Eur Spine J (2015) 24:2315–2320 DOI 10.1007/s00586-015-4059-y
ORIGINAL ARTICLE
Redundant nerve roots of the cauda equina in lumbar spinal canal stenosis, an MR study on 500 cases Masoud Poureisa1 • Mohammad Hossein Daghighi1 • Payam Eftekhari1 Kaveh Rezaei Bookani2 • Daniel Fadaei Fouladi3
•
Received: 24 February 2015 / Revised: 9 May 2015 / Accepted: 7 June 2015 / Published online: 14 June 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose The purpose of this study was to evaluate magnetic resonance (MR)-detected redundant nerve roots (RNRs) of the cauda equina in patients with lumbar spinal canal stenosis. Methods A total of 500 lumbar MR studies in patients with lumbar spinal canal stenosis were reviewed for the presence and characteristics of RNRs of the cauda equina. The length of the RNRs relative to the height of the upper vertebral body of the level of the stenosis was used as a prognostic indicator. Results RNRs were detected in 15 % of the patients, the majority above the level of the stenosis (85 %) and loop shaped (72 %). Advanced age (i.e., C56 years old, odds ratio = 1), a lumbar spinal canal stenosis at L2–4 (odds ratio = 2.5), and the presence of an intracanal protuberance with sharp margin in the site of the stenosis (odds ratio = 7.2) were independent risk factors for the development of RNRs. A direct, significant correlation was found between the relative length of the RNRs and patients’ age (Pearson r = 0.36, p = 0.001). The mean relative length of the RNRs was significantly higher in patients with RNRs located above the level of the stenosis than those with RNRs located below the site of the block.
& Daniel Fadaei Fouladi [email protected] 1
Department of Radiology, Imam Reza Hospital, Tabriz University of Medical Sciences, Tabriz, Iran
2
Department of Radiology, Imam Khomeini Hospital, Urmia University of Medical Sciences, Urmia, Iran
3
Neurosciences Research Center, Imam Reza Teaching Hospital, Tabriz University of Medical Sciences, PO Box: 5166614756, Golgasht Street, Tabriz, Iran
The degree of stenosis was associated with neither the presence nor the relative length of the RNRs. Conclusions With an occurrence rate of 15 %, RNRs of the cauda equina are not uncommon in cases with lumbar spinal canal stenosis. Advanced age, a canal stenosis at L2–4, and the presence of a sharp intracanal protuberance in the site of the stenosis are the related risk factors. Patients’ age and the location of RNRs may be of prognostic value. Keywords Lumbar spinal canal stenosis Redundant nerve roots (RNRs) of the cauda equina Magnetic resonance imaging Location, length Degree of stenosis Demographics Prognosis Risk factor
Introduction A lumbar spinal canal stenosis is a frequent condition, affecting over 0.5 million Americans, most aged[60 years [1]. First described by Verbiest in 1954 [2] and subsequently coined by Cressman and Pawl [3], the redundant nerve roots (RNRs) syndrome of the cauda equina is a common finding in which elongated, tortuous, or serpiginous nerve roots are present in the subarachnoid space in close relationship with a significant lumbar spinal canal stenosis [4, 5]. Although over a half-century has passed from the first recognition of the RNRs, and while the clinical relevance of this syndrome is still a matter of hot debate [6], relatively little information is available about its characteristics and pathophysiology [7]. Unlike in the past, cutting-edge imaging modalities such as magnetic resonance imaging (MRI) offer an opportunity to detect and scrutinize large numbers of cases with RNRs of the cauda equina accurately and noninvasively [4, 5, 8].
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This study seeks to evaluate MR-detected RNRs of the cauda equina in 500 patients with lumbar spinal canal stenosis.
Eur Spine J (2015) 24:2315–2320
Other study variables were patients’ demographic data, the level of stenosis, and the location of RNRs in relation to the site of stenosis. Statistical analysis
Materials and methods A total of 500 MR studies in patients with low back pain and lumbar spinal canal stenosis were reviewed in a private clinic between January 2014 and October 2014. Patients with congenital spinal anomalies or previous spinal operation in the lumbosacral region were excluded. The ethics committee of a local university approved this study. Patients were divided into two groups with and without RNRs of the cauda equina next to the stenotic level. MR imaging was performed using a 1.5 Tesla scanner (MAGNETOM Avanto 1.5 Tesla MRI system; Siemens, Erlangen, Germany). The digitized images were stored on a picture archive and communication system. RNRs of the cauda equina were defined as elongated, tortuous, or coiled nerve roots in the subarachnoid space in patients with lumbar spinal stenosis evident in sagittal T2-weighted MR images (Fig. 1) [8–10]. The eFilm Workstation v.2.1.2 (Merge Healthcare, Milwaukee, WI, USA) was used for measurements, including the anteroposterior (AP) diameter of the spinal canal at the narrowest level of the stenosis (degree of stenosis) at mid sagittal section; the length of the RNRs relative to the height of the upper vertebral body of the level of the stenosis at mid sagittal section following a method described by Min et al. [8–10]; the morphologic appearance of RNRs (loop shaped versus serpentine shaped) [11]; and the presence or absence of intracanal protuberances in the site of stenosis with their morphology (with soft or sharp margin, Fig. 2) on mid sagittal MR images.
