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Gait Function in Adults Aged 50 Years and Older With Spina Bifida

Open AccessPublished:November 06, 2020DOI:https://doi.org/10.1016/j.apmr.2020.10.118

      Abstract

      Objective

      To study gait function among individuals with spina bifida (SB) aged 50 years or older.

      Design

      A cross-sectional study conducted in 2017.

      Setting

      Home-dwelling participants from all regions in Norway.

      Participants

      Individuals between the ages of 51 and 76 years (N=26; 16 women) categorized as independent walkers (n=9), walkers with aids (n=10) and nonwalkers (n=7).

      Interventions

      Not applicable.

      Main Outcome Measures

      Questionnaire, pain assessment, anthropometry, Falls Efficacy Scale International (FES-I), objective gait analysis, 6-minute walk test (6MWT), and timed Up and Go (TUG).

      Results

      Walking speed correlated with SB severity (ρ=–.59; P=.008). Individuals who walked slower than 0.81 m/s had a higher body mass index (BMI) than those who walked faster (P=.008). Independent walkers walked slower than healthy age-matched walkers (P=.046); spatiotemporal variables showed that this was owing to shorter steps rather than cadence. The mean TUG was 10.6±2.6 seconds in independent walkers and 20.2±6.5 in walkers with aids (P<.01). The mean 6MWT was 504±126 meters in independent walkers and 316±88 in walkers with aids (P<.01). The mean pain intensity (numeric rating scale) was 4.9±2.2 in independent walkers and 4.2±1.6 in walkers with aids, but the difference was not statistically significant. FES-I was significantly lower among independent walkers (mean, 23.6±3.9) than walkers with aids (mean, 31.4±10.0) (P=.042).

      Conclusions

      Participants commonly experienced an early onset deterioration in gait function, and walking speed was influenced by SB severity and BMI. This highlights the importance of early monitoring and weight management during follow-up for SB.

      Keywords

      List of abbreviations:

