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No support that early selective dorsal rhizotomy increase frequency of scoliosis and spinal pain – a longitudinal population-based register study from four to 25 years of age

No support that early selective dorsal rhizotomy increase frequency of scoliosis and spinal pain... Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 https://doi.org/10.1186/s12891-020-03782-5 RESEARCH ARTICLE Open Access No support that early selective dorsal rhizotomy increase frequency of scoliosis and spinal pain – a longitudinal population-based register study from four to 25 years of age 1,2* 1,3 Annika Lundkvist Josenby and Lena Westbom Abstract: Spasticity interfering with gross motor development in cerebral palsy (CP) can be reduced with selective dorsal rhizotomy (SDR). Although reported, it is unknown if SDR surgery causes later spine problems. Using CP-registry data from a geographically defined population, the objectives were to compare frequency and time to scoliosis, and spinal pain up to adult age after SDR-surgery or not in all with same medical history, functional abilities, CP-subtype and level of spasticity at 4 years of age. Variables associated with scoliosis at 20 years of age were explored. Method: In the total population with CP spastic diplegia in Skåne and Blekinge, born 1990–2006, 149 individuals had moderate to severe spasticity and no medical contraindications against SDR at 4 years of age and were included; 36 had undergone SDR at a median age of 4.0 years (range 2.5–6.6 years), and 113 had not. Frequency of scoliosis and age when scoliosis was identified, and frequency of spinal pain at 10, 15, 20 and 25 years of age were analysed using Kaplan-Meier survival curves and Fisher’s exact test. Multivariable logistic regression was performed to identify variables to explain scoliosis at 20 yearsofage. Gross MotorFunctionClassification System (GMFCS) levels at 4 years of age were used for stratification. Result: Frequency of scoliosis did not significantly differ between groups having had early SDR surgery or not. In GMFCS IV, the SDR group had later onset and lower occurrence of scoliosis (p = 0.004). Frequency of spinal pain did not differ between the groups (p- levels > 0.28). GMFCS level was the background variable that in the logistic regression explained scoliosis at 20 years of age. Conclusion: Frequency of back pain and scoliosis in adulthood after early SDR are mainly part of the natural development with age, and not a surgery complication. Keywords: Cerebral palsy, Selective dorsal rhizotomy, Complications, Scoliosis, Spinal pain, Population-based, Controlled registry study * Correspondence: annika.lundkvist@med.lu.se Children’s Hospital, Skåne University Hospital, Lund, Sweden Faculty of Medicine, Department of Health Sciences, Lund University, Lund, Sweden Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long 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 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 article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 2 of 13 Introduction that scoliosis was seen in younger ages in children with Selective dorsal rhizotomy (SDR) is a neurosurgical pro- higher GMFCS levels meaning more severe functional cedure for children with spastic diplegic cerebral palsy limitations. The incidence of scoliosis increased with age (CP) that permanently reduces spasticity in the lower and GMFCS level. The incidence of spinal pain in CP limbs by cutting parts of lumbosacral rootlets at spinal was shown to increase with increasing scoliosis severity, levels L2-S2. SDR is always combined with physical ther- and scoliosis incidence increased with severity of gross apy, and it is mainly used in young children to improve fu- motor dysfunction [16, 17]. ture functional skills [1]. Neurosurgeons use either Today it is unknown whether the above figures regard- multilevel or single level laminotomy surgery to access the ing spine problems after SDR actually differ from the situ- rootlets. As the intervention includes surgery to the spine ation in persons with the corresponding type and severity and spinal nerve roots, there is a hypothetical risk that of CP who are not treated with SDR. In a recently pub- SDR will cause spinal deformities and pain may develop. lished review of spinal deformities after SDR, the authors The single level laminotomy technique was developed for suggested that the occurrence of spinal deformities were the advantages of decreased time for surgery, postopera- most likely not different, or only minimally higher after tive pain and to minimize the risk of progressive lumbar SDR, than in the natural history of CP, girls were more instability [2]. In a short-term follow-up, no significant dif- likely to develop scoliosis, and that the deformity develops ferences between the two techniques has been found [3]. over a long time, but the evidence base was weak [4]. After SDR, scoliosis was reported to be the most com- Incidence of spinal deformity and pain after SDR is an mon spinal deformity occurring at a weighted mean inci- important complication to consider, when deciding dence of 31.6% [4], and Cobb angles ≥20° have been whether to proceed with the procedure or not, as spinal reported at 3–9% 2.8–11.6 years after SDR [5–7]. In an- deformity can have a major impact on quality of life other study of children with pre-existing scoliosis prior [18]. There is a need for longitudinal follow-up studies to SDR, 5% improved Cobb angle, 70% were unchanged, of spinal pain and deformities in individuals undergoing and 25% had worsened at a mean follow-up time of 4.3 SDR, taking the natural development in cerebral palsy years [8]. Peter et al. and Langerak et al. followed the into account. same ambulatory cohort over time, and at the five-year The objectives of the present study were to compare follow-up after SDR, scoliosis of ≥10° was found in 16% frequency and age when scoliosis was diagnosed, and at 4.5 years and 57% at 21 years follow-up, of which 7% frequency of spinal pain in individuals who had under- had Cobb angles of ≥30°. None of the participants had gone SDR, and in a control group with same CP-type, scoliosis prior to SDR [9, 10]. medical history, body structure and functions at 4 years In follow-up studies from 3.6 to 21.4 years after SDR, of age, living in the same geographically defined total hyperlordosis was found to increase compared to base- population, followed from birth to adult age in the same line in 10–50%, and a hyperkyphosis was reported in 1– structured program and registry. Another objective was 9%. Individuals who were walking with and without to explore if any of the variables SDR surgery, sex, spas- walking aids generally had, postoperatively, larger lum- ticity and GMFCS level at 4 years of age, was associated bar lordosis [6, 8, 9, 11–13]. with the presence of scoliosis at 20 years of age in this Spondylolisthesis was uncommon preoperatively and population. postoperative prevalence ranged from 2 to 27%, mainly minor to grade 1 slippage [6, 7, 9, 11–13]. In a 20–28- Methods year follow-up after SDR, Park et al. found 31% with A retrospective population based controlled long-term scoliosis and other spinal problems [14]. outcome study using data from the Swedish cerebral On the other hand, persons with CP are generally palsy follow-up program (CPUP) including prospectively more frequently affected by spinal abnormalities, par- registered results from repeated, most often yearly, clin- ticularly scoliosis, than the general population [15]. ical assessments in children, adolescents and adults with Follow-up studies of adult individuals walking with or CP, living in a defined geographical area in southern without devices, who had undergone SDR during the Sweden [19]. preschool years to early school age, show occurrence of spinal pain in 17–23% [9] and pain in spine and lower Setting limbs in 28% [14]. In a follow-up with shorter time CPUP frame, spinal pain was reported at a lower level, 5% in The secondary prevention follow-up program in cerebral an self- ambulant cohort 5.8 years post SDR [13]. palsy (CPUP) was started in the regions of Skåne and In previous population based studies, excluding per- Blekinge in 1994, as a cooperation project between the sons treated with SDR, Kaplan–Meier survival estimates child orthopaedic and paediatric neurology departments based on the results of the clinical examination showed in tertiary care level, and the local child (re) habilitation Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 3 of 13 services and orthopaedic units in the area. The aims were during the years 1994–2015; there were 267 persons par- to prevent hip dislocations and severe contractures, in- ticipating in the CPUP-program and seven (2.5%) who crease cooperation, and generate more knowledge about did not. Demographic, medical and functional character- CP, especially the natural history and long-term results of istics of the population with CP spastic diplegia in the different treatments. New treatment modalities at the time study area, and the distribution of these characteristics were intrathecal baclofen (ITB) and SDR [20]. in the study groups are presented in Table 1. The original program was based on structured follow- up and evaluation of hip radiographs and repeated, SDR group structured, often annual physiotherapy (PT) assessments Of the 267 CPUP participants with spastic diplegia, there [19]. To identify all children with CP in the population, were 36 persons who had undergone SDR surgery at a regularly repeated inventories were performed in Skåne median age of 4.0 years (range 2.5–6.6 years). They were and Blekinge to find the youngest children, not yet in- followed to a median age of 22.3 years (range 11.3–27.2); vited to the program, and later on, after 4 years of age to 30 of the 36 SDR-operated persons had CPUP assess- decide on CP diagnosis and subtype for children in the ments at 20 years of age; eight had reached and been program [21, 22]. assessed at 25 years of age at the end of the study, Janu- Data for this study was retrieved from the CPUP ary 1st, 2018 (Table 1) (Fig. 1). demographic patient forms, neuropediatric, PT assess- ments, and operations forms from 1994 to 2018, vali- Excluded dated and completed by scrutinizing medical records Of the remaining 231 persons with CP spastic diplegia covering most of the health care systems in the two re- in the study population, there were 55 persons with gions during the study period. Demographic data was medical contraindications to SDR; congenital malforma- checked against the Swedish population registry every tions or syndromes in 25 persons, severe perinatal as- year, including dates for births, deaths, moving in and phyxia in 17, post-neonatal brain injuries in eight, and out of the area. five persons had other severe somatic disorders. Classification of spasticity level at 4 years of age, as de- SDR scribed below, was mild in 63 persons, without any indi- Some of the children with BSCP and moderate to severe cation for SDR, and they were therefore excluded from spasticity, were referred from their local (re-)habilitation the comparison (Table 1) (Fig. 1). units in the Skåne-Blekinge area for evaluation regarding spasticity management, and if selected for SDR, the surgi- Control group cal intervention and the immediate postoperative rehabili- The remaining 113 persons with CP spastic diplegia, tation took place at the Skåne University Hospital in moderate-severe spasticity level and no medical contra- Lund. Indications for SDR were spastic cerebral palsy with indications against SDR constituted the control group more involvement in the legs than the arms, pure spasti- (Table 1) (Fig. 1). As of January 1, 2018, this natural his- city without dystonia and ataxia, spasticity interfering with tory control group was followed to a median of 19.6 functional development, enough muscular control and years of age (range 8.9–27.3 years). strength to reach the individual functional goals, and ac- Six children treated with ITB were excluded from the cess to regular postoperative physical therapy and orthotic control group after the ITB-operation at 5, 6, 11, 14, 16 and services. Individual goals were set together with family, 18 years of age respectively. In addition, two persons in the local (re) habilitation unit and the spasticity team [23]. control group showed to be too young (< 8 years of age) at During the last two decades Magnetic Resonance Imaging the latest assessment and were not included in the com- (MRI) of