Fig. 1 A sagittal T2-weighted magnetic resonance image of the lumbar spine with redundant nerve roots of the cauda equina (arrow)
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The SPSS software version 19.0 (IBM Corporation, NY, USA) was used in the statistical analysis. A Chi-square test, an independent samples t test, one-way ANOVA, and a correlation analysis (calculating the Pearson productmoment coefficient) were used, when appropriate. A receiver operator characteristics (ROC) curve was plotted to define an optimal cut-off value. A logistic regression model was used in the multivariate analysis. A significance level of p B 0.05 was used.
Results A total of 500 spinal MR studies obtained from 289 females (57.8 %) and 211 males (42.2 %) with a mean age of 52.79 ± 14.97 years (range 29–92) were reviewed. A lumbar spinal canal stenosis was present at L1–2 in 25 cases (5 %), at L2–3 in 60 cases (12 %), at L3–4 in 139 cases (27.8 %), at L4–5 in 247 cases (49.4 %), and at L5– S1 in 29 cases (5.8 %). The mean degree of stenosis was 4.46 ± 1.3 mm (range 1–9). No or soft intracanal protuberances in the site of stenosis were documented in 385 patients (77 %). Intracanal protuberances with sharp margins were present in the site of stenosis in 115 patients (23 %). RNRs of the cauda equina were present in 75 patients (15 %). They were located above the level of the stenosis in 63 cases (84 %) and below it in 12 cases (16 %). The RNRs were loop shaped in 54 cases (72 %) and serpentine shaped in 21 cases (28 %). The mean relative length of the RNRs was 2.51 ± 0.85 (range 1.16–6.26). The study variables are compared between patients with and without RNRs in Table 1. The two groups were comparable in terms of sex (Chi-square test p = 0.36). The patients with RNRs were significantly older (independent sample t test p \ 0.001). The related optimal cutoff point was 56 years old (area under the curve: 0.64, p \ 0.001, sensitivity: 60 %, specificity: 61 %, Fig. 3). In patients with RNRs, the spinal canal stenosis was significantly more frequent at L2–4 (Chi-square test p \ 0.001). The patients with RNRs had significantly more sharp intracanal protuberances in the site of stenosis (p \ 0.001). According to the results of a logistic regression analysis, age (p = 0.01, odds ratio = 1.00), the location of stenosis (p \ 0.001, odds ratio = 2.5), and the presence of a sharp
Eur Spine J (2015) 24:2315–2320
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Fig. 2 Examples of intracanal protuberances in the site of stenosis with soft (a) and sharp (b, c) margins on mid sagittal magnetic resonance images of the lumbar spine along with their schematic depictions Table 1 Study variables in patients with and without redundant nerve roots (RNRs) of the cauda equina
Variable
With RNRs (n = 75)
Without RNRs (n = 425)
p value
Male
28 (37.3 %)
183 (43.1 %)
Female
47 (62.7 %)
242 (56.9 %)
Mean age (year)
59.05 ± 13.78
51.68 ± 14.91
\0.001*
L1–L2
8 (10.7 %)
17 (4 %)
\0.001*
L2–L3
23 (30.7 %)
37 (8.7 %)
L3–L4
29 (38.7 %)
110 (25.9 %)
L4–L5
15 (20 %)
232 (54.6 %)
L5–S1
0 (0 %)
29 (6.8 %)
Sex 0.36
Level of stenosis
Intracanal protuberance in the site of stenosis No/soft
11 (14.7 %)
374 (88 %)
Sharp
64 (85.3 %)
51 (12 %)
\0.001*
* A p value B0.05 is statistically significant
Fig. 3 A receiver operator characteristics (ROC) curve representing age of the patients with lumbar spinal canal stenosis in predicting redundant nerve roots of the cauda equina (area under the curve: 0.64, p \ 0.001)
intracanal protuberance in the site of stenosis (p \ 0.001, odds ratio = 7.24) were significantly and independently associated with the presence of RNRs. Associations between the relative length of the RNRs and the study variables are examined in Table 2. Accordingly, the relative length of the RNRs was not associated with the sex of patients (independent samples t test p = 0.67), the shape of RNRs (independent samples t test p = 0.40), the level of stenosis (independent samples t test p = 0.47), or the presence of intracanal protuberance in the site of stenosis (independent samples t test p = 0.30). The mean relative length of the RNRs, however, was significantly higher in the cases with RNRs above the stenosis than those with RNRs below the stenosis (independent samples t test p = 0.01). A significant, positive correlation was present between the relative length of the RNRs and the patients’ age (Pearson r = 0.36, p = 0.001) (Fig. 4). No significant correlation was found between the relative length of the RNRs and the degree of stenosis (Pearson r = -0.12, p = 0.31).
