Spinal shape modulation in a porcine model by a highly flexible and extendable non-fusion implant system

Adolescent idiopathic scoliosis (AIS) is a complex three-dimensional deformity of the spine and trunk. The deformation is typically characterized by axial vertebral rotation, apical lordosis and lateral deviation of the spine and has a significant impact on patients, both mentally and physically [1, 2]. In severe cases, surgical correction and spinal fusion (spondylodesis) are required. Since the 1960s, many systems have become available and considerable technical improvements have been made [3, 4]. Besides the strategy of posterior correction and fusion, several researchers have recognized the possibility to guide the growing spine by selective tethering. This method has been shown to be effective in animal models and clinically in carefully selected patients [5, 6]. However, certain important disadvantages remain unsolved in all current systems such as loss of motion and growth arrest of the treated segments [7, 8]. Therefore, other strategies that either maintain mobility or allow growth have been explored [9, 10]. Examples are the application of tethering ligaments [11‐13], growing rod systems [14, 15] and passive or motor-driven lengthening implants [16]. These strategies still have considerable limitations, e.g., not attempting to recreate normal spinal anatomy, being too stiff or requiring additional operations.

We developed a novel posterior non-fusion scoliosis correction system, referred to as the XSLATOR [17, 18]. This system applies continuous coronal and axial corrective forces. Unlike the tethering techniques used by, e.g., Braun and Schwab [12, 19], which are intrinsically similar to asymmetrical growth inhibition, the XSLATOR preserves spinal flexibility, is fully capable of growth facilitation and therefore will not inhibit growth. The system consists of two posterior implants (Fig. 1). One implant, the XSLAT (eXtendable implant correcting Scoliosis in LAT bending), is a lateral bending element, which is based on the recently developed application of shape-memory metal in posterior implants for enhanced post-operative correction [20]. The other (XSTOR; eXtendable implant correcting Scoliosis in TORsion) is a torsion-generating element that uses spinal growth for post-operative correction. Due to the flexibility of both elements, the additional stiffness to the spine is in the order of 10 % [17], which allows physiological motion. The important advantages of this are a much lower likelihood of spontaneous fusion and lower stresses on the proximal and distal anchors.

The aim of the current study is to analyze the functioning of the lateral deformation device (XSLAT) and the rotation device (XSTOR) in a growing pig model. Furthermore, the maintenance of growth, absence of fusion and soft tissue reaction will be monitored.

In the current study, we have shown that both the torsional and lateral bending devices were capable of inducing a spinal deformity with similarities to (human) scoliosis. Moreover, the spines remained mobile and could elongate with growth. In contrast to the methods used by Braun and Schwab [12, 19], the devices were designed such that correction and induction of scoliosis are aimed for in a similar fashion. Whether these devices can permanently reduce a “true” scoliosis in the clinical setting remains speculative, since we induced instead of reduced a scoliosis in porcine spines that are fundamentally different in terms of geometry and loading (quadrupedal vs. bipedal). To our knowledge, there are no animal models of “true” scoliosis. Therefore, we believe that the goal of animal studies can only be modest, to merely investigate the potential to deform. Especially for our devices, where growth and mobility were important research outcomes, we preferred a healthy, untouched spine and therefore refrained from first inducing a scoliosis.

Cobb angles of XSLAT spines progressed with time, although the rate of progression declined. Undoubtedly, short-term (minutes to hours) and intermediate-term (several days) viscoelastic effects play a role in this. However, after 8 weeks, the Cobb angle induced by XSLAT was far beyond the neutral zone and the physiological ROM of porcine spines that are reported in literature [22]. Also, the apical vertebra showed a distinct wedge shape. Based on these observations, we conclude that the lateral deformation was also the result of growth adaptation as described by Hueter and Volkmann [26].

After 8 weeks, the apical torsion angle as well as the Cobb angle induced by XSTOR were far beyond the neutral zone and the physiological ROM of porcine spines that are reported in literature [22]. Although we did not investigate the effect of surgery alone, we believe that a bias due to surgery is unlikely, because the spines and pedicle entrees were always exposed on both sides of the eventual scoliotic curve. Therefore, we conclude that both the axial rotation and the lateral deformation were largely induced by the implants and mainly facilitated by adaptive tissue processes.