      6MWT (6-minute walk test), AFO (ankle-foot orthosis), BMI (body mass index), FES-I (Fall Efficacy Scale – International), GC (gait cycle), NRS (numeric rating scale), SB (spina bifida)
      Spina bifida (SB) is a developmental disorder caused by a neural tube defect.
      • Copp A.J.
      • Adzick N.S.
      • Chitty L.S.
      • Fletcher J.M.
      • Holmbeck G.N.
      • Shaw G.M.
      Spina bifida.
      The outcomes of the disorder vary depending on the neurologic level and severity, as well as whether other conditions, such as hydrocephalus and Arnold Chiari malformation, are present.
      • Copp A.J.
      • Adzick N.S.
      • Chitty L.S.
      • Fletcher J.M.
      • Holmbeck G.N.
      • Shaw G.M.
      Spina bifida.
      ,
      • Webb T.S.
      Optimizing health care for adults with spina bifida.
      In individuals with SB, gait function is influenced by multiple factors, and the neurologic level is a strong predictor.
      • Verhoefen M.
      • Barf H.A.
      • Post M.W.M.
      • van Asbeck F.W.A.
      • Gooskens R.H.J.M.
      • Prevo A.J.H.
      Functional independence among young adults with spina bifida, in relation to hydrocephalus and level of cele.
      ,
      • Fabry G.
      • Molenaers G.
      • Desloovere K.
      • Eyssen M.
      Gait Analysis in myelpmeningocele: possibilities and applications.
      At and below the neurologic level, muscle function, sensation, and autonomic function may be affected to varying degrees.
      • Perry J.
      • Burnfield J.M.
      Gait analysis: normal and pathological function.
      Most individuals with thoracic and high-lumbar defects have paresis or paralyses in the gluteal muscles, quadriceps, and plantar and dorsal flexors. Their decreased strength in hip abduction results in a typical Trendelenburg gait and persistent knee flexion in stance.
      • Duffy C.M.
      • Hill A.E.
      • Cosgrove A.P.
      • Corry I.S.
      • Mollan R.A.
      • Graham H.K.
      Three-dimensional gait analysis in spina bifida.
      ,
      • Gutierrez E.M.
      • Bartonek A.
      • Haglund-Akerlind Y.
      • Saraste H.
      Characteristic gait kinematics in persons with lumbosacral myelomeningocele.
      Such individuals may walk while young but often lose this ability during growth.
      • Dicianno B.E.
      • Karmarkar A.
      • Houtrow A.
      • et al.
      Factors associated with mobility outcomes in a national spina bifida patient registry.
      Likewise, low lumbar and sacral neurologic levels predominantly affect the distal muscles in the lower extremities.
      • Gutierrez E.M.
      • Bartonek A.
      • Haglund-Akerlind Y.
      • Saraste H.
      Characteristic gait kinematics in persons with lumbosacral myelomeningocele.
      Individuals with low neurologic levels are more commonly expected to gain and maintain gait function through childhood and youth.
      • Verhoefen M.
      • Barf H.A.
      • Post M.W.M.
      • van Asbeck F.W.A.
      • Gooskens R.H.J.M.
      • Prevo A.J.H.
      Functional independence among young adults with spina bifida, in relation to hydrocephalus and level of cele.
      Gait function in SB is also affected by typical orthopedic matters, such as scoliosis, clubfoot, hip dysplasia, or contractures, and the interventions for these problems.
      • Fabry G.
      • Molenaers G.
      • Desloovere K.
      • Eyssen M.
      Gait Analysis in myelpmeningocele: possibilities and applications.
      ,
      • Dicianno B.E.
      • Karmarkar A.
      • Houtrow A.
      • et al.
      Factors associated with mobility outcomes in a national spina bifida patient registry.
      Knowledge about gait function in adults with SB is mainly based on clinical experience, whereas several studies
      • Gutierrez E.M.
      • Bartonek A.
      • Haglund-Akerlind Y.
      • Saraste H.
      Characteristic gait kinematics in persons with lumbosacral myelomeningocele.
      ,
      • Battibugli S.
      • Gryfakis N.
      • Dias L.
      • Kelp-Lenane C.
      • Figlioli S.
      • Fitzgerald E.
      • et al.
      Functional gait comparison between children with myelomeningocele: shunt versus no shunt.
      • Rao S.
      • Dietz F.
      • Yack H.J.
      Kinematics and kinetics during gait in symptomatic and asymptomatic limbs of children with myelomeningocele.
      • Schoenmakers M.A.G.C.
      • Gooskens R.H.J.M.
      • Gulmans V.A.M.
      • et al.
      Long-term outcome of neurosurgical untethering on neurosegmental motor and ambulation levels.
      of children and youth have been published. Because functional gait is regarded as essential for retaining independence and participating in social life and work, it is important to elaborate on this theme. Oakeshott et al
      • Oakeshott P.
      • Poulton A.
      • Hunt G.M.
      • Reid F.
      Walking and living independently with spina bifida: a 50-year prospective cohort study.
      conducted a prospective study of adults with SB and found that mobility appeared to decline with age, with obesity suggested as a possible cause.
      Insights into the natural history of SB throughout the lifespan are important for development of models of health promotion and health services. The Norwegian SB community has highlighted gait function in middle-aged and older individuals as a research priority. In addition, based on clinical experiences, adults with SB often report a decline in gait function at a younger age than the general population. This is in accordance with findings from other diagnoses such as cerebral palsy.
      • Morgan P.
      • McGinley J.
      Gait function and decline in adults with cerebral palsy: a systematic review.
      In the disability field, the need to better understand the challenges of ageing has been stressed.
      • Roebroeck M.E.
      • Jahnsen R.
      • Carona C.
      • Kent R.M.
      • Chamberlain M.A.
      Adult outcomes and lifespan issues for people with childhood-onset physical disability.
      In this study, we present results on gait and physical functioning perspectives. The research questions addressed are: (1) What is the functional status of middle-aged and older adults with SB, measured with objective gait analyses?; (2) What factors influence walking speed?; and (3) What are the advantages of mobility tests and objective gait analyses when evaluating gait function?
      In a previous study, we shared findings on participation in society, overall health issues, and health service usage among these adults with SB.
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.
      We also presented study methods and justified the generalizability of the results to individuals aged 50 years and older with SB, without hydrocephalus.
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.

      Methods

      We conducted a cross-sectional study of 30 adults with SB aged 50 years or older. The study design, recruitment, and the representativeness of the study population have been described previously.
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.
      Participation was voluntarily, and written consent was collected. The data collection took place in 2017 and consisted of a clinical examination, questionnaires, and assessments of mobility and gait function. Four participants were excluded from this part of the study because 3 of them were seen in their respective homes and 1 used a prosthesis while walking.
      Control group values were drawn from normative gait data previously collected at the Sunnaas Motion Laboratory. The control group consisted of 30 age-matched healthy adults (22 women; mean age, 61.4y; age range, 51-76y). Normative spatiotemporal values for the age segment from 50 to 60 years were drawn from our adult reference group database (age, 18-60y), with data collected using a Vicon motion capture system.a Spatiotemporal values for healthy adults aged 60 years and older were based on data collected in a previous study
      • Rennie L.
      • Lofgren N.
      • Moe-Nilssen R.
      • Opheim A.
      • Dietrichs E.
      • Franzen E.
      The reliability of gait variability measures for individuals with Parkinson's disease and healthy older adults - the effect of gait speed.
      that used an electronic pressure sensor walkway.b Good reliability and agreement were previously demonstrated between the 2 systems for spatiotemporal data.
      • Webster K.E.
      • Wittwer J.E.
      • Feller J.A.
      Validity of the GAITRite® walkway system for the measurement of averaged and individual step parameters of gait.
      None of the controls had an ongoing or recent history of neuromuscular conditions or illness or of previous joint replacements. The study was preapproved by the Regional Committee for Medical and Health Research Ethics in Oslo, Norway.

