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Abstract

PURPOSE:

To describe pulmonary function and determine the impact of neurological level, scoliosis, and obesity on pulmonary function in people with spina bifida (SB).

METHODS:

Participants with SB ( $N=$ 29) (15 females; age, 30 $\pm$ 12 years) completed spirometry and body plethysmographic lung volume testing. Univariate and multivariate regression analyses were used to describe the factors associated with pulmonary function in people with SB.

RESULTS:

Distribution of category of impairment in pulmonary function was: 55% ( $n=$ 16) restricted, 6.9% ( $n=$ 2) spirometric restricted, 1 combined obstructed and restricted, and 35.5% ( $n=$ 10) normal. In univariate analyses, neurological level was negatively associated with pulmonary function parameters, i.e., forced vital capacity (FVC) ( $p=$ 0.005), forced expiratory volume in 1 second (FEV ${}_{1}$ ) ( $p=$ 0.008), total lung capacity (TLC) ( $p=$ 0.001), and degree of scoliosis were inversely associated with FVC ( $p=$ 0.005), FEV ${}_{1}$ ( $p=$ 0.003), and TLC ( $p=$ 0.004). In multivariate models, level of lesion and degree of scoliosis independently contributed to the degree of lung function impairment. Restrictive pulmonary function was observed in 9/10 (90%) of those with thoracic neurological levels and was associated with decreased inspiratory capacity (IC) and expiratory reserve volume (ERV). Lumbar level lesions were associated with either normal lung function or an isolated reduction in FVC due to reduction in only ERV and preserved TLC representing spirometric restriction.

CONCLUSIONS:

High prevalence of restrictive pulmonary physiology is present in people with SB, with more rostral neurological levels and greater degree of scoliosis associated with a higher degree of pulmonary function impairment.

Keywords

Spina bifida myelomeningocele pulmonary function scoliosis neurological level restrictive lung disease total lung capacity wheelchair spirometry lung volume spirometric restriction mobility impairment

1. Background and purpose

Spina bifida results from failure or incomplete closure of the neural tube during embryogenesis; the estimated incidence in the United States is 3.50 per 10,000 live births [1]. Life-long mobility impairments result from myelomeningocele, the most severe form of spina bifida. Assistive devices (e.g., wheelchairs, braces, crutches) are often required to accommodate mobility impairments resulting from the denervation of the sensory and motor nerves at and below the spinal lesion. Spina bifida can also lead to secondary conditions that require collaborative multidisciplinary medical care, including hydrocephalus, Chiari II malformation, renal dysfunction, neurogenic bowel and bladder, neuromuscular scoliosis, lower extremity joint contractures, and pelvic obliquity [2, 3, 4]. The risk of obesity, hypertension, cardiovascular disease, metabolic syndrome, pulmonary complications, and sleep disordered breathing are also high [5, 6, 7, 8, 9, 10, 11].

In people with spina bifida, pulmonary dysfunction is understudied despite the fact that pulmonary complications are a source of morbidity and mortality in this population [12]; pneumonia (9%, $n=$ 7,760) and respiratory failure (7%, $n=$ 7,760) are the second and the third leading causes of mortality [12]. Further, 18–39 year olds with spina bifida were 3.2 times more likely to be hospitalized with pneumonia compared to people in the United States without disabilities [12]. Restrictive lung disease is a predisposing factor for pneumonia, impaired exercise tolerance, and poor quality of life [13].

Commonly occurring secondary conditions in people with spina bifida that could contribute to pulmonary impairment include scoliosis, obesity, denervation of the internal intercostal musculature (muscles that aid in inspiration), and denervation of the abdominal and external intercostal muscles (muscles that aid in expiration) [14].

Scoliosis may impact pulmonary function and increase the work of breathing in neuromuscular conditions through reduction of chest wall compliance, uneven lung expansion, and ineffective length-tension relationship of the respiratory muscles affecting their actions on the rib cage [15, 16]. Scoliosis (defined as Cobb angle $>$ 20 degrees) is prevalent in 52% of people with spina bifida age 10 and older [17]. Those with myelomeningocele who are non-ambulatory are more likely to develop scoliosis compared to people with spina bifida who are ambulatory [4, 18].

Obesity could also contribute to pulmonary restriction by reducing chest wall compliance and interfering with diaphragmatic excursion [14, 19]. Obesity is prevalent (35%) in adults with spina bifida [11, 14]. In addition, obesity increases the risk of cardiovascular disease, metabolic syndrome, hypertension, and sleep disordered breathing [6, 7, 8, 10].

Denervation of the inspiratory musculature of the thorax can reduce chest wall expansion resulting in a decrement in total lung capacity (TLC) and forced vital capacity (FVC) known as restrictive lung impairment [19]. Denervation of abdominal musculature can decrease cough effectiveness and impact expiratory reserve volume, contributing to a reduction in forced vital capacity (FVC). Reduction in FVC in the absence of TLC reduction is commonly termed spirometric restriction [20, 21, 22, 23]. Studies to understand pulmonary function in people with spinal cord injury have been completed [19, 24, 25, 26] however, there are a limited number of studies that have explored the pulmonary function of people with spina bifida. Sherman et al. found that 58% ( $n=$ 12) of ambulatory children with myelomeningocele age 10–17 who also used wheelchairs, crutches, or braces for mobility had restrictive lung disease [5]. In a retrospective study, (100%, $N=$ 32) children with myelomeningocele and scoliosis had reduced FVC that was unrelated to scoliosis; the impact of neurological level was not assessed. Prospective studies that include adults with spina bifida, especially those who are full-time wheelchair users, have not been conducted. Furthermore, the impact of level of spinal cord involvement on the lung volume partitions of inspiratory capacity (due to impairment in muscles of inspiration) and expiratory reserve volume (due to impairment in muscles of expiration) which in combination contribute to the restrictive impairment have not been evaluated.

