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Assessment of the levels of termination of the conus medullaris and thecal sac in the pediatric population

Assessment of the levels of termination of the conus medullaris and thecal sac in the pediatric... Purpose This study assessed the position of the termination of the conus medullaris (the point where the spinal cord tapers to an end) and thecal sac (the sheath of dura mater that surrounds the spinal cord and caudal nerve roots) in a large pediatric population, to characterise the nature of the pediatric Gaussian distribution and assess whether age affected the distribution. The study further aimed to assess the effect of gender on termination positions. Methods A total of 520 MRI spine studies of children aged between 1 month and 19 years old were collected from two pediatric tertiary referral centres in the UK and Italy. Studies with pathological findings were excluded, and normal scans were found using keyword search algorithms on a database of radiologists’ reports. The reported scans were individually assessed and reviewed by two experienced neuroradiologists. The termination points of the conus medullaris and thecal sac were determined for each study. Local IRB approvals were sought. Results The results showcased a Gaussian distribution in both conus medullaris (r=0.8997) and thecal sac termination levels (r=0.9639). No statistically significant results were noted with increasing age for the termination positions of the conus medullaris or thecal sac (p = 0.154, 0.063). No statistical significance was observed with gender variation with either anatomical landmark. A weak positive correlation was observed between the termination levels of the conus medullaris and the thecal sac (r=0.2567) Conclusion Termination levels across all pediatric age range followed a Gaussian distribution. Knowledge of normal ter- mination levels has relevant clinical implications, including the assessment of patients with suspected spinal dysraphism. Keywords Conus medullaris · Thecal sac · Conus termination · Pediatric spine Introduction Embryologically, the spinal cord forms mostly from the neural plate generated during primary neurulation, with only its caudal metameres (i.e., S3-S5 and coccygeal levels) and filum terminale deriving from the processes of junc- Kshitij Mankad and Andrea Rossi are joint senior authors. tional and secondary neurulation [1]. The conus medullaris * Kshitij Mankad (CM) is the point where the spinal cord tapers and comes kshitij.mankad@gosh.nhs.uk to an end. During fetal development, the CM progressively “ascends” along the vertebral column as a combined result University College London Medical School, London, UK of the phenomenon of retrogressive differentiation of the Neuroradiology Unit, Hospital Central do Funchal – secondary neural tube and the differential longitudinal SESARAM, Madeira, Portugal growth rates of the vertebral column and spinal cord. The Great Ormond Street Hospital Radiology, London, UK CM eventually occupies its final, “adult” position shortly Neuroradiology Unit, IRCCS Insituto Giannina Gaslini, after birth, but studies have differed on the precise time at Genoa, Italy which this is reached, i.e., whether the conus settles in its Department of Health Sciences (DISSAL), University final position at 2 months or at 5 months of age [2 ]. In fact, of Genoa, Genoa, Italy Vol.:(0123456789) 1 3 Neuroradiology some of the literature has suggested that no further ascent The patient databases were narrowed down using these occurs after birth and that the ascent entirely occurs within inclusion and exclusion criteria, and the relevant MRI gestation, especially between weeks 9 and 16 [3]. Thus, this studies were reviewed. Each data point was subsequently study sought to further clarify the matter and to provide sta- manually reported by two experienced neuroradiologists. tistically significant conclusions on the timeframe when the The sequences were acquired using 1.5T scanners as part final position is achieved. of routine clinical protocols which included T1, T2 axial, Although the variation of its position is found among and sagittal sequences and/or Short-TI Inversion Recovery individuals, its peak incidence in the adult population has (STIR). The images were taken in the supine position as per been reported at the level of the L1 vertebra [4], with a mean standard clinical practice. Termination level was selected variation ranging from the T12 to the upper L3 vertebrae. at the level where the tapering of the conus and thecal sac Similarly, slight variation is seen in the adult position of the could be seen most clearly, with all slices considered before thecal sac terminus (TS); however, TS is generally expected the optimal slice selection. to terminate at the level of the S2 vertebra, with mean vari- The selection process included reviewing patient data- ation ranging from the lower L5 to the lower S3 vertebrae bases on tens of thousands of imaging reports and restricting [4, 5]. our search to only those where an experienced neuroradiolo- Several studies have long established a Gaussian distri- gist had previously reported that the spine appeared nor- bution in the termination levels of the conus medullaris and mal, or similar words to that effect. This technique excluded the thecal sac in the adult population. However, there lies several thousand cases, with the remaining cases assessed existing variation in the literature as to what age the adult chronologically, until an adequate sample size was obtained. termination position is achieved. Thus, this study aimed to Studies with unclear quality were excluded, due to the pos- characterise the pediatric Gaussian distribution further and sibility of bias. assess whether any changes existed across the age range. There was no assessment for interrater agreement for the Few studies have been conducted solely in the pediatric measurements; however, in equivocal cases, a joint opinion age groups, and there is yet to be sufficient literature ascer - between two experienced neuroradiologists was agreed upon taining whether changes in the Gaussian distribution occur The images were analysed in the sagittal plane, and the across increasing pediatric age and gender. This study, with same technique was used to measure the level of both termi- its large sample size (n=520) aimed to reinforce this distri- nations of the CM and TS. Lines were drawn to triangulate bution amongst pediatric populations. the exact point at which each structure terminated so that Prior studies [6] have employed similar methodologies to the corresponding vertebral level could be ascertained by assess at which age in particular the adult termination level drawing a perpendicular line from the termination point. is attained. This study sought to further quantitatively out- The vertebral level was found by counting from top down- line the nature of the Gaussian distribution itself, and ascer- wards and upwards from the last lumbar vertebra, which was tain whether age or gender had an important role to play in identified as the last well-formed vertebral body above the this respect. Previous literature [7] has assessed the effect sacrum. Fig. 1 shows the approach to assessing the level of of gender of distribution, however, was limited by an upper termination. range of 6 months of age, as opposed to the entire pediatric In accordance with techniques adopted in similar previous age range. In addition, this study only considered ultrasound studies, the specific vertebra where the structures terminated as the imaging modality, which has its own limitations. was then divided into thirds (upper, middle, and lower) so that the level of termination could be ascribed to a more spe- cific part of the vertebra. In cases where they terminated at an intervertebral disc, they were labelled as being at the level Methods and materials of the appropriate disc. Finally, to conduct statistical analy- sis, each vertebral level was allocated a numerical value. For This study was a retrospective observational study conducted the termination of the conus medullaris, it ranged from 1 in two tertiary referral centres in the UK and Italy with local (lower third of T11) to 16 (middle third of L3), and for the- IRB approvals. The selected age range of subjects was 1 cal sac termination from 1 (L5-S1 disc) to 13 (S3-S4 disc). month to 19 years (mean age 7.78 years). The inclusion cri- teria included subjects with normal MRI whole spine. We Statistical analysis included patients with brain tumours and cranial trauma with normal spinal imaging. Patients with spinal dysraphism, ver- The Product Moment Correlation Coefficient was used to tebral segmentation anomalies, those with previous spinal describe the normality of the data, whereby our obtained cord disease or injury, or, those who had undergone previous dataset was contrasted to a perfectly generated counterpart spinal surgery for whatever reason were excluded. using its key parameters. This technique has been employed 1 3 Neuroradiology Age in months Frequency 0m 1 1m 6 2m 3 3m 7 4m 5 5m 12 6m 9 7m 4 8m 6 9m 3 10m 13 11m 2 12m 32 Age in years Frequency 2 28 3 41 4 30 5 22 6 21 7 26 8 22 9 33 10 37 Fig. 1 A showcase of how the level of termination of the thecal sac 11 30 and the conus medullaris were measured in steps 1–3 12 23 13 22 14 17 in previous studies. We further calculated kurtosis and skew- 15 29 ness values, to reinforce the Gaussian distribution. 16 15 The effect of gender on the level of termination was 17 15 assessed using the Wilcoxon signed rank test. The effect 18 6 of age on the termination levels was assessed using the Kruskal−Wallis ANOVA test. The Product Moment Cor- relation Coefficient was used to assess for any correlation between the termination levels of the conus medullaris and Results the thecal sac. The statistical analysis was conducted and cross-checked A total of 520 MRI studies were assessed from the two cen- internally, by researchers with backgrounds in statistics. tres (250 females and 270 males). Materials Level of termination of the conus medullaris This study comprised 520 children across two tertiary refer- A Gaussian distribution to the level of the conus termination ral centres, with an age breakdown denoted in the below was found, with the mean at the level of lower L1. When tables. The study aimed to assess a sufficient number of the data was contrasted to that of its perfectly normally dis- cases across each age group, with special emphasis on those tributed counterpart data, an extremely strong positive cor- in the first year of life, assessing 103 individuals. Relatively relation (r=0.8997) was produced (Fig. 2). The population few imaging studies were available in the first month of life mean was calculated to be 7.904 (95% CI 7.71 to 8.09). The across both centres. termination levels ranged from upper T12 to the L2/L3 disc. 1 3 Neuroradiology results, with a Gaussian distribution clearly visualised. The CONU S MEDULLARI S mean level of termination was 7.128 (95% CI (6.95, 7.31)), TERMINATIO N LEVEL corresponding to mid-S2. The data ranged from the L5-S1 120 disc to the S3-S4 disc. Eec ff t of gender on termination levels of conus medullaris and thecal sac The thecal sac data, classified by gender, also showcased a strong Gaussian distribution. The male data was shown to have a strong positive correlation (r= 0.9397). The mean level of termination of the thecal sac was 7.28 (95% CI 7.15, 7.43) in males and 6.94 (95% CI 6.78, 7.10) in females, both at the level of lower S2 (Figs. 4 and 5). The data ranged from Fig. 2 Graph showing the distribution of conus medullaris termina- the L5-S1 disc to the level of lower S3 in males, and the tion levels in the patient population. Termination position is shown L5-S1 disc to the S3-S4 disc in females. on the x-axis, and the number of studies terminating at each level is A 2-tailed Wilcoxon rank sum test was performed and did shown on the y-axis not allow rejection of the null hypothesis at the 5% signifi- cance level (p=0.9955). This showed no statistically signifi- Eec ff t of gender on termination level of conus cant difference between the distribution of termination posi- tions in the male and female populations. This strengthens medullaris the previously published view that gender has no noteworthy impact on the positions of termination. The study showed Gaussian distributions in both female and male subset populations. In males, the data for the conus Correlation between the position of conus medullaris showed a strong positive correlation against its normally distributed dataset (r= 0.9717). Within the female medullaris termination and thecal sac termination pediatric population, the data was also shown to be nor- mally distributed for the conus medullaris (r=0.8942). The A positive correlation (r=0.2567) was noted between the levels of termination of the conus medullaris and thecal sac mean level of termination of the conus medullaris was 7.88 in males (95% CI 7.74 to 8.04) and 7.93 (95% CI 7.78 to in each patient respectively (Fig. 6). This is in line with the published data in adults (5). 