Correlation Between Neurologic Impairment Grade and Ambulation Status in the Adult Spina Bifida Population

Abstract

Objective:

The aim of the study was to identify which neurologic impairment scales correlate with ambulation status in adults with spina bifida.

Design:

A retrospective chart review was performed on patients seen at the University of Pittsburgh Medical Center Adult Spina Bifida Clinic. Findings were graded using several neurologic impairment scales: two versions of the National Spina Bifida Patient Registry classification, the International Standards for Neurological Classification of Spinal Cord Injury motor level, and the Broughton Neurologic Impairment Scale. Ambulation ability was ranked using the Hoffer classification system.

Results:

Data collected from 409 patient records showed significant correlations between Hoffer ambulation status and all neurologic impairment scales evaluated. The strongest correlation was noted with the Broughton classification (r_s = −0.771, P < 0.001). High correlations were also noted with both versions of the National Spina Bifida Patient Registry: strength 3/5 or greater (r_s = −0.763, P < 0.001), and strength 1/5 or greater (r_s = −0.716, P < 0.001). For the International Standards for Neurological Classification of Spinal Cord Injury motor level, only a moderate correlation was observed (r_s = −0.565, P < 0.001).

Conclusions:

Multiple grading scales can be used to measure motor function in adult spina bifida patients. Although the Broughton classification seems to be the most highly correlated with ambulation status, the less complex National Spina Bifida Patient Registry scale is also highly correlated and may be easier to administer in busy clinic settings.

Spina bifida is a congenital condition caused by incomplete closure of the neural tube around the third to fourth week of gestation.¹ It can be associated with disruptions in the upper and/or lower motor and sensory pathways, which often leads to neurologic impairments, orthopedic defects, and partial or complete paralysis of the lower limbs.^2,3 Each year in the United States, approximately 1500 people are born with spina bifida,⁴ making it the most common congenital condition resulting in physical disability.⁵ The most common yet severe form of spina bifida, myelomeningocele, is frequently associated with hydrocephalus, Chiari II malformation, neurogenic bladder and bowel, tethered cord, muscle contractures, and spinal deformity, all of which can lead to additional impairments in function.⁶

The spectrum of impairment stemming from spina bifida creates a wide range of mobility levels and everyday functional ability among patients. Mobility is an important aspect of maintaining independence and enjoying a higher quality of life.^7,8 As more than 75% of people with spina bifida are now living into adulthood, preserving functional mobility into the later decades of life has become increasingly important.^8,9 Hoffer et al.¹⁰ described the following four broad ambulation categories that are commonly used for classification: community ambulation, household ambulation, therapeutic/nonfunctional ambulation, and lack of ambulation. The main goal in treatment of spina bifida, as with any disability, is attainment of walking ability or at least maintenance of functional level.¹¹ Maintaining ambulation and function is important because it can help prevent conditions, such as osteoporosis, skin breakdown, contractures, and weight gain, and can ultimately lead to better health outcomes.^7,12,13

Many factors may influence the level of ambulation in spina bifida. Studies show various effects of age, obesity, cognitive status, motivation, hydrocephalus, spasticity, spinal deformities, contractures, and other orthopedic problems on motor performance and ambulation; no single scale would be expected to encompass each of these factors.^10,14 There is consensus among investigators that there is a strong correlation between neurologic level and ambulatory status; however, there is often disagreement as to which muscle groups should be used to determine neurological level and, therefore, which impairment scale to use.^{2,7,10,14–21} Furthermore, it is unknown how these scales correlate to ambulation status in the modern era.

Since 2009, patient data has been collected in the National Spina Bifida Patient Registry (NSBPR) from more than 20 spina bifida clinics across the country.²² Currently, the database uses a five-point scale to classify functional impairment levels. Patients are assigned to one of the following five categories based on the findings of muscle strength testing: thoracic, high-lumbar, mid-lumbar, low-lumbar, and sacral levels.²² The database does not, however, specify minimum criteria for muscle strength in each of the tested areas. Although this scale is easy to administer, it is not as comprehensive as other scales such as the International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI) and the Broughton scale.^23,24

The purpose of the study was to evaluate the relationship between ambulatory status and four of the most modern and commonly used neurologic scales for individuals with spina bifida: ISNCSCI motor level, Broughton classification, and two versions of the NSBPR classification. We hypothesized that the neurologic impairment level, as graded by these four scales, would be inversely correlated with ambulation status in adults with spina bifida (i.e., higher neurological impairment results in lower levels of ambulation).