The first aim of this study is to describe the pulmonary function of adolescents and adults with spina bifida based on the results of spirometry and plethysmographic lung volume testing. The second aim of this study is to determine the impact of neurological level of spinal injury, scoliosis, and obesity on the severity and pattern of lung function impairment through univariate and multiple regression analysis.

2. Methods

This observational cross-sectional study was conducted at a large university based laboratory. Following approval by the University of Pittsburgh Institutional Review Board, participants were recruited through flyer mailings, advertisements, and local pediatric and adult spina bifida clinics. All participants signed an informed consent. The inclusion and exclusion criteria for the parent study which also assessed upper extremity exercise capacity were published elsewhere [27].

Eligible participants were: (a) age 13–80 years, (b) diagnosed with spina bifida (not spina bifida occulta without neurological impairments), (c) had scoliosis, and (d) were unable to pedal a standard (two-wheel) bicycle. Potential participants were excluded if they had (a) a history of recent or acute cardiopulmonary conditions that precluded safety of exercise testing (e.g., myocardial infarction, pneumothorax, active pneumonia, or use of a ventilator), (b) a history of conditions that precluded safety of load incremented arm ergometry exercise stress testing (e.g., upper extremity injury, upper extremity or thoracic surgery in the last 6 months, loss of shoulder, elbow, and/or wrist range of motion), and (c) had a medical condition that would contraindicate arm exercise stress testing as indicated by a primary care physician. After the primary care physician’s written medical release was received, participants were scheduled for pulmonary function testing and arm ergometry exercise stress testing. This paper addresses the pulmonary function testing.

2.1 Outcome measures

During the visit, sociodemographic information, body composition, and functional mobility measures were gathered. Sociodemographic variables included race, gender and diagnosis. Body composition included weight, arm span, and body mass index (BMI). Weight was measured using a wheelchair accessible scale. Overestimation of BMI can occur with spina bifida patients who are more likely to have reductions in height due to scoliosis, pelvic obliquity, and lower extremity joint contractures. Therefore, arm span was used as a proxy for height in the BMI formula (kg/m ${}^{2}$ ) [6, 28, 29].

A medical chart review was also conducted dating back to the first entry for each participant in order to document a history of comorbid conditions associated with spina bifida that may affect breathing including Chiari II malformation, sleep apnea, and primary lung conditions such as pneumonia. Neurological level was calculated from physical exam findings using the American Spinal Injury Association Impairment Scale (AIS): International Standards for Neurological Classification of Spinal Cord Injury [30, 31]. Cobb angle [32] was calculated from scoliosis radiographs. When scoliosis was too severe for an angle to be calculated, scoliosis was categorized as “severe”. When no radiograph was available (31%, $n=$ 9), scoliosis was categorized as mild, moderate, or severe based on physical exam notes.

Pulmonary function testing was completed by experienced respiratory technicians using a SensorMedics V6200 Vmax Auto Box Respiratory Analyzer (SensorMedics Corporation, Yorba Linda, CA). Pulmonary function measures were conducted at the University of Pittsburgh Emphysema COPD Research Center. The data collection procedures were defined prior to the start of the study and data were recorded in a protocolized manner. Pulmonary function testing (i.e., spirometry and body plethysmography determination of lung volumes) was completed according to the American Thoracic Society and European Respiratory Society Task Force (ATS/ERS) pulmonary function standards and interpreted using standard prediction equations by an experienced pulmonologist (FS) [33, 34, 35, 36]. Arm span was used as a proxy for height in the calculation of predicted values [5]. As reported in the parent study publication, participants also completed incremental arm ergometry testing [27].

2.2 Analysis

Test results were classified as restriction, spirometric restriction, normal, or mixed (obstructed and restricted). Restrictive lung disease was defined as TLC $<$ 80% with a FEV ${}_{1}$ /FVC ratio $\geqslant$ 0.70 [37]. Spirometric restriction [20, 21, 38] was defined at TLC $>$ 80% and FVC $<$ 80%. Mixed obstructive/restrictive lung disease was defined as a FEV ${}_{1}$ /FVC ratio $<$ 0.70 with TLC $<$ 80%. Notably for the category within this manuscript, we have defined spirometric restriction exclusively as the finding of a reduced FVC and normal FEV ${}_{1}$ /FVC without a reduction in TLC, although the term has been used in the literature with or without the TLC limitation. An editorial in the European Respiratory Journal by a notable pulmonary function expert [38] highlighted that the clinical correlates in the group with this pattern historically have been poorly defined.