8.11) in females, both corresponding to the mid-L1 level. The termination level of the conus ranged from upper T12 Eec ff t of age on the levels of termination to the L2-L3 disc in males, whereas it ranged from upper T12 to the mid-L3 vertebrae in females. This is all strongly of the conus medullaris and the thecal sac in keeping with Gaussian distributions across both genders. A similar Gaussian distribution was noted for the level The data across pediatric age ranges was compared for any trends. Firstly, the subset of the first 6 months of life was of the tip of the thecal sac (r=0.9639). Fig. 3 showcases the Fig. 3 Graph showing the distribution of termination levels of the conus medullaris in male and female pediatric patients. Termination position is shown on the x-axis, and the number of studies terminating at each level is shown on the y-axis 1 3 Neuroradiology Fig. 4 Graph showing the distri- bution of thecal sac termination levels in the patient population. Termination position is shown on the x-axis, and the number of studies terminating at each level is shown on the y-axis Fig. 5 Graph showing the distribution of termination levels of the thecal sac in male and female pediatric patients. Termination position is shown on the x-axis, and the number of studies terminating at each level is shown on the y-axis considered in isolation to further elucidate whether a clear test was performed to assess whether age had a significant ascent was noted within this time frame (Fig. 7). The graph impact on the level of termination of the conus medullaris shows no noteworthy changes in termination level across in the age range of 0–19 years. A non-significant p value of age in the first year of life. A Kruskal-Wallis ANOVA test 0.1543 was obtained, suggesting that age has no significant was performed to assess whether age had a significant influence on the termination level of the conus medullaris. impact on the level of termination of the conus medullaris Similar methods were used to assess the termination in the first 6 months of life. A non-significant p value of positions of the thecal sac in the first year of life and 0.1218 was obtained, suggesting no ascent occurs in the across the pediatric age range respectively. The Kruskal- first 6 months. Wallis analysis obtained p values of 0.2859 and 0.063 The entire pediatric age range was subsequently consid- respectively, suggesting that age has no significant impact ered and is shown in supplementary figure 1. The graph on the termination level of the thecal sac. Fig. 8 shows the shows no noteworthy changes in termination levels across change in the termination positions of the thecal sac in the age in the pediatric population. A Kruskal-Wallis ANOVA first year of life. 1 3 Neuroradiology Fig. 6 Graph showing the cor- relation between the levels of termination of the conus medul- laris and thecal sac. Termina- tion levels of conus medullaris are shown on the x-axis and that of the thecal sac on the y-axis Fig. 7 Graph showing the effect of age on the distributions of Variation in termination level of the CM in the first year termination level of the conus of life medullaris in the first year of life. Age in months is shown on the x-axis, and the termination L3/L4 position is shown on the y-axis. Disc MidL3 L2/L3 Disc MidL2 L1/L2 Disc MidL1 T12/L1 Disc Mid T12 T11/T12 Disc Mid T11 02 4 681012 Age at MRI in months of the underlying tumour. Whilst contouring and placement Discussion are continually improving, significant variability is still being observed amongst high-volume practitioners [9]. The clinical This study has several important clinical implications. Irradia- risk of underestimating the contour may lead to greater rates of tion for spinal tumours is traditionally performed by placing central neuropathy [9]. This serves to denote the extreme clini- the caudal border of the spinal field at S2/S3 intervertebral cal importance of a correct understanding of the distribution space [8]. However, such a placement has been shown to miss of the thecal sac and likely termination position in children. 8.7% of thecal sacs [8], risking a failure of successful treatment 1 3 Levell of termination of CM Neuroradiology Fig. 8 Graph showing the effect of age on the distributions of VARIATION IN TERMINATION LEVEL OF THE TS termination level of the thecal IN THE FIRST YEAR OF LIFE sac in the first year of life. Age in months is shown on the x-axis, and termination position Lower S3 is shown on the y-axis Upper S3 Lower S2 Upper S2 Lower S1 Upper S1 Lower L5 24 68 10 12 AGE AT MRI IN MONTHS Accurate knowledge of the normal position of the conus procedures, as there is no increased risk of overestimating is imperative for a correct evaluation of patients suspected or underestimating contours. of harboiring a spinal dysraphism. In fact, low positioning of the conus is one of the features that neurosurgeons consider Correlation between the position of conus when selecting patients who are candidates for detethering medullaris termination and thecal sac termination surgery. The resultant correlation (r=0.2567) is in line with previous studies which have shown a correlation in adult populations to Level of termination of conus medullaris be r=0.309 and 0.32 respectively [4, 12]. This allows extrap- olation that a similar correlation exists and is maintained The mean level of termination of the conus in populations of throughout all ages. This correlation is unlikely to be due to adults was noted to be at upper L1 [4, 10]. This study found the result of error, due to both its replicability from previous a mean pediatric termination around mid-L1 level. This may studies [4] and the relatively large sample sizes in the studies. suggest the conus medullaris is more low-lying in pediatric Accurate knowledge of the relationship between the CM populations; however, no statistical significance was noted. and TS terminuses can be very important in the assess- This study has concluded that the absolute lower limit ment of patients with suspected cord tethering who have for a normal conus medullaris is at the level of the L2-L3 a conus in a normal position. That is, the overall position disc. This is in line with previous literature [4]. The current of the conus may still be “normal” in general terms (e.g., ISPN position is that any conus below mid-L2 should be L2), but the conus is actually tethered and stretched. In this considered tethered until proven otherwise [11]. This may case, there could be a loss of proportionality between the suggest a new definition