Motor and Functional Outcome of Selective Dorsal Rhizotomy in Children with Spastic Diplegia (PDF)

Acta Neurochirurgica (2021) 163:2837–2844 https://doi.org/10.1007/s00701-021-04954-5 ORIGINAL ARTICLE - FUNCTIONAL NEUROSURGERY - MOVEMENT DISORDERS Motor and functional outcome of selective dorsal rhizotomy in children with spastic diplegia at 12 and 24 months of follow‑up Tarik Alp Sargut1 ·...

Acta Neurochirurgica (2021) 163:2837–2844 https://doi.org/10.1007/s00701-021-04954-5 ORIGINAL ARTICLE - FUNCTIONAL NEUROSURGERY - MOVEMENT DISORDERS Motor and functional outcome of selective dorsal rhizotomy in children with spastic diplegia at 12 and 24 months of follow‑up Tarik Alp Sargut1 · Hannes Haberl2 · Simone Wolter3 · Sascha Tafelski3 · Anne van Riesen4,5 · Maijana Linhard4,5 · Angela M. Kaindl4,5,6 · Ulrich‑Wilhelm Thomale1 · Matthias Schulz1 Received: 29 April 2021 / Accepted: 24 July 2021 / Published online: 21 August 2021 © The Author(s) 2021, corrected publication 2021 Abstract Background Selective dorsal rhizotomy (SDR) in ambulatory children affected by cerebral palsy (CP) is a surgical treat- ment option to lower spasticity and thereby improve gait and ambulation. The aim of the current study is to investigate the outcome of children with respect to spasticity, muscle strength, and overall function after SDR. Methods All children who underwent SDR via a single-level laminotomy in the time period from January 2007 to April 2015 at our center were enrolled in this study. Within a standardized evaluation process, the following was assessed routinely pre-operatively and 12 and 24 months following surgery: extent of spasticity at hip adductors and hamstrings as character- ized by the Modified Ashworth Scale (MAS), maximal muscle strength as characterized by the Medical Council Research Scale (MRC), overall function regarding ambulation as characterized by the Gross Motors Function Classification System (GFMCS), and overall function as characterized by the Gross Motor Function Measure (GMFM-88). Results Matching sets of pre- and post-operative assessments of the chosen outcome parameters were available for 109 of the 150 children who underwent SDR within the observation period. After 24 months, the MAS scores of hip adductors (n = 59) improved in 71% and 76% of children on the right and left side, respectively. In 20% and 19%, it remained unchanged and worsened in 9% and 5% of children on the right and left side, respectively (p < 0.00625). For hamstrings, the rates for the right and left sides were 81% and 79% improvement, 16% and 16% unchanged, and 4% and 5% worsened, respectively (p < 0.00625). Muscle strength of ankle dorsiflexion and knee extension significantly improved after 24 months. Overall function assessed by GMFM-88 improved significantly by 4% after 12 months (n = 77) and by 7% after 24 months (n = 56, p < 0.0001). Conclusions The presented data underlines the benefit of SDR in a pediatric patient collective with bilateral spastic CP. The procedure resulted in an effective and permanent reduction of spasticity and improved overall function without causing relevant weakness of the lower extremities. Keywords Cerebral palsy · Spasticity · Selective dorsal rhizotomy · Modified Ashworth Scale This article is part of the Topical Collection on Functional Neurosurgery – Movement disorders 4 * Matthias Schulz Center for Chronically Sick Children, Charité [email protected] - Universitätsmedizin Berlin, Berlin, Germany 5 1 Department of Pediatric Neurology, Charité Pediatric Neurosurgery, Charité - Universitätsmedizin - Universitätsmedizin Berlin, Berlin, Germany Berlin, Berlin, Germany 6 2 Institute of Cell Biology and Neurobiology, Charité Division of Pediatric Neurosurgery, Universitätsklinikum - Universitätsmedizin Berlin, Berlin, Germany Bonn, Bonn, Germany 3 Department of Anesthesiology and Operative Intensive Care Medicine, Charité - Universitätsmedizin Berlin, Berlin, Germany 13 Vol.:(0123456789) 2838 Acta Neurochirurgica (2021) 163:2837–2844 Introduction 01/2007 to 04/2015 were enrolled. The study was approved by the local ethics committee (EA1/138/11, EA2/167/16). Cerebral palsy (CP) is one of the most common neurologi- Patient selection was based on an assessment by a mul- cal disorders in childhood worldwide with an incidence of tidisciplinary team of pediatric neurologists, pediatric 2–4 per 1000 live births. The underlying pathophysio- neurosurgeons, pediatric