Table 1
Sociodemographic and disease characteristics of individuals with spina bifida

	Total group
	( $N=$ 29)
	$n$ (%)
Age (mean/SD)	30.48 (12.5)
Gender
Female	15 (51.7)
Male	14 (48.3)
Race
Caucasian	26 (89.7)
Black or African American	3 (10.3)
Diagnosis
Myelomeningocele	26 (89.7)
Lipomyelomeningoele	2 (6.9)
Sacral agenesis	1 (3.4)
Mobility assistive equipment
Orthotics and/or cane, crutches and/or walker	4 (13.8)
Ultralight manual wheelchair	23 (79.3)
Power wheelchair	2 (6.9)
Smoking history
Non-smoker	23 (79.3)
Current smoker	2 (6.9)
Past smoker	4 (13.8)
Living arrangement
Lives at home with family	13 (44.8)
Lives in own home	1 (3.4)
Lives in apartment	12 (41.4)
Lives in supportive group home with peers	3 (10.3)
Hours of weekly assistance for ADL’s/IADLs	13.6 (20.5)
(mean/SD)
Vocation
Not working, volunteering or going to school	11 (37.9)
Working part-time volunteering, or going to school	9 (31.0)
Working full-time volunteering, or going to school	9 (31.0)
Neurological level*
Thoracic level (T12 above)	19 (65.5)
Lumbosacral level (L1 to S1)	10 (34.5)
Scoliosis**
$<$ 19 degrees or mild	18 (62.1)
20–45 degrees or moderate	3 (10.3)
$>$ 45 degrees or severe	8 (27.6)

Key: $N$ : total sample size, %: percentage, SD: standard deviation, ADLs/IADLs: activities of daily living/instrumental activities of daily living. Note: *Neurological level measured was by American Spinal Injury Association Impairment Scale. **Scoliosis was measured by Cobb angle or medical record report of mild, moderate, or severe scoliosis.

Body mass index was classified into four categories: Underweight ( $<$ 18.5 lbs.), normal (18.5–24.9 lbs.), overweight (25–29.9 lbs.), and obese ( $>$ 30 lbs.), then treated as an ordinal variable in regression analysis. Neurological level was treated as a binary variable (thoracic versus lumbosacral) in the regression analysis. To describe scoliosis, the Cobb angle of scoliosis was classified into three clinically relevant groups based on previous literature [4, 17, 39]: 1) scoliosis $<$ 19 degrees or medical record reporting mild scoliosis, and 2) scoliosis 20 to 45 degrees or medical record reporting moderate scoliosis, 3) scoliosis $>$ 45 degrees or medical record reporting severe scoliosis. Scoliosis was treated as a binary variable in the regression analysis (mild versus moderate versus severe scoliosis).

Statistical analyses were performed using IMB SPSS version 22.0 for Windows (IBM Corporation, Armonk, NY, USA). Alpha was set at $p\leqslant$ 0.05 a priori. To describe the pulmonary function of this cohort, the percentage of people classified with pulmonary conditions was calculated. Medians and interquartile ranges were calculated for spirometry and lung volume variables for all participants as well as restricted and normal groups. The mean was calculated for the spirometrically restricted participants. A histogram was created to demonstrate the partitioning of lung volumes including the impact on TLC and its components IC and ERV for the general population and for those with lumbosacral and thoracic neurological level lesions.

Univariate analyses using Spearman’s rho were conducted to analyze the relationship between pulmonary function measures (i.e., FVC, FEV ${}_{1}$ , TLC) and conditions in spina bifida that could alter lung function (i.e., BMI, neurological level, scoliosis). Box plots of group means for FEV ${}_{1}$ , FVC, TLC, expiratory reserve volume (ERV), inspiratory capacity (IC) and residual volume (RV) based on degree of scoliosis and neurological level are presented. Multiple linear regression analysis was used to determine the most significant predictors (i.e., BMI, neurological level, and scoliosis) of the dependent variables (i.e., FVC, FEV ${}_{1}$ , and TLC) and to develop significant regression models for each. Variable selection was performed using backwards elimination. The independent variables (i.e., BMI, scoliosis, and neurological level) were entered into the model for FVC. A similar process was followed for FEV ${}_{1}$ and TLC. The backward regression variables were eliminated according to the one that had the least contribution based on R ${}^{2}$ . The final model was chosen when the overall model was significant. Models adjusted for age and gender did not influence the significance of scoliosis and neurological level in the models (data not shown).

Table 2

Results of pulmonary function tests for all participants by type of lung condition

	By type of lung condition					All participants
	Normal ( $n=$ 10)		Restricted ( $n=$ 16)		SR ( $n=$ 2)	( $n=$ 29**)
	Median	IQR	Median	IQR	Mean*	Median	IQR
SPIROMETRY
FVC (%)	102.5	94.0–114.5	53.5	42.8–72.3	72.5	75.0	49.0–97.5
FEV ${}_{1}$ (%)	105.5	93.5–117.5	52.0	44.3–68.8	78.5	69.0	49.5–98.5
FEV ${}_{1}$ /FVC ratio (%)	86.0	81.5–93.3	84.0	80.5–97.3	86.0	84.0	80.0–94.0
FEF 25%–75% (%)	103.0	92.8–121.3	53.5	39.0–70.3	92.5	71.0	48.5
PEF (liter/sec)	6.5	5.5–9.6	4.0	2.6–5.9	5.2	5.22	103.0
PIF (liter/sec)	2.5	1.5–3.7	1.7	1.3–2.7	2.28	1.85	1.3–2.8
MVV (liter/minute)	103.95	95.0–143.6	63.9	41.6–79.8	90.5	80.15	54.1–102.6
Lung volumes
FRC (%)	102.0	62.8–123.8	60.0	52.5–72.3	102.0	66.0	57.0–91.5
IC (%)	115.5	107.5–120.0	59.5	39.3–85.5	72.0	84.0	56.0–113.0
TLC (%)	108.0	92.0–116.0	61.5	50.8–74.5	86.5	76.0	60–92.5
ERV (%)	64.5	36.3–18.3	18.0	9.5–38.5	61.5	34.0	14.5–64.5
RV (%)	107.0	73.5–133.3	86.0	74.3–10.3	114.0	92.0	76.5–117.0
RV/TLC ratio (%)	24.0	17.8–31.5	36.5	29.0–45.5	38.5	33.0	24.5–39.0