of the absolute lower limit of the CM and TS. In the reverse cases, i.e. in patients with caudal CM is warranted regression syndrome type I, both the cord terminus and TS are typically higher than normal. Thus, this reinforces the Level of termination of the thecal sac need to assess for proportionality between the CM and TS positions, that is, assisting in the evaluation of the aforemen- Once again, these results support the previously published tioned subtle cases. literature on the level of termination of the tip of the thecal sac in adult populations [4]. Similar mean positions were Eec ff t of gender on position of conus medullaris termination and thecal sac termination noted, with the tip lying around the level of mid-S2. Previous literature in pediatric populations has concluded an average In both male and female children, the mean level of the conus position of upper S2 [8], although amongst a small sam- ple size (n=23). The results are clinically valuable as they medullaris and thecal sac terminations were equally mid- L1 and S2, respectively. This suggests gender has a limited may suggest no specific age adjustment needs to be made with respect to the positioning of spinal fields in irradiation effect on the positions of the conus medullaris and thecal 1 3 LEVEL OF TERMINATION OF TS Neuroradiology sac. However, the mean conus level across both genders was Confounding factors such as child height were difficult extremely similar, which disagrees with previous studies in to control, especially in tertiary referral centres catering to adults [4] which found that gender has a small but significant diverse communities where significant changes in pediatric impact on termination levels of the conus medullaris. How- height were observed. ever, studies amongst children [3] have equally demonstrated no significant difference across genders. This may suggest that gender may only become an influencing factor once adulthood Conclusion is reached. This notion is strengthened in a prior study where women, particularly elderly aged ones, had a lower lying conus This study reaffirmed the fact that a Gaussian distribution medullaris [13]. This may suggest that a more complex rela- exists with respect to the levels of termination of both the tionship between gender, age, and termination positions exists. CM and TS within the pediatric population. Gender was shown to have a limited effect, and there was no general relationship between increasing age and termination levels, Eec ff t of age on the levels of termination suggesting that the final level is obtained at birth. of the conus medullaris and the thecal sac Future work should be conducted to elucidate the rela- tionship between increasing age on termination positions. Prior studies in children aged 1–6 months have found a mean This study highlighted the critical importance of imaging termination position of upper L2 [3]. This study obtained a investigations in light of this Gaussian distribution and the mean position of lower L1 (8.56) for the termination level knock-on effects they play in patient care. of the CM in the first 6 months, suggesting variability exists. Furthermore, researchers have found that in 15–20-year- Supplementary Information The online version contains supplemen- olds, the mean termination level was the middle third of tary material available at https://doi. or g/10. 1007/ s00234- 022- 03111-8 . L1 [3]. These studies implied that the conus may have been Funding No funding was needed for this work. more low-lying in pediatric populations and may, in fact, ascend into adulthood, but that its termination position may Declarations gradually increase across increasing childhood age ranges and in fact further into adulthood. Conflicts of interest/Competing interests None of the authors have No statistically significant differences were observed any conflicts of interest to disclose. with increasing age on the final termination position of the Ethics approval The centres in Italy and UK had respective IRBs. For- conus medullaris within the first 6 months of life. This seems mal ethics was not needed as the analysis was done on a retrospective incongruent with the notion that the conus medullaris reaches case notes review basis. its final adult position at 2 or 5 months old. Non-significant Informed consent Not required for this study. results were additionally obtained for increased age on the termination level of the conus medullaris across the entire Open Access This article is licensed under a Creative Commons Attri- pediatric population. This supports the idea that no further bution 4.0 International License, which permits use, sharing, adapta- ascent occurs following childbirth and supports the notion tion, distribution and reproduction in any medium or format, as long that ascent is entirely in utero, between weeks 9 and 16 [14]. as you give appropriate credit to the original author(s) and the source, No statistically significant difference was noted amongst 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 age ranges and the termination level of the thecal sac. included in the article's Creative Commons licence, unless indicated These results are in agreement with the literature [4,15] that otherwise in a credit line to the material. If material is not included in increasing age has no impact on the thecal sac level and this the article's Creative Commons licence and your intended use is not suggests no ascent occurs following childbirth. 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://cr eativ ecommons. or g/licen ses/ b y/4.0/ . Limitations The relative paucity of studies amongst the age group of References 0-1 years of life is a limitation of this study. However, this is to be expected given routine spinal MRI in an otherwise 1. Nene Y, Jilani TN (2022) Neuroanatomy, Conus Medullaris. In: asymptomatic infant is uncommon. StatPearls. StatPearls Publishing, Treasure Island (FL) https:// www. ncbi. nlm. nih. gov/ books/ NBK54 5227 The assessment method employed in the study may have 2. Kesler H, Dias M, Kalapos P (2007) Termination of the normal introduced observer bias between neuroradiologists, and this conus medullaris in children: a whole-spine magnetic resonance was minimised by consensus reads in equivocal cases. 1 3 Neuroradiology imaging study. Neurosurgical Focus. 23(2):1–5. https:// doi. org/ recommendations for safe practice. International Journal of Radia- 10. 3171/ FOC- 07/ 08/ E7 tion Oncology*Biology*Physics. 112(1):114–120. https://doi. or g/ 3. Jung J, Kim E, Song I, Lee J, Kim H, Kim J (2016) The influence 10. 1016/j. ijrobp. 2021. 08. 023 of age on positions of the conus medullaris, Tuffier’s line, dural 10. Saifuddin A, Burnett S, White J (1998) The variation of posi- sac, and sacrococcygeal membrane in infants, children, adoles- tion of the conus medullaris in an adult population. Spine. cents, and young adults. 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Assessment of the levels of termination of the conus medullaris and thecal sac in the pediatric population