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2318 Table 2 Relative length of redundant nerve roots (RNRs) of the cauda equina stratified by study variables
Eur Spine J (2015) 24:2315–2320
Variables
Number
Relative length of RNRs (mean ± SD)
p value
Male
28
2.45 ± 0.91
0.67
Female
47
2.54 ± 0.82
Above the stenosis
63
2.62 ± 0.86
Below the stenosis
12
1.93 ± 0.57
Loop
54
2.45 ± 0.78
Serpentine
21
2.64 ± 1.03
L1–L2
8
2.43 ± 0.80
L2–L3
23
2.47 ± 0.83
L3–L4
29
2.68 ± 0.89
L4–L5
15
2.26 ± 0.84
Sex
Location of RNRs 0.01*
Shape of RNRs 0.40
Level of stenosis
Intracanal protuberance in the site of stenosis No/soft 11 2.78 ± 0.91 Sharp
64
0.47
0.30
2.46 ± 0.84
* p value B0.05 is statistically significant
Fig. 4 A single scatter-plot representing a significant, positive correlation between the relative length of the redundant nerve roots (RNRs), and the age of patients with RNRs of the cauda equina (Pearson r = 0.36, p = 0.001)
Discussion The true prevalence of RNRs of the cauda equina in patients with lumbar canal stenosis is not known, varying between 8.2 and 42 % in different settings [5, 10]. The detection rate of RNRS was 15 % in the current study.
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Although MRI is a sensitive tool in detecting RNRs [5, 8], its accuracy may be influenced by two factors. One is the position of patients during examination. It has been reported that the detection rate is higher in extension than in flexion or neutral position [12, 13]. The other factor is thought to be the morphology of RNRs. It has been shown that while MRI is very sensitive in detecting loop-shaped RNRs, its accuracy decreases dramatically in visualizing serpentine-shaped RNRs [11]. Although in conformity with a previous report [11] the majority of RNRs in the present work were loop shaped (72 %), it is not known with certainty that whether serpentine-shaped RNRs actually occur less frequently or they just go unnoticed because of MRI imperfection. Nevertheless, it should be noted that even if MRI is not as accurate as lumbar myelogram in detecting RNRs [14], it is noninvasive and more importantly, it demonstrates more advanced RNRs, which are thought to represent important clinical findings [5]. RNRs were found more frequently in female patients in the present work (62.7 %). This association, however, was not statistically significant. Min et al. [8] also found RNRs more frequently in females (65.2 %), with no significant sex-related difference between the two groups with and without RNRs. In line with previous reports [8, 15], the patients with RNRs in the present study were significantly older than those without RNRs. It is not clear why RNRs of the cauda equina tend to develop in older subjects. Higher incidence of degenerative changes in advanced ages and age-
Eur Spine J (2015) 24:2315–2320
dependent changes in the spinal canal may play a role in this regard [16]. An interesting and unique finding in this study was that the presence of sharp intracanal protuberances in the site of stenosis, when compared to patients with no or soft protuberances, significantly increased the risk of RNRs by 7.24 times independent of patients’ age and the level of the stenosis. Although the exact cause of RNRs is not known, a mechanical trapping at the level of stenosis [17] with squeezing forces owing to chronic compression [10] is the most plausible hypothesis, because postmortem studies have shown that all RNRs pass through the maximum point of stenosis in the spinal canal [15]. A mechanical effect of a spinal stenosis is believed to be implemented through producing constriction or tethering of the nerve roots, leading to restricted normal movements of the nerve roots, their stretching during spinal flexion and extension, and resultant elongation, redundancy, and tortuosity. A more common occurrence of RNRs above the level of stenosis supports this mechanism [1]. Intracanal protuberances with soft margins, as described in this work, are usually protruded or extruded intervertebral disk materials [18], whereas intracanal protuberances with sharp margins usually represent degenerative spondylotic encroachments [10] or bony overgrowth [19] in the site of stenosis. Our finding could be supported by some previous studies that demonstrated RNRs develop more frequently in pathologies with hard tissue compression such as degenerative etiologies and bony overgrowth than those along with soft compressive forces such as ligamentous hypertrophy, metastatic epidural tumor and cauda equina syndrome [7, 10, 19]. In the current work, 84 % of the detected RNRs were located above the site of the stenosis and 16 % were located below it. The preponderance of RNRs on the cephalic side of the block is not a new finding in patients with spinal canal stenosis [9, 20, 21]. It is not exactly known why most of observed RNRs occur above the site of the