METHODS

This project was approved by the institutional review board at the University of Pittsburgh using a waiver of informed consent. The STROBE guidelines were used to ensure proper reporting (see Supplemental Checklist, Supplemental Digital Content 1, http://links.lww.com/PHM/A772). We compiled a database of 409 patients who were examined at the University of Pittsburgh Medical Center Adult Spina Bifida Clinic between August 2005 and May 2016. The University of Pittsburgh Medical Center Adult Spina Bifida Clinic, located in Pittsburgh, Pennsylvania, is the only spina bifida program in western Pennsylvania for adults and is one of the few nationwide to specialize in adult spina bifida care. A retrospective chart review of the patients within the database was performed to identify ambulatory status and additional patient information from each patient’s most recent clinic visit. Ambulatory ability was ranked using the following four-point classification system published by Hoffer et al.¹⁰:

• Community ambulator – Walks indoors and outdoors for most activities and may need crutches or braces or both. Uses a wheelchair only for long trips out of the community.

• Household ambulator – Walks only indoors and with apparatus. Able to get in and out of the chair and bed with little if any assistance. May use the wheelchair for some indoor activities at home and school and for all activities in the community.

• Therapeutic ambulator – Walks only for a therapy session in school or in the hospital. Otherwise uses a wheelchair to get from place to place and to satisfy all needs for transportation.

• Nonambulator – Uses a wheelchair exclusively for transportation, but usually can transfer from chair to bed.

Next, the following variables were extracted: demographics (sex, age at most recent visit, ethnicity, and race), subtype of spina bifida (myelomeningocele, meningocele, lipomyeloeningocele, thickened/fatty filum, split cord malformation, terminal myelocystocele, and “other,” which includes occulta), and enrollment status in the NSBPR (yes/no).

In addition, data were collected on individuals’ muscle strength on physical examination at their most recent clinic visit. These findings were then used to grade the patients’ neurologic impairment using criteria from the following three existing scales:

• The NSBPR scale was used to classify patients into the following five functional levels of lesion: thoracic (flaccid lower limbs), high-lumbar (hip-flexion present), mid-lumbar (knee extension present), low-lumbar (foot dorsiflexion present), and sacral (foot plantar flexion present). The NSBPR instructions state that the functional level is “the lowest level of independent movement which can be reproduced by the patient.”² Because this definition is somewhat ambiguous, we tested two possible interpretations: movement defined by a muscle strength of 1/5 or greater (i.e., flicker of the muscle only) or movement defined by a muscle strength of 3/5 or greater (i.e., movement occurs against gravity but not against resistance).

• The ISNCSCI scale categorizes patients into levels from C2 through S4-S5.²⁴ This scale typically uses both motor and sensory examinations to determine an overall neurologic lesion level; however, for our study, we used only the motor component. In the ISNCSCI scale, the extensor hallucis longus is used to test L5 motor strength; however, because of orthopedic foot deformities in our patients, the extensor hallucis longus is often difficult to test. Therefore, we used hip abduction (gluteus medius) as an alternative measure for this motor level.²⁵

• The Broughton classification is a nine-point motor scale developed for patients with spina bifida.²³ We applied this scale to group patients into the following nine levels: thoracic, L1, L2, L3, L4, L5, S1, S2, or no loss of motor function. The Broughton classification defines S2 level as gastrocnemius/soleus strength grade 3/5 or better and gluteus medius and gluteus maximus grade 4/5 or better, while also meeting criteria for S1. However, because of orthopedic deformities and contractures, it is sometimes difficult to test the gluteus maximus. We therefore assigned an S2 level when gastrocnemius/soleus was 3/5 or better, gluteus medius was 4/5 or better, and all criteria for S1 were met.

Statistical Analysis

Descriptive statistics were used for summarizing the data. Spearman’s ρ testing was performed to evaluate for a correlation between Hoffer ambulation status and each neurologic impairment scale. Alpha levels were set at 0.05. Data analyses were performed on an anonymized database using the Statistical Package for the Social Sciences (SPSS), Version 24 (International Business Machines (IBM) Corporation, Armonk, NY).