orthopedic surgeons, and physi- logical mechanism is a damage during early brain develop- otherapists. The criteria defined by Peacock and Staudt ment in the prenatal or perinatal period of life. According were used to select children to undergo SDR. Accord- to the predominant movement disorder, spastic, dystonic, ingly, candidates suitable for the procedure presented with atactic, or mixed clinical presentation are distinguished spastic, bilateral paraparesis of the lower extremities and. The spastic subtype is the most common and can lead predominately represented grade I, II, or III of the Gross to an impaired mobility or inability to ambulate. The Motor Function Classification System (GMFCS). Motiva- ability to ambulate is commonly graded according to the tion to ambulate and sufficient cognitive skills to actively Gross Motor Function Classification System (GMFCS, participate in the mandatory post-operative rehabilitation ) and detailed scales such as the Gross Motor Function constituted further prerequisites. Exclusion criteria were Measure (GMFM-88, ) document functional ability inability to ambulate (GMFCS grade V) presence of severe and changes over a period of time or changes due to an contractures or joint dislocation, function-limiting deform- intervention. ities or contractures of the skeletal system, and previous Alleviation of spasticity and impaired ambulation operations on the spinal column over several segments. as well as improvement of the resulting delayed motor The surgical procedure was performed via a single level development require a multidisciplinary and multimodal laminotomy according to the technique described by Park approach involving physiotherapy, occupational therapy, et al. [21, 22]. A pre-operative MRI of the spine was used to oral medication or intrathecal application of baclofen, and identify the position of the conus and the respective overly- intramuscular botulinum toxin injections. The introduction ing lamina intended for laminotomy (usually the L1 lamina, of selective dorsal rhizotomy (SDR) widened the arma- less frequent L2 or Th12). Intraoperatively, the access via mentarium of treatment options. This procedure consti- the performed laminotomy exposed the distal conus and the tutes of a surgical intervention to transect a portion of lowest exiting (sacral) nerve roots. The sacral nerve roots each lumbar sensory nerve root bilaterally to reduce lower lower than S1 were covered by a microsurgical patty inserted extremities’ spasticity and originates from the pioneering between the estimated S1 and S2 sensory rootlets (later veri- work of Sherrington and Foerster among others [11, 31]. fied by intraoperative EMG). The performed single-level L1 The surgical procedure of SDR involves either a mul- (or L2) laminotomy furthermore allowed for exact identifica- tisegmental laminotomy [25, 26] or a tailored interlaminar tion of the L1 sensory root a either the caudal (or cranial) access through two or three interlaminar spaces [13, 32] exposed neuroforamen, thereby defining all exposed sensory to address the sensory nerve roots at their neuroforaminal nerve roots in-between itself and the caudally inserted patty exit. Alternatively, a monosegmental laminotomy overly- as the L2 to S1 roots — positioned in an orientation from ing the conus to perform the transection in proximity of lateral to medial. After transection of 50% of the sensory the dorsal root entry was introduced by Park et al. [21, L1 root, the 5 separate sensory nerve roots L2 to S1 were 23]. Regardless of the surgical approach, depending on then partially transected following their anatomical posi- the institutional protocol between 20 and 70% of the vol- tion from lateral to medial. The correct assignment of the ume of each sensory nerve root from L1 to S1 (or S2) treated nerve root to the assumed topographical level was are transected bilaterally. The aim of the current study verified using stimulated EMG and evaluation of the respec- is to investigate the outcome of children with respect to tive motor responses. For the first children of the series, spasticity, muscle strength, and overall function 12 and this was further confirmed by simultaneous direct clinical 24 months after SDR. assessment of the motor response. Uniformly, 50 to 70% of the volume of all lumbar (L1 to L5) and of S1 sensory nerve root were transected bilaterally. Starting in 2011 