stenosis. Although the ‘‘squeeze’’ hypothesis could explain this phenomenon [18], the ischemia of previously supposed watershed vascular zone in the proximal portion of the nerve roots following compression-induced compromised arterial flow from the distal radicular artery [7] may also be relevant. Another unique finding in this study was that the RNRs were observed more frequently in cases with stenosis at the middle lumbar levels (i.e. L2–4) than in those with stenosis at more lower lumbar segments (odds ratio = 2.5). The fact that the lower lumbar spine is less mobile and flexible than the middle segments may explain this finding. Although not yet a consensus, it has been suggested that the evidence of RNRs of the cauda equina is along with irreversible abnormalities of the nerve roots and poor prognosis in patients with lumbar spinal canal
2319
stenosis [4, 5, 10, 11, 15, 22]. On the basis of these reports, some investigators have proposed that the presence of RNRs in patients with lumbar spinal canal stenosis and borderline symptoms or trivial imaging findings might assist in decision-making for invasive interventions [7, 23]. In a study by Min et al. [8], a higher relative length of the RNRs was suggested as a robust indicator of a good prognosis. In their work, the postoperative outcome was better in patients with greater relative length of the RNRs. They related this finding to a better capability of accommodation in longer RNRs during spinal mobility. In our work, the relative length of the RNRs correlated directly with patients’ age, and the mean relative length of the RNRs was significantly higher in the RNRs located above the stenosis compared with those located below the stenosis. These findings may indicate better prognosis in older patients and in association with RNRs located above the site of the stenosis compared to those below the block. They need, however, to be tested in future studies. Although no statistically significant association was found between the relative length of the RNRs and the presence or type of intracanal protuberances in the site of the stenosis, the mean value was lower in the cases with sharp protuberances. This finding may be clinically important because it could suggest a prognostic role for this imaging finding. Low number of patients with no or soft protuberances prevents reaching a solid conclusion in this regard. An insignificant association between the relative length of the RNRs and the degree of stenosis in the present work has been also found in previous studies [8, 23]. Besides its novelty in some aspects such as using a large number of patients with spinal canal stenosis and RNRs along with introducing some less known features of RNRs, this study bears some limitations. Because of clear reasons, we were unable to include myelography as the gold standard method in detecting RNRs. As discussed earlier, however, MRI is also a very sensitive method, particularly in revealing clinically consequential RNRs [5]. It was also not applicable to incorporate actual clinical outcome of patients in our analysis. Instead, the relative length of the RNRs, as a good prognostic indicator [8], was employed. In summary, this study showed that RNRs of the cauda equina are not uncommon in patients with lumbar spinal canal stenosis. In line with previous reports, the majority of RNRs in the present work was loop shaped and located above the level of the stenosis. Advanced age, a lumbar spinal canal stenosis at L2–4, and the presence of sharp intracanal protuberances in the site of stenosis were independent risk factors for the occurrence of RNRs of the cauda equina. Using the relative length of the RNRs as an indicator of prognosis showed that advanced age and the
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occurrence of RNRs above the level of the stenosis might be associated with better outcome compared to younger patients and those with RNRs located below the site of the block. Conflict of interest of interest.
None of the authors have any potential conflict
References 1. Ozturk AK, Gokaslan ZL (2013) Clinical significance of redundant nerve roots of the Cauda Equina. World Neurosur. doi:10. 1016/j.wneu.2013.10.047 2. Verbiest H (1954) A radicular syndrome from developmental narrowing of the lumbar vertebral canal. J Bone Joint Surg Br 36-B(2):230–237 3. Cressman MR, Pawl RP (1968) Serpentine myelographic defect caused by a redundant nerve root. Case report. J Neurosurg 28(4):391–393. doi:10.3171/jns.1968.28.4.0391 4. Hakan T, Celikoglu E, Aydoseli A, Demir K (2008) The redundant nerve root syndrome of the Cauda equina. Turk Neurosurg 18(2):204–206 5. Ono A, Suetsuna F, Irie T, Yokoyama T, Numasawa T, Wada K, Toh S (2007) Clinical significance of the redundant nerve roots of the cauda equina documented on magnetic resonance imaging. J Neurosurg Spine 7(1):27–32. doi:10.3171/SPI-07/07/027 6. Nogueira-Barbosa MH, Savarese LG, Herrero CFPdS, Defino HLA (2012) Redundant nerve roots of the cauda equina: review of the literature. Radiol Bras 45:155–159 7. Mattei TA, Mendel E (2013) Redundans Nervi Radix Cauda Equina: pathophysiology and Clinical Significance of an Intriguing Radiologic Sign. World Neurosurg. doi:10.1016/j. wneu.2013.10.048 8. Min JH, Jang JS, Lee SH (2008) Clinical significance of redundant nerve roots of the cauda equina in lumbar spinal stenosis. Clin Neurol Neurosurg 110(1):14–18. doi:10.1016/j.clineuro. 