Growth of the spines was clearly observed. Whether this growth is comparable to the normal growth of porcine spines is unclear, as normal growth data for young porcine spines are not available from literature. If, however, the implant had hampered the spinal growth (posterior tethering), one would expect the elongation of the spines to be larger than the elongation of the implants, which was not observed. Also, posterior tethering typically results in secondary lordotic curves, which was not observed.

A moderate detrimental effect on the facet joints was found in the outer instrumented segments. This was not related to the presence of pedicle screws and therefore appears to be related to either surgical exposure of this part of the spine or less physiological mobility due to the added stiffness or pain. Only one of the 60 facet joints in the instrumented area was fused, while all others remained mobile. This is encouraging because the fast-growing porcine spine is more likely to fuse than the human spine [27]. The effect of fusionless scoliosis instrumentation on facet joints and other tissues in human and animal models has been poorly researched and still remains unclear [28, 29].

In most pigs, some bone formation was observed in the tissue surrounding the pedicle screw fixations, likely caused by damaging of the periosteum during insertion of the screws and placement of the bridges. This minor bone formation was interpreted as acceptable and may be preferable because it will consolidate the fixation anchors. In some pigs, minor bone formation was found in the tissue surrounding the implant at other locations as well. It is believed to be the result of periosteal damage caused by implants rubbing against the spinous processes, lamina or facet joints during daily movements. Since facet and interlaminar fusions in lower animals, such as sheep, dogs, goats and pigs, are commonly achieved more easily than in humans [27, 30], we consider this minor bone formation to be acceptable.

This study has some limitations. First, we used wide and narrow versions of each implant. The use of narrow implants, which delivered slightly less lateral bending moment (for XSLAT) and torque (for XSTOR), did not seem to result in altered deformation. XSLAT-narrow created slightly larger mean Cobb angle than XSLAT-wide, while XSTOR-wide created a slightly larger mean torsion angle than XSTOR-narrow. These differences were not significant; nonetheless, this could be attributed to the small sample size.

Second, the reference X rays (day 0) were taken after the pigs spent several hours in a prone position during surgery, thereby inducing some lordosis due to the viscoelastic deformation of the spine. For the post-surgical radiographing (1, 4, 8 and 12 weeks after surgery), the time spent in the prone position was much shorter and thus less viscoelastic deformation was present. Given the flexibility of the spines postmortem (manually examined), it is most likely that this viscoelastic effect is the sole explanation for the effect of the implant on kyphosis.

The third limitation of our study is the lack of sham conditions, as the surgery itself will have an effect on the growing spine, especially in the sagittal plane. However, with respect to the intended deformations, it can be expected that this “sham” effect would be similarly present for both types of posterior implants. In fact, we did not observe any rotation in the XSLAT, and the observed lateral bending in the XSTOR where the convexity was on the implant side was actually the opposite of the curve generated by XSLAT.

Fourth, from the radiographs, accurate determination of torsion angles was not possible. For this, we used the CT analysis that was, however, only made after terminating the pigs, thus not allowing for a time-effect analysis. Visually, we did not see rotation in the animals directly after implanting the torsion device, nor on the day 0 radiographs. In conclusion, the study showed that particularly the XSTOR was capable of inducing deformities in two different planes, in accordance with the coupled motions that have been suggested previously in literature [18, 31, 32]. Our system will indirectly influence the sagittal profile by gradual reduction in the other two planes, since it has been shown in spinal motion segments that rotational, lateral and sagittal motion are coupled [18].

We believe this study can be regarded as a proof of concept of the investigated devices. Therefore, these devices may contribute to a future non-fusion approach of idiopathic scoliosis correction in humans.

In this study, we did not attempt to create a stable spine after deforming it with our inverse approach. We believe that would not yield a proper indication for creating a stable corrected spine. However, our ultimate goal is to create a stable, non-scoliotic spine. Whether the XSLATOR is capable of that will be studied in future research.