with the 84th patient of this series, approximately 50% of the Material and methods sensory S2 root volume was bilaterally transected as well. The correct differentiation of S1 and S2 — and possible Patients and study design adjustment of the above-mentioned anatomical identifica- tion — was based on stimulated EMG with characteristic For this retrospective cohort study, 150 children who S2 response of abductor hallucis muscle and on the distribu- underwent a SDR procedure in the time period from tion of responses of the external anal sphincter between the two nerve roots. Pudendal dorsal-root action potential 13 Acta Neurochirurgica (2021) 163:2837–2844 2839 (pDRAP) was recorded after respective peripheral stimula- and 61 boys (56%). The mean age at the time of surgery of tion from S1, S2, and S3 by placement of two recording these 109 patients was 6 ± 2.73 years (range 2–17 years). electrodes in close proximity the nerve exits at the conus The majority of children (83/109, 76%) were born prema- [8, 16]. While never a significant amount of pPDAP was turely (Table 1). For a minority of the children (20/109, measured for S1, its recording allowed the preservation of 18%), cranial MRIs were available, all confirming the pres- bladder innervation either in the non-transected part of S2 ence of periventricular leucomalacia (PVL). or in S3. Post-operative care included appropriate analgesia and mobilization after post-operative day 2. Children were Spasticity transferred routinely to a pediatric rehabilitation facility for an extensive inpatient rehabilitation program 1 week after Adductors A complete pre- and 12-month post-operative surgery. Follow-up examinations were performed 6, 12, and examination of the adductor spasticity on both sides was per- 24 months post-operatively. formed in 85 patients. MAS values had improved 12-month post-operatively in 58 children (68%) with respect to the Outcome measurements right-sided adductors and in 61 children (72%) for the left- sided adductors. The MAS values had worsened in 3 (4%) Pre- and post-surgical assessment consisted of a medical children for the right and in 5 (6%) children for the left side. history, clinical examination, and evaluation of the follow- MAS values were unchanged in 24 (28%) and 19 (22%) chil- ing standardized scales: (i) Muscle strength was recorded dren for the right and left adductors, respectively. according to the Medical Research Council (MRC) Scale After 24 months, scores for 59 children were available of for Muscle strength from grade 0 to 5 [18, 24]. (ii) Spas- whom 42 (71%) and 45 (76%) demonstrated right and left ticity was recorded using the 6-point Modified Ashworth side improvement, respectively. The MAS of 12 (20%) and Scale (MAS, [3, 5]). (iii) Overall motor function regard- 11 (19%) children remained unchanged on the right and left ing ambulation was graded according to the 5-grade Gross side, respectively. It worsened in 5 (9%) and 3 (5%) chil- Motors Function Classification System (GFMCS). (iv) The dren on the right and left side, respectively. The proportion Gross Motor Function Measure (GMFM-88) was utilized as of children with no detectable spasticity of the adductors a measure to evaluate overall motor function. The GMFM- increased from 10 to 35 for the right and from 7 to 36 for the 88 is a validated score which computes the performance in left side after 24 months. The overall improvement in MAS 88 tasks in 5 major subgroups and yields an overall perfor- after 24 months was bilaterally significant (p < 0.00625, mance score from 0% to a maximum of 100%. Fig. 1). Statistics MAS scores of the bilateral adductors and hamstring (ischi- ocrural) muscles to assess spasticity and MRC scores of bilateral dorsiflexion of the ankle and extension of the knee joint to assess muscle strength were chosen as outcome measures for statistical analysis. Values of paired samples of pre- and post-operative MAS and MRC and changes in GMFM-88 were analyzed by the Wilcoxon matched-pairs signed rank test. A level of p < 0.05 was considered to indicate statistical significance for changes of GMFM-88. Significance level for changes of MAS and MRC scores were adjusted with Bonferroni’s correction to indicate sig- nificance at a p < 0.00625. Standard statistical software was used for all calculations (SPSS Statistics 25, IBM, USA). Results Within the cohort of 150 patients who had undergone SDR during the