Key: FVC: forced vital capacity; FEV ${}_{1}$ : forced expiratory volume in one second; FEV ${}_{1}$ /FVC: the ratio of forced expiratory volume in one second over forced vital capacity; FEF 25%–75%: maximum expiratory flow over the middle 50% of the vital capacity; PEF: peak expiratory flow; PIF: peak inspiratory flow; MVV: maximal voluntary ventilation, calculated from FEV ${}_{1}$ $\times$ 35; FRC: functional residual capacity; IC: inspiratory capacity; TLC: total lung capacity; ERV: expiratory reserve volume; RV: residual volume; RV/TLC: the ratio of residual volume over total lung capacity; SR $=$ Spirometrically restricted. *Mean presented for spirometrically restricted participants due to $n=$ 2 in each row. ** $n=$ 1 patient combined obstructive/restrictive not included in table. Values for $n=$ 1 were as follows: TLC $=$ 72, FEV ${}_{1}$ $=$ 55, FVC $=$ 75, RV $=$ 99, FEV ${}_{1}$ /FVC $=$ 67.

Table 3

Distribution of restricted versus non-restricted participants classified by level of lesion, scoliosis and body mass index

	Neurological level*		Scoliosis**			Body mass index***
	( $N=$ 29)		( $N=$ 29)			( $N=$ 29)
	Thoracic	Lumbo-sacral	$<$ 19 deg.	20–45 deg.	$>$ 45 deg.	Under weight	Normal	Overweight	Obesity
			or mild	or moderate	or severe	( $<$ 18.5)	(18.5–24.9)	(25–29.9)	( $>$ 30)
$n$ (%)	( $n=$ 10)	( $n=$ 19)	( $n=$ 18)	( $n=$ 3)	( $n=$ 8)	( $n=$ 5)	( $n=$ 13)	( $n=$ 5)	( $n=$ 6)
PFTs ( $N=$ 29)
Normal ( $n=$ 10)	1 (3.4%)	9 (31%)	8 (27.5%)	1 (3.4%)	1 (3.4%)	1 (3.4%)	5 (17.2%)	1 (3.4%)	3 (10.3%)
Restricted ( $n=$ 16)	9 (31%)	7 (24.1%)	8 (27.5%)	1 (3.4%)	7 (24.1%)	3 (10.3%)	6 (20.7%)	4 (13.8%)	3 (10.3%)
Spirometric restricted	0	2 (6.9%)	1 (3.4%)	1 (3.4%)	0	1 (3.4%)	1 (3.4%)	0	0
( $n=$ 2)
Combined restricted	0	1 (3.4%)	1 (3.4%)	0	0	0	1 (3.4%)	0	0
obstructed ( $n=$ 1)

Key: PFTs – Pulmonary condition or normal based on pulmonary function tests; deg. $=$ degree; $n=$ frequency; % $=$ percentage. *Neurological level measured using American Spinal Injury Scale **Scoliosis measured by Cobb angle or medical record report of mild, moderate or severe scoliosis. ***Body mass index calculated using kg/m ${}^{2}$ formula, substituting arm span for height.

3. Results

3.1 Characteristics of participants

Participants were 29 individuals (15 females; mean $\pm$ SD, 30 $\pm$ 12; range 17–71) with spina bifida (Table 1). Sociodemographic information and assistive device use are described in Table 1. Two participants were adolescents, age 17. A manual wheelchair ( $n=$ 19, 79%) or power wheelchair ( $n=$ 2, 7%) was the primary mobility-assisted equipment used by the majority of participants. Nearly 90% of participants were diagnosed with myelomeningocele (Table 1). The results of the medical chart review showed that 41% ( $n=$ 12) had Chiari II malformation and of those 4/12 had Chiari II surgery, 31% ( $n=$ 9) underwent spinal fusion, 17% ( $n=$ 5) had sleep apnea and 48% ( $n=$ 14) had past conditions (i.e. pneumonia, bronchitis, pleural effusion) that often occurred following surgery. Participants’ neurological levels ranged from T7 to S1; 34% ( $n=$ 10) had thoracic neurological levels and 65% ( $n=$ 19) had lumbosacral neurological levels (Table 1).