2007.08.005 9. Rigsby CM, Virapongse C, Duncan C (1983) Positional variability in redundant lumbar nerve-root syndrome. Surg Neurol 19(6):513–516 10. Suzuki K, Ishida Y, Ohmori K, Sakai H, Hashizume Y (1989) Redundant nerve roots of the cauda equina: clinical aspects and consideration of pathogenesis. Neurosurgery 24(4):521–528
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11. Yokoyama K, Kawanishi M, Yamada M, Tanaka H, Ito Y, Hirano M, Kawabata S, Kuroiwa T (2013) Clinical significance of postoperative changes in redundant nerve roots after decompressive laminectomy for lumbar spinal canal stenosis. World Neurosurg. doi:10.1016/j.wneu.2013.09.024 12. Murphy RW (1977) Nerve roots and spinal nerves in degenerative disk disease. Clin Orthop Relat Res 129:46–60 13. Yamada H, Oya M, Okada T, Shiozawa Z (1972) Intermittent cauda equina compression due to narrow spinal canal. J Neurosurg 37(1):83–88. doi:10.3171/jns.1972.37.1.0083 14. Ouaknine GE, Couillard P (1985) Syndrome of redundant nerve roots of the cauda equina. Apropos of 2 cases. Neurochirurgie 31(5):442–448 15. Suzuki K, Takatsu T, Inoue H, Teramoto T, Ishida Y, Ohmori K (1992) Redundant nerve roots of the cauda equina caused by lumbar spinal canal stenosis. Spine 17(11):1337–1342 16. Tsuji H, Tamaki T, Itoh T, Yamada H, Motoe T, Tatezaki S, Noguchi T, Takano H (1985) Redundant nerve roots in patients with degenerative lumbar spinal stenosis. Spine 10(1):72–82 17. Ehni G, Moiel RH, Bragg TG (1970) The ‘‘redundant’ or ‘‘knotted’’ nerve root: a clue to spondylotic cauda equina radiculopathy. Case report. J Neurosurg 32(2):252–254. doi:10. 3171/jns.1970.32.2.0252 18. Koda M, Rokkaku T, Mannoji C, Okamoto Y, Kon T, Murakami M, Furuya T, Yamazaki M (2012) Spontaneous migration of a redundant nerve root accompanied by absorption of lumbar disk herniation. A case report. Neuroradiol J 25(5):617–620 19. Reinstein L, Twardzik FG, Russo GL, Bose P (1984) Electromyographic abnormalities in redundant nerve root syndrome of the cauda equina. Arch Phys Med Rehabil 65(5):270–272 20. Mendelsohn DB, Hertzanu Y (1984) Migratory redundant lumbar nerve roots. A case report. South African Med J Suid-Afrikaanse tydskrif vir geneeskunde 66(12):461–462 21. Yang SM, Park HK, Cho SJ, Chang JC (2013) Redundant nerve roots of cauda equina mimicking intradural disc herniation: a case report. Korean J Spine 10(1):41–43. doi:10.14245/kjs.2013.10.1.41 22. Naguib MG, Latchaw RE, Erickson DL, Seljeskog EL (1981) Redundant nerve roots of the cauda equina. Neurosurgery 9(4):444–449 23. Mattei TA (2013) A gaze beyond the surface: acknowledging the little we know about radiographic parameters for evaluation of lumbar spinal stenosis. Neurosurgery 72(1):E135–E140. doi:10. 1227/NEU.0b013e3182752bb7
ORIGINAL ARTICLE
Redundant nerve roots of the cauda equina in lumbar spinal canal stenosis, an MR study on 500 cases Masoud Poureisa1 • Mohammad Hossein Daghighi1 • Payam Eftekhari1 Kaveh Rezaei Bookani2 • Daniel Fadaei Fouladi3
•
Received: 24 February 2015 / Revised: 9 May 2015 / Accepted: 7 June 2015 / Published online: 14 June 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose The purpose of this study was to evaluate magnetic resonance (MR)-detected redundant nerve roots (RNRs) of the cauda equina in patients with lumbar spinal canal stenosis. Methods A total of 500 lumbar MR studies in patients with lumbar spinal canal stenosis were reviewed for the presence and characteristics of RNRs of the cauda equina. The length of the RNRs relative to the height of the upper vertebral body of the level of the stenosis was used as a prognostic indicator. Results RNRs were detected in 15 % of the patients, the majority above the level of the stenosis (85 %) and loop shaped (72 %). Advanced age (i.e., C56 years old, odds ratio = 1), a lumbar spinal canal stenosis at L2–4 (odds ratio = 2.5), and the presence of an intracanal protuberance with sharp margin in the site of the stenosis (odds ratio = 7.2) were independent risk factors for the development of RNRs. A direct, significant correlation was found between the relative length of the RNRs and patients’ age (Pearson r = 0.36, p = 0.001). The mean relative length of the RNRs was significantly higher in patients with RNRs located above the level of the stenosis than those with RNRs located below the site of the block.