observation period, a pre- vs. post-operative Fig. 1  Development of Modified Ashworth Scores distribution of comparison with available matching sets of pre- and post- bilateral adductors 12 and 24 months after SDR demonstrates a sig- operative data was possible for 109 patients, 48 girls (44%) nificantly reduced spasticity 13 2840 Acta Neurochirurgica (2021) 163:2837–2844 Hamstrings A similar improvement was seen for the MAS of the hamstring muscles of 85 patients with available pre- and post-operative data. MAS values had improved 12-month post-operatively in 69 (81%) and 71 (83%) chil- dren with respect to the right and left hamstrings, respec- tively. For 15 (18%) and 11 (13%) children, the right and left MAS score remained unchanged, respectively. The MAS worsened in one child (1%) for the right and in 3 children (4%) for the left hamstrings. After 24 months, the MAS scores of the hamstrings were available for 58 children of whom 47 (81%) and 46 (79%) improved on the right and left side, respectively. The MAS of 9 (16%) remained unchanged on both the right and the left side, and it worsened on the left in 2 (3%) and on the right in 3 (5%) children. The proportion of children with no detectable spasticity of the hamstrings increased from 2 to 34 for the right and from 2 to 32 for the left side after 24 months. The change of MAS was significant bilaterally after 24 months (p < 0.00625, Fig. 2). Fig. 3  Significantly improved strength of bilateral knee extension and ankle dorsiflexion 24 months after SDR Muscle strength (p < 0.00625, Fig. 3). Regarding the strength of further Pre- and post-operative manual muscle strength values of muscle groups such as hip flexion and extension, knee flex- the right and left ankle dorsiflexion were available for 41 ion, and ankle flexion, this improved or remained stable in a children and demonstrated significantly improved strength majority of children. Only in a minority of children the post- on both sides after 24 months (p < 0.00625, Fig. 3). Like- operative MRC scores were lower than the pre-operative wise, for 46 and 45 children, comparison of pre- and post- values (Table 2). operative strength of knee extension demonstrated a sig- nificant improvement of bilateral strength after 24 months Overall functional outcomes — GMFM88 and GMFCS Pre- and 12-month post-operative GMFM-88 values were available for 77 children. By 12 months after surgery, the mean GMFM-88 had increased significantly by 4% (95% confidence interval [2.0–5.4]) from an average of 79 to 83 (p < 0.0001). After 24 months, an even stronger increase of the GMFM-88 by 7% (95% confidence interval [5.0–9.4]) from 79 to 86 was observed (n = 56) (p < 0.0001, Fig. 4). GMFCS level data were available for 64 patients 24 months post-operatively. The majority of children (78%) remained at the same GMFCS level at follow-up 2 years post-oper- ative, yet 20% improved by one level and one child (2%) Table 1  Demographic data Observation period 01/2007 to 04/2015 SDR patients (total) n = 150 SDR patients (with pre-and post-operative data, n = 109 included for evaluation) Female/male 48/61 Fig. 2  Development of Modified Ashworth Scores distribution of Age (mean ± SD, n = 109) 6 ± 2.73 bilateral hamstrings 12 and 24 months after SDR demonstrates a sig- Premature birth 83 of 109 nificantly reduced spasticity 13 Acta Neurochirurgica (2021) 163:2837–2844 2841 Table 2  Development of muscle Improved Unchanged Worse p strength (MRC score) after 24 months Hip Extension right (n = 37) 17 (46%) 11 (30%) 9 (24%) Extension left (n = 37) 18 (49%) 15 (40%) 4 (11%) Flexion right (n = 47) 18 (38%) 19 (40%) 10 (21%) Flexion left (n = 47) 16 (34%) 22 (47%) 9 (19%) Knee Extension right (n = 46) 20 (43%) 22 (48%) 4 (9%) p < 0.00625 Extension left (n = 45) 18 (40%) 24 (53%) 3 (7%) p < 0.00625 Flexion right (n = 46) 13 (28%) 24 (52%) 9 (20%) Flexion left (n = 46) 10 (22%) 26 (57%) 10 (22%) Ankle Extension right (n = 41) 23 (56%) 14 (34%) 4 (10%) p < 0.00625 Extension left (n = 41) 23 (56%) 14 (34%) 4 (10%) p < 0.00626 Flexion right (n = 33) 15 (46%) 7 (21%) 11 (33%) Flexion left (n = 33) 13 (39%) 7 (21%) 13 (39%) Fig. 4  Significantly improved GMFM-Scores 12 and 24 months after Fig. 5  Development of GMFCS 12 and 24 months after SDR SDR deteriorated after 24 months (p < 0.01, Fig. 5). After significantly increased strength of bilateral knee extension 12 months, only 5% had already improved their GMFCS