      Questionnaires

      A physiotherapist (K.L.L.) and a physician (I.B.L.) conducted face-to-face interviews with predefined fixed questions.
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.
      The participants were asked if they had experienced changes in gait function and at what age those changes occurred. Their usage of walking aids was noted. Moreover, participants were asked about past orthopedic surgery and tethered cord release.

      Pain

      The participants answered whether they had experienced pain during the last week. Pain sites were marked on a sketch of a human body. The perceived intensity of pain was indicated on a numeric rating scale (NRS) from 0 to 10.
      • Fredheim O.M.S.
      • Borchgrevink P.C.
      • Landmark T.
      • Schjødt B.
      • Breivik H.
      [A new form for mapping of pain] [Norwegian].

      Falls Efficacy Scale – International

      Participants scored their concerns related to fear of falling during basic and more demanding indoor and outdoor activities. The good validity and reliability of the Falls Efficacy Scale – International (FES-I) has been documented for home-dwelling older individuals.
      • Delbaere K.
      • Close J.C.
      • Mikolaizak A.S.
      • Sachdev P.S.
      • Brodaty H.
      • Lord S.R.
      The Falls Efficacy Scale International (FES-I). A comprehensive longitudinal validation study.

      Clinical examination

      Anthropometry

      Weight (to the nearest kg) and height (in cm) was measured. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared (kg/m2).

      Gait assessments

      The 26 participants were categorized into 3 groups: independent walkers (those who walked without aids) (n=9), walkers with aids (n=10), and nonwalkers (n=7). The nonwalkers were excluded from the gait assessments.

      Spatiotemporal variables

      Participants were instructed to walk back and forth on a 10-meter walkway at a self-selected walking speed. A foot model consisting of 3 reflective markers was used. Markers were placed on the lateral malleolus, the center of the heel cap of the shoe, and the tip of the shoe. Gait data were recorded using Vicon Motion Capture Systems with 6 infrared cameras,a 2 force platforms,c and 2 digital video cameras.d

      6-minute walk test

      While wearing shoes and using walking aids, if necessary, participants were told to walk as fast as possible for 6 minutes. They walked back and forth between 2 cones placed 30 meters apart in a corridor. After the test, the total distance walked was measured.
      • Bohannon R.W.
      • Crouch R.
      Minimal clinically important difference for change in 6-minute walk test distance of adults with pathology: a systematic review.
      Age, sex, and weight- and height-related reference values were obtained from the FYSIOPRIM database.
      University of Oslo
      FYSIOPRIM.

      Timed Up and Go

      The time it took for each participant to rise from a sitting position, walk 3 meters, turn around, walk back, and sit down again was measured. The participants used their walking aids if needed, and they were told to walk safely at their usual pace. The mean of 2 tests was calculated.
      • Fredheim O.M.S.
      • Borchgrevink P.C.
      • Landmark T.
      • Schjødt B.
      • Breivik H.
      [A new form for mapping of pain] [Norwegian].

      Data processing

      Data processing and the calculation of spatiotemporal variables were conducted using Nexus 2.4 and ProCalc 1.0e based on 3 valid trials. Each trial consisted of at least 3 gait cycles. The chosen spatiotemporal variables were walking speed (m/s), cadence (steps/min), step length (m), step width (m), gait cycle (GC) length (m), and stance phase (% of GC) with single and double stances (% of GC). The variables were exported to SPSSf for further statistical analysis.