& Daniel Fadaei Fouladi [email protected] 1
Department of Radiology, Imam Reza Hospital, Tabriz University of Medical Sciences, Tabriz, Iran
2
Department of Radiology, Imam Khomeini Hospital, Urmia University of Medical Sciences, Urmia, Iran
3
Neurosciences Research Center, Imam Reza Teaching Hospital, Tabriz University of Medical Sciences, PO Box: 5166614756, Golgasht Street, Tabriz, Iran
The degree of stenosis was associated with neither the presence nor the relative length of the RNRs. Conclusions With an occurrence rate of 15 %, RNRs of the cauda equina are not uncommon in cases with lumbar spinal canal stenosis. Advanced age, a canal stenosis at L2–4, and the presence of a sharp intracanal protuberance in the site of the stenosis are the related risk factors. Patients’ age and the location of RNRs may be of prognostic value. Keywords Lumbar spinal canal stenosis Redundant nerve roots (RNRs) of the cauda equina Magnetic resonance imaging Location, length Degree of stenosis Demographics Prognosis Risk factor
Introduction A lumbar spinal canal stenosis is a frequent condition, affecting over 0.5 million Americans, most aged[60 years [1]. First described by Verbiest in 1954 [2] and subsequently coined by Cressman and Pawl [3], the redundant nerve roots (RNRs) syndrome of the cauda equina is a common finding in which elongated, tortuous, or serpiginous nerve roots are present in the subarachnoid space in close relationship with a significant lumbar spinal canal stenosis [4, 5]. Although over a half-century has passed from the first recognition of the RNRs, and while the clinical relevance of this syndrome is still a matter of hot debate [6], relatively little information is available about its characteristics and pathophysiology [7]. Unlike in the past, cutting-edge imaging modalities such as magnetic resonance imaging (MRI) offer an opportunity to detect and scrutinize large numbers of cases with RNRs of the cauda equina accurately and noninvasively [4, 5, 8].
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This study seeks to evaluate MR-detected RNRs of the cauda equina in 500 patients with lumbar spinal canal stenosis.
Eur Spine J (2015) 24:2315–2320
Other study variables were patients’ demographic data, the level of stenosis, and the location of RNRs in relation to the site of stenosis. Statistical analysis
Materials and methods A total of 500 MR studies in patients with low back pain and lumbar spinal canal stenosis were reviewed in a private clinic between January 2014 and October 2014. Patients with congenital spinal anomalies or previous spinal operation in the lumbosacral region were excluded. The ethics committee of a local university approved this study. Patients were divided into two groups with and without RNRs of the cauda equina next to the stenotic level. MR imaging was performed using a 1.5 Tesla scanner (MAGNETOM Avanto 1.5 Tesla MRI system; Siemens, Erlangen, Germany). The digitized images were stored on a picture archive and communication system. RNRs of the cauda equina were defined as elongated, tortuous, or coiled nerve roots in the subarachnoid space in patients with lumbar spinal stenosis evident in sagittal T2-weighted MR images (Fig. 1) [8–10]. The eFilm Workstation v.2.1.2 (Merge Healthcare, Milwaukee, WI, USA) was used for measurements, including the anteroposterior (AP) diameter of the spinal canal at the narrowest level of the stenosis (degree of stenosis) at mid sagittal section; the length of the RNRs relative to the height of the upper vertebral body of the level of the stenosis at mid sagittal section following a method described by Min et al. [8–10]; the morphologic appearance of RNRs (loop shaped versus serpentine shaped) [11]; and the presence or absence of intracanal protuberances in the site of stenosis with their morphology (with soft or sharp margin, Fig. 2) on mid sagittal MR images.
Fig. 1 A sagittal T2-weighted magnetic resonance image of the lumbar spine with redundant nerve roots of the cauda equina (arrow)
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The SPSS software version 19.0 (IBM Corporation, NY, USA) was used in the statistical analysis. A Chi-square test, an independent samples t test, one-way ANOVA, and a correlation analysis (calculating the Pearson productmoment coefficient) were used, when appropriate. A receiver operator characteristics (ROC) curve was plotted to define an optimal cut-off value. A logistic regression model was used in the multivariate analysis. A significance level of p B 0.05 was used.