Table 4
Univariate linear regression analysis (each variable was included separately in the regression model), $N=$ 29

DVs*	Predictor	R-squared	Unstandardized coefficients B (SE)	$t$	$p$ -value**
FVC (%)	BMI	0.006	2.28 (5.4)	0.42	0.676
	Neurological level	0.257	$-$ 30.00 (9.9)	$-$ 3.06	0.005**
	Scoliosis	0.257	$-$ 16.16 (5.3)	$-$ 3.06	0.005**
FEV ${}_{1}$ (%)	BMI	0.010	2.89 (5.5)	0.53	0.603
	Neurological Level	0.230	$-$ 28.94 (10.2)	$-$ 2.84	0.008**
	Scoliosis	0.278	$-$ 17.18 (5.3)	$-$ 3.23	0.003**
TLC (%)	BMI	0.007	2.04 (4.6)	0.44	0.660
	Neurological level	0.330	$-$ 29.02 (7.9)	$-$ 3.65	0.001**
	Scoliosis	0.265	$-$ 14.00 (4.5)	$-$ 3.124	0.004**

Key: %: percent; DVs: dependent variables; SE: standardized error; FVC: forced vital capacity; FEV ${}_{1}$ : forced expiratory volume in one second; TLC: total lung capacity. *All three DVs (FVC/FEV ${}_{1}$ /TLC) are highly correlated. ** $p<$ 0.05 is significant.

Table 5

Final model using multiple linear regression analysis, $N=$ 29

DVs	Predictor	Unstandardized coefficients B (SE)	$t$	$p$ -value
MODEL 1: FVC $=$ 89.06 $+$ ( $-$ 23.52 $\times$ Neurological Level) $+$ ( $-$ 19.23 $\times$ Scoliosis)
FVC (%)	(Constant)	89.06 (6.03)	14.77	$<$ 0.0001*
	Neurological Level	$-$ 23.52 (9.86)	$-$ 2.39	0.025*
	Scoliosis	$-$ 19.23 (9.66)	$-$ 1.99	0.057
MODEL 2: FEV ${}_{1}$ $=$ 89.21 $+$ ( $-$ 21.93 $\times$ Neurological Level) $+$ ( $-$ 20.79 $\times$ Scoliosis)
FEV ${}_{1}$ (%)	(Constant)	89.21 (6.22)	14.33	$<$ 0.0001*
	Neurological Level	$-$ 21.93 (10.18)	$-$ 2.15	0.041*
	Scoliosis	$-$ 20.79 (9.97)	$-$ 2.08	0.047*
MODEL 3: TLC $=$ 92.22 $+$ ( $-$ 24.01 $\times$ Neurological Level) + ( $-$ 14.85 $\times$ Scoliosis)
TLC (%)	(Constant)	92.22 (4.91)	18.76	$<$ 0.0001*
	Neurological Level	$-$ 24.01 (8.04)	$-$ 2.98	0.006*
	Scoliosis	$-$ 14.85 (7.87)	$-$ 1.89	0.070

Key: %: percent predicted; DVs: dependent variables; SE: standardized error; FVC: forced vital capacity; FEV ${}_{1}$ : forced expiratory volume in one second; TLC: total lung capacity. * $p<$ 0.05 is significant.

The distribution of category of pulmonary impairment for the cohort ( $n=$ 29) was as follows: 55% ( $n=$ 16) restriction, 7% ( $n=$ 2) spirometric restriction, one combined obstruction/restriction, and 36% ( $n=$ 10) non-restricted (normal). Restrictive pulmonary function was observed in nine of ten (90%) people who had thoracic level lesions of T11 or higher. The spirometry and lung volume results for the normal, restricted, spirometrically restricted, and overall group are presented in Table 2. The presence or absence of pulmonary impairment by neurological level, degree of scoliosis, and body mass index is presented in Table 3. Individuals with thoracic level lesions had substantial restriction (reduced TLC) and reduction in FVC, likely resulting from an impact on the muscles of inspiration (impacting inspiratory capacity, IC) and/or abdominal muscles of expiration (impacting expiratory reserve volume, ERV). Lumbar level lesions resulted in more mild reductions in TLC and on 2 occasions isolated FVC reduction (spirometric restriction), most likely due to isolated impact on the abdominal muscles of expiration impacting ERV but not IC (Fig. 1).

Figure 1.

Spirometry and pulmonary function outcomes for people with spina bifida with lumbosacral and thoracic neurological level compared to predicted normal total lung capacity. Key: TLC $=$ total lung capacity, Normal $=$ people without disabilities, FRC $=$ functional residual capacity, RV $=$ residual volume, ERV $=$ expiratory reserve volume, IC $=$ inspiratory capacity, Normal $=$ people without disabilities, Lumbosacral $=$ lumbosacral neurological level, Thoracic $=$ thoracic neurological level. Individuals with thoracic level lesions had substantial reduction in TLC and FVC (i.e. restriction) resulting from both an impact on the muscles of inspiration (impacting inspiratory capacity, IC) and abdominal muscles of expiration (impacting expiratory reserve volume, ERV). However, lumbar level lesions resulted in less impact on TLC and more isolated impact on the abdominal muscles of expiration impacting ERV and FVC.

Univariate analysis showed a significant inverse correlation between level of lesion and scoliosis and all pulmonary metrics, FEV ${}_{1}$ , FVC, and TLC (Table 4). Box plots demonstrate that a more severe impairment in all lung function measures was observed in patients with thoracic compared to lumbar level lesions; further, scoliosis negatively and independently impacted lung function (i.e., FEV ${}_{1}$ , FVC, TLC, ERV, IC, and RV) (Fig. 2).