      Statistical analysis

      Descriptive analyses were performed and presented using means ± SD and ranges. To compare data between groups, parametric t tests or nonparametric Mann-Whitney U tests were used. To examine the associations between walking speed (m/s) (n=19) and selected continuous covariates (age in y; SB composite score range, 4-10
      • Hommeyer J.S.
      • Holmbeck G.N.
      • Wills K.E.
      • Coers S.
      Condition severity and psychosocial functioning in pre-adolescents with spina bifida: disentangling proximal functional status and distal adjustment outcomes.
      ), we performed Spearman correlation analyses, presented as Spearman’s rank correlation coefficient (ρ) with P value. Furthermore, we dichotomized walking speed into those walking less than 0.81 m/s and those walking faster
      • Castell M.-V.
      • Sánchez M.
      • Julián R.
      • Queipo R.
      • Martín S.
      • Otero Á.
      Frailty prevalence and slow walking speed in persons age 65 and older: implications for primary care.
      and compared the 2 groups in terms of selected categorical variables (sex, BMI (<24.9, 25-29.9, ≥30), tethered cord surgery (yes or no), and lower extremity orthopedic surgery (yes or no) by using the chi-square test or the Fisher’s exact test. We calculated an SB severity composite
      • Hommeyer J.S.
      • Holmbeck G.N.
      • Wills K.E.
      • Coers S.
      Condition severity and psychosocial functioning in pre-adolescents with spina bifida: disentangling proximal functional status and distal adjustment outcomes.
      based on the following variables: (1) shunt status (1, no; 2, yes); (2) myelomeningocele (1, no; 2, yes); (3) lesion level (1, sacral; 2, lumbar; 3, thoracic); and (4) ambulation status (1, independent walking; 2, walkers with aids; 3, nonwalkers). The total scores ranged from 4 to 10, with higher scores reflecting more severe SB. Hommeyer et al
      • Hommeyer J.S.
      • Holmbeck G.N.
      • Wills K.E.
      • Coers S.
      Condition severity and psychosocial functioning in pre-adolescents with spina bifida: disentangling proximal functional status and distal adjustment outcomes.
      documented the validity of the severity composite. The internal consistency of the composite in the current study population was α of 0.63, whereas Hommeyer et al reported a Cronbach’s alpha of 0.70.
      • Hommeyer J.S.
      • Holmbeck G.N.
      • Wills K.E.
      • Coers S.
      Condition severity and psychosocial functioning in pre-adolescents with spina bifida: disentangling proximal functional status and distal adjustment outcomes.
      Missing data were omitted from the analysis, and all participants are presented in Table 1, Table 2, Table 3. The statistical tests were 2-tailed, and the statistical significance level was set at a P value of less than .05. Analyses were carried out in SPSS.f
      Table 1Characteristics of the participants according to functional status and reference group values
      CharacteristicsIndependent Walkers (n=9)Walkers With Aids (n=10)Nonwalkers (n=7)Reference Group (n=30)
      Sex, women/men5/47/34/322/8
      Age, y, mean ± SD (range)58.9±7.5 (51-76)57.9±3.5 (53-64)55.7±6.6 (51-70)61.4±7.4 (51-76)
      Neurologic level, n (%)
       Thoracic---
       Lumbar4 (44)5 (50)7 (100)
       Sacral5 (56)5 (50)-
      Hydrocephalus, n (%)-
      One person answered “Do not know.”
      1 (10)3 (43)
      SB composite score, range 4-10, mean ± SD (range)
      Hommeyer.22
      5.0±1.0 (4-6)6.7±0.68 (6-8)
      Height, cm, mean ± SD (range)166.4±11.3 (144-185)162.0±13.0 (135-189)162.0±13.5
      One missing.
      (148-178)
      172.1±9.6 (156-192)
      Weight, kg, mean ± SD (range)73.8±17.7 (50-99)78.5±12.7 (63-103)88.3±38.3
      One missing.
      (48.5-148)
      75.5±12.4 (56-117)
      BMI, kg/m
      • Webb T.S.
      Optimizing health care for adults with spina bifida.
      , mean ± SD (range)
      26.4±4.9 (18.6-34.0)30.3±6.1 (20-39.7)34.7±14.8
      One missing.
      (21.5-57.8)
      25.6±3.2 (20.2-35.2)
      BMI groups, n (%)
       Underweight---
      One missing.
       Normal2 (22)3 (30)3 (43)
       Overweight5 (56)2 (20)1 (14)
       Obesity class I2 (22)3 (30)-
       Obesity class II-2 (20)-
       Obesity class III--2 (28)
      Tethered cord surgery, n (%)-4 (40)
      One person answered “Do not know.”
      3 (43)
      Lower extremity orthopedic surgery, n (%)4 (44)10 (100)6 (86)
      NOTE. BMI groups are as follows: underweight (<18.5), normal (18.5-24.9), overweight (25-29.9), obese class I (30-34.9), obese class II (35-39.9), and obese class III (≥40).