Results A total of 500 spinal MR studies obtained from 289 females (57.8 %) and 211 males (42.2 %) with a mean age of 52.79 ± 14.97 years (range 29–92) were reviewed. A lumbar spinal canal stenosis was present at L1–2 in 25 cases (5 %), at L2–3 in 60 cases (12 %), at L3–4 in 139 cases (27.8 %), at L4–5 in 247 cases (49.4 %), and at L5– S1 in 29 cases (5.8 %). The mean degree of stenosis was 4.46 ± 1.3 mm (range 1–9). No or soft intracanal protuberances in the site of stenosis were documented in 385 patients (77 %). Intracanal protuberances with sharp margins were present in the site of stenosis in 115 patients (23 %). RNRs of the cauda equina were present in 75 patients (15 %). They were located above the level of the stenosis in 63 cases (84 %) and below it in 12 cases (16 %). The RNRs were loop shaped in 54 cases (72 %) and serpentine shaped in 21 cases (28 %). The mean relative length of the RNRs was 2.51 ± 0.85 (range 1.16–6.26). The study variables are compared between patients with and without RNRs in Table 1. The two groups were comparable in terms of sex (Chi-square test p = 0.36). The patients with RNRs were significantly older (independent sample t test p \ 0.001). The related optimal cutoff point was 56 years old (area under the curve: 0.64, p \ 0.001, sensitivity: 60 %, specificity: 61 %, Fig. 3). In patients with RNRs, the spinal canal stenosis was significantly more frequent at L2–4 (Chi-square test p \ 0.001). The patients with RNRs had significantly more sharp intracanal protuberances in the site of stenosis (p \ 0.001). According to the results of a logistic regression analysis, age (p = 0.01, odds ratio = 1.00), the location of stenosis (p \ 0.001, odds ratio = 2.5), and the presence of a sharp
Eur Spine J (2015) 24:2315–2320
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Fig. 2 Examples of intracanal protuberances in the site of stenosis with soft (a) and sharp (b, c) margins on mid sagittal magnetic resonance images of the lumbar spine along with their schematic depictions Table 1 Study variables in patients with and without redundant nerve roots (RNRs) of the cauda equina
Variable
With RNRs (n = 75)
Without RNRs (n = 425)
p value
Male
28 (37.3 %)
183 (43.1 %)
Female
47 (62.7 %)
242 (56.9 %)
Mean age (year)
59.05 ± 13.78
51.68 ± 14.91
\0.001*
L1–L2
8 (10.7 %)
17 (4 %)
\0.001*
L2–L3
23 (30.7 %)
37 (8.7 %)
L3–L4
29 (38.7 %)
110 (25.9 %)
L4–L5
15 (20 %)
232 (54.6 %)
L5–S1
0 (0 %)
29 (6.8 %)
Sex 0.36
Level of stenosis
Intracanal protuberance in the site of stenosis No/soft
11 (14.7 %)
374 (88 %)
Sharp
64 (85.3 %)
51 (12 %)
\0.001*
* A p value B0.05 is statistically significant
Fig. 3 A receiver operator characteristics (ROC) curve representing age of the patients with lumbar spinal canal stenosis in predicting redundant nerve roots of the cauda equina (area under the curve: 0.64, p \ 0.001)
intracanal protuberance in the site of stenosis (p \ 0.001, odds ratio = 7.24) were significantly and independently associated with the presence of RNRs. Associations between the relative length of the RNRs and the study variables are examined in Table 2. Accordingly, the relative length of the RNRs was not associated with the sex of patients (independent samples t test p = 0.67), the shape of RNRs (independent samples t test p = 0.40), the level of stenosis (independent samples t test p = 0.47), or the presence of intracanal protuberance in the site of stenosis (independent samples t test p = 0.30). The mean relative length of the RNRs, however, was significantly higher in the cases with RNRs above the stenosis than those with RNRs below the stenosis (independent samples t test p = 0.01). A significant, positive correlation was present between the relative length of the RNRs and the patients’ age (Pearson r = 0.36, p = 0.001) (Fig. 4). No significant correlation was found between the relative length of the RNRs and the degree of stenosis (Pearson r = -0.12, p = 0.31).
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2318 Table 2 Relative length of redundant nerve roots (RNRs) of the cauda equina stratified by study variables
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Variables
Number
Relative length of RNRs (mean ± SD)
p value
Male
28
2.45 ± 0.91
0.67
Female
47
2.54 ± 0.82
Above the stenosis
63
2.62 ± 0.86
Below the stenosis
12
1.93 ± 0.57
Loop
54
2.45 ± 0.78
Serpentine
21
2.64 ± 1.03
L1–L2
8
2.43 ± 0.80
L2–L3
23
2.47 ± 0.83
L3–L4
29
2.68 ± 0.89
L4–L5
15
2.26 ± 0.84
Sex
Location of RNRs 0.01*
Shape of RNRs 0.40
Level of stenosis
Intracanal protuberance in the site of stenosis No/soft 11 2.78 ± 0.91 Sharp
64
0.47
0.30
2.46 ± 0.84
* p value B0.05 is statistically significant
Fig. 4 A single scatter-plot representing a significant, positive correlation between the relative length of the redundant nerve roots (RNRs), and the age of patients with RNRs of the cauda equina (Pearson r = 0.36, p = 0.001)
Discussion The true prevalence of RNRs of the cauda equina in patients with lumbar canal stenosis is not known, varying between 8.2 and 42 % in different settings [5, 10]. The detection rate of RNRS was 15 % in the current study.