Figure 2.

Box plots of group means of PFT’s in people with spina bifida with mild or moderate/severe scoliosis coupled with lumbosacral or thoracic neurological level. Box Plots of lung function parameters demonstrate more severe impairment in all measures in patients with thoracic vs. lumbar neurological level lesions and indicate that scoliosis severity results in an independent impact on lung function that compounds the pulmonary impairment for any neurological level. Key: FVC $=$ Forced Vital Capacity, TLC $=$ Total Lung Capacity, FEV ${}_{1}$ $=$ Forced Expiratory Volume in 1 Second, ERV $=$ expiratory reserve volume, IC $=$ inspiratory capacity, and RV $=$ residual Volume. For all box plots graph labels defined as: Mod/Severe-Lumbosacral $=$ moderate to severe scoliosis and lumbosacral neurological level. Mild-Lumbosacral $=$ mild scoliosis and lumbosacral neurological level. Mod/Severe-Thoracic $=$ moderate to severe scoliosis and thoracic neurological level, Mild-Thoracic $=$ mild thoracic scoliosis with thoracic neurological level.

In multiple linear regression models for FEV ${}_{1}$ , FVC and TLC, both neurological level and scoliosis contributed to the models with $p$ -values that were significant or strongly trending toward significance. Results of the final models for FEV ${}_{1}$ , FVC, and TLC are reported in Table 5. BMI was removed from all three models during the univariate variable selection process. For FEV ${}_{1}$ , the overall model including the two predictors was significant, $F(1,25)=$ 6.706, $p=$ 0.004, with $R^{2}=$ 0.340 and adjusted $R^{2}=$ 0.290. People with lesions at the thoracic level had FEV ${}_{1}$ % of predicted values that were 22 points lower than people who had lesions at the lumbosacral level ( $\beta=$ $-$ 21.93, $t=$ $-$ 2.15, $p=$ 0.041). For patients with moderate (20–45 degrees) to severe ( $<$ 45 degrees) scoliosis, their FEV ${}_{1}$ % of predicted values were 21 points lower than the FEV ${}_{1}$ for patients with mild ( $<$ 19 degrees) scoliosis ( $\beta=$ $-$ 20.79, $t=$ $-$ 2.08, $p=$ 0.047). For FVC, the overall model was significant $F(1,25)=$ 7.17, $p=$ 0.003, with $R^{2}=$ 0.356 and adjusted $R^{2}=$ 0.306. People with lesions at the thoracic level had FVC% of predicted values that were 23 points lower than people who had lesions at the lumbosacral level ( $\beta=$ $-$ 23.52, $t=$ $-$ 2.38, $p=$ 0.025). For patients with moderate to severe scoliosis, FVC% of predicted values were 19 points lower than for people with mild scoliosis ( $\beta=$ $-$ 19.23, $t=$ $-$ 1.99, $p=$ 0.057). For TLC, the overall model was significant $F(1,25)=$ 9.08, $p=$ 0.001, with $R^{2}=$ 0.411 and adjusted $R^{2}=$ 0.366. People with lesions at the thoracic level had TLC% of predicted values that were 24 points lower than people who had lesions at the lumbosacral level ( $\beta=$ $-$ 24.01, $t=$ $-$ 2.98, $p=$ 0.006). For those with moderate to severe scoliosis, TLC % of predicted values were 15 points lower than for those with mild scoliosis ( $\beta=$ $-$ 14.85, $t=$ $-$ 1.86, $p=$ 0.070).

4. Discussion

4.1 Review of findings

Restrictive lung impairment is common in patients with spina bifida, with 90% of patients who have lesions at the thoracic level experiencing restrictive lung physiology. Neurological level (more rostral lesions) and scoliosis were significantly related to FVC, FEV ${}_{1}$ and TLC in a univariate model and were independent contributors to overall significant regression models for FVC, FEV ${}_{1}$ , and TLC (Table 5, Figs 1 and 2). These findings suggest that restrictive lung impairment results from loss of inspiratory and expiratory musculature as well as the mechanical distortion of the chest wall associated with scoliosis.

4.2 Comparison of study findings to literature

The findings from this study (55% restricted, 7% spirometrically restricted, $N=$ 29) support and further extend the observations of Sherman et al. That study reported that 58% ( $N=$ 12) of ambulatory children with myelomeningocele and scoliosis who used wheelchairs, braces or crutches on a part-time basis had pulmonary restriction [5]. Both studies followed similar testing methods including use of arm span as a proxy for height [5]. Both studies also had a limited sample size [5]. In contrast to Sherman’s and other studies in people with spina bifida [5, 40], the present study included primarily adult wheelchair users and provided a richer description of factors that were related (neurological level, scoliosis) and unrelated (body mass index) to pulmonary restriction. The present study further described the impact of factors on inspiratory and expiratory partitioning of lung volume.

