slice: 76; slice thickness: 2.0 mm; FOV: 380 × 380 mm; matrix size: 288 × 288; scanning time: 3 min and 33 s. Post-processing measurements of all images were accomplished by two radiologists independently (W-F, W-W-W; 3 and 6 years of experience in the department of neuroradiology respectively) on GE ADW 4.6 workstation who were blinded to subjects’ profiles. The CSAs and SI of lumbosacral nerve roots were measured on reconstructed axial 3D MERGE images. Detailed procedures were as follows (take S1 for example) [25]: Firstly, drew a transverse line at the middle of S1/S2 intervertebral disc and this line was defined as the slice to measure CSA and SI. Secondly, located bilateral S1 nerve roots and adjacent psoas muscle on the predefined slice of reconstructed axial images. Thirdly, drew ROIs manually around the boundary of SI nerve roots. And lastly, placed a ROI with the similar size as S1 nerve root in the psoas muscle. The signal intensity of S1 nerve root was defined as SI (S1 nerve root)/ SI (psoas muscle) [21]. The same method was used to measure the CSAs and SI of L3, L4 and L5 nerve roots. (Fig. 1) The measurements were repeated three times by each observer and the average values were used. For each subject, CSAmean and SImean were calculated by averaging over all 4 slices. To investigate the intra observer variability, one of the radiologist (W-F) repeated the post-processing and the measurements after two months. The reliability and reproducibility were investigated by calculating intraclass correlation coefficients (ICCs).
2.2. Nerve conduction studies
2.4. Statistically analysis
All CIDP patients underwent nerve conduction studies performed by a board-certified neurologist (Q-K, with more than 10 years’ experience in electrodiagnostic department) with skin temperature of lower extremities maintaining at 31 °C. The motor nerve conduction studies were carried out on bilateral tibial nerves and common peroneal nerves. The sensory nerve conduction studies were performed antidromically on bilateral sural nerves and superficial peroneal nerves. The distal latency, compound muscle action potential (CMAP) amplitude,
Statistical analysis was conducted on SPSS (version 22.0) and P < 0.05 was considered statistically significant unless stated otherwise. All values were shown as Mean ± SD. Independent -samples t-test was performed to compare the differences of size and signal in two groups. Additionally, receiver operating characteristic(ROC) curves in different slices were performed to assess the diagnostic accuracy of CSAs and SI. Pearson correlation tests were used for continuous variables satisfying normal distribution while Spearman correlation tests
2. Materials and methods 2.1. Subjects
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were used for the correlation between central latency of tibial nerve and other parameters because data of central latency showed a nonnormal distribution. 3. Results 3.1. Clinical characteristics A total of 21 subjects were enrolled in CIDP group including 8 females and 13 males. Their ages ranged from 28 to 67 years old and mean age ± SD was 51.3 ± 14.7 years old. Disease duration at the time of study varied dramatically, ranging from 2 months to 84 months and the median disease duration was 7 months. In CIDP group, one patient was diagnosed as Lewis-Sumner Syndrome and another one as distal acquired demyelinating symmetric neuropathy. All the rest patients met the diagnostic criteria of typical CIDP. By the time of this study was conducted, 14 patients had received treatments, including intravenous immunoglobulin, oral steroids or plasm exchange. Detailed patients’ profiles were summarized in supplementary Table 1. 21 healthy volunteers were enrolled in our control group, with age and sex matched. Their ages ranged from 24 to 68 years old and mean age ± SD was 51.2 ± 15.0 years old.
Fig. 3. ROC curves of L3 to S1 nerve root CSA and CSAmean.
3.2. CSAs of lumbosacral nerve roots Compared to healthy control group, patients with CIDP exhibited significantly enlarged nerve root CSA in all slices (P < 0.001 for all nerve roots, Fig. 2). The average values of four nerve roots were 28.04 ± 8.55mm2 for CIDP patients and 14.91 ± 2.36mm2 for control group. The CSAs of individual nerve root were shown in the supplementary Table 2. ROC curves of different slices showed the CSAmean had the best diagnostic value, with the area under the curve(AUC) 0.968 (Fig. 3). When the cut-off value was 19.20 mm2, it had a sensitivity of 85.7 % and a specificity of 100 %. The inter observer variability ranged from 0.732 to 0.918 and the intra observer variability ranged from 0.750 to 0.935, which indicated moderate reliability and reproducibility. (supplementary Table 3)
Fig. 4. SI of L3 to S1 nerve roots and SImean in CIDP and control group. * P < 0.05.
3.3. SI of lumbosacral nerve roots The SI of L3, L4, L5 and S1 nerve roots was significantly higher in CIDP patients than that in control group (P < 0.05 for all nerve roots, Fig. 4). The SImean was 1.314 ± 0.199 in CIDP patients and 1.155 ± 0.094 in control subject. The signal values of L3 to S1 nerve roots were shown in the supplementary Table2. ROC curves showed the diagnostic performance was best for signal intensity of L4 nerve roots with an AUC of 0.763 and cut-off value of 1.066 (Fig. 5). The SImean showed an AUC of 0.739 in ROC analysis. The inter observer variability ranged from 0.718 to 0.828 and the intra observer variability ranged from 0.736 to 0.948, which meant good reliability and reproducibility.
Fig. 5. ROC curves of L3 to S1 nerve root SI and SImean.