the brain has been recommended at about 18– parison. In the control group, 54/113 had reached and had 24 months of age in children with CP, which, although assessments at 20 years of age, and 16/113 at 25 years. mostly seen clinically as dyskinesia or ataxia, has added in- volvement of thalamus/basal ganglia or cerebellum to the Definitions and classifications contraindications for SDR. Cerebral palsy (CP) was defined according to Much et al. 1992 [24] and the Surveillance of Cerebral Palsy in Participants Europe (SCPE) [25]. Population The prevalence of CP in the study area was 2.7/1000 CP subtype children 4–11 years of age as of Jan 1st, 2002, of which Subtypes were defined by the dominating neurological 38% was spastic diplegia [21]. The present study was symptom between four and 7 years of age. All patients based on all persons born 1990–2006, with CP spastic in this study had Bilateral Spastic CP (BSCP) as defined diplegia, who lived in Skåne-Blekinge for at least 2 years by the SCPE, and all also fulfilled the definition of the Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 4 of 13 Table 1 Characteristic of all participants in CPUP with CP spastic diplegia, N = 267 SDR No contraindication - no SDR Excluded with group contraindication Non-SDR group Excluded mild spasticity n = for SDR n = 113 (%) n = 63 (%) 36(%) n = 55 (%) Year of birth* 1990–1993 13 (36) 31 (27) 12 (19) 13 (23,5) 1994–1997 14 (39) 27 (24) 22 (35) 9 (16.5) 1998–2001 7 (19.5) 27 (24) 13 (21) 14 (25.5) 2002–2006 2 (5.5) 28 (25) 16 (25) 19 (34.5) Birth country other than Sweden 6 (17) 12 (11) 11 (16) 6 (11) Sex Male 25 (69) 60 (53) 37 (60) 41 (74.5) Female 11 (31) 53 (47) 26 (40) 14 (25.5) Gestational Age (GA) GA < 26 weeks 2 (6) 7 (6) 8 (12.5) 1 (2) GA 26–27 weeks 3 (8) 17 (15) 5 (8) 1 (2) GA 28–31 weeks 16 (44.5) 31 (27.5) 13 (21) 2 (3,5) GA 32–36 weeks 8 (22) 24 (21) 19 (30.5) 13 (23.5) GA > 36 weeks 7 (19.5) 29 (25.5) 12 (19) 35 (63.5) Unknown 0 5 (4) 6 (9.5) 3 (5.5) Birth weight < 1000 g 3 (8) 23 (20) 11 (17.5) 2 (4) 1000–1499 g 8 (22) 21 (19) 11 (17.5) 1 (2) 1500–2499 g 15 (42) 23 (20) 14 (22) 7 (12.5) 2500–4999 g 9 (25) 26 (23) 14 (22) 27 (49) Unknown 1 (3) 20 (18) 13 (21) 18 (32.5) Multiple pregnancy 5 (14) 25 (22) 6 (10) 2 (4) Severe asphyxia > GA 34 weeks 1 (3) 0 0 15 (27) Post-neonatal CP 0 0 0 7 (13) CNS imaging (dominating pattern) Maldevelopments 0 0 8 (13) 26 (47.5) Predominant white matter injury (periventricular) 17 (47) 74 (65.5) 33 (52) 16 (29) Basal ganglia/thalamus lesions 0 0 0 0 Cortical/subcortical grey matter lesions 1 (3) 4 (3.5) 2 (3) 5 (9) Normal 2 (6) 9 (8) 4 (6) 5 (9) No CNS imaging 16 (44) 26 (23) 16 (26) 3 (5.5) Shunted hydrocephalus 4 (11) 15 (13) 13 (21) 20 (36) Epilepsy 6 (17) 27 (24) 12 (19) 23 (42) Intellectual disability None or mild (IQ > 50) 34 (94) 93 (82) 57 (90) 36 (65) Moderate or severe (IQ < 50) 2 (6) 20 (18) 6 (10) 18 (33) Missing info 0 0 0 1 (2) Severe visual disability/blindness 4 (11) 20 (18) 7 (11) 10 (18) GMFCS levels at 4 years I 2 (5.5) 43 (38) 44 (70) 16 (30) II 11 (30.5) 18 (16) 6 (10) 12 (22) Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 5 of 13 Table 1 Characteristic of all participants in CPUP with CP spastic diplegia, N = 267 (Continued) SDR No contraindication - no SDR Excluded with group contraindication Non-SDR group Excluded mild spasticity n = for SDR n = 113 (%) n = 63 (%) 36(%) n = 55 (%) III 11 (30.5) 20 (18) 8 (12) 15 (28) IV 12 (33.5) 23 (20) 5 (8) 4 (7) V 0 9 (8) 0 7 (13) Missing info 0 0 0 1 Spasticity level at 4 years*** Mild 0 0 50 (79) 13 (24) Moderate 12 (33) 83 (73) 0 29 (53) Severe 24 (67) 30 (27) 0 10 (18) Missing info 0 0 13 (21) 3 (5) Legend: CPUP The Swedish national secondary prevention follow-up program in cerebral palsy, SDR Selective Dorsal Rhizotomy, CP Cerebral Palsy, GA Gestational Age, ITB Intrathecal Baclofen, GMFCS Gross Motor Function Classification System, CNS Central Nervous System, IQ Tested or estimated cognitive level. Differences between the SDR group and the control group n.s., except regarding birth year cohorts* (p < 0.05) and spasticity levels*** (p < 0.001) Fig. 1 Flow chart illustrating inclusion and exclusion of individuals in SDR group and control group Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 6 of 13 subtype spastic diplegia in the Hagberg classification [21, Estimated spasticity level at 4 years of age was classi- 25]. CP spastic diplegia includes all five GMFCS-levels, fied based on muscle tone (MAS summation score) and as long as there is greater involvement of the legs than clinical signs, such as degree of leg scissoring (none, of the arms, and can be asymmetrical, with more in- mild, severe) in rest and in activity, and foot clonus (yes/ volvement of either left or right side of the body [26]. no), as assessed by each child’s local PT according to the Brain morphology was classified based on the dominat- structured follow-up form in CPUP (http://cpup.se/in- ing pattern on brain imaging according to the SCPE [27]. english/manuals-and-evaluation-forms). Severe asphyxia was classified based on low Apgar Spasticity level was defined as mild if the MAS sum- scores (< 4 at 5 min), clinical and EEG-verified seizure mation score was within the first quartile 0–3, moderate activities within the first 72 h after birth. if in the second quartile 4–6, and severe if summation Epilepsy was defined as having had at least two unpro- score was 13 or higher. In the third quartile, MAS sum- voked seizures after the neonatal period. mation scores 7–12 the spasticity level was defined as se- Intellectual disability was assessed at about 4 years of vere if combined with severe scissoring in activity, and if age. Only parts of the cohort were formally IQ-tested at not, it was classified as a moderate spasticity level. that age, and only moderate to severe intellectual disabil- Scoliosis was assessed by inspection by the physiother- ity was defined as intellectual disability in this paper. For apist and registered to be either present or not. If the majority of the children, this is a clinical estimation present, mild: scoliosis visible only when leaning forward with inherent uncertainty. with aligned pelvis, moderate: scoliosis visible both in The Gross Motor Function Classification System (GMFC leaning forward in sitting and when sitting straight, and S) [28] was used to classify gross motor function at each severe: scoliosis, not correctable, with need of support in PT assessment in CPUP. The GMFCS level classified at sitting or standing. The CPUP PT assessment of the the first assessment after the child’s fourth birthday, or spine has shown to have high inter-rater reliability and pre-operatively if earlier SDR surgery, was used. The specificity in screening for moderate to severe scoliosis GMFCS was used for classification of gross motor func- in this population [32]. tion in the CPUP from the year 1995 by some physiother- In the present study, scoliosis status was dichotomized: apists as part of the development/testing of the no scoliosis if there was no scoliosis at examination or classification, and from 1998, the classification was intro- when a scoliosis was assessed as being correctable, and duced for all PT assessments in CPUP and have shown existing scoliosis if scoliosis was assessed by the PT as good stability in previous studies in this population [29]. being severe or moderate and not correctable, or if the The GMFCS-level was classified by the child’sphysio- individual had been undergoing scoliosis surgery. Dates/ therapist in 239 of all 267 persons with BSCP. In the old- age at first PT assessment with existing scoliosis and at est cohort, the GMFCS level was classified using other scoliosis surgery were noted. entered CPUP-data; the reliability of such a retrospective Questions about experienced pain and localization of classification was first confirmed, see Additional file 1. pain were introduced in the PT assessments from Janu- The classification was performed on de-identified data ary 2007 [33]. Presence of pain was assessed by either with no information available regarding if the child the person him/herself or by proxy. For children (< 18 belonged to the control or the SDR group. years) pain in the spine was reported by answering yes/ Muscle tone was assessed according to the Bohannon no and for adults (> 18 years) recalling the last 4 weeks Modified Ashworth Scale (MAS) [30]. MAS-scores for for spinal pain that was classified as being moderate or five muscle groups (hip-flexors, hip-adductors, knee- severe. After 2016, children were also asked to recall extensors, knee-flexors, and plantar-flexors) in both legs presence of pain during the last 4 weeks. were summed up for each CPUP participant with BSCP, who had complete recordings from all included muscle Statistics groups at 4 years of age. The MAS scores 1 and 1+ were Kaplan-Meier survival analyses were performed to both counted as 1. Median MAS summation score was 7 analyze time to scoliosis in relation to the following di- (range 0–32, inter- quartile range 4–12). chotomous variables; SDR surgery (yes vs no), GMFCS Muscle tone assessed with MAS is closely related to level (I-II vs III-V), level of base-line spasticity (moderate GMFCS level [31]. When occasional single MAS-scores vs severe) and sex (male vs female). were missing in the study groups, imputation was there- Kaplan Meier survival analysis was further used to fore performed by using the median score for the miss- compare time to scoliosis, stratifying for SDR, and sever- ing specific muscle group(s) of all with completely ity of gross motor function limitation, defined as GMFC recorded MAS scores and the same GMFCS level. Six S level at 4 years of age. Sub-groups were created ac- children in the SDR group and 12 in the control group cording to GMFCS levels; I-II (n = 74), III (n = 31) and had imputed single MAS scores. IV-V (n = 44). Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 7 of 13 Two-sided Pearson’s Chi-Square and Fisher’s exact tests All 12 in the SDR group GMFCS IV were followed to were used for comparisons between the SDR and the non- age 15 years, and 11 were followed to age 20 years; one SDR group background factors (Table 1) and pain at dif- SDR group participant GMFCS IV had scoliosis at age ferent age, and Kappa agreement test to check validity of 14 years, and one at age 23 years. Eight of the 23 control retrospective GMFCS-classifications (Additional file 1). group participants GMFCS IV developed a scoliosis at To explore which variables that influenced the devel- 12, 12, 12, 13, 16, 18, 18, and 19 years of age respectively. opment of scoliosis at 20 years of age, the first step was Six of the 14 in the control group followed to at least 15 to perform univariable logistic regression analyses of di- years of age had scoliosis before end of study, and all five chotomous variables in those who had reached this age followed to at least their 20th birthday had scoliosis be- (n = 82). Following variables were analyzed; SDR (yes/ fore that age (Fig. 3c). no), GMFCS at 4 years of age (I-II vs III-V), spasticity at In the univariable analysis, GMFCS level was the vari- 4 years of age (moderate/severe) and sex (male/female). able that significantly explained the presence of moder- All the before mentioned variables, except sex, were ate- severe scoliosis at 20 years of age. In the included in the model when we, as the second step, per- multivariable analysis, the result was maintained formed the multivariable logistic regression analysis. (Table 2). Neither the variables SDR surgery nor base- Due to the small number of participants with scoliosis in line spasticity level made statistically significant contri- both the SDR and non-SDR group, only a small number bution in explaining scoliosis at 20 years of age in the re- of variables could be included in the model. gression model (Table 1). Statistical significance was set at p < 0.05; n.s. denotes no statistically significant difference. Spinal pain IBM SPSS statistics, version 25 was used for analyses [34]. Patient’s reports of spinal pain at 10, 15, 20 and 25 years of age are presented in Table 3. No statistically signifi- cant difference was observed between the SDR and the Results control group (Table 3). Questions regarding pain were The background factors were similar in the SDR group introduced in CPUP in January 2007, and therefore pain and control group (Table 1). A higher proportion were assessments at 10 and 15 years of age were missing for SDR-operated in the first two birth cohorts than in the the oldest cohorts. Younger