The findings of level of lesion and scoliosis as predictive factors for pulmonary function were theorized to be true based on past literature [4]. The high prevalence of restriction in people with thoracic spinal lesions and the strong significant relation of neurological level with pulmonary metrics (i.e., FEV ${}_{1}$ , FVC and TLC) were consistent with the spinal cord injury literature. According to a study by Linn et al. similar to the present study, the higher the neurological level in spinal cord injury, the greater the reduction in FVC and FEV ${}_{1}$ [41]. Based on the spinal cord injury literature it is likely that in our participants who had paraplegia (i.e., highest neurological level was T7), neuromuscular weakness of the lateral external intercostal, rectus abdominis, external oblique, internal oblique, and transverse abdominis muscles reduced FEV ${}_{1}$ , FVC and TLC [19]. Further, in people with traumatic spinal cord injury, a more caudal injury is known to be associated with less impaired respiratory function compared to a more rostral injury [19, 42]. One study in participants with spinal injury and neurological levels ranging from C5 to T11 ( $N=$ 20), demonstrated that those with lower thoracic neurological levels had better lung function values than those with higher thoracic and cervical injuries [43]. Similarly, participants with spina bifida from this study with higher neurological levels had lower lung function, namely that those with thoracic neurological levels had more considerable restriction as indicated by reduced TLC. Based on our findings, neurological level appears to play the strongest role in pulmonary restriction in people with spina bifida. Based on these findings, clinicians may consider referring people with higher neurological level for baseline pulmonary function testing and routine monitoring by a pulmonologist.

The combined effect of scoliosis with neurological level should also be considered in the treatment of spina bifida based on the results from this and other studies [15]. Individuals with neurologic conditions like spina bifida are at greater risk for hospitalization from respiratory infections including pneumonia and bronchitis. Those with co-occurring conditions like scoliosis have the highest rates of hospitalizations from respiratory infections [13]. Therefore, understanding the relationship between pulmonary function and scoliosis could have lifelong health implications for people with spina bifida. For children with spina bifida, decisions for the treatment of neuromuscular scoliosis are often based on preventing decline of respiratory function (FVC falling below 40%); spinal fusion is an option [4]. For adults, surgical intervention would be less likely as growth has stopped, fixed spinal deformities may have developed, and spinal fusion surgery may have been completed as a child (e.g., 31%, $n=$ 29 had spinal fusion in this study). Current conservative treatment options for adults to improve functional limitations include a thoracolumbar support orthosis with abdominal cutout, physical therapy for sitting balance, range of motion, posture, energy conservation, as well as pain management through a physiatrist. Wheelchair seating system modifications and customizations can be determined by a multidisciplinary team (i.e., therapist, physiatrist, assistive technology provider) [4]. Studies have indicated that scoliosis can have other effects on respiration that would be important to consider, including an association with reduced TLC especially in curves $>$ 70 degrees, reductions in expiratory flow due to mechanical changes (i.e., vertebral rotation leading to lateral shift of ribs and sternum that compresses the lung) and a weakened diaphragm resulting from abnormal rotational forces in the thorax [44]. Indeed, this study confirmed a significant inverse association of scoliosis with TLC ( $p=$ 0.004) (Table 4), showing that TLC% predicted was about 15 points lower for scoliotic curves that were moderate to severe than for those with mild scoliosis (Table 5). Scoliosis severity had an independent impact that compounded the pulmonary impairment at any neurological level (Fig. 2).

Contrary to this study, Patel et al. found no association of scoliosis with pulmonary restriction [45]. One explanation could be that the retrospective nature of their study did not allow for examination of testing quality, and that their study included only spirometry but not plethysmographic lung volume testing. In addition, all the participants were children compared to our cohort who were primarily adults. Although age could have been a factor, we found that the regression models were not affected by age. Another reason for the difference in results could be that the present study included full-time wheelchair users. For people with spina bifida, a wheelchair seating system that lacks customized postural support could compound oxygen transport impairments by contributing to poor posture, fatigue of respiratory musculature, hindrance of chest wall and diaphragmatic excursion [4, 16, 45, 46]. The participants in this study used customized manual and power wheelchairs provided through a multidisciplinary assistive technology clinic involving a physiatrist, physical or occupational therapist and assistive technology certified wheelchair supplier, which is best practice for providing assistive technology [47]. Because best practice was followed for wheelchair provision in our participants, body position in the wheelchair would be less likely to contribute to pulmonary dysfunction.

We have further identified the impact of neurological level on the components of lung volume that contribute to restriction (Fig. 1). Individuals with thoracic level lesions had the greatest reductions in TLC and FVC related to substantial reduction in IC, most likely impacted by weakness in the muscles of inspiration as well as ERV impacted by the muscles of expiration, including the abdominal muscles. Lumbar level lesions, on the other hand, resulted in less impact on TLC due to more isolated impact on the abdominal muscles of expiration impacting ERV but not impacting IC (Fig. 1). In fact, two patients with lumbar lesions had spirometric restriction represented by isolated reduction in FVC with preserved TLC which is consistent with isolated impact on the muscles of expiration but not inspiration. This is particularly notable since the underlying mechanisms resulting in spirometric restriction are not fully understood [38, 48]. The observation of this spirometry pattern in only low level spinal defects supports an etiology of isolated expiratory muscle impairment as a clinical condition resulting in this pattern of lung function impairment, thus clarifying the gap identified in the Enright editorial [35].

4.3 Strengths and implications

This study was the first to measure pulmonary function in a diverse sample that included mostly adult (93%) wheelchair users (86%) from a wide age range (17–71 years) with spina bifida. We further advance the field by defining the independent pathogenic contributions to pulmonary impairment in SB. In addition, we offer a more granular understanding of the mechanisms leading to restrictive lung impairment in spina bifida by describing the plausible associations between neurological level and impairments in the inspiratory and expiratory lung volume partitions.