RESULTS

The average age of the 409 patients at their most recent visit was 36.9 (SD = 12.2) yrs, ranging from 20.4 to 85.7 yrs. Additional demographic information of the 409 individuals can be seen in Table 1. Using the Hoffer ambulatory classification, 190 patients (46.5%) were nonambulators, 174 (42.5%) were community ambulators, 34 (8.3%) were household ambulators, and 11 (2.7%) were therapeutic/nonfunctional ambulators. Significant inverse correlations were found between all neurologic impairment scales and Hoffer ambulation status. The strongest correlation was noted with the Broughton classification (r_s = −0.771, P < 0.001) in Figure 1. As illustrated in Figure 1, the scatter plot is a visual representation of the strength of the significant correlation between the Broughton classification and Hoffer ambulation status. Most data points are clustered around the trend line, as indicated by the size of the bubbles. The larger bubbles represent a large clustering of participants, whereas the smaller bubbles indicate smaller clusters. High correlations were also noted with both versions of NSBPR (Figs. 2, 3): strength 3/5 or greater (r_s = −0.763, P < 0.001) and strength 1/5 or greater (r_s = −0.716, P < 0.001). For the ISNCSCI motor level, only a moderate correlation was observed (r_s = −0.565, P < 0.001), as seen in Figure 4.

TABLE 1.

Demographic characteristics of 409 individuals with spina bifida

	n	%
Sex
Male	186	45.5
Female	223	54.5
Race
White	388	94.9
Black/African-American	19	4.6
Asian-American	2	0.5
Ethnicity
Non-Hispanic or non-Latino	407	99.5
Hispanic or Latino	2	0.5
Subtype
1. Myelomeningocele	300	73.3
2. Occulta/other	56	13.7
3. Lipomyelomeningocele	28	6.8
4. Thickened/fatty filum	17	4.2
5. Meningocele	4	1.0
6. Split cord malformation	4	1.0
Registered in NSBPR
1. Yes	175	42.8
2. No	234	57.2

FIGURE 1.

Relationship of Hoffer ambulatory status to Broughton scale. Legend: Hoffer ambulation status rated 1–4 (community ambulation, household ambulation, therapeutic/nonfunctional ambulation, lack of ambulation) compared with Broughton classification rated 0–8 (thoracic, L1, L2, L3, L4, L5, S1, S2, no loss) using Spearman’s ρ testing.

FIGURE 2.

Relationship of Hoffer ambulatory status to NSBPR scale ≥ 3/5. Legend: Hoffer ambulation status rated 1–4 (community ambulation, household ambulation, therapeutic/nonfunctional ambulation, lack of ambulation) compared with the NSBPR scale with muscle strength of 3/5 or greater rated 0–4 (thoracic, high-lumbar, mid-lumbar, low-lumbar, sacral) using Spearman’s ρ testing.

FIGURE 3.

Relationship of Hoffer ambulatory status to NSBPR scale ≥ 1/5. Legend: Hoffer ambulation status rated 1–4 (community ambulation, household ambulation, therapeutic/nonfunctional ambulation, lack of ambulation) compared with the NSBPR scale with muscle strength of 1/5 or greater rated 0–4 (thoracic, high-lumbar, mid-lumbar, low-lumbar, sacral) using Spearman’s ρ testing.

FIGURE 4.

Relationship of Hoffer ambulatory status to ISNCSCI scale. Legend: Hoffer ambulation status rated 1–4 (community ambulation, household ambulation, therapeutic/nonfunctional ambulation, lack of ambulation) compared to the ISNCSCI scale rated 2–28 (C2 through S4-S5) using Spearman’s ρ testing.

DISCUSSION

Bartonek et al.¹⁴ described six scales used to classify motor function of individuals with spina bifida. These scales were published by Sharrard,²⁵ Hoffer et al.,¹⁰ Lindseth,²⁶ Broughton et al.,²³ Ferrari et al.,²⁷ and McDonald et al.^15,28 Our study, however, is, to our knowledge, the largest study to examine the relationships between commonly used neurologic impairment scales and ambulation status in adults with spina bifida. Our findings were consistent with our hypothesis in that each of the four neurologic impairment scales we tested was significantly inversely correlated with Hoffer ambulatory status.