      One person answered “Do not know.”
      Hommeyer.
      • Hommeyer J.S.
      • Holmbeck G.N.
      • Wills K.E.
      • Coers S.
      Condition severity and psychosocial functioning in pre-adolescents with spina bifida: disentangling proximal functional status and distal adjustment outcomes.
      One missing.
      Table 2Gait function tests of participants (n=19) and reference data
      TestIndependent Walkers (n=9)Walkers With Aids (n=10)P Value
      Independent sample t test.
      (95% CI)
      Reference Group
      Age-matched healthy adults without any diseases, injuries, or conditions that affect gait function.
      (n=30)
      6MWT distance, m, mean ± SD (range)
      Two missing because 1 participant in each group was not able to undertake the 6MWT.
      504±126 (315-723)316±88 (200-455)<.01
      Statistically significant difference between the groups (P<.05).
      (77-299)
      595±67
      Estimated reference value and walking distance for the participants (n=17).21
      (474-718)
      TUG time, s, mean ± SD (range)10.6±2.6 (8.1-15.6)20.2±6.5 (11.9-33.0)<.01
      Statistically significant difference between the groups (P<.05).
      (–14.5 to –4.7)
      Mean: 8.1
      Bohannon and Crouch (n=176).20
      95% CI: 7.1-9.0
      Abbreviations: CI, confidence interval; TUG, timed Up and Go.
      Independent sample t test.
      Age-matched healthy adults without any diseases, injuries, or conditions that affect gait function.
      Two missing because 1 participant in each group was not able to undertake the 6MWT.
      § Statistically significant difference between the groups (P<.05).
      Estimated reference value and walking distance for the participants (n=17).
      University of Oslo
      FYSIOPRIM.
      Bohannon and Crouch (n=176).
      • Bohannon R.W.
      • Crouch R.
      Minimal clinically important difference for change in 6-minute walk test distance of adults with pathology: a systematic review.
      Table 3Walking speed and spatiotemporal variables in independent walkers (n=9) and walkers with aids (n=10) compared with reference values (n=30)
      VariableIndependent Walkers (n=9)P Value
      Independent sample t test.
      (95% CI)
      Walkers With Aids (n=10)P Value
      Independent sample t test.
      (95% CI)
      Reference Group
      Age-matched healthy adults without any diseases, injuries, or conditions that affect gait function.
      (n=30)
      Walking speed, m/s, mean ± SD (range)1.27±0.32 (0.78-1.83).046 (–0.35 to –0.004)0.71±0.24 (0.33-1.03)<.01
      Statistically significant difference between the groups (P<.05).
      (–0.89 to –0.59)
      1.44±0.19 (1.14-1.89)
      Cadence, steps/min, mean ± SD (range)115.7±14.23 (98-147).62 (–10.79 to 6.55)79.8±13.3 (58-103)<.01
      Statistically significant difference between the groups (P<.05).
      (–46.3 to –29.9)
      117.8±10.29 (102-138)
      Step length, m, mean ± SD (range)0.64±0.13 (0.40-0.83)<.01
      Statistically significant difference between the groups (P<.05).
      (–0.17 to –0.03)
      0.53±0.11 (0.35-0.71)<.01
      Statistically significant difference between the groups (P<.05).
      (–0.27 to –0.14)
      0.74±0.08 (0.63-0.91)
      Step width, m, mean ± SD (range)0.12±0.05 (0.06-0.21).02
      Statistically significant difference between the groups (P<.05).
      (0.01-0.05)
      0.21±0.06 (0.15-0.33)<.01
      Statistically significant difference between the groups (P<.05).
      (0.09-0.14)
      0.09±0.03 (0.05-0.14)
      Stance phase, % of GC, mean ± SD (range)64.3±2.03 (62-68)<.01
      Statistically significant difference between the groups (P<.05).
      (2.28-4.95)
      66.8±4.9 (59.9-77.4)<.01
      Statistically significant difference between the groups (P<.05).
      (4.03-8.15)
      60.7±1.64 (57.7-64.4)
      Single stance, % of GC, mean ± SD (range)35.7±2.1 (32-38)<.01
      Statistically significant difference between the groups (P<.05).
      (–4.86 to 2.21)
      33.1±5.0 (22-40)<.01
      Statistically significant difference between the groups (P<.05).
      (–8.17 to –4.04)
      39.2±1.59 (35.6-42.8)
      Double stance, % of GC, mean ± SD (range)28.7±4.1 (24-36)<.01
      Statistically significant difference between the groups (P<.05).
      (4.52-9.77)
      33.7±9.9 (20-55)<.01
      Statistically significant difference between the groups (P<.05).
      (8.07-16.28)
      21.5±3.18 (14.9-28.8)
      Independent sample t test.
      Age-matched healthy adults without any diseases, injuries, or conditions that affect gait function.
      Statistically significant difference between the groups (P<.05).