and ankle dorsiflexion. level (p = 0.11). Overall function Since the re-emergence of the SDR proce- dure at the middle of the last century and after many refine- ments, this procedure has become a relevant and unique Discussion option in the treatment of children who are affected by spas- tic CP. The procedure differs from other options to treat spas- Here we describe the outcome of a large ambulatory pediat- ticity, because it targets to treat spasticity at neuronal rather ric patient cohort with bilateral, spastic CP following SDR than the muscular level. The transection of sensory rootlets via a monosegmental laminotomy. The study focuses on that demonstrated exacerbated EMG-responses through their spasticity, functional status, and muscle strength. As main intramedullary and spinal relay during intraoperative testing findings, we highlight 24 months after SDR reduced spastic- alters muscle tone and reduces spasticity. The reduction of ity of bilateral adductor and hamstring muscles, improved spasticity establishes the opportunity to improve gait and functional score by 7% in the GMFM-88 test battery, and ambulation which were previously hindered by its presence. 13 2842 Acta Neurochirurgica (2021) 163:2837–2844 Therefore, SDR usually does not stand alone but is embed- changed score within the MAS scale to a significantly better ded in a program of intense physiotherapy and rehabilitation level after 24 months. This was the case for 71% and 76% for to utilize the established potential of less spasticity [19, 29]. right and left hip adductors, respectively, and for 81% and The classical indication for SDR is ambulatory children — 79% for right and left hamstrings, respectively. Apparently, usually classified as GMFCS I–III — with a spastic bilat- there are data indicating that the post-operative course of eral presentation of CP. The intention of the procedure is spasticity of hip adductors and other muscle groups might to improve ambulation and gait. However, the indication to differ. For hip adductors, several publications describe a last- perform SDR has been widened to include more severely ing reduction of spasticity even after more than 10 years affected, non-ambulatory children of GMFCS IV and V after SDR. For knee extension and ankle flexion, lower as an alternative to intrathecal Baclofen. For those MAS scores in the early years after SDR than after long- children, the aim of the procedure would be alleviation of term follow-up have been reported, which would indicate daily care; a progression to an ambulatory state cannot be partial recurrence of spasticity. This would be in accord- expected. The rate of children who change their level at the ance with the slightly lower GMFM scores and could explain GFMCS scale is usually considered to be low; commonly this observation. The explanation for the apparent worsening the children improve within their pre-operative GMFCS of spasticity remains yet unexplained, but could be related level. However, a portion of children of this cohort changed to puberty-induced changes of physical appearance. The on the GMFCS scale to a lower (better) grade — 5% after 24-month follow-up of the presented patient cohort does 12 months and 20% after 24 months. Throughout literature, not allow statements about long-term development of spas- the rate of change of GMFCS level is variable from 4.8% ticity for this cohort; the evaluation of future data needs to after 12 months and up to 23% after longer follow-up [1, 7]. be awaited. To compare the results of the presented cohort, even longer follow-up periods will be needed. Muscle strength As a measurement for overall function, the GMFM-88 score was evaluated pre- and post-operatively. An increase One major concern towards SDR is the apprehension to elicit by 4% and 7% was demonstrated after 12 and 24 months, muscular weakness after the procedure. The decreased tone respectively. After 20 months, an increase by 5% has been in the anti-gravity musculature of the lower extremities can published by Engsberg et al., which is similar to the pre- produce an impression of muscular weakness and impaired sented results. Regarding the long-term development security when ambulating immediately post-operatively. of GMFM-88, divergent results have been published. An This represents rather the unmasked true underlying mus- increase of GMFM-88 over the follow-up of 1 to 5 years, fol- cular strength