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Abstract

Purpose This study assessed the position of the termination of the conus medullaris (the point where the spinal cord tapers to an end) and thecal sac (the sheath of dura mater that surrounds the spinal cord and caudal nerve roots) in a large pediatric population, to characterise the nature of the pediatric Gaussian distribution and assess whether age affected the distribution. The study further aimed to assess the effect of gender on termination positions. Methods A total of 520 MRI spine studies of children aged between 1 month and 19 years old were collected from two pediatric tertiary referral centres in the UK and Italy. Studies with pathological findings were excluded, and normal scans were found using keyword search algorithms on a database of radiologists’ reports. The reported scans were individually assessed and reviewed by two experienced neuroradiologists. The termination points of the conus medullaris and thecal sac were determined for each study. Local IRB approvals were sought. Results The results showcased a Gaussian distribution in both conus medullaris (r=0.8997) and thecal sac termination levels (r=0.9639). No statistically significant results were noted with increasing age for the termination positions of the conus medullaris or thecal sac (p = 0.154, 0.063). No statistical significance was observed with gender variation with either anatomical landmark. A weak positive correlation was observed between the termination levels of the conus medullaris and the thecal sac (r=0.2567) Conclusion Termination levels across all pediatric age range followed a Gaussian distribution. Knowledge of normal ter- mination levels has relevant clinical implications, including the assessment of patients with suspected spinal dysraphism. Keywords Conus medullaris · Thecal sac · Conus termination · Pediatric spine Introduction Embryologically, the spinal cord forms mostly from the neural plate generated during primary neurulation, with only its caudal metameres (i.e., S3-S5 and coccygeal levels) and filum terminale deriving from the processes of junc- Kshitij Mankad and Andrea Rossi are joint senior authors. tional and secondary neurulation [1]. The conus medullaris * Kshitij Mankad (CM) is the point where the spinal cord tapers and comes kshitij.mankad@gosh.nhs.uk to an end. During fetal development, the CM progressively “ascends” along the vertebral column as a combined result University College London Medical School, London, UK of the phenomenon of retrogressive differentiation of the Neuroradiology Unit, Hospital Central do Funchal – secondary neural tube and the differential longitudinal SESARAM, Madeira, Portugal growth rates of the vertebral column and spinal cord. The Great Ormond Street Hospital Radiology, London, UK CM eventually occupies its final, “adult” position shortly Neuroradiology Unit, IRCCS Insituto Giannina Gaslini, after birth, but studies have differed on the precise time at Genoa, Italy which this is reached, i.e., whether the conus settles in its Department of Health Sciences (DISSAL), University final position at 2 months or at 5 months of age [2 ]. In fact, of Genoa, Genoa, Italy Vol.:(0123456789) 1 3 Neuroradiology some of the literature has suggested that no further ascent The patient databases were narrowed down using these occurs after birth and that the ascent entirely occurs within inclusion and exclusion criteria, and the relevant MRI gestation, especially between weeks 9 and 16 [3]. Thus, this studies were reviewed. Each data point was subsequently study sought to further clarify the matter and to provide sta- manually reported by two experienced neuroradiologists. tistically significant conclusions on the timeframe when the The sequences were acquired using 1.5T scanners as part final position is achieved. of routine clinical protocols which included T1, T2 axial, Although the variation of its position is found among and sagittal sequences and/or Short-TI Inversion Recovery individuals, its peak incidence in the adult population has (STIR). The images were taken in the supine position as per been reported at the level of the L1 vertebra [4], with a mean standard clinical practice. Termination level was selected variation ranging from the T12 to the upper L3 vertebrae. at the level where the tapering of the conus and thecal sac Similarly, slight variation is seen in the adult position of the could be seen most clearly, with all slices considered before thecal sac terminus (TS); however, TS is generally expected the optimal slice selection. to terminate at the level of the S2 vertebra, with mean vari- The selection process included reviewing patient data- ation ranging from the lower L5 to the lower S3 vertebrae bases on tens of thousands of imaging reports and restricting [4, 5]. our search to only those where an experienced neuroradiolo- Several studies have long established a Gaussian distri- gist had previously reported that the spine appeared nor- bution in the termination levels of the conus medullaris and mal, or similar words to that effect. This technique excluded the thecal sac in the adult population. However, there lies several thousand cases, with the remaining cases assessed existing variation in the literature as to what age the adult chronologically, until an adequate sample size was obtained. termination position is achieved. Thus, this study aimed to Studies with unclear quality were excluded, due to the pos- characterise the pediatric Gaussian distribution further and sibility of bias. assess whether any changes existed across the age range. There was no assessment for interrater agreement for the Few studies have been conducted solely in the pediatric measurements; however, in equivocal cases, a joint opinion age groups, and there is yet to be sufficient literature ascer - between two experienced neuroradiologists was agreed upon taining whether changes in the Gaussian distribution occur The images were analysed in the sagittal plane, and the across increasing pediatric age and gender. This study, with same