      Results

      Description of participants

      Table 1 presents the 26 participants’ characteristics. Twenty-two had myelomeningocele, and 4 had SB occulta. Nine of the walkers with aids used 2 forearm crutches, and 1 used walking poles. In addition, 3 participants used bilateral ankle-foot orthoses (AFO), and 1 used a unilateral AFO. Among the independent walkers, 1 walked with a knee orthosis, but none used AFOs.

      Gait function

      Among the 9 independent walkers, 5 reported gait function deterioration, 3 reported no change in gait function, and 1 reported improvements (fig 1). Nine of the 10 walkers with aids reported deterioration in gait function. Although not statistically significant, the independent walkers experienced deterioration in gait function at a slightly higher mean age (42.6y) compared with walkers with aids (36.7y) and non-walkers (33.7y). It is worth noting that 4 walkers with aids (age, 55-60y) had a sacral level of the neural defect without hydrocephalus. These participants all had a history of medical complications, including tethered cord, spinal stenosis, and syringomyelia, and 2 were obese with a BMI greater than 35. Among the nonwalkers, only 1 participant had never been able to walk (see fig 1).
      Figure thumbnail gr1
      Fig 1The distribution of age at onset of perceived deterioration in gait function in the 3 groups (n=20).
      Walking speed was correlated to SB composite score (ρ=–.59; P=.008), which means that those with lower scores (ie, less severe SB) were walking with higher speed. However, walking speed was not correlated with age (P=.64). Furthermore, those walking slower than 0.81 m/s had statistically significantly (P=.008) higher BMI values compared with those walking faster. Those walking slower than 0.81 m/s were not statistically significantly different based on sex (P=.17), history of tethered cord surgery (P=.08), or lower extremity surgery (P=.25) compared with individuals who had a faster walking speed.
      Figure 2A to 2D illustrates the level of the neural defect, hydrocephalus status, and history of tethered cord surgery and lower extremity surgery. It is worth noting that few participants had hydrocephalus,
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.
      and none of those participants were independent walkers. None of the independent walkers had undergone tethered cord surgery, and few had undergone orthopedic surgery. The timed Up and Go and 6-minute walk test (6MWT) showed that independent walkers scored close to reference values, but within a larger range (table 2). Table 3 presents the walking speed and spatiotemporal results with comparisons between independent walkers and walkers with aids, as well as against reference values.
      Figure thumbnail gr2
      Fig 2Illustration of the level of the neural defect, presence of hydrocephalus, and past surgery for the 3 groups (n=26).
      Independent walkers scored moderate to high fear of falling (23.6±3.9) and significantly lower (P=.042) than walkers with aids (31.4±10.0). The independent walkers also had a slightly higher mean pain intensity score (NRS, 4.9±2.2) compared with the walkers with aids (NRS, 4.2±1.6), but the difference was not statistically significant. The most common pain sites for all groups were the lumbar area, the hips, and the legs.
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.