cohorts had not yet reached younger cohorts born from 1998 (p = 0.043). Another dif- the oldest ages at data extraction. ference was a lower proportion of severe spasticity in the Of all those in GMFCS IV who were followed to the 20 control group than in the SDR group (p =0) (Table 1). years assessment, one of 12 in the SDR and one of seven in the non-SDR group reported spinal pain; both had had Scoliosis scoliosis surgery more than 4 years earlier, and both had Only two of the SDR-operated children were in GMFCS severe spinal pain, interfering with daily activities. level I, and neither had scoliosis at the end of the study. Two of the 43 in the control group GMFCS level I had Discussion scoliosis at the end of the study (n.s.). No child in This is the first population based controlled SDR long- GMFCS V had had SDR-surgery. Two of the seven indi- term outcome study. All individuals in the geographically viduals in the non-SDR group GMFCS V assessed at 20 defined population (98% participating in the CPUP regis- years of age had scoliosis. try) with a medical background and clinical expression In GMFCS levels II-IV no child in either group, had that matched the selection criteria for SDR at baseline scoliosis before 10 years of age. Scoliosis was less fre- were included in the study [1]. Among these all having quent and developed later in GMFCS II-III with higher had SDR-surgery were compared to all who had not. . level of motor function, than in GMFCS IV. Prospectively collected longitudinal follow-up data are In the Kaplan-Meier analyses, the variables GMFCS presented for scoliosis and spinal pain from the popula- (p < 0.001), and base-line spasticity level showed signifi- tion of children with spastic diplegic CP, where a group cant differences between the two groups (p = 0.045) in of individuals had undergone SDR at a young age. Nei- development of scoliosis, however SDR surgery (p = ther scoliosis nor spinal pain was more prevalent during 0.822) and sex (p = 0.387) did not. (Fig. 2a-d). 20 years of follow-up in the SDR group, after the cauda Individuals in GMFCS levels IV-V undergoing SDR equina multilevel surgery, compared to the control had less scoliosis and a later onset of scoliosis compared group representing the natural history in children with to the non- SDR group (p = 0.026) using the Kaplan- about the same base-line prerequisites, and with same Meier analysis. In GMFCS subgroups I-II and III, the standard of care before and during follow up. In children differences were not statistically significant (p = 0.567 at GMFCS-level IV at baseline, without functional walk- and p = 0.778 respectively) (Fig. 3a-c). ing ability, scoliosis developed later and less often in the Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 8 of 13 Fig. 2 a. Kaplan-Meier survival curves illustrating the influence of SDR surgery (SDR vs no SDR) in the development of scoliosis (n = 149) p = 0.822. b. Kaplan-Meier survival curves illustrating the influence of GMFCS level at the age of 4 years in the development of scoliosis (n = 149) p < 0.001. c. Kaplan-Meier survival curves illustrating the influence of spasticity at the age of 4 years (moderate vs severe) in the development of scoliosis (n = 149) p = 0.045. d. Kaplan-Meier survival curves illustrating the influence of sex (male vs female) in the development of scoliosis (n = 149) p = 0.387 SDR group during the following 20 years than in the recorded by the person’s own physiotherapist at certain control group (Fig. 3c). ages, same procedures for all individuals, regardless of As SDR has been a challenged treatment option, few whether they had undergone SDR surgery or not [19]. children have been referred for evaluation. This study in- All persons in the study were treated at the same pub- dicates that feared complications to early SDR, such as lic health care units; orthopedic and pediatric hospital increased frequency of back pain and scoliosis in adult- health care departments, and the habilitation services in hood, are mainly part of the natural development with cooperation. Physiotherapy, occupational therapy, social age, and not a surgery complication. We now can inform and psychological support, orthoses, braces, orthopedic rehabilitation professionals and parents of future SDR surgery, ITB, SDR and from 1998 botulinum toxin injec- candidates that permanent spasticity reduction by SDR tions were part of standard care, and with no or very can be obtained without increased occurrence of scoli- low economic costs for the patients. osis or spinal pain, at least until and including early Almost all children with CP spastic diplegia in the area adulthood. Still, spinal problems are common in cerebral were included. Ten children enrolled in CPUP after SDR; palsy and should be early identified and treated in order their preoperative GMFCS level and muscle tone was to minimize future discomfort and pain. assessed and recorded in the medical records by the spasticity-team physiotherapist. All other assessments were performed and recorded in CPUP by the person’s Population, registry and standard of care issues local (re) habilitation personnel, which made it possible to The CPUP registry data provided information from stan- study effects of SDR in this population, without any selec- dardized and regular assessments performed and tion bias or bias regarding expectations on SDR-results. Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 9 of 13 Fig. 3 a. Kaplan-Meier curve illustrating age when scoliosis according to the study definition was first reported in GMFCS level I-II, p = 0.567. b. Kaplan-Meier curve illustrating age when scoliosis according to the study definition was first reported in GMFCS level III, p = 0.778. c. Kaplan-Meier curve illustrating age when scoliosis according to the study definition was first reported in GMFCS level IV-V, p = 0.026 Natural history non-SDR group the aims were to follow the natural history and relation When SDR was introduced in Lund 1993, three North to long-term results of treatments [20]. The program American randomized controlled trials (RCTs) were un- was started in Skåne and Blekinge 1994 and included derway and preliminary results were forthcoming [35]. persons with CP born in 1990 and later, followed regu- At the time, an RCT in the Lund university hospital up- larly since that time. take region was considered both unethical and non- The CPUP registry data indicated that only few of the feasible due to the small population eligible. Even if the children who could have benefited from an SDR were available RCTs showed promising short-term results, referred to the spasticity clinic during early childhood, monitoring of long-term effects of SDR was needed. In especially after treatment with botulinum toxin was in- addition to practice-based follow up [36, 37], the CPUP troduced in 1998. It is thus likely that more children program/registry was planned at SDR-start, and among might have been recommended SDR if they had been re- ferred to the tertiary spasticity clinic where selection for SDR was performed. For this study, we could create a Table 2 Variables influencing development of scoliosis or not at group for comparison with clinical background and 20 years of age in univariable and multivariable analyses (n = 82) physical expression to match the selection criteria for Variables Univariable Multivariable SDR [38]. Some may have had features not visible in the OR 95% CI p OR 95% CI p registry data that differed from those who actually SDR 0.65 0.21–2.04 0.460 0.37 0.093–1.50 0.164 underwent SDR, such as dependence on spasticity for GMFCS at 4 yrs 7.85 2.08–29.6 0.0023 8.54 2.01–36.4 0.004 walking and standing, or other barriers to reach the de- Spasticity at 4 yrs 1.94 0.70–5.36 0.204 1.27 0.33–4.89 0.729 sired functional goals with the intervention. There were also some children included in the non-SDR group who Sex 1.17 0.41–3.36 0.766 –– – were recommended SDR by the spasticity team, but their Legend: Selective dorsal rhizotomy (SDR), Gross Motor Function Classification System (GMFCS), Odds ratio (OR), Confidence interval (CI) parents did not choose the intervention. Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 10 of 13 Table 3 Reported spinal pain at different ages in GMFCS levels II-IV, SDR and non-SDR groups Groups 10 years 15 years 20 years 25 years Pain No pain Pain No pain Pain No pain Pain No pain SDR 1 14 5 26 6 22 4 4 Non-SDR 1 39 6 42 3 20 1 6 p- value p = 0.475 p = 0.7436 p = 0.488 p = 0.282 Legend: GMFCS Gross Motor Function Classification System, SDR Selective Dorsal Rhizotomy The pediatric spasticity team members at Skåne Uni- GMFCS versity Hospital have had the same selection criteria and The GMFCS levels were classified after and as close to follow-up procedures since the start in 1993 [23]. Con- the fourth birthday as possible, and they were used to traindications to SDR were exclusion criteria in the stratify the study population at baseline. At 4 years of present study, such as mild spasticity, malformation syn- age, the GMFCS level, CP diagnosis, and CP subtype can dromes, postneonatally acquired CP, CP due to pre- be decided with high or acceptable accuracy [25, 40]. natal/congenital infections, severe birth asphyxia, and Retrospective, although not psychometrically tested, dyskinetic, ataxic, unilateral spastic, or mixed CP classification of GMFCS levels based on clinical descrip- subtypes. tions in medical records was used in the 2002 metanaly- Periventricular leukomalacia or hemorrhages, often in sis of the three North American SDR RCTs [35]. In the combination with premature birth, are associated with the present study, structured data from the CPUP registry CP subtype spastic diplegia, often suited for the SDR- on functional performance and capability was available intervention [1]. Such white matter brain lesions were for retrospective classification of GMFCS levels at base- present in the majority of both the SDR group (17/20, line date before the GMFCS was introduced. The kappa 85%) and the control group (74/87, 85%) who had had analysis of this classification showed good agreement brain imaging (Table 1). Less CNS-imaging in the SDR (κ = 0.732, p < 0.001), as described in Additional file 1, group than among controls was due to the higher propor- and the oldest birth year cohorts could be included in tion SDR-surgery in the oldest age cohorts, before brain the study. imaging was recommended in CP diagnostic work-up. To be able to use the GMFCS level in the logistic re- gression, the levels were dichotomized into levels I-II and III-V. According to Hägglund et al. [17], scoliosis Spasticity mainly appear in GMFCS III-V, and very seldom in Even if the MAS have shown weak psychometrical prop- GMFCS I-II and thus the subgroups I-II vs III-V make erties [39] it has been used by physiotherapists for asses- clinical sense. sing muscle tone in the CPUP follow-up since the start in 1994. To create study groups at baseline that corres- pond to the selection criteria for SDR, an estimated Scoliosis spasticity level classification was performed as described. The multilevel laminoplasty technique used to access the The MAS is an ordinal scale and does not methodo- rootlets for the SDR procedureinthe presentstudy in- logically allow such calculations, however it estimates a cluded reinstatement of laminae and did not increase the clinically significant entity used for classification and not occurrence of scoliosis after SDR. For the SDR GMFCS IV- for evaluation of interventions. It makes clinical sense group, scoliosis occurred even to a lesser extent and with that a child with a high degree of muscle tone in all later onset than for GMFCS IV-control group (Fig. 3c). De- muscle groups will get a high summation score in con- velopment of contractures and asymmetries, especially trast to a child with less tone, who may show an increase commoninhigherGMFCS-levels[17, 41, 42], maybeless in just distal muscle groups. In our study, we added clin- severe after SDR combined with physiotherapy, as use of ical signs of spasticity to the MAS summation score orthoses, sitting and supported standing positions with quartiles, such as leg scissoring at rest and activity, to more symmetric spine may be more easy to obtain after classify muscle tone increase into mild, moderate and se- tonus reduction. vere estimated spasticity levels. We found clear cut-offs In the logistic regression analysis of variables to ex- between the mild, moderate and severe spasticity level plain scoliosis or not in the whole group at 20 years of groups using