technique was used to measure the level of both termi- its large sample size (n=520) aimed to reinforce this distri- nations of the CM and TS. Lines were drawn to triangulate bution amongst pediatric populations. the exact point at which each structure terminated so that Prior studies [6] have employed similar methodologies to the corresponding vertebral level could be ascertained by assess at which age in particular the adult termination level drawing a perpendicular line from the termination point. is attained. This study sought to further quantitatively out- The vertebral level was found by counting from top down- line the nature of the Gaussian distribution itself, and ascer- wards and upwards from the last lumbar vertebra, which was tain whether age or gender had an important role to play in identified as the last well-formed vertebral body above the this respect. Previous literature [7] has assessed the effect sacrum. Fig. 1 shows the approach to assessing the level of of gender of distribution, however, was limited by an upper termination. range of 6 months of age, as opposed to the entire pediatric In accordance with techniques adopted in similar previous age range. In addition, this study only considered ultrasound studies, the specific vertebra where the structures terminated as the imaging modality, which has its own limitations. was then divided into thirds (upper, middle, and lower) so that the level of termination could be ascribed to a more spe- cific part of the vertebra. In cases where they terminated at an intervertebral disc, they were labelled as being at the level Methods and materials of the appropriate disc. Finally, to conduct statistical analy- sis, each vertebral level was allocated a numerical value. For This study was a retrospective observational study conducted the termination of the conus medullaris, it ranged from 1 in two tertiary referral centres in the UK and Italy with local (lower third of T11) to 16 (middle third of L3), and for the- IRB approvals. The selected age range of subjects was 1 cal sac termination from 1 (L5-S1 disc) to 13 (S3-S4 disc). month to 19 years (mean age 7.78 years). The inclusion cri- teria included subjects with normal MRI whole spine. We Statistical analysis included patients with brain tumours and cranial trauma with normal spinal imaging. Patients with spinal dysraphism, ver- The Product Moment Correlation Coefficient was used to tebral segmentation anomalies, those with previous spinal describe the normality of the data, whereby our obtained cord disease or injury, or, those who had undergone previous dataset was contrasted to a perfectly generated counterpart spinal surgery for whatever reason were excluded. using its key parameters. This technique has been employed 1 3 Neuroradiology Age in months Frequency 0m 1 1m 6 2m 3 3m 7 4m 5 5m 12 6m 9 7m 4 8m 6 9m 3 10m 13 11m 2 12m 32 Age in years Frequency 2 28 3 41 4 30 5 22 6 21 7 26 8 22 9 33 10 37 Fig. 1 A showcase of how the level of termination of the thecal sac 11 30 and the conus medullaris were measured in steps 1–3 12 23 13 22 14 17 in previous studies. We further calculated kurtosis and skew- 15 29 ness values, to reinforce the Gaussian distribution. 16 15 The effect of gender on the level of termination was 17 15 assessed using the Wilcoxon signed rank test. The effect 18 6 of age on the termination levels was assessed using the Kruskal−Wallis ANOVA test. The Product Moment Cor- relation Coefficient was used to assess for any correlation between the termination levels of the conus medullaris and Results the thecal sac. The statistical analysis was conducted and cross-checked A total of 520 MRI studies were assessed from the two cen- internally, by researchers with backgrounds in statistics. tres (250 females and 270 males). Materials Level of termination of the conus medullaris This study comprised 520 children across two tertiary refer- A Gaussian distribution to the level of the conus termination ral centres, with an age breakdown denoted in the below was found, with the mean at the level of lower L1. When tables. The study aimed to assess a sufficient number of the data was contrasted to that of its perfectly normally dis- cases across each age group, with special emphasis on those tributed counterpart data, an extremely strong positive cor- in the first year of life, assessing 103 individuals. Relatively relation (r=0.8997) was produced (Fig. 2). The population few imaging studies were available in the first month of life mean was calculated to be 7.904 (95% CI 7.71 to 8.09). The across both centres. termination levels ranged from upper T12 to the L2/L3 disc. 1 3 Neuroradiology results, with a Gaussian distribution clearly visualised. The CONU S MEDULLARI S mean level of termination was 7.128 (95% CI (6.95, 7.31)), TERMINATIO N LEVEL corresponding to mid-S2. The data ranged from the L5-S1 120 disc to the S3-S4 disc. Eec ff t of gender on termination levels of conus medullaris and thecal sac The thecal sac data, classified by gender, also showcased a strong Gaussian distribution. The male data was shown to have a strong positive correlation (r= 0.9397). The mean level of termination of the thecal sac was 7.28 (95% CI 7.15, 7.43) in males and 6.94 (95% CI 6.78, 7.10) in females, both at the level of lower S2 (Figs. 4 and 5). The data ranged from Fig. 2 Graph showing the distribution of conus medullaris termina- the L5-S1 disc to the level of lower S3 in males, and the tion levels in the patient population. Termination position is shown L5-S1 disc to the S3-S4 disc in females. on the x-axis, and the number of studies terminating at each level is A 2-tailed Wilcoxon rank sum test was performed and did shown on the y-axis not allow rejection of the null hypothesis at the 5% signifi- cance level (p=0.9955). This showed no statistically signifi- Eec ff t of gender on termination level of conus cant difference between the distribution of termination posi- tions in the male and female populations. This strengthens medullaris the previously published view that gender has no noteworthy impact on the positions of termination. The study showed Gaussian distributions in both female and male subset populations. In males, the data for the conus Correlation between the position of conus medullaris showed a strong positive correlation against its normally distributed dataset (r= 0.9717). Within the female medullaris termination and thecal sac termination pediatric population, the data was also shown to be nor- mally distributed for the conus medullaris (r=0.8942). The A positive correlation (r=0.2567) was noted between the levels of termination of the conus medullaris and thecal sac mean level of termination of the conus medullaris was 7.88 in males (95% CI 7.74 to 8.04) and 7.93 (95% CI 7.78 to in each patient respectively (Fig. 6). This is in line with the published data in adults (5). 