Spina bifida and cardiorespiratory profile: the impact of leisure sport activities on physical fitness

Spinal dysraphism (SD), also called spina bifida (SB), is a general term that includes a spectrum of congenital multifactorial abnormalities derived from a maldevelopment of the ectodermal, mesodermal and neuroectodermal tissues between 17 and 30 days of fetal development [1‐3]. The severity of the disorder can range from completely asymptomatic to functionally impaired [4]. The commonest and severe form is the myelomeningocele (MMC), characterized by a dorsally opened spinal cord [3]; other conditions, such as myeloschisis, meningocele, lipomeningomyelocele, and tethered cord, may be usually less severe and are part of the closed type of SD, also called “occult.” This condition also correlates with cutaneous alterations, including hemangiomas, hypertrichosis, pigmentary nevi, pendulous fibroma, lipomas, dermal sinuses, and gluteal sulcus deviation [5]. These children also present Arnold-Chiari malformation (hypoplasia of the posterior cranial fossa and cerebellum, with associated hydrocephalus from obstruction of cerebrospinal fluid flow at the level of the third and fourth cerebral ventricles), paraplegia, “neurogenic” bowel and bladder, and, in some cases, hydrocephalus [6]. Furthermore, the 50% of them develop urinary tract infections (UTIs) [7] during the first 15 months of life [8]. In addition, it is important to remember that, during the third week of embryonic life, an ectodermal-derived structure called the “neural crest” differentiates, whose cells originate from the dorsolateral region of the neural tube, which in the case of spina bifida sufferers, as already mentioned, manifests a closure defect.

Depending on the type and level of the lesion, impairments related to deficits in cognition, motor function, and sensory function may arise [9, 10]. A systematic review conduct in 2014 provided a critical synthesis of physical fitness components and effects of exercise training on these components in individuals with SB: patients with SB have impaired cardiorespiratory endurance, muscle strength, body composition, and flexibility compared with healthy peers, and cardiorespiratory endurance and muscle strength components seem to improve with exercise training [11]. Poor cardiorespiratory endurance in childhood has been described as having important consequences for the development of cardiovascular disease in later life [12]. Moreover, moderate and high levels of cardiorespiratory fitness have been associated with lower risk of mortality from all-causes regardless of gender, age, and body composition [13]. Therefore, to prevent cardiovascular diseases and reduce mortality rates, it is crucial to enhance cardiorespiratory endurance in individuals with SB since early childhood. Furthermore, children and adolescents with spina bifida who use a manual wheelchair are less physically active and more sedentary than typically developing youth [14]; therefore, in addition to the main pathology, they are associated with a series of other co-morbidities that are the inevitable consequence of forced inactivity.

Aim of this study is to describe the cardiorespiratory characteristics of our cohort of patients with spinal dysraphism to evaluate any eventual alteration. Moreover, given the common origin of part of the neural tube with certain cardiovascular structures, as mentioned above, our research group considered it reasonable to carry out a cardiological study to rule out possible congenital heart diseases, such as abnormal origins of the coronary arteries or congenital cardiac outflow tract anomalies (conotruncal heart malformations), in the pediatric spina bifida patient population. These conditions should always be ruled out because they represent a contraindication to the practice of sporting activity, including leisure ones.

In the period between May 2022 and April 2023, we recruited patients afferent to the spina bifida and Malformative Uropathies Centre of the “Agostino Gemelli” University Polyclinic Foundation – IRCCS in Rome, in order to better assess cardiorespiratory function and bone mineral density profile.

The study protocol included:

The examination was carried out using “Hologic Discovery DXA” bone densitometer and the results analyzed using “Hologic Discovery DXA System” software (Hologic Inc., Mississauga, Ontario, Canada).

Thirty-four patients (15 females, 44.1%) affected by spinal dysraphism were enrolled in the period between May 2022 and April 2023. The median age of our sample was 18 years (12.0–22.2); 23 of them (67.6%) were affected by myelomeningocele (MMC) and 11 patients (32.4%) by lipomeningocele (LMC). The mean BMI was 24.3 (± 5.7) and it resulted pathological in 17 patients (50%). Twelve patients (35.3%) practiced physical activity with a median of 2 days (1.2–2.7) a week. The detailed characteristics of our sample are reported in Table 1.