      Discussion

      Our main findings revealed that severe SB and high BMI appeared to negatively influence walking speed. Furthermore, most of the participants perceived deterioration in gait function within their fourth decade. Although clinical studies on gait function in middle-aged and older adults with SB are lacking, Oakeshott et al
      • Oakeshott P.
      • Poulton A.
      • Hunt G.M.
      • Reid F.
      Walking and living independently with spina bifida: a 50-year prospective cohort study.
      conducted a postal questionnaire survey (n=37) that included questions on gait function. They showed that 45% of middle-aged adults with SB with sensory levels below L3 and 38% of those with quadriceps activity at birth were able to walk more than 50 meters at the age of 50 years. All of our nonwalkers had lumbar levels of neural defect, whereas the independent walkers and the walkers with aids had lumbar or sacral levels of neural defect. Our objective functional assessments showed that 90% of the participants with gait function could walk at least 200 meters indoors. Six of the 7 nonwalkers had previously been able to walk, which means that approximately 23% of our total study sample had lost the ability to walk. Among those studied by Oakeshott et al,
      • Oakeshott P.
      • Poulton A.
      • Hunt G.M.
      • Reid F.
      Walking and living independently with spina bifida: a 50-year prospective cohort study.
      53% lost their ability to walk 50 meters as they got older.
      In a retrospective study, Seitzberg et al
      • Seitzberg A.
      • Lind M.
      • Biering-Sorensen F.
      Ambulation in adults with myelomeningocele. Is it possible to predict the level of ambulation in early life?.
      compared the ambulation status of young adults with SB (n=52) aged between 18 and 37 years with their level of motor function in childhood. The authors concluded that adult ambulatory function was more difficult to predict from childhood motor levels L3 to L5. However, levels above L2 and at or below S1 predicted adult gait function to some extent. Furthermore, they stated that the presence of shunted hydrocephalus did not correlate with loss of gait function from childhood to adulthood.
      Oakeshott et al
      • Oakeshott P.
      • Poulton A.
      • Hunt G.M.
      • Reid F.
      Walking and living independently with spina bifida: a 50-year prospective cohort study.
      did not find any association between shunt history and the ability to walk a minimum of 50 meters. In contrast, a study of 161 children with SB aged between 4 and 18 years demonstrated that participants without shunted hydrocephalus tended to walk faster and have greater stride lengths.
      • Battibugli S.
      • Gryfakis N.
      • Dias L.
      • Kelp-Lenane C.
      • Figlioli S.
      • Fitzgerald E.
      • et al.
      Functional gait comparison between children with myelomeningocele: shunt versus no shunt.
      This was in line with our results, as none of the independent walkers had hydrocephalus. However, owing to the small number of participants with hydrocephalus in our study, it is impossible to draw conclusions on its association with gait function. The limited research and conflicting results highlighted above underline the need to further explore gait function throughout the lifespan of individuals with SB with and without hydrocephalus.
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.
      With gait laboratory assessments, we achieved valid and reliable objective findings, which represents a special contribution to the knowledge base on ambulatory function in adult SB. The independent walkers had lower walking speeds than the healthy age-matched adult walkers owing to shorter steps, not to cadence. Several authors have also shown that children and youth with SB have the same gait pattern with lower walking speeds and shorter steps.
      • Rao S.
      • Dietz F.
      • Yack H.J.
      Kinematics and kinetics during gait in symptomatic and asymptomatic limbs of children with myelomeningocele.
      ,
      • Gutierrez E.M.
      • Bartonek Å.
      • Haglund-Åkerlind Y.
      • Saraste H.
      Centre of mass motion during gait in persons with myelomeningocele.
      Meanwhile, increased time in double stance, decreased time in single stance, and increased step width indicated poor balance. This was substantiated with the finding that a majority of the independent walkers scored moderate to high levels for fear of falling. Based on these results, balance training should be an essential part of exercise for adults with SB. Information collected from objective gait analysis may also be important for evaluating gait function before and after surgical interventions,
      • Mueske N.M.
      • Ounpuu S.
      • Ryan D.D.
      • et al.
      Impact of gait analysis on pathology identification and surgical recommendations in children with spina bifida.
      introducing walking aids and orthoses, and monitoring gait development in adults with SB.
      Dicianno et al
      • Dicianno B.E.
      • Karmarkar A.
      • Houtrow A.
      • et al.
      Factors associated with mobility outcomes in a national spina bifida patient registry.
      investigated factors influencing ambulatory status and analyzed data of 381 patients (mean age, 15y; age range, 5-57y) recorded in the National Spina Bifida Patient Register in North America. They found that a history of release surgery of contractures in the hip or knee was associated with less ambulatory function, whereas past tethered cord surgery was not statistically significantly associated with ambulatory status.
      • Dicianno B.E.
      • Karmarkar A.
      • Houtrow A.
      • et al.
      Factors associated with mobility outcomes in a national spina bifida patient registry.
      In contrast, Schoenmakers et al
      • Schoenmakers M.A.G.C.
      • Gooskens R.H.J.M.
      • Gulmans V.A.M.
      • et al.
      Long-term outcome of neurosurgical untethering on neurosegmental motor and ambulation levels.
      found that obesity and retethering surgery were strongly associated with deterioration in ambulatory function among children at the time of surgery and at follow-up.
      • Schoenmakers M.A.G.C.
      • Gooskens R.H.J.M.
      • Gulmans V.A.M.
      • et al.
      Long-term outcome of neurosurgical untethering on neurosegmental motor and ambulation levels.
      In our study, only walkers with aids and nonwalkers had undergone tethered cord surgery. A history of lower limb orthopedic surgery was also more common in those groups than among independent walkers. However, walking speed was not statistically significantly associated with a history of tethered cord or lower extremity surgery. Prospective studies, including registry studies on larger cohorts, to assess physical function in relation to surgery in the long term, are warranted.
      Several authors have highlighted problems posed by overweight and obesity in children and adolescents with SB.
      • Schoenmakers M.A.G.C.
      • Gooskens R.H.J.M.
      • Gulmans V.A.M.
      • et al.
      Long-term outcome of neurosurgical untethering on neurosegmental motor and ambulation levels.
      ,
      • Oakeshott P.
      • Poulton A.
      • Hunt G.M.
      • Reid F.
      Walking and living independently with spina bifida: a 50-year prospective cohort study.
      ,
      • Polfuss M.
      • Bandini L.G.
      • Sawin K.J.
      Obesity prevention for individuals with spina bifida.
      ,
      • McPherson A.C.
      • Swift J.A.
      • Yung E.
      • Lyons J.
      • Church P.
      The assessment of weight status in children and young people attending a spina bifida outpatient clinic: a retrospective medical record review.
      Sedentary lifestyle and limited participation in physical activity and sports are among the factors contributing to obesity in these patients. Weight problems may lead to medical complications, decline in ambulatory function, and challenges with social activities and participation in general.
      • Polfuss M.
      • Bandini L.G.
      • Sawin K.J.
      Obesity prevention for individuals with spina bifida.
      ,
      • McPherson A.C.
      • Swift J.A.
      • Yung E.
      • Lyons J.
      • Church P.
      The assessment of weight status in children and young people attending a spina bifida outpatient clinic: a retrospective medical record review.
      In a cross-sectional study of adults with Sb between the ages of 20 and 58 years, 37% were obese, particularly women, and this group had a significantly lower proportion of ambulators than the non-obese group.
      • Dosa N.P.
      • Foley J.T.
      • Eckrich M.
      • Woodall-Ruff D.
      • Liptak G.S.
      Obesity across the lifespan among persons with spina bifida.
      Our study group had a higher average age and a high proportion of obesity (43%).
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.
      In addition, mean BMI was low in the independent walkers, especially compared with the nonwalkers, and walking speed was statistically significantly associated with BMI. This highlights the importance of early interventions and education on weight management for children and adolescents in addition to programs adapted for adults with SB, as underlined by other authors.
      • Polfuss M.
      • Bandini L.G.
      • Sawin K.J.
      Obesity prevention for individuals with spina bifida.
      ,
      • McPherson A.C.
      • Swift J.A.
      • Yung E.
      • Lyons J.
      • Church P.
      The assessment of weight status in children and young people attending a spina bifida outpatient clinic: a retrospective medical record review.