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Although MRI is a sensitive tool in detecting RNRs [5, 8], its accuracy may be influenced by two factors. One is the position of patients during examination. It has been reported that the detection rate is higher in extension than in flexion or neutral position [12, 13]. The other factor is thought to be the morphology of RNRs. It has been shown that while MRI is very sensitive in detecting loop-shaped RNRs, its accuracy decreases dramatically in visualizing serpentine-shaped RNRs [11]. Although in conformity with a previous report [11] the majority of RNRs in the present work were loop shaped (72 %), it is not known with certainty that whether serpentine-shaped RNRs actually occur less frequently or they just go unnoticed because of MRI imperfection. Nevertheless, it should be noted that even if MRI is not as accurate as lumbar myelogram in detecting RNRs [14], it is noninvasive and more importantly, it demonstrates more advanced RNRs, which are thought to represent important clinical findings [5]. RNRs were found more frequently in female patients in the present work (62.7 %). This association, however, was not statistically significant. Min et al. [8] also found RNRs more frequently in females (65.2 %), with no significant sex-related difference between the two groups with and without RNRs. In line with previous reports [8, 15], the patients with RNRs in the present study were significantly older than those without RNRs. It is not clear why RNRs of the cauda equina tend to develop in older subjects. Higher incidence of degenerative changes in advanced ages and age-
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dependent changes in the spinal canal may play a role in this regard [16]. An interesting and unique finding in this study was that the presence of sharp intracanal protuberances in the site of stenosis, when compared to patients with no or soft protuberances, significantly increased the risk of RNRs by 7.24 times independent of patients’ age and the level of the stenosis. Although the exact cause of RNRs is not known, a mechanical trapping at the level of stenosis [17] with squeezing forces owing to chronic compression [10] is the most plausible hypothesis, because postmortem studies have shown that all RNRs pass through the maximum point of stenosis in the spinal canal [15]. A mechanical effect of a spinal stenosis is believed to be implemented through producing constriction or tethering of the nerve roots, leading to restricted normal movements of the nerve roots, their stretching during spinal flexion and extension, and resultant elongation, redundancy, and tortuosity. A more common occurrence of RNRs above the level of stenosis supports this mechanism [1]. Intracanal protuberances with soft margins, as described in this work, are usually protruded or extruded intervertebral disk materials [18], whereas intracanal protuberances with sharp margins usually represent degenerative spondylotic encroachments [10] or bony overgrowth [19] in the site of stenosis. Our finding could be supported by some previous studies that demonstrated RNRs develop more frequently in pathologies with hard tissue compression such as degenerative etiologies and bony overgrowth than those along with soft compressive forces such as ligamentous hypertrophy, metastatic epidural tumor and cauda equina syndrome [7, 10, 19]. In the current work, 84 % of the detected RNRs were located above the site of the stenosis and 16 % were located below it. The preponderance of RNRs on the cephalic side of the block is not a new finding in patients with spinal canal stenosis [9, 20, 21]. It is not exactly known why most of observed RNRs occur above the site of the stenosis. Although the ‘‘squeeze’’ hypothesis could explain this phenomenon [18], the ischemia of previously supposed watershed vascular zone in the proximal portion of the nerve roots following compression-induced compromised arterial flow from the distal radicular artery [7] may also be relevant. Another unique finding in this study was that the RNRs were observed more frequently in cases with stenosis at the middle lumbar levels (i.e. L2–4) than in those with stenosis at more lower lumbar segments (odds ratio = 2.5). The fact that the lower lumbar spine is less mobile and flexible than the middle segments may explain this finding. Although not yet a consensus, it has been suggested that the evidence of RNRs of the cauda equina is along with irreversible abnormalities of the nerve roots and poor prognosis in patients with lumbar spinal canal
2319
stenosis [4, 5, 10, 11, 15, 22]. On the basis of these reports, some investigators have proposed that the presence of RNRs in patients with lumbar spinal canal stenosis and borderline symptoms or trivial imaging findings might assist in decision-making for invasive interventions [7, 23]. In a study by Min et al. [8], a higher relative length of the RNRs was suggested as a robust indicator of a good prognosis. In their work, the postoperative outcome was better in patients with greater relative length of the RNRs. They related this finding to a better capability of accommodation in longer RNRs during spinal mobility. In our work, the relative length of the RNRs correlated directly with patients’ age, and the mean relative length of the RNRs was significantly higher in the RNRs located above the stenosis compared with those located below the stenosis. These findings may indicate better prognosis in older patients and in association with RNRs located above the site of the stenosis compared to those below the block. They need, however, to be tested in future studies. Although no statistically significant association was found between the relative length of the RNRs and the presence or type of intracanal protuberances in the site of the stenosis, the mean value was lower in the cases with sharp protuberances. This finding may be clinically important because it could suggest a prognostic role for this imaging finding. Low number of patients with no or soft protuberances prevents reaching a solid conclusion in this regard. An insignificant association between the relative length of the RNRs and the degree of stenosis in the present work has been also found in previous studies [8, 23]. Besides its novelty in some aspects such as using a large number of patients with spinal canal stenosis and RNRs along with introducing some less known features of RNRs, this study bears some limitations. Because of clear reasons, we were unable to include myelography as the gold standard method in detecting RNRs. As discussed earlier, however, MRI is also a very sensitive method, particularly in revealing clinically consequential RNRs [5]. It was also not applicable to incorporate actual clinical outcome of patients in our analysis. Instead, the relative length of the RNRs, as a good prognostic indicator [8], was employed. In summary, this study showed that RNRs of the cauda equina are not uncommon in patients with lumbar spinal canal stenosis. In line with previous reports, the majority of RNRs in the present work was loop shaped and located above the level of the stenosis. Advanced age, a lumbar spinal canal stenosis at L2–4, and the presence of sharp intracanal protuberances in the site of stenosis were independent risk factors for the occurrence of RNRs of the cauda equina. Using the relative length of the RNRs as an indicator of prognosis showed that advanced age and the
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occurrence of RNRs above the level of the stenosis might be associated with better outcome compared to younger patients and those with RNRs located below the site of the block. Conflict of interest of interest.
None of the authors have any potential conflict
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