together with a possibly altered proprioception lowed by stable score up to15 years post-SDR, was reported than elicited weakness by the SDR procedure. Clinically, by Dudley et al.. On the contrary, some of the publica- this situation is usually limited to a few weeks after which tions report the largest increase of GMFM-88 at 3–5 years this impression subsides. Correspondingly, the data of the post-operatively, followed by a decline to still significantly presented cohort demonstrated a significant improvement better than pre-operative scores at the long-term follow-up of the primary endpoint muscles for knee extension and of more than 10 years [1, 6, 36]. Given the relatively short ankle dorsiflexion after 24 months. For all other examined follow-up of 24 months of the presented patient cohort, muscle groups, a majority of patients either improved or progressive gain of function during the next years could be remained stable, only a minority demonstrated lower MRC expected. values at the 24-month post-operative examination. This appears to be in line with previous publication which has Spasticity Spasticity constitutes the clinical target symp- documented improved strength in several lower extremities’ tom for SDR; its presence negatively influences ambula- muscle groups [1, 10, 15]. Therefore, the presented data of tion, and its reduction improves overall function. The MAS the cohort along with the literature rather demonstrate an (like the MRC scale) is an ordinal and not an interval scale. improved muscular strength after SDR and disprove the Therefore, the evaluation of the numeric amount of absolute assumption of impaired strength as an argument against this changes (differences of pre- and post-operative means on surgical procedure. those scales) — although often published, e.g., for MAS [1, 15] — is not statistically sound and is therefore omitted in Operative technique the presented manuscript. Although the absolute amount of reduced spasticity cannot be calculated by the used MAS The operative access to the sensory lumbar and sacral nerve score, the overall development of spasticity is well pictured roots was achieved via a one level laminoplasty centered over by pre- and post-operative comparison of those scores. For the conus position as compared to a 5-level laminectomy or the two evaluated muscle groups, a majority of patients laminoplasty. Previously published data of this patient cohort 13 Acta Neurochirurgica (2021) 163:2837–2844 2843 indicated a lesser incidence of mild scoliosis of 10% as com- procedure resulted in an effective and permanent reduction pared to a 55% rate after 5-level laminectomy [14, 34, 35]. of spasticity and improved overall function without causing The 10% incidence would be comparable with the natural relevant weakness during the evaluated follow-up. incidence of scoliosis of ambulatory children affected by CP. Since the reduction of spasticity and improvement of overall function seem to be independent from surgical access, Declarations the single-level laminotomy should be preferred because of the better risk profile regarding secondary spinal deformity. Alter- Conflict of interest The authors declare no competing interests. natively, the described keyhole access for a SDR through three Open Access This article is licensed under a Creative Commons Attri- interlaminar spaces will likewise carry significantly lower risk bution 4.0 International License, which permits use, sharing, adapta- for developing a post-operative spinal deformity compared to tion, distribution and reproduction in any medium or format, as long multilevel laminotomies [13, 32]. as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are Limitations included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in The lack of a control group does not allow for direct com- the article's Creative Commons licence and your intended use is not parison and allows only a descriptive statistical evaluation of permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a the patient cohort. However, given the multiplicity of reports copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. about efficiency of SDR, the set-up of a randomized con- trolled trial would be problematic, because it would deprive a group of children off this treatment option and parents’ consent to such a study design would be questionable. 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