4.4 Limitations

The study results primarily apply to a population of wheelchair users with spina bifida. This more neurologically involved population may not be representative of the broader population of people with spina bifida who have comparatively more functional impairment. In fact, this study included 44% ( $n=$ 13) individuals who lived at home with family and 38% ( $n=$ 11) who were not working, attending school, or volunteering. The sample size was small and some of the $p$ values of the independent variables in the multiple regression analysis did not firmly reach 0.05; however, the direction consistently trended toward significance, and the overall models were significant. Another weakness is that the lack of availability of radiographs for all participants and measurement errors due to differences in how the Cobb angle is measured may have impacted our results. However, physical examination is known to be a reliable and sensitive method for detecting thoracic curves $>$ 20 degrees [49]. There were also two cases when, for example, the scoliosis was so severe with complex rotational components that radiologists were simply unable to measure Cobb angle. In addition, information was not gathered from the medical record regarding the flexibility of the curve. The scarcity of reliable measures for height, and thus the need to use arm length as a surrogate, may have also affected our calculation of BMI. Although we described the impact of central respiratory impairments secondary to Chiari II malformation, the description of the prevalence provided for this cohort tells us only a part of the story.

4.5 Clinical implications

Clinicians who are treating a person with thoracic level spina bifida and scoliosis for a musculoskeletal condition, or for physical deconditioning, should be aware that the risk of pulmonary dysfunction is high. Clinicians can estimate the likelihood of pulmonary restriction in their patients using the regression equations developed in this study. Referral to a pulmonologist may be warranted. A relevant treatment aspect to these observations is that pulmonary restriction could be amenable to treatment with respiratory muscle strength training (RMT) [16, 50, 51, 52, 53]. Studies in persons with spinal cord injury have shown that RMT which included resisted breathing weight lifting or normocapnic hyperpnea, showed trends for improving expiratory muscle strength and vital capacity [54]. In persons with neuromuscular disorders (i.e., Duchenne’s muscular dystrophy) inspiratory RMT improved postoperative FVC; in addition, RMT conducted and controlled through video games improved lung function in this population [55, 56].

4.6 Future studies

Future directions should include investigation into the effects of wheelchair positioning and standers on pulmonary function in people with spina bifida. Ideally, studies that utilized radiographs should use standardized positioning and calculation of Cobb angles, with one radiologist completing the measures to reduce measurement error. Kyphosis measurements should also be included, based on the strong significant inverse association found between kyphosis and FEV ${}_{1}$ and FVC by Patel et al. Future studies should investigate whether BMI based on arm span is an accurate measure of body composition for the spina bifida population by comparing BMI based on arm span to Dual-energy X-ray absorptiometry or doubly labeled water in people with spina bifida. Further, pulmonary function measures could be conducted in this population before and after surgeries requiring anesthesia, as justified by our medical chart review revealing that various primary pulmonary conditions developed post-surgically. Finally, future studies should examine the effect of Chiari II malformation on central respiratory drive and associated disability in people with spina bifida.

5. Conclusion

Pulmonary restriction was common in this cohort of people with spina bifida, with more rostral neurological levels associated with a higher degree of pulmonary function impairment than more caudal levels; restrictive pulmonary impairment was observed in the majority (90%, $n=$ 9) of those with thoracic neurological levels. Neurological level and degree of scoliosis were significantly negatively associated with FVC, TLC and FEV ${}_{1}$ in univariate analyses. Level of lesion and degree of scoliosis independently contributed to degree of lung function impairment in multiple regression models. Finally, more caudal spinal involvement tends to be associated with reductions in ERV but not with IC when compared to more rostral level lesions.

Footnotes

Acknowledgments

Funding for this study was provided by the Spina Bifida Association and Ashley Rose Foundation through the Spina Bifida Association Young Investigators Award. This paper is written in honor of Ashley Rose, the beloved daughter of Mr. and Mrs. Raymond and Linda Pitek who had spina bifida. Special thanks to Dr. Ann Spungen, James J. Peters Veterans Affairs Medical Center, Bronx, NY, for initial concept, Dr. Christina Zigler, Department of Physical Medicine and Rehabilitation, University of Pittsburgh School of Medicine, for assistance with statistical analyses and presentation of tables and Chad Karoleski at the University of Pittsburgh, Emphysema COPD Research Center for assistance with statistics and presentation of graphics.

Conflict of interest

The authors have no conflict of interest to report.

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Impact of neurological level and spinal curvature on pulmonary function in adults with spina bifida

Abstract

PURPOSE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Background and purpose

2. Methods

2.1 Outcome measures

2.2 Analysis

Table 1 Sociodemographic and disease characteristics of individuals with spina bifida

3.1 Characteristics of participants

Table 4 Univariate linear regression analysis (each variable was included separately in the regression model), N = 29

4.1 Review of findings

4.2 Comparison of study findings to literature

4.3 Strengths and implications

4.4 Limitations

4.5 Clinical implications

4.6 Future studies

5. Conclusion

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Sociodemographic and disease characteristics of individuals with spina bifida

Table 4
Univariate linear regression analysis (each variable was included separately in the regression model), $N=$ 29