the described classification, and they were age, the variable GMFCS contributed significantly. The retrospectively found to fit the overall clinical picture; other variables; SDR surgery, spasticity level at base-line, none of the children in the SDR group ended up in the and sex did not contribute to explain scoliosis at 20 mild spasticity level group at baseline. years of age. Several studies have previously shown that Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 11 of 13 girls are more affected by scoliosis than boys [16, 17]. differences were not statistically significant. Although However, in the present study children with contraindi- possible reduction of pain in adults with CP after early cations to SDR, such as ataxic or dyskinetic traits were SDR is reported [44], the authors are anxious to find out excluded, obstructing comparisons. whether SDR at a young age is causing more spinal pain In SDR, other forms of spinal misalignments, especially than expected from natural history. Information of pain spondylolisthesis have been reported more frequent than intensity, duration, effect on daily living or quality of life in the general population [6, 7, 9, 11, 12], even if scoliosis was available only in the adult age CPUP forms. was reported to be the most common deformity following Spinal pain several years after surgical correction of SDR [4]. Studies reporting spinal deformities after SDR scoliosis, as described in the present study, was found are not population based and with no or small comparison also in a population based study with high number of groups [4]. To further explore spinal misalignments after participants [16]. Increased awareness among health SDR in the present population, results regarding imaging professionals of the importance of pain assessments in of the spine beyond scoliosis and Cobb angles would be this population led to extended pain questions in the needed. Absence of spinal pain may, however, indicate ab- most recent version of the CPUP PT-form, so more and sence of significant spinal problems. higher quality data will be available in the future. Due to the relatively small numbers of individuals with Pain scoliosis and spinal pain, more simple statistical methods Pain in the CP population has previously not been prop- were used for the analyses, and the data allowed only few erly noticed [33], even if it is one of the most common variables to be included in the logistic regression models. co-morbidities [43]. Beside no increase in scoliosis devel- opment after SDR, the other main finding of the present Generalizability study was that the frequency of spinal pain did not differ This study represents the real-life situation in the ordinary between the SDR group and the control group at 10, 15, health care, in contrast to RCTs, or other experimental study 20 and 25 years of age (Table 3). designs, usually conducted at tertial health care level after rigorous selection of participants. The total population with Limitations CP in certain age cohorts were included in the present study, Only variables already included in the CPUP registry without selection bias. Results would be generalizable in pop- were available, which limits the research. However, a ulations where the socio-economic and health care standards major strength of the registry data available from a total are comparable to those in Sweden. Also, the surgery tech- Swedish population of individuals with CP continuously, nique, multi-level SDR without permanent removal of the collected during the last 25 years. spinal laminae/spinous processes, was used for all individuals The low proportion of individuals born 1990–1997, in the study, and is commonly used internationally. available to serve as natural history comparison group in adult age, is a limitation (Table 1). The control group Conclusion thus included a higher proportion of younger persons, This population based longitudinal matched outcome who probably received somewhat different care com- study, provides evidence against long-term complications pared to the older cohorts [19, 20]. In study participants from the spine caused by the SDR surgery. Individuals born 1994 and later, in contrast to those born 1990– undergoing SDR had similar development of scoliosis as 1993, some were treated with botulinum toxin with a comparable controls. In addition, individuals with most lowered muscle tone at the baseline assessment. functional limitations, GMFCS IV, who had SDR in young Assessments and registrations were performed regu- age had later onset and lower occurrence of scoliosis than larly using a standardized methodology by clinicians in their peers in the non-SDR group. GMFCS was the vari- their daily practice, and limited information was avail- able that best could explain scoliosis at 20 years of age; able, as only the most important items can be included SDR surgery, sex or base-line spasticity level did not. to keep a register acceptably time-consuming. The spinal Spinal pain was reported at similar levels for SDR oper- screening lacked information on other misalignments ated and controls up to the age of 25 years. than scoliosis. Cobb angles were inconsistently registered at the time data was extracted from the register, but Supplementary Information have been completed later, available for future studies. The online version contains supplementary material available at https://doi. The late introduction of pain screening in the registry org/10.1186/s12891-020-03782-5. resulted in low numbers of recorded answers about spinal pain at different ages, which is another limitation. Additional file 1: Retrospectively performed Gross Motor Function Classification System (GMFCS)-assessments using other Cerebral Palsy There were slightly more frequent recordings of spinal follow-UP registry (CPUP) data of gross motor function. Table Appendix. pain in the SDR than in the control group, although the Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 12 of 13 scoliosis in ambulatory children with cerebral palsy. Childs Nerv Syst. 2016; Retrospectively assessed GMFCS levels by researcher using CPUP data, 32(5):819–25. compared to assessment by local physiotherapis. 6. Johnson MB, Goldstein L, Thomas SS, Piatt J, Aiona M, Sussman M. Spinal deformity after selective dorsal rhizotomy in ambulatory patients with Abbreviations cerebral palsy. J Pediatr Orthop. 2004;24(5):529–36. CP: Cerebral palsy; BSCP: Bilateral spastic CP; SDR: Selective Dorsal Rhizotomy; 7. van Schie PE, Schothorst M, Dallmeijer AJ, Vermeulen RJ, van Ouwerkerk WJ, GMFCS: Gross Motor Functions Classification System; ITB: Intrathecal Baclofen; Strijers RL, et al. Short- and long-term effects of selective dorsal rhizotomy CPUP: The Swedish national secondary prevention follow-up program in on gross motor function in ambulatory children with spastic diplegia. J cerebral palsy; PT: Physiotherapy; MAS: Modified Ashworth Scale; Neurosurg Pediatr. 2011;7(5):557–62. SCPE: Surveillance of Cerebral Palsy in Europe 8. Steinbok P, Hicdonmez T, Sawatzky B, Beauchamp R, Wickenheiser D. Spinal deformities after selective dorsal rhizotomy for spastic cerebral palsy. J Acknowledgements Neurosurg. 2005;102(4 Suppl):363–73. We thank the children and families for participating in the CPUP, the 9. Langerak NG, Vaughan CL, Hoffman EB, Figaji AA, Fieggen AG, Peter JC. professionals working with the registry as well as Elisabeth O’Regan for Incidence of spinal abnormalities in patients with spastic diplegia 17 to 26 language revision and Heléne Jacobsson for statistical consultation. years after selective dorsal rhizotomy. Childs Nerv Syst. 2009;25(12):1593–603. 10. Peter JC, Hoffman EB, Arens LJ, Peacock WJ. Incidence of spinal deformity in children after multiple level laminectomy for selective posterior rhizotomy. Authors’ contributions Childs Nerv Syst. 1990;6(1):30–2. ALJ and LW designed the study, wrote and finalized the paper. The author(s) 11. Golan JD, Hall JA, O'Gorman G, Poulin C, Benaroch TE, Cantin MA, et al. read and approved the final manuscript. Spinal deformities following selective dorsal rhizotomy. J Neurosurg. 2007; 106(6 Suppl):441–9. Funding 12. Li Z, Zhu J, Liu X. Deformity of lumbar spine after selective dorsal rhizotomy Linnéa and Josef Carlssons Foundation supported the study for salary to the for spastic cerebral palsy. Microsurgery. 2008;28(1):10–2. first author and for consultation of a statistician. Open Access funding 13. Spiegel DA, Loder RT, Alley KA, Rowley S, Gutknecht S, Smith-Wright DL, provided by Lund University. et al. Spinal deformity following selective dorsal rhizotomy. J Pediatr Orthop. 2004;24(1):30–6. Availability of data and materials 14. Park TS, Liu JL, Edwards C, Walter DM, Dobbs MB. Functional outcomes of Data used in this study are stored at the National Quality Registry CPUP childhood selective dorsal Rhizotomy 20 to 28 years later. Cureus. 2017;9(5):e1256. (http://rcsyd.se/anslutna-register/cpup). Data are not publicly available and 15. Koop SE. Scoliosis in cerebral palsy. Dev Med Child Neurol. 2009;51(Suppl 4):92–8. permission to extract data can be obtained from the registry holder on reasonable request. Information on variables used for the present study is 16. Hagglund G, Czuba T, Alriksson-Schmidt AI. Back pain is more frequent in available from the authors. girls and in children with scoliosis in the context of cerebral palsy. Acta Paediatr. 2019;108(12):2229–34. 17. Hagglund G, Pettersson K, Czuba T, Persson-Bunke M, Rodby-Bousquet E. Ethics approval and consent to participate Incidence of scoliosis in cerebral palsy. Acta Orthop. 2018;89(4):443–7. The Regional Ethical Review Board at Lund University, Sweden (443–99, 18. Kotwicki T, Jozwiak M. Conservative management of neuromuscular revised 2009) approved the study. Permission to extract data from the CPUP scoliosis: personal experience and review of literature. Disabil Rehabil. 2008; registry was obtained by the registry holder and the personal data 30(10):792–8. responsible authority (Region Skåne). 19. Alriksson-Schmidt AI, Arner M, Westbom L, Krumlinde-Sundholm L, The parent or the legal guardian provided oral consent prior to participation Nordmark E, Rodby-Bousquet E, et al. A combined surveillance program and in CPUP, and the children provided verbal assent, as applicable. Verbal quality register improves management of childhood disability. Disabil consent is sufficient for participating in the Swedish national quality Rehabil. 2017;39(8):830–6. registries. Participation can be discontinued at any time, and the decision to withdraw will not affect the healthcare received. 20. Hagglund G, Alriksson-Schmidt A, Lauge-Pedersen H, Rodby-Bousquet E, Wagner P, Westbom L. Prevention of dislocation of the hip in children with cerebral palsy: 20-year results of a population-based prevention programme. Consent for publication Bone Joint J. 2014;96-B(11):1546–52. Not applicable. 21. Westbom L, Hagglund G, Nordmark E. Cerebral palsy in a total population of 4-11 year olds in southern Sweden. Prevalence and distribution Competing interests according to different CP classification systems. BMC Pediatr. 2007;7:41. The authors declare that they have no competing interests. 22. Alriksson-Schmidt A, Hagglund G. Pain in children and adolescents with cerebral palsy: a population-based registry study. Acta Paediatr. 2016;105(6):665–70. Author details 1 2 23. Nordmark E, Josenby AL, Lagergren J, Andersson G, Stromblad LG, Children’s Hospital, Skåne University Hospital, Lund, Sweden. Faculty of Westbom L. Long-term outcomes five years after selective dorsal rhizotomy. Medicine, Department of Health Sciences, Lund University, Lund, Sweden. BMC Pediatr. 2008;8:54. Faculty of Medicine, Department of Clinical Sciences Lund, Paediatrics, Lund University, Lund, Sweden. 24. Mutch L, Alberman E, Hagberg B, Kodama K, Perat MV. Cerebral palsy epidemiology: where are we now and where are we going? Dev Med Child Received: 4 June 2020 Accepted: 9 November 2020 Neurol. 1992;34(6):547–51. 25. 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Dev Med Child comparison of outcomes after single-level versus multi-level laminectomy Neurol. 2017;59(1):57–64. technique. Can J Neurosci Nurs. 2010;32(3):17–24. 4. Wheelwright M, Selvey PJ, Steinbok P, Singhal A, Ibrahim G, Fallah A, et al. 28. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Systematic review of spinal deformities following multi-level selective dorsal Development and reliability of a system to classify gross motor function in rhizotomy. Child's Nerv Syst. 2020;36:1025–35. children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214–23. 5. Funk JF, Haberl H. Monosegmental laminoplasty for selective dorsal 29. Alriksson-Schmidt A, Nordmark E, Czuba T, Westbom L. Stability of the gross rhizotomy--operative technique and influence on the development of motor function classification system in children and adolescents with Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 13 of 13 cerebral palsy: a retrospective cohort registry study. Dev Med Child Neurol. 2017;59(6):641–6. 30. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67(2):206–7. 31. Himmelmann K, Beckung E, Hagberg G, Uvebrant P. Bilateral spastic cerebral palsy--prevalence through four decades, motor function and growth. Eur J Paediatr Neurol. 2007;11(4):215–22. 32. Persson-Bunke M, Czuba T, Hagglund G, Rodby-Bousquet E. Psychometric evaluation of spinal assessment methods to screen for scoliosis in children and adolescents with cerebral palsy. BMC Musculoskelet Disord. 2015;16:351. 33. Westbom L, Rimstedt A, Nordmark E. 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Spine (Phila Pa 1976). 2012;37(12):E708–13. 43. Novak I. Evidence-based diagnosis, health care, and rehabilitation for children with cerebral palsy. J Child Neurol. 2014;29(8):1141–56. 44. Tedroff K, Lowing K, Astrom E. A prospective cohort study investigating gross motor function, pain, and health-related quality of life 17 years after selective dorsal rhizotomy in cerebral palsy. Dev Med Child Neurol. 2015; 57(5):484–90. Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Musculoskeletal Disorders Springer Journals