Several lessons were learned about application of these neurological scales. First, because both interpretations of the NSBPR impairment scale (muscle strength 1/5 or greater and 3/5 or greater) were highly correlated with ambulatory status (r_s = −0.716 and r_s = −0.763, respectively), some variation in a clinician’s or researcher’s measurement of muscle strength may be acceptable when using it to predict ambulatory ability. Second, our findings show that the nine-point Broughton scale was only slightly more correlated (r_s = −0.771) than each interpretation of the NSBPR scale, although it uses almost twice as many muscle strength tests. A disadvantage of the Broughton scale is that it uses many muscle groups that can be difficult to test in a busy clinical setting. For example, it may not be clinically practical to test differences in medial and lateral hamstring strength. However, in the Broughton scale, varying strength in these muscles results in a classification of different motor levels. Third, the ISNCSCI motor scale, while being by far the most comprehensive, had the lowest correlation with ambulatory status of any scale (r_s = −0.565). This is likely due to the fact that the scale defines motor level as the most caudal segment graded as 3/5 or 4/5, with all others that are rostral graded as intact, or 5/5. Under these criteria, patients may be labeled as having a higher level of injury, even when distal strength is sufficient to allow for ambulation. Taken together, these results indicate that a simpler scale may be just as good or better at assessing mobility potential in this population than a more comprehensive scale. Using a simpler scale would allow clinicians to more quickly determine functional lesion level and to ensure more accurate correlative ability regarding Hoffer ambulatory status.

Several limitations in this study deserve discussion. First, because of the retrospective nature of this study and limitations in testing certain muscle groups, data needed for neurological classification were sometimes not available. Therefore, substitutions of testable muscle groups had to be made for classification in the Broughton and ISNCSCI scales. Gluteus medius and gluteus maximus are both innervated by L5 and S1.²⁹ Substitution of hip abduction for extensor hallucis longus may have resulted in some individuals being classified as L5 on the ISNCSCI scale who otherwise would have been classified as S1. Likewise, some individuals lacking data on gluteus maximus strength may have been classified as S2 on the Broughton scale when they otherwise would have been classified as S1. A second limitation was that multiple examiners performed the muscle testing. This may have introduced some interrater variability. However, the clinic is run by a single supervising attending physiatrist who independently conducted or verified all physical examinations throughout the duration of the study. Third, our study focused only on motor function. The ISNCSI impairment scale includes a sensory component. We did not incorporate sensory testing because most scales used in spina bifida focus only on motor function, presumably because sensory function is sometimes used in spinal cord injury rehabilitation as a predictor of motor recovery, which is not expected in a congenital condition such as spina bifida. In addition, sensory information can often be difficult to assess in some individuals with spina bifida because of cognitive impairment and would have added additional interrater variability. Nevertheless, future studies could investigate whether adding sensory testing improves ability to predict ambulatory function. Fourth, the low sensitivity of the Hoffer ambulation scale may limit the reliability of the correlations; however, this is the most commonly used scale for classification of ambulatory status in patients with spina bifida.¹⁰ Finally, our sample size consisted of a large majority of white, non-Hispanic/non-Latino individuals; therefore, the results of this study should be applied with discretion to populations with differing demographic characteristics.

As more data become available from adults with spina bifida, especially with the growth of the National Spina Bifida Patient Registry,²² further studies should examine the precision of neurologic impairment scales. Determining which components of the scales are most clinically useful and finding a way to streamline the functional assessment of these patients could maximize the utility of information collected in the clinic and in research. Development of a standardized, easy-to-use neurologic impairment scale could give clinicians and researchers better ability to assess functional neurologic level of lesion for patients with spina bifida and could better predict their future ambulatory outcomes.

CONCLUSIONS

Multiple neurologic impairment grading scales can be used to measure motor function in adult patients with spina bifida. Although the Broughton classification seems to be the most highly correlated with ambulation status, the less comprehensive NSBPR scale is also highly correlated and may be easier to administer in a busy clinical setting. The development of a simple and representative neurologic impairment scale would assist physicians’ efforts remarkably in predicting future ambulatory status among patients with spina bifida.

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CME Objectives:

Upon completion of this article, the reader should be able to: (1) Explain the clinical significance of identifying ambulation status and maximizing ambulation potential in adults with spina bifida; (2) Describe each of the neurologic grading scales examined in this study, identifying potential shortcomings in applying them to the adult spina bifida population; and (3) Administer the National Spina Bifida Patient Registry (NSBPR) impairment scale motor assessment in a standard adult spina bifida outpatient clinic visit.

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