(supplementary Table 3)
3.4. Correlations with clinical and electrophysiological parameters F-wave of common peroneal nerve was not provoked in more than half of the patients so its central latency was not analyzed in this study. Correlations between morphological parameters of each spinal nerve root, clinical and electrophysiological indices were shown in supplementary Table 4. The CSAs of L5 and S1 nerve roots correlated positively with central
Fig. 2. CSAs of L3 to S1 nerve roots and CSAmean in CIDP and control group. **P < 0.001. 3
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Fig. 6. Correlations between morphological indices of L4, L5 and S1 nerve roots and electrophysiological parameters. A, correlation of L5 nerve root CSA with conduction velocity of tibial nerve; B, correlation of L5 nerve root CSA with central latency of tibial nerve; C, correlation of L5 nerve root CSA with CMAP amplitude of tibial nerve; D, correlation of S1 nerve root CSA with conduction velocity of tibial nerve; E, correlation of L5 nerve root SI with latency of sural nerve; F, correlation of L4 nerve root SI with SNAP amplitude of sural nerve * P < 0.05
indices were not significant either.
latency of tibial nerve (P = 0.046 and P = 0.002 respectively). L5 nerve root showed an inverse correlation between CSA and conduction velocity of tibial nerve (P = 0.027). Additionally, CSA of L5 nerve root correlated inversely with CMAP amplitude of tibial nerve (P = 0.010) (Fig. 6). No correlations were found between CSAs of lumbosacral nerve roots and electrophysiological parameters of common peroneal nerve and sensory nerves. The SI of L5 nerve root correlated positively with the latency of sural nerve (P = 0.040). L4 nerve root showed a negative correlation between the SI and SNAP amplitude of sural nerve (P = 0.040) (Fig. 6). There was no significant correlation between SI of L3 to S1 nerve roots and electrophysiological parameters of superficial peroneal nerve and motor nerves. The correlations between morphological parameters and clinical
4. Discussion In this study, we quantified the size and signal of L3 to S1 nerve roots in 21 CIDP patients and 21 volunteers with MR Neurography. Compared to healthy controls, CIDP patients exhibited significantly increased cross-sectional areas as well as signal intensity in every single nerve root, which was caused by the proliferation of Schwann cell and the edema in the endoneurium [6,26]. Up to now, few studies have systematically evaluated the morphological features of lumbosacral nerve roots of CIDP patients on MRN quantitatively. Tazawa et al. assessed only size but not signal of lumbosacral nerve roots in CIDP patients with STIR [20]. They didn’t 4
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conduction examinations.
evaluate the nerve roots of healthy subjects either, for lumbosacral plexuses of them were hard to identify in MR images. In STIR images, vessels adjacent to spinal nerves were hyperintense and could impede the delineation of spinal nerves and influence the measurement of signal intensity. We instead utilized 3D MERGE to visualize all subjects’ lumbosacral spinal nerves in this study because it had a higher SNR and cost much less time than STIR [25]. Kronlage et al. measured CSA as well as SI of two lumbosacral nerve roots whereas our study had a larger coverage. In our research, CIDP patients showed hypertrophic nerve roots with increased signal intensity in every single nerve root, which has nerve been investigated in detail before. ROC analysis demonstrated that nerve root CSA had a better diagnostic performance than the signal, which was compatible with the results of prior study [21]. When the average CSA of L3 to S1 nerve roots was 19.20 mm2, it could distinguish CIDP patients from healthy people, yielding a sensitivity of 85.7 % and specificity of 100 %. We believed this finding was valuable, since it provided an important reference value in clinical practice. Another important finding was the correlation between morphological indices of lumbosacral nerve roots and electrophysiological parameters of lower extremities. The central latency of tibial nerve prolonged while the conduction velocity decreased with the increase of L5 or S1 CSA. Here we used central latency instead of minimal latency of F-wave, for it represented the conduction time from cord to stimulus sites, reflecting demyelinative damage of proximal nerve roots more precisely [23]. The SI of nerve roots also demonstrated a good correlation with electrophysiological parameters and the latency of sural nerve prolonged with the increase of L5 nerve root signal intensity. As is known, central latency and conduction velocity of motor nerves as well as latency of sensory nerves were electrophysiological parameters in demyelinating neuropathy. Considering fibers from L5 and S1 nerve root participate in the formation of tibial and sural nerves, these results suggested that higher CSA and SI of L5 and S1 nerve roots correlated with more demyelination of tibial and sural nerves and morphological changes of lumbosacral nerve roots could reflect the impairment of nerve conduction function in both motor and sensory nerves of lower extremities [20]. Additionally, there was an interesting point that SI of L4 and CSA of L5 correlated inversely with the amplitude of tibial CMAP and sural SNAP respectively, which seemed contradictory to the above results. In severe CIDP, demyelination could trigger secondary axon loss. We speculated patients in this cohort had relatively severe conditions so that nerve axons were involved as well. Our study has some limitations. First, the sample size is relatively small. Second, due to a low prevalence, we didn’t examine other peripheral neuropathies such as multifocal motor neuropathy, which had a different distribution of nerve hypertrophy in brachial plexus [27,28]. In the future, we will further enlarge our patient cohort and assess both brachial and lumbosacral plexus to investigate the value of MRN in the differential diagnosis of peripheral nerve disorders. In conclusion, CIDP patients showed significantly hypertrophic lumbosacral nerve roots with increased signal intensity on MRN, some of which correlated well with electrophysiological parameters with regard to demyelination. ROC curves demonstrated CSAmean had the best diagnostic performance with cut-off value 19.20 mm2. Quantification of lumbosacral nerve roots on MRN may serve as an important supporting diagnostic tool in CIDP.
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Declaration of Competing Interest The authors have no conflicts of interest to declare. Acknowledgments This work was supported by the National Key Research and Development Plan (Grant No. 2017YFC0112904). We are grateful to Jing Wang for her writing assistance and Kai Qiao for her job in nerve 5
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