No support that early selective dorsal rhizotomy increase frequency of scoliosis and spinal pain – a longitudinal population-based register study from four to 25 years of age

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Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 https://doi.org/10.1186/s12891-020-03782-5 RESEARCH ARTICLE Open Access No support that early selective dorsal rhizotomy increase frequency of scoliosis and spinal pain – a longitudinal population-based register study from four to 25 years of age 1,2* 1,3 Annika Lundkvist Josenby and Lena Westbom Abstract: Spasticity interfering with gross motor development in cerebral palsy (CP) can be reduced with selective dorsal rhizotomy (SDR). Although reported, it is unknown if SDR surgery causes later spine problems. Using CP-registry data from a geographically defined population, the objectives were to compare frequency and time to scoliosis, and spinal pain up to adult age after SDR-surgery or not in all with same medical history, functional abilities, CP-subtype and level of spasticity at 4 years of age. Variables associated with scoliosis at 20 years of age were explored. Method: In the total population with CP spastic diplegia in Skåne and Blekinge, born 1990–2006, 149 individuals had moderate to severe spasticity and no medical contraindications against SDR at 4 years of age and were included; 36 had undergone SDR at a median age of 4.0 years (range 2.5–6.6 years), and 113 had not. Frequency of scoliosis and age when scoliosis was identified, and frequency of spinal pain at 10, 15, 20 and 25 years of age were analysed using Kaplan-Meier survival curves and Fisher’s exact test. Multivariable logistic regression was performed to identify variables to explain scoliosis at 20 yearsofage. Gross MotorFunctionClassification System (GMFCS) levels at 4 years of age were used for stratification. Result: Frequency of scoliosis did not significantly differ between groups having had early SDR surgery or not. In GMFCS IV, the SDR group had later onset and lower occurrence of scoliosis (p = 0.004). Frequency of spinal pain did not differ between the groups (p- levels > 0.28). GMFCS level was the background variable that in the logistic regression explained scoliosis at 20 years of age. Conclusion: Frequency of back pain and scoliosis in adulthood after early SDR are mainly part of the natural development with age, and not a surgery complication. Keywords: Cerebral palsy, Selective dorsal rhizotomy, Complications, Scoliosis, Spinal pain, Population-based, Controlled registry study * Correspondence: annika.lundkvist@med.lu.se Children’s Hospital, Skåne University Hospital, Lund, Sweden Faculty of Medicine, Department of Health Sciences, Lund University, Lund, Sweden Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long 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 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 article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 2 of 13 Introduction that scoliosis was seen in younger ages in children with Selective dorsal rhizotomy (SDR) is a neurosurgical pro- higher GMFCS levels meaning more severe functional cedure for children with spastic diplegic cerebral palsy limitations. The incidence of scoliosis increased with age (CP) that permanently reduces spasticity in the lower and GMFCS level. The incidence of spinal pain in CP limbs by cutting parts of lumbosacral rootlets at spinal was shown to increase with increasing scoliosis severity, levels L2-S2. SDR is always combined with physical ther- and scoliosis incidence increased with severity of gross apy, and it is mainly used in young children to improve fu- motor dysfunction [16, 17]. ture functional skills [1]. Neurosurgeons use either Today it is unknown whether the above figures regard- multilevel or single level laminotomy surgery to access the ing spine problems after SDR actually differ from the situ- rootlets. As the intervention includes surgery to the spine ation in persons with the corresponding type and severity and spinal nerve roots, there is a hypothetical risk that of CP who are not treated with SDR. In a recently pub- SDR will cause spinal deformities and pain may develop. lished review of spinal deformities after SDR, the authors The single level laminotomy technique was developed for suggested that the occurrence of spinal deformities were the advantages of decreased time for surgery, postopera- most likely not different, or only minimally higher after tive pain and to minimize the risk of progressive lumbar SDR, than in the natural history of CP, girls were more instability [2]. In a short-term follow-up, no significant dif- likely to develop scoliosis, and that the deformity develops ferences between the two techniques has been found [3]. over a long time, but the evidence base was weak [4]. After SDR, scoliosis was reported to be the most com- Incidence of spinal deformity and pain after SDR is an mon spinal deformity occurring at a weighted mean inci- important complication to consider, when deciding dence of 31.6% [4], and Cobb angles ≥20° have been whether to proceed with the procedure or not, as spinal reported at 3–9% 2.8–11.6 years after SDR [5–7]. In an- deformity can have a major impact on quality of life other study of children with pre-existing scoliosis prior [18]. There is a need for longitudinal follow-up studies to SDR, 5% improved Cobb angle, 70% were unchanged, of spinal pain and deformities in individuals undergoing and 25% had worsened at a mean follow-up time of 4.3 SDR, taking the natural development in cerebral palsy years [8]. Peter et al. and Langerak et al. followed the into account. same ambulatory cohort over time, and at the five-year The objectives of the present study were to compare follow-up after SDR, scoliosis of ≥10° was found in 16% frequency and age when scoliosis was diagnosed, and at 4.5 years and 57% at 21 years follow-up, of which 7% frequency of spinal pain in individuals who had under- had Cobb angles of ≥30°. None of the participants had gone SDR, and in a control group with same CP-type, scoliosis prior to SDR [9, 10]. medical history, body structure and functions at 4 years In follow-up studies from 3.6 to 21.4 years after SDR, of age, living in the same geographically defined total hyperlordosis was found to increase compared to base- population, followed from birth to adult age in the same line in 10–50%, and a hyperkyphosis was reported in 1– structured program and registry. Another objective was 9%. Individuals who were walking with and without to explore if any of the variables SDR surgery, sex, spas- walking aids generally had, postoperatively, larger lum- ticity and GMFCS level at 4 years of age, was associated bar lordosis [6, 8, 9, 11–13]. with the presence of scoliosis at 20 years of age in this Spondylolisthesis was uncommon preoperatively and population. postoperative prevalence ranged from 2 to 27%, mainly minor to grade 1 slippage [6, 7, 9, 11–13]. In a 20–28- Methods year follow-up after SDR, Park et al. found 31% with A retrospective population based controlled long-term scoliosis and other spinal problems [14]. outcome study using data from the Swedish cerebral On the other hand, persons with CP are generally palsy follow-up program (CPUP) including prospectively more frequently affected by spinal abnormalities, par- registered results from repeated, most often yearly, clin- ticularly scoliosis, than the general population [15]. ical assessments in children, adolescents and adults with Follow-up studies of adult individuals walking with or CP, living in a defined geographical area in southern without devices, who had undergone SDR during the Sweden [19]. preschool years to early school age, show occurrence of spinal pain in 17–23% [9] and pain in spine and lower Setting limbs in 28% [14]. In a follow-up with shorter time CPUP frame, spinal pain was reported at a lower level, 5% in The secondary prevention follow-up program in cerebral an self- ambulant cohort 5.8 years post SDR [13]. palsy (CPUP) was started in the regions of Skåne and In previous population based studies, excluding per- Blekinge in 1994, as a cooperation project between the sons treated with SDR, Kaplan–Meier survival estimates child orthopaedic and paediatric neurology departments based on the results of the clinical examination showed in tertiary care level, and the local child (re) habilitation Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 3 of 13 services and orthopaedic units in the area. The aims were during the years 1994–2015; there were 267 persons par- to prevent hip dislocations and severe contractures, in- ticipating in the CPUP-program and seven (2.5%) who crease cooperation, and generate more knowledge about did not. Demographic, medical and functional character- CP, especially the natural history and long-term results of istics of the population with CP spastic diplegia in the different treatments. New treatment modalities at the time study area, and the distribution of these characteristics were intrathecal baclofen (ITB) and SDR [20]. in the study groups are presented in Table 1. The original program was based on structured follow- up and evaluation of hip radiographs and repeated, SDR group structured, often annual physiotherapy (PT) assessments Of the 267 CPUP participants with spastic diplegia, there [19]. To identify all children with CP in the population, were 36 persons who had undergone SDR surgery at a regularly repeated inventories were performed in Skåne median age of 4.0 years (range 2.5–6.6 years). They were and Blekinge to find the youngest children, not yet in- followed to a median age of 22.3 years (range 11.3–27.2); vited to the program, and later on, after 4 years of age to 30 of the 36 SDR-operated persons had CPUP assess- decide on CP diagnosis and subtype for children in the ments at 20 years of age; eight had reached and been program [21, 22]. assessed at 25 years of age at the end of the study, Janu- Data for this study was retrieved from the CPUP ary 1st, 2018 (Table 1) (Fig. 1). demographic patient forms, neuropediatric, PT assess- ments, and operations forms from 1994 to 2018, vali- Excluded dated and completed by scrutinizing medical records Of the remaining 231 persons with CP spastic diplegia covering most of the health care systems in the two re- in the study population, there were 55 persons with gions during the study period. Demographic data was medical contraindications to SDR; congenital malforma- checked against the Swedish population registry every tions or syndromes in 25 persons, severe perinatal as- year, including dates for births, deaths, moving in and phyxia in 17, post-neonatal brain injuries in eight, and out of the area. five persons had other severe somatic disorders. Classification of spasticity level at 4 years of age, as de- SDR scribed below, was mild in 63 persons, without any indi- Some of the children with BSCP and moderate to severe cation for SDR, and they were therefore