All patients performed electrocardiography and echocardiography. One patient presented an altered ECG (right axis deviation) while no patients presented an altered echocardiography. In Tables 2 and 3 are detailed the results of those two exams.

Twenty-seven patients (79,4%) performed a Cardiopulmonary Exercise Test (CPET) that resulted pathological in all of them. All the patients presented a pathological VO₂ peak value, with a mean of 1191.0 (± 248.2); the mean VO₂/Kg peak was 20.2 (± 4.4) and the mean VO₂ peak % of the predict was 51.1 (± 7.8). The mean VO₂/BCM ratio was 60.7 (± 17.3) and the VO₂/FFM ratio was 29.3 (± 5.5) (Table 4).

The Body impedance assessment (BIA) has been performed in all patients and the results are reported in Table 5.

Thirty-one patients (91.2%) performed a DEXA scan. The mean BMC was 1.6 (± 0.4), the mean FM was 22.7 (± 10.2), the mean FFM was 35.4 (± 8.6), the mean FFM + BMC value was 37.0 (± 8.9) and the mean FM% was 36.6 (± 9.5).

For 27 patients the lumbar-rachides T-score was collected and its mean value resulted of − 2.0 (± 1.8). Osteopenia was diagnosticated in 10 patients (37.0%) and osteoporosis in 8 patients (29.6%) (Table 6).

In Table 7 is reported a comparison between patients performing physical activity and patients not performing physical activity. The only statistically significative difference was the median lumbar T-Score, lower in the group not performing physical activity (− 2 (− 3.8 ÷  − 1.3) vs − 0.6 (− 1.7 ÷  − 0.05); p = 0.009) (Fig. 1).

Patients with SB have several degrees of motor impairment which impacts on physical activity, depending, as reported, on the type and the level of neurological lesion.

In literature, there are few studies that evaluate the cardiological and respiratory profile and the bone mineralization status in patients with SB, especially about those who practice physical activity.

In a review published in 2018 [15], the bone fragility in patients with SB has been evaluated. The risk factors for the occurrence of fracture in SB include: high level of neurological involvement [16], hypomobility, the presence of hypercalciuria [17], and body mass index (BMI) values [18].

Computerized Bone Mineralometry has been the technique of choice for the measurement of bone mineral density (BMD) and, therefore, for the assessment of the presence of osteopenia and osteoporosis by detection of the T-score. A decrease in BMD is correlated with an increase in the neurological level of the lesion [19]; it has been observed a reduction of BMD values for all sites examined (lower extremities, lumbar region, and forearms), approximately 1 to 3 standard deviation (SD) scores below the mean of age and gender [20, 21].

According to this, in our study, we observed a compatible reduction of lumbar T-score (− 2 (− 3.8 ÷  − 1.3) vs − 0.6 (− 1.7 ÷  − 0.05); p = 0.009) (Fig. 1), but in literature is not reported a comparison between patients with SB who performing physical activity or not. The difference between the two groups highlights how physical activity could play a protective role in this category of patients.

In citated update are also reported the local risk factors that involve to the deficit of muscular strength, caused by neurological injury, that compromise BMD and increase the risk of occurrence of fractures [17]. The authors also suggested the role of systemic factors:

Authors have recognized the presence of other additional factors such as diet, environment, genetic, stress and strain on mechanical loads, and acidosis due to urinary diversion/augmentation cystoplasty.

Although with the inherent limitations of a small workload, our study is the first to report a significant difference in bone mineralization values between physically active and sedentary spina bifida patients. Further studies, on larger samples, are needed to better investigate this association.

Lastly, by means of the echocardiogram, congenital vascular anomalies affecting the main arterial vessels originating from the heart (aorta and pulmonary trunk), which could be suspected on the basis of the common embryological origin discussed above and which may also represent an absolute contraindication to the practice of leisure sport activities too, were ruled out in our patient population.