      Study limitations

      The objective assessments of gait function and the use of validated questionnaires are major strengths of this study. The study sample represents about one-third of all individuals older than 50 years with SB but without hydrocephalus in Norway.
      • Lidal I.B.
      • Lundberg Larsen K.
      • Hoff M.
      50 Years and older - born with spina bifida: participation, health issues and physical function.
      Therefore, the study results are generalizable to Norwegian middle-aged and older individuals with SB without hydrocephalus. It should be noted, however, that some self-reported data concerning medical history might introduce recall bias. Furthermore, the study design was cross-sectional, and the sample size was small, limiting our ability to detect associations and draw conclusions. Finally, it should be mentioned that Castell et al
      • Castell M.-V.
      • Sánchez M.
      • Julián R.
      • Queipo R.
      • Martín S.
      • Otero Á.
      Frailty prevalence and slow walking speed in persons age 65 and older: implications for primary care.
      have recommended dichotomizing walking speed (0.81 and faster) for the elderly. However, this has not been validated for SB.
      Future studies should prospectively evaluate gait function in adults with SB and preferably include data from patients in their 30s. The evaluation should include assessments of fear of falling, pain, and objective gait tests. The effects of weight management, physical activity, and exercise throughout a lifespan of individuals with SB are other important topics. We welcome multicenter studies.

      Conclusions

      Middle-aged and older individuals with SB commonly experience an early decline in gait function. Their walking speed seems influenced by SB severity and BMI. The timed Up and Go and the 6MWT tests are easy to use when evaluating mobility and endurance in these patients. Gait analysis with detailed data on spatiotemporal variables demands more sophisticated equipment and might be useful when planning and evaluating treatment, such as surgery, or adjusting orthopedic aids.

      Suppliers

      • a.
        MX13, 100HZ; Vicon Motion Capture Systems.
      • b.
        GAITRite; CIR Systems Inc.
      • c.
        AMTI OR6-7; Advanced Mechanical Technology, Inc.
      • d.
        JVC Kenwood Corp.
      • e.
        Nexus 2.4 and ProCalc 1.0; Vicon Motion Systems.
      • f.
        IBM SPSS Statistics for Windows, version 25; IBM Corp.

      Acknowledgments

      We thank our reference group from The Norwegian Association for Spina Bifida and Hydrocephalus for their advice. We also thank Marie Hoff, MD, and Olga de Vries, Senior Physiotherapist, MSc, at the TRS Resource Center for reading and commenting on our manuscript.

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