excluded from spasticity, were referred from their local (re-)habilitation the comparison (Table 1) (Fig. 1). units in the Skåne-Blekinge area for evaluation regarding spasticity management, and if selected for SDR, the surgi- Control group cal intervention and the immediate postoperative rehabili- The remaining 113 persons with CP spastic diplegia, tation took place at the Skåne University Hospital in moderate-severe spasticity level and no medical contra- Lund. Indications for SDR were spastic cerebral palsy with indications against SDR constituted the control group more involvement in the legs than the arms, pure spasti- (Table 1) (Fig. 1). As of January 1, 2018, this natural his- city without dystonia and ataxia, spasticity interfering with tory control group was followed to a median of 19.6 functional development, enough muscular control and years of age (range 8.9–27.3 years). strength to reach the individual functional goals, and ac- Six children treated with ITB were excluded from the cess to regular postoperative physical therapy and orthotic control group after the ITB-operation at 5, 6, 11, 14, 16 and services. Individual goals were set together with family, 18 years of age respectively. In addition, two persons in the local (re) habilitation unit and the spasticity team [23]. control group showed to be too young (< 8 years of age) at During the last two decades Magnetic Resonance Imaging the latest assessment and were not included in the com- (MRI) of the brain has been recommended at about 18– parison. In the control group, 54/113 had reached and had 24 months of age in children with CP, which, although assessments at 20 years of age, and 16/113 at 25 years. mostly seen clinically as dyskinesia or ataxia, has added in- volvement of thalamus/basal ganglia or cerebellum to the Definitions and classifications contraindications for SDR. Cerebral palsy (CP) was defined according to Much et al. 1992 [24] and the Surveillance of Cerebral Palsy in Participants Europe (SCPE) [25]. Population The prevalence of CP in the study area was 2.7/1000 CP subtype children 4–11 years of age as of Jan 1st, 2002, of which Subtypes were defined by the dominating neurological 38% was spastic diplegia [21]. The present study was symptom between four and 7 years of age. All patients based on all persons born 1990–2006, with CP spastic in this study had Bilateral Spastic CP (BSCP) as defined diplegia, who lived in Skåne-Blekinge for at least 2 years by the SCPE, and all also fulfilled the definition of the Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 4 of 13 Table 1 Characteristic of all participants in CPUP with CP spastic diplegia, N = 267 SDR No contraindication - no SDR Excluded with group contraindication Non-SDR group Excluded mild spasticity n = for SDR n = 113 (%) n = 63 (%) 36(%) n = 55 (%) Year of birth* 1990–1993 13 (36) 31 (27) 12 (19) 13 (23,5) 1994–1997 14 (39) 27 (24) 22 (35) 9 (16.5) 1998–2001 7 (19.5) 27 (24) 13 (21) 14 (25.5) 2002–2006 2 (5.5) 28 (25) 16 (25) 19 (34.5) Birth country other than Sweden 6 (17) 12 (11) 11 (16) 6 (11) Sex Male 25 (69) 60 (53) 37 (60) 41 (74.5) Female 11 (31) 53 (47) 26 (40) 14 (25.5) Gestational Age (GA) GA < 26 weeks 2 (6) 7 (6) 8 (12.5) 1 (2) GA 26–27 weeks 3 (8) 17 (15) 5 (8) 1 (2) GA 28–31 weeks 16 (44.5) 31 (27.5) 13 (21) 2 (3,5) GA 32–36 weeks 8 (22) 24 (21) 19 (30.5) 13 (23.5) GA > 36 weeks 7 (19.5) 29 (25.5) 12 (19) 35 (63.5) Unknown 0 5 (4) 6 (9.5) 3 (5.5) Birth weight < 1000 g 3 (8) 23 (20) 11 (17.5) 2 (4) 1000–1499 g 8 (22) 21 (19) 11 (17.5) 1 (2) 1500–2499 g 15 (42) 23 (20) 14 (22) 7 (12.5) 2500–4999 g 9 (25) 26 (23) 14 (22) 27 (49) Unknown 1 (3) 20 (18) 13 (21) 18 (32.5) Multiple pregnancy 5 (14) 25 (22) 6 (10) 2 (4) Severe asphyxia > GA 34 weeks 1 (3) 0 0 15 (27) Post-neonatal CP 0 0 0 7 (13) CNS imaging (dominating pattern) Maldevelopments 0 0 8 (13) 26 (47.5) Predominant white matter injury (periventricular) 17 (47) 74 (65.5) 33 (52) 16 (29) Basal ganglia/thalamus lesions 0 0 0 0 Cortical/subcortical grey matter lesions 1 (3) 4 (3.5) 2 (3) 5 (9) Normal 2 (6) 9 (8) 4 (6) 5 (9) No CNS imaging 16 (44) 26 (23) 16 (26) 3 (5.5) Shunted hydrocephalus 4 (11) 15 (13) 13 (21) 20 (36) Epilepsy 6 (17) 27 (24) 12 (19) 23 (42) Intellectual disability None or mild (IQ > 50) 34 (94) 93 (82) 57 (90) 36 (65) Moderate or severe (IQ < 50) 2 (6) 20 (18) 6 (10) 18 (33) Missing info 0 0 0 1 (2) Severe visual disability/blindness 4 (11) 20 (18) 7 (11) 10 (18) GMFCS levels at 4 years I 2 (5.5) 43 (38) 44 (70) 16 (30) II 11 (30.5) 18 (16) 6 (10) 12 (22) Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 5 of 13 Table 1 Characteristic of all participants in CPUP with CP spastic diplegia, N = 267 (Continued) SDR No contraindication - no SDR Excluded with group contraindication Non-SDR group Excluded mild spasticity n = for SDR n = 113 (%) n = 63 (%) 36(%) n = 55 (%) III 11 (30.5) 20 (18) 8 (12) 15 (28) IV 12 (33.5) 23 (20) 5 (8) 4 (7) V 0 9 (8) 0 7 (13) Missing info 0 0 0 1 Spasticity level at 4 years*** Mild 0 0 50 (79) 13 (24) Moderate 12 (33) 83 (73) 0 29 (53) Severe 24 (67) 30 (27) 0 10 (18) Missing info 0 0 13 (21) 3 (5) Legend: CPUP The Swedish national secondary prevention follow-up program in cerebral palsy, SDR Selective Dorsal Rhizotomy, CP Cerebral Palsy, GA Gestational Age, ITB Intrathecal Baclofen, GMFCS Gross Motor Function Classification System, CNS Central Nervous System, IQ Tested or estimated cognitive level. Differences between the SDR group and the control group n.s., except regarding birth year cohorts* (p < 0.05) and spasticity levels*** (p < 0.001) Fig. 1 Flow chart illustrating inclusion and exclusion of individuals in SDR group and control group Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 6 of 13 subtype spastic diplegia in the Hagberg classification [21, Estimated spasticity level at 4 years of age was classi- 25]. CP spastic diplegia includes all five GMFCS-levels, fied based on muscle tone (MAS summation score) and as long as there is greater involvement of the legs than clinical signs, such as degree of leg scissoring (none, of the arms, and can be asymmetrical, with more in- mild, severe) in rest and in activity, and foot clonus (yes/ volvement of either left or right side of the body [26]. no), as assessed by each child’s local PT according to the Brain morphology was classified based on the dominat- structured follow-up form in CPUP (http://cpup.se/in- ing pattern on brain imaging according to the SCPE [27]. english/manuals-and-evaluation-forms). Severe asphyxia was classified based on low Apgar Spasticity level was defined as mild if the MAS sum- scores (< 4 at 5 min), clinical and EEG-verified seizure mation score was within the first quartile 0–3, moderate activities within the first 72 h after birth. if in the second quartile 4–6, and severe if summation Epilepsy was defined as having had at least two unpro- score was 13 or higher. In the third quartile, MAS sum- voked seizures after the neonatal period. mation scores 7–12 the spasticity level was defined as se- Intellectual disability was assessed at about 4 years of vere if combined with severe scissoring in activity, and if age. Only parts of the cohort were formally IQ-tested at not, it was classified as a moderate spasticity level. that age, and only moderate to severe intellectual disabil- Scoliosis was assessed by inspection by the physiother- ity was defined as intellectual disability in this paper. For apist and registered to be either present or not. If the majority of the children, this is a clinical estimation present, mild: scoliosis visible only when leaning forward with inherent uncertainty. with aligned pelvis, moderate: scoliosis visible both in The Gross Motor Function Classification System (GMFC leaning forward in sitting and when sitting straight, and S) [28] was used to classify gross motor function at each severe: scoliosis, not correctable, with need of support in PT assessment in CPUP. The GMFCS level classified at sitting or standing. The CPUP PT assessment of the the first assessment after the child’s fourth birthday, or spine has shown to have high inter-rater reliability and pre-operatively if earlier SDR surgery, was used. The specificity in screening for moderate to severe scoliosis GMFCS was used for classification of gross motor func- in this population [32]. tion in the CPUP from the year 1995 by some physiother- In the present study, scoliosis status was dichotomized: apists as part of the development/testing of the no scoliosis if there was no scoliosis at examination or classification, and from 1998, the classification was intro- when a scoliosis was assessed as being correctable, and duced for all PT assessments in CPUP and have shown existing scoliosis if scoliosis was assessed by the PT as good stability in previous studies in this population [29]. being severe or moderate and not correctable, or if the The GMFCS-level was classified by the child’sphysio- individual had been undergoing scoliosis surgery. Dates/ therapist in 239 of all 267 persons with BSCP. In the old- age at first PT assessment with existing scoliosis and at est cohort, the GMFCS level was classified using other scoliosis surgery were noted. entered CPUP-data; the reliability of such a retrospective Questions about experienced pain and localization of classification was first confirmed, see Additional file 1. pain were introduced in the PT assessments from Janu- The classification was performed on de-identified data ary 2007 [33]. Presence of pain was assessed by either with no information available regarding if the child the person him/herself or by proxy. For children (< 18 belonged to the control or the SDR group. years) pain in the spine was reported by answering yes/ Muscle tone was assessed according to the Bohannon no and for adults (> 18 years) recalling the last 4 weeks Modified Ashworth Scale (MAS) [30]. MAS-scores for for spinal pain that was classified as being moderate or five muscle groups (hip-flexors, hip-adductors, knee- severe. After 2016, children were also asked to recall extensors, knee-flexors, and plantar-flexors) in both legs presence of pain during the last 4 weeks. were summed up for each CPUP participant with BSCP, who had complete recordings from all included muscle Statistics groups at 4 years of age. The MAS scores 1 and 1+ were Kaplan-Meier survival analyses were performed to both counted as 1. Median MAS summation score was 7 analyze time to scoliosis in relation to the following di- (range 0–32, inter- quartile range 4–12). chotomous variables; SDR surgery (yes vs no), GMFCS Muscle tone assessed with MAS is closely related to level (I-II vs III-V), level of base-line spasticity (moderate GMFCS level [31]. When occasional single MAS-scores vs severe) and sex (male vs female). were missing in the study groups, imputation was there- Kaplan Meier survival analysis was further used to fore performed by using the median score for the miss- compare time to scoliosis, stratifying for SDR, and sever- ing specific muscle group(s) of all with completely ity of gross motor function limitation, defined as GMFC recorded MAS scores and the same GMFCS level. Six S level at 4 years of age. Sub-groups were created ac- children in the SDR group and 12 in the control group cording to GMFCS levels; I-II (n = 74), III (n = 31) and had imputed single MAS scores. IV-V (n = 44). Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 7 of 13 Two-sided Pearson’s Chi-Square and Fisher’s exact tests All 12 in the SDR group GMFCS IV were followed to were used for comparisons between the SDR and the non- age 15 years, and 11 were followed to age 20 years; one SDR group background factors (Table 1) and pain at dif- SDR group participant GMFCS IV had scoliosis at age ferent age, and Kappa agreement test to check validity of 14 years, and one at age 23 years. Eight of the 23 control retrospective GMFCS-classifications (Additional file 1). group participants GMFCS IV developed a scoliosis at To explore which variables that influenced the devel- 12, 12, 12, 13, 16, 18, 18, and 19 years of age respectively. opment of scoliosis at 20 years of age, the first step was Six of the 14 in the control group followed to at least 15 to perform univariable logistic regression analyses of di- years of age had scoliosis before end of study, and all five chotomous variables in those who had reached this age followed to at least their 20th birthday had scoliosis be- (n = 82). Following variables were analyzed; SDR (yes/ fore that age (Fig. 3c). no), GMFCS at 4 years of age (I-II vs III-V), spasticity at In the univariable analysis, GMFCS level was the vari- 4 years of age (moderate/severe) and sex (male/female). able that significantly explained the presence of moder- All the before mentioned variables, except sex, were ate- severe scoliosis at 20 years of age. In the included in the model when we, as the second step, per- multivariable analysis, the result was maintained formed the multivariable logistic regression analysis. (Table 2). Neither the variables SDR surgery nor base- Due to the small number of participants with scoliosis in line spasticity level made statistically significant contri- both the SDR and non-SDR group, only a small number bution in explaining scoliosis at 20 years of age in the re- of variables could be included in the model. gression model (Table 1). Statistical significance was set at p < 0.05; n.s. denotes no statistically significant difference. Spinal pain IBM SPSS statistics, version 25 was used for analyses [34]. Patient’s reports of spinal pain at 10, 15, 20 and 25 years of age are presented in Table 3. No statistically signifi- cant difference was observed between the SDR and the Results control group (Table 3). Questions regarding pain were The background factors were similar in the SDR group introduced in CPUP in January 2007, and therefore pain and control group (Table 1). A higher proportion were assessments at 10 and 15 years of age were missing for SDR-operated in the first two birth cohorts than in the the oldest cohorts. Younger cohorts had not yet reached younger cohorts born from 1998 (p = 0.043). Another dif- the oldest ages at data extraction. ference was a lower proportion of severe spasticity in the Of all those in GMFCS IV who were followed to the 20 control group than in the SDR group (p =0) (Table 1). years assessment, one of 12 in the SDR and one of seven in the non-SDR group reported spinal pain; both had had Scoliosis scoliosis surgery more than 4 years earlier, and both had Only two of the SDR-operated children were in GMFCS severe spinal pain, interfering with daily activities. level I, and neither had scoliosis at the end of the study. Two of the 43 in the control group GMFCS level I had Discussion scoliosis at the end of the study (n.s.). No child in This is the first population based controlled SDR long- GMFCS V had had SDR-surgery. Two of the seven indi- term outcome study. All individuals in the geographically viduals in the non-SDR group GMFCS V assessed at 20 defined population (98% participating in the CPUP regis- years of age had scoliosis. try) with a medical background and clinical expression In GMFCS levels II-IV no child in either group, had that matched the selection criteria for SDR at baseline scoliosis before 10 years of age. Scoliosis was less fre- were included in the study [1]. Among these all having quent and developed later in GMFCS II-III with higher had SDR-surgery were compared to all who had not. . level of motor function, than in GMFCS IV. Prospectively collected longitudinal follow-up data are In the Kaplan-Meier analyses, the variables GMFCS presented for scoliosis and spinal pain from the popula- (p < 0.001), and base-line spasticity level showed signifi- tion of children with spastic diplegic CP, where a group cant differences between the two groups (p = 0.045) in of individuals had undergone SDR at a young age. Nei- development of scoliosis, however SDR surgery (p = ther scoliosis nor spinal pain was more prevalent during 0.822) and sex (p = 0.387) did not. (Fig. 2a-d). 20 years of follow-up in the SDR group, after the cauda Individuals in GMFCS levels IV-V undergoing SDR equina multilevel surgery, compared to the control had less scoliosis and a later onset of scoliosis compared group representing the natural history in children with to the non- SDR group (p = 0.026) using the Kaplan- about the same base-line prerequisites, and with same Meier analysis. In GMFCS subgroups I-II and III, the standard of care before and during follow up. In children differences were not statistically significant (p = 0.567 at GMFCS-level IV at baseline, without functional walk- and p = 0.778 respectively) (Fig. 3a-c). ing ability, scoliosis developed later and less often in the Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 8 of 13 Fig. 2 a. Kaplan-Meier survival curves illustrating the influence of SDR surgery (SDR vs no SDR) in the development of scoliosis (n = 149) p = 0.822. b. Kaplan-Meier survival curves illustrating the influence of GMFCS level at the age of 4 years in the development of scoliosis (n = 149) p < 0.001. c. Kaplan-Meier survival curves illustrating the influence of spasticity at the age of 4 years (moderate vs severe) in the development of scoliosis (n = 149) p = 0.045. d. Kaplan-Meier survival curves illustrating the influence of sex (male vs female) in the development of scoliosis (n = 149) p = 0.387 SDR group during the following 20 years than in the recorded by the person’s own physiotherapist at certain control group (Fig. 3c). ages, same procedures for all individuals, regardless of As SDR has been a challenged treatment option, few whether they had undergone SDR surgery or not [19]. children have been referred for evaluation. This study in- All persons in the study were treated at the same pub- dicates that feared complications to early SDR, such as lic health care units; orthopedic and pediatric hospital increased frequency of back pain and scoliosis in adult- health care departments, and the habilitation services in hood, are mainly part of the natural development with cooperation. Physiotherapy, occupational therapy, social age, and not a surgery complication. We now can inform and psychological support, orthoses, braces, orthopedic rehabilitation professionals and parents of future SDR surgery, ITB, SDR and from 1998 botulinum toxin injec- candidates that permanent spasticity reduction by SDR tions were part of standard care, and with no or very can be obtained without increased occurrence of scoli- low economic costs for the patients. osis or spinal pain, at least until and including early Almost all children with CP spastic diplegia in the area adulthood. Still, spinal problems are common in cerebral were included. Ten children enrolled in CPUP after SDR; palsy and should be early identified and treated in order their preoperative GMFCS level and muscle tone was to minimize future discomfort and pain. assessed and recorded in the medical records by the spasticity-team physiotherapist. All other assessments were performed and recorded in CPUP by the person’s Population, registry and standard of care issues local (re) habilitation personnel, which made it possible to The CPUP registry data provided information from stan- study effects of SDR in this population, without any selec- dardized and regular assessments performed and tion bias or bias regarding expectations on SDR-results. Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 9 of 13 Fig. 3 a. Kaplan-Meier curve illustrating age when scoliosis according to the study definition was first reported in GMFCS level I-II, p = 0.567. b. Kaplan-Meier curve illustrating age when scoliosis according to the study definition was first reported in GMFCS level III, p = 0.778. c. Kaplan-Meier curve illustrating age when scoliosis according to the study definition was first reported in GMFCS level IV-V, p = 0.026 Natural history non-SDR group the aims were to follow the natural history and relation When SDR was introduced in Lund 1993, three North to long-term results of treatments [20]. The program American randomized controlled trials (RCTs) were un- was started in Skåne and Blekinge 1994 and included derway and preliminary results were forthcoming [35]. persons with CP born in 1990 and later, followed regu- At the time, an RCT in the Lund university hospital up- larly since that time. take region was considered both unethical and non- The CPUP registry data indicated that only few of the feasible due to the small population eligible. Even if the children who could have benefited from an SDR were available RCTs showed promising short-term results, referred to the spasticity clinic during early childhood, monitoring of long-term effects of SDR was needed. In especially after treatment with botulinum toxin was in- addition to practice-based follow up [36, 37], the CPUP troduced in 1998. It is thus likely that more children program/registry was planned at SDR-start, and among might have been recommended SDR if they had been re- ferred to the tertiary spasticity clinic where selection for SDR was performed. For this study, we could create a Table 2 Variables influencing development of scoliosis or not at group for comparison with clinical background and 20 years of age in univariable and multivariable analyses (n = 82) physical expression to match the selection criteria for Variables Univariable Multivariable SDR [38]. Some may have had features not visible in the OR 95% CI p OR 95% CI p registry data that differed from those who actually SDR 0.65 0.21–2.04 0.460 0.37 0.093–1.50 0.164 underwent SDR, such as dependence on spasticity for GMFCS at 4 yrs 7.85 2.08–29.6 0.0023 8.54 2.01–36.4 0.004 walking and standing, or other barriers to reach the de- Spasticity at 4 yrs 1.94 0.70–5.36 0.204 1.27 0.33–4.89 0.729 sired functional goals with the intervention. There were also some children included in the non-SDR group who Sex 1.17 0.41–3.36 0.766 –– – were recommended SDR by the spasticity team, but their Legend: Selective dorsal rhizotomy (SDR), Gross Motor Function Classification System (GMFCS), Odds ratio (OR), Confidence interval (CI) parents did not choose the intervention. Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 10 of 13 Table 3 Reported spinal pain at different ages in GMFCS levels II-IV, SDR and non-SDR groups Groups 10 years 15 years 20 years 25 years Pain No pain Pain No pain Pain No pain Pain No pain SDR 1 14 5 26 6 22 4 4 Non-SDR 1 39 6 42 3 20 1 6 p- value p = 0.475 p = 0.7436 p = 0.488 p = 0.282 Legend: GMFCS Gross Motor Function Classification System, SDR Selective Dorsal Rhizotomy The pediatric spasticity team members at Skåne Uni- GMFCS versity Hospital have had the same selection criteria and The GMFCS levels were classified after and as close to follow-up procedures since the start in 1993 [23]. Con- the fourth birthday as possible, and they were used to traindications to SDR were exclusion criteria in the stratify the study population at baseline. At 4 years of present study, such as mild spasticity, malformation syn- age, the GMFCS level, CP diagnosis, and CP subtype can dromes, postneonatally acquired CP, CP due to pre- be decided with high or acceptable accuracy [25, 40]. natal/congenital infections, severe birth asphyxia, and Retrospective, although not psychometrically tested, dyskinetic, ataxic, unilateral spastic, or mixed CP classification of GMFCS levels based on clinical descrip- subtypes. tions in medical records was used in the 2002 metanaly- Periventricular leukomalacia or hemorrhages, often in sis of the three North American SDR RCTs [35]. In the combination with premature birth, are associated with the present study, structured data from the CPUP registry CP subtype spastic diplegia, often suited for the SDR- on functional performance and capability was available intervention [1]. Such white matter brain lesions were for retrospective classification of GMFCS levels at base- present in the majority of both the SDR group (17/20, line date before the GMFCS was introduced. The kappa 85%) and the control group (74/87, 85%) who had had analysis of this classification showed good agreement brain imaging (Table 1). Less CNS-imaging in the SDR (κ = 0.732, p < 0.001), as described in Additional file 1, group than among controls was due to the higher propor- and the oldest birth year cohorts could be included in tion SDR-surgery in the oldest age cohorts, before brain the study. imaging was recommended in CP diagnostic work-up. To be able to use the GMFCS level in the logistic re- gression, the levels were dichotomized into levels I-II and III-V. According to Hägglund et al. [17], scoliosis Spasticity mainly appear in GMFCS III-V, and very seldom in Even if the MAS have shown weak psychometrical prop- GMFCS I-II and thus the subgroups I-II vs III-V make erties [39] it has been used by physiotherapists for asses- clinical sense. sing muscle tone in the CPUP follow-up since the start in 1994. To create study groups at baseline that corres- pond to the selection criteria for SDR, an estimated Scoliosis spasticity level classification was performed as