8.11) in females, both corresponding to the mid-L1 level. The termination level of the conus ranged from upper T12 Eec ff t of age on the levels of termination to the L2-L3 disc in males, whereas it ranged from upper T12 to the mid-L3 vertebrae in females. This is all strongly of the conus medullaris and the thecal sac in keeping with Gaussian distributions across both genders. A similar Gaussian distribution was noted for the level The data across pediatric age ranges was compared for any trends. Firstly, the subset of the first 6 months of life was of the tip of the thecal sac (r=0.9639). Fig. 3 showcases the Fig. 3 Graph showing the distribution of termination levels of the conus medullaris in male and female pediatric patients. Termination position is shown on the x-axis, and the number of studies terminating at each level is shown on the y-axis 1 3 Neuroradiology Fig. 4 Graph showing the distri- bution of thecal sac termination levels in the patient population. Termination position is shown on the x-axis, and the number of studies terminating at each level is shown on the y-axis Fig. 5 Graph showing the distribution of termination levels of the thecal sac in male and female pediatric patients. Termination position is shown on the x-axis, and the number of studies terminating at each level is shown on the y-axis considered in isolation to further elucidate whether a clear test was performed to assess whether age had a significant ascent was noted within this time frame (Fig. 7). The graph impact on the level of termination of the conus medullaris shows no noteworthy changes in termination level across in the age range of 0–19 years. A non-significant p value of age in the first year of life. A Kruskal-Wallis ANOVA test 0.1543 was obtained, suggesting that age has no significant was performed to assess whether age had a significant influence on the termination level of the conus medullaris. impact on the level of termination of the conus medullaris Similar methods were used to assess the termination in the first 6 months of life. A non-significant p value of positions of the thecal sac in the first year of life and 0.1218 was obtained, suggesting no ascent occurs in the across the pediatric age range respectively. The Kruskal- first 6 months. Wallis analysis obtained p values of 0.2859 and 0.063 The entire pediatric age range was subsequently consid- respectively, suggesting that age has no significant impact ered and is shown in supplementary figure 1. The graph on the termination level of the thecal sac. Fig. 8 shows the shows no noteworthy changes in termination levels across change in the termination positions of the thecal sac in the age in the pediatric population. A Kruskal-Wallis ANOVA first year of life. 1 3 Neuroradiology Fig. 6 Graph showing the cor- relation between the levels of termination of the conus medul- laris and thecal sac. Termina- tion levels of conus medullaris are shown on the x-axis and that of the thecal sac on the y-axis Fig. 7 Graph showing the effect of age on the distributions of Variation in termination level of the CM in the first year termination level of the conus of life medullaris in the first year of life. Age in months is shown on the x-axis, and the termination L3/L4 position is shown on the y-axis. Disc MidL3 L2/L3 Disc MidL2 L1/L2 Disc MidL1 T12/L1 Disc Mid T12 T11/T12 Disc Mid T11 02 4 681012 Age at MRI in months of the underlying tumour. Whilst contouring and placement Discussion are continually improving, significant variability is still being observed amongst high-volume practitioners [9]. The clinical This study has several important clinical implications. Irradia- risk of underestimating the contour may lead to greater rates of tion for spinal tumours is traditionally performed by placing central neuropathy [9]. This serves to denote the extreme clini- the caudal border of the spinal field at S2/S3 intervertebral cal importance of a correct understanding of the distribution space [8]. However, such a placement has been shown to miss of the thecal sac and likely termination position in children. 8.7% of thecal sacs [8], risking a failure of successful treatment 1 3 Levell of termination of CM Neuroradiology Fig. 8 Graph showing the effect of age on the distributions of VARIATION IN TERMINATION LEVEL OF THE TS termination level of the thecal IN THE FIRST YEAR OF LIFE sac in the first year of life. Age in months is shown on the x-axis, and termination position Lower S3 is shown on the y-axis Upper S3 Lower S2 Upper S2 Lower S1 Upper S1 Lower L5 24 68 10 12 AGE AT MRI IN MONTHS Accurate knowledge of the normal position of the conus procedures, as there is no increased risk of overestimating is imperative for a correct evaluation of patients suspected or underestimating contours. of harboiring a spinal dysraphism. In fact, low positioning of the conus is one of the features that neurosurgeons consider Correlation between the position of conus when selecting patients who are candidates for detethering medullaris termination and thecal sac termination surgery. The resultant correlation (r=0.2567) is in line with previous studies which have shown a correlation in adult populations to Level of termination of conus medullaris be r=0.309 and 0.32 respectively [4, 12]. This allows extrap- olation that a similar correlation exists and is maintained The mean level of termination of the conus in populations of throughout all ages. This correlation is unlikely to be due to adults was noted to be at upper L1 [4, 10]. This study found the result of error, due to both its replicability from previous a mean pediatric termination around mid-L1 level. This may studies [4] and the relatively large sample sizes in the studies. suggest the conus medullaris is more low-lying in pediatric Accurate knowledge of the relationship between the CM populations; however, no statistical significance was noted. and TS terminuses can be very important in the assess- This study has concluded that the absolute lower limit ment of patients with suspected cord tethering who have for a normal conus medullaris is at the level of the L2-L3 a conus in a normal position. That is, the overall position disc. This is in line with previous literature [4]. The current of the conus may still be “normal” in general terms (e.g., ISPN position is that any conus below mid-L2 should be L2), but the conus is actually tethered and stretched. In this considered tethered until proven otherwise [11]. This may case, there could be a loss of proportionality between the suggest a new definition of the absolute lower limit of the CM and TS. In the reverse cases, i.e. in patients with caudal CM is warranted regression syndrome type I, both the cord terminus and TS are typically higher than normal. Thus, this reinforces the Level of termination of the thecal sac need to assess for proportionality between the CM and TS positions, that is, assisting in the evaluation of the aforemen- Once again, these results support the previously published tioned subtle cases. literature on the level of termination of the tip of the thecal sac in adult populations [4]. Similar mean positions were Eec ff t of gender on position of conus medullaris termination and thecal sac termination noted, with the tip lying around the level of mid-S2. Previous literature in pediatric populations has concluded an average In both male and female children, the mean level of the conus position of upper S2 [8], although amongst a small sam- ple size (n=23). The results are clinically valuable as they medullaris and thecal sac terminations were equally mid- L1 and S2, respectively. This suggests gender has a limited may suggest no specific age adjustment needs to be made with respect to the positioning of spinal fields in irradiation effect on the positions of the conus medullaris and thecal 1 3 LEVEL OF TERMINATION OF TS Neuroradiology sac. However, the mean conus level across both genders was Confounding factors such as child height were difficult extremely similar, which disagrees with previous studies in to control, especially in tertiary referral centres catering to adults [4] which found that gender has a small but significant diverse communities where significant changes in pediatric impact on termination levels of the conus medullaris. How- height were observed. ever, studies amongst children [3] have equally demonstrated no significant difference across genders. This may suggest that gender may only become an influencing factor once adulthood Conclusion is reached. This notion is strengthened in a prior study where women, particularly elderly aged ones, had a lower lying conus This study reaffirmed the fact that a Gaussian distribution medullaris [13]. This may suggest that a more complex rela- exists with respect to the levels of termination of both the tionship between gender, age, and termination positions exists. CM and TS within the pediatric population. Gender was shown to have a limited effect, and there was no general relationship between increasing age and termination levels, Eec ff t of age on the levels of termination suggesting that the final level is obtained at birth. of the conus medullaris and the thecal sac Future work should be conducted to elucidate the rela- tionship between increasing age on termination positions. Prior studies in children aged 1–6 months have found a mean This study highlighted the critical importance of imaging termination position of upper L2 [3]. This study obtained a investigations in light of this Gaussian distribution and the mean position of lower L1 (8.56) for the termination level knock-on effects they play in patient care. of the CM in the first 6 months, suggesting variability exists. Furthermore, researchers have found that in 15–20-year- Supplementary Information The online version contains supplemen- olds, the mean termination level was the middle third of tary material available at https://doi. or g/10. 1007/ s00234- 022- 03111-8 . L1 [3]. These studies implied that the conus may have been Funding No funding was needed for this work. more low-lying in pediatric populations and may, in fact, ascend into adulthood, but that its termination position may Declarations gradually increase across increasing childhood age ranges and in fact further into adulthood. Conflicts of interest/Competing interests None of the authors have No statistically significant differences were observed any conflicts of interest to disclose. with increasing age on the final termination position of the Ethics approval The centres in Italy and UK had respective IRBs. For- conus medullaris within the first 6 months of life. This seems mal ethics was not needed as the analysis was done on a retrospective incongruent with the notion that the conus medullaris reaches case notes review basis. its final adult position at 2 or 5 months old. Non-significant Informed consent Not required for this study. results were additionally obtained for increased age on the termination level of the conus medullaris across the entire Open Access This article is licensed under a Creative Commons Attri- pediatric population. This supports the idea that no further bution 4.0 International License, which permits use, sharing, adapta- ascent occurs following childbirth and supports the notion tion, distribution and reproduction in any medium or format, as long that ascent is entirely in utero, between weeks 9 and 16 [14]. as you give appropriate credit to the original author(s) and the source, No statistically significant difference was noted amongst 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 age ranges and the termination level of the thecal sac. included in the article's Creative Commons licence, unless indicated These results are in agreement with the literature [4,15] that otherwise in a credit line to the material. If material is not included in increasing age has no impact on the thecal sac level and this the article's Creative Commons licence and your intended use is not suggests no ascent occurs following childbirth. 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://cr eativ ecommons. or g/licen ses/ b y/4.0/ . Limitations The relative paucity of studies amongst the age group of References 0-1 years of life is a limitation of this study. However, this is to be expected given routine spinal MRI in an otherwise 1. Nene Y, Jilani TN (2022) Neuroanatomy, Conus Medullaris. In: asymptomatic infant is uncommon. StatPearls. StatPearls Publishing, Treasure Island (FL) https:// www. ncbi. nlm. nih. gov/ books/ NBK54 5227 The assessment method employed in the study may have 2. 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Journal

Neuroradiology – Springer Journals

Published: Apr 1, 2023

Keywords: Conus medullaris; Thecal sac; Conus termination; Pediatric spine

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