described. The multilevel laminoplasty technique used to access the The MAS is an ordinal scale and does not methodo- rootlets for the SDR procedureinthe presentstudy in- logically allow such calculations, however it estimates a cluded reinstatement of laminae and did not increase the clinically significant entity used for classification and not occurrence of scoliosis after SDR. For the SDR GMFCS IV- for evaluation of interventions. It makes clinical sense group, scoliosis occurred even to a lesser extent and with that a child with a high degree of muscle tone in all later onset than for GMFCS IV-control group (Fig. 3c). De- muscle groups will get a high summation score in con- velopment of contractures and asymmetries, especially trast to a child with less tone, who may show an increase commoninhigherGMFCS-levels[17, 41, 42], maybeless in just distal muscle groups. In our study, we added clin- severe after SDR combined with physiotherapy, as use of ical signs of spasticity to the MAS summation score orthoses, sitting and supported standing positions with quartiles, such as leg scissoring at rest and activity, to more symmetric spine may be more easy to obtain after classify muscle tone increase into mild, moderate and se- tonus reduction. vere estimated spasticity levels. We found clear cut-offs In the logistic regression analysis of variables to ex- between the mild, moderate and severe spasticity level plain scoliosis or not in the whole group at 20 years of groups using the described classification, and they were age, the variable GMFCS contributed significantly. The retrospectively found to fit the overall clinical picture; other variables; SDR surgery, spasticity level at base-line, none of the children in the SDR group ended up in the and sex did not contribute to explain scoliosis at 20 mild spasticity level group at baseline. years of age. Several studies have previously shown that Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 11 of 13 girls are more affected by scoliosis than boys [16, 17]. differences were not statistically significant. Although However, in the present study children with contraindi- possible reduction of pain in adults with CP after early cations to SDR, such as ataxic or dyskinetic traits were SDR is reported [44], the authors are anxious to find out excluded, obstructing comparisons. whether SDR at a young age is causing more spinal pain In SDR, other forms of spinal misalignments, especially than expected from natural history. Information of pain spondylolisthesis have been reported more frequent than intensity, duration, effect on daily living or quality of life in the general population [6, 7, 9, 11, 12], even if scoliosis was available only in the adult age CPUP forms. was reported to be the most common deformity following Spinal pain several years after surgical correction of SDR [4]. Studies reporting spinal deformities after SDR scoliosis, as described in the present study, was found are not population based and with no or small comparison also in a population based study with high number of groups [4]. To further explore spinal misalignments after participants [16]. Increased awareness among health SDR in the present population, results regarding imaging professionals of the importance of pain assessments in of the spine beyond scoliosis and Cobb angles would be this population led to extended pain questions in the needed. Absence of spinal pain may, however, indicate ab- most recent version of the CPUP PT-form, so more and sence of significant spinal problems. higher quality data will be available in the future. Due to the relatively small numbers of individuals with Pain scoliosis and spinal pain, more simple statistical methods Pain in the CP population has previously not been prop- were used for the analyses, and the data allowed only few erly noticed [33], even if it is one of the most common variables to be included in the logistic regression models. co-morbidities [43]. Beside no increase in scoliosis devel- opment after SDR, the other main finding of the present Generalizability study was that the frequency of spinal pain did not differ This study represents the real-life situation in the ordinary between the SDR group and the control group at 10, 15, health care, in contrast to RCTs, or other experimental study 20 and 25 years of age (Table 3). designs, usually conducted at tertial health care level after rigorous selection of participants. The total population with Limitations CP in certain age cohorts were included in the present study, Only variables already included in the CPUP registry without selection bias. Results would be generalizable in pop- were available, which limits the research. However, a ulations where the socio-economic and health care standards major strength of the registry data available from a total are comparable to those in Sweden. Also, the surgery tech- Swedish population of individuals with CP continuously, nique, multi-level SDR without permanent removal of the collected during the last 25 years. spinal laminae/spinous processes, was used for all individuals The low proportion of individuals born 1990–1997, in the study, and is commonly used internationally. available to serve as natural history comparison group in adult age, is a limitation (Table 1). The control group Conclusion thus included a higher proportion of younger persons, This population based longitudinal matched outcome who probably received somewhat different care com- study, provides evidence against long-term complications pared to the older cohorts [19, 20]. In study participants from the spine caused by the SDR surgery. Individuals born 1994 and later, in contrast to those born 1990– undergoing SDR had similar development of scoliosis as 1993, some were treated with botulinum toxin with a comparable controls. In addition, individuals with most lowered muscle tone at the baseline assessment. functional limitations, GMFCS IV, who had SDR in young Assessments and registrations were performed regu- age had later onset and lower occurrence of scoliosis than larly using a standardized methodology by clinicians in their peers in the non-SDR group. GMFCS was the vari- their daily practice, and limited information was avail- able that best could explain scoliosis at 20 years of age; able, as only the most important items can be included SDR surgery, sex or base-line spasticity level did not. to keep a register acceptably time-consuming. The spinal Spinal pain was reported at similar levels for SDR oper- screening lacked information on other misalignments ated and controls up to the age of 25 years. than scoliosis. Cobb angles were inconsistently registered at the time data was extracted from the register, but Supplementary Information have been completed later, available for future studies. The online version contains supplementary material available at https://doi. The late introduction of pain screening in the registry org/10.1186/s12891-020-03782-5. resulted in low numbers of recorded answers about spinal pain at different ages, which is another limitation. Additional file 1: Retrospectively performed Gross Motor Function Classification System (GMFCS)-assessments using other Cerebral Palsy There were slightly more frequent recordings of spinal follow-UP registry (CPUP) data of gross motor function. Table Appendix. pain in the SDR than in the control group, although the Lundkvist Josenby and Westbom BMC Musculoskeletal Disorders (2020) 21:782 Page 12 of 13 scoliosis in ambulatory children with cerebral palsy. Childs Nerv Syst. 2016; Retrospectively assessed GMFCS levels by researcher using CPUP data, 32(5):819–25. compared to assessment by local physiotherapis. 6. Johnson MB, Goldstein L, Thomas SS, Piatt J, Aiona M, Sussman M. Spinal deformity after selective dorsal rhizotomy in ambulatory patients with Abbreviations cerebral palsy. J Pediatr Orthop. 2004;24(5):529–36. CP: Cerebral palsy; BSCP: Bilateral spastic CP; SDR: Selective Dorsal Rhizotomy; 7. van Schie PE, Schothorst M, Dallmeijer AJ, Vermeulen RJ, van Ouwerkerk WJ, GMFCS: Gross Motor Functions Classification System; ITB: Intrathecal Baclofen; Strijers RL, et al. Short- and long-term effects of selective dorsal rhizotomy CPUP: The Swedish national secondary prevention follow-up program in on gross motor function in ambulatory children with spastic diplegia. J cerebral palsy; PT: Physiotherapy; MAS: Modified Ashworth Scale; Neurosurg Pediatr. 2011;7(5):557–62. SCPE: Surveillance of Cerebral Palsy in Europe 8. Steinbok P, Hicdonmez T, Sawatzky B, Beauchamp R, Wickenheiser D. Spinal deformities after selective dorsal rhizotomy for spastic cerebral palsy. J Acknowledgements Neurosurg. 2005;102(4 Suppl):363–73. We thank the children and families for participating in the CPUP, the 9. Langerak NG, Vaughan CL, Hoffman EB, Figaji AA, Fieggen AG, Peter JC. professionals working with the registry as well as Elisabeth O’Regan for Incidence of spinal abnormalities in patients with spastic diplegia 17 to 26 language revision and Heléne Jacobsson for statistical consultation. years after selective dorsal rhizotomy. Childs Nerv Syst. 2009;25(12):1593–603. 10. Peter JC, Hoffman EB, Arens LJ, Peacock WJ. Incidence of spinal deformity in children after multiple level laminectomy for selective posterior rhizotomy. Authors’ contributions Childs Nerv Syst. 1990;6(1):30–2. ALJ and LW designed the study, wrote and finalized the paper. The author(s) 11. Golan JD, Hall JA, O'Gorman G, Poulin C, Benaroch TE, Cantin MA, et al. read and approved the final manuscript. Spinal deformities following selective dorsal rhizotomy. J Neurosurg. 2007; 106(6 Suppl):441–9. Funding 12. Li Z, Zhu J, Liu X. Deformity of lumbar spine after selective dorsal rhizotomy Linnéa and Josef Carlssons Foundation supported the study for salary to the for spastic cerebral palsy. Microsurgery. 2008;28(1):10–2. first author and for consultation of a statistician. Open Access funding 13. Spiegel DA, Loder RT, Alley KA, Rowley S, Gutknecht S, Smith-Wright DL, provided by Lund University. et al. Spinal deformity following selective dorsal rhizotomy. J Pediatr Orthop. 2004;24(1):30–6. Availability of data and materials 14. Park TS, Liu JL, Edwards C, Walter DM, Dobbs MB. Functional outcomes of Data used in this study are stored at the National Quality Registry CPUP childhood selective dorsal Rhizotomy 20 to 28 years later. Cureus. 2017;9(5):e1256. (http://rcsyd.se/anslutna-register/cpup). Data are not publicly available and 15. Koop SE. Scoliosis in cerebral palsy. Dev Med Child Neurol. 2009;51(Suppl 4):92–8. permission to extract data can be obtained from the registry holder on reasonable request. Information on variables used for the present study is 16. Hagglund G, Czuba T, Alriksson-Schmidt AI. Back pain is more frequent in available from the authors. girls and in children with scoliosis in the context of cerebral palsy. Acta Paediatr. 2019;108(12):2229–34. 17. Hagglund G, Pettersson K, Czuba T, Persson-Bunke M, Rodby-Bousquet E. Ethics approval and consent to participate Incidence of scoliosis in cerebral palsy. Acta Orthop. 2018;89(4):443–7. The Regional Ethical Review Board at Lund University, Sweden (443–99, 18. Kotwicki T, Jozwiak M. Conservative management of neuromuscular revised 2009) approved the study. Permission to extract data from the CPUP scoliosis: personal experience and review of literature. Disabil Rehabil. 2008; registry was obtained by the registry holder and the personal data 30(10):792–8. responsible authority (Region Skåne). 19. Alriksson-Schmidt AI, Arner M, Westbom L, Krumlinde-Sundholm L, The parent or the legal guardian provided oral consent prior to participation Nordmark E, Rodby-Bousquet E, et al. A combined surveillance program and in CPUP, and the children provided verbal assent, as applicable. Verbal quality register improves management of childhood disability. Disabil consent is sufficient for participating in the Swedish national quality Rehabil. 2017;39(8):830–6. registries. Participation can be discontinued at any time, and the decision to withdraw will not affect the healthcare received. 20. Hagglund G, Alriksson-Schmidt A, Lauge-Pedersen H, Rodby-Bousquet E, Wagner P, Westbom L. Prevention of dislocation of the hip in children with cerebral palsy: 20-year results of a population-based prevention programme. Consent for publication Bone Joint J. 2014;96-B(11):1546–52. Not applicable. 21. Westbom L, Hagglund G, Nordmark E. Cerebral palsy in a total population of 4-11 year olds in southern Sweden. 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