Loss of temperature and pain sensation as risk marker of neurological complications in surgical correction of severe spinal deformity

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Introduction

Treatment of severe spine deformities is a serious surgical problem [1–5], and iatrogenic spinal cord injury remains a dangerous complication. Previous studies have shown that the frequency of postoperative neurologic complications ranges from 0.37% to 10% [6–10]. Intraoperative neurophysiological monitoring (IONM) of the spinal tracts is used as a preventive measure [5].

Transcranial motor evoked potentials (MEPs) are extremely sensitive to changes in blood flow in the spinal cord due to hypotension or compression (lesions) of the blood vessels [8, 9] and currently are an important component of the IONM gold standard for the correction of spinal deformities [8, 11–15]. Changes in MEP parameters in response to surgical aggression are often detected sooner than the changes in somatosensory evoked potentials, which facilitate faster identification of an impending spinal cord injury [8]. However, some researchers believe there is insufficient evidence about IONM reducing the incidence of a new or the exacerbation of an existing sensorimotor deficiency [16, 17]. IONM tools cannot differentiate changes in the control parameters associated with the surgeon’s actions and the reactions caused by general transformation of the functional state of the central nervous system [12, 18]. In this regard, further prospective studies are required.

Study of thermal and pain sensitivity in Th1–S2 dermatomes in patients with severe spinal deformities allows assessing the integrity of the skin’s sensory system’s functions and its compensatory adaptive capabilities in the correction of spinal deformities. Our study aimed to determine the correlation between the degree of defects of the thermal and pain sensitivity in the Th1–S2 dermatomes and the intensity of the spinal tracts’ reaction to surgical correction of severe spinal
deformities.

Materials and methods

Our study sample included 58 patients (24 males and 34 females) aged 2.9–27 years (15.7 ± 0.8 years), with severe spinal deformities. The causes of deformity were idiopathic scoliosis in 26 cases, congenital scoliosis in 22 cases, type I neurofibromatosis in four cases, neuromuscular scoliosis in three cases, and other factors (such as neoplasms) in three cases. The average angle of deformity of the primary curve was 80.1° ± 7.1° (range, 50°–145°), whereas that of the secondary curve was 51.8° ± 9.4° (range, 20°–135°).

Deformities of all patients were corrected under the IONM control (63 protocols), followed by fixation of segments of the thoracic/thoracolumbar spine using different immersible transpedicular fixation systems [19–22]. The following procedures were performed: seven osteotomies, five vertebrotomies, three extirpations of the semivertebra, release, and discotomy.

Anesthetic support combined (i) intravenous anesthesia as a combination of a hypnotic, propofol (10–2 mg/kg/h), with a narcotic-analgesic, fentanyl (10–1 μg/kg/h), (ii) an intravenous microfluid injection through an infusion pump, and (iii) artificial lung ventilation through an endotracheal tube. During intubation, esmeron, a muscle relaxant of average action, was used. The surgery duration averaged 235.0 ± 13.5 min (range, 60–470 min), and intraoperative blood loss amounted to 556.0 ± 51.4 mL (range, 100–1500 mL).

The study was approved by the Ethics Committee of the Federal State Budgetary Institution, Ilizarov Russian Research Center of Restorative Traumatology and Orthopedics, Ministry of Health of Russia (Minutes No 7 [32] of 12.24.2012). It was conducted in compliance with the ethical standards set forth in the World Medical Association’s “WMA Declaration of Helsinki: Ethical Principles for Medical Research Involving Human Subjects” (as revised in 2013). Patients aged ≥18 years as well as parents or legal guardians of pediatric patients signed informed consent for diagnostic studies and publication of the data without personal identification.

Thermal and pain sensitivities were tested before and after 2–3 weeks of surgery (depending on each patient’s condition) with an electrical esthesiometer (a thermistor, EPCOS Inc., Germany) with simultaneous skin temperature registration (Termostar, Nihon Kohden, Japan). To test the thermal and pain sensitivities, we evaluated the temperature perception in response to local heating of the skin in the selected dermatome region. Temperature sensations were divided into two categories: (i) “thermal” and (ii) “pain from heat.” The contact area of the thermoelectric couple was 1 cm2, the temperature ranged from 10°C to 50°C, and the rate of temperature increase was 2°C/min. Assessment of thermal and pain sensitivities was performed in accordance with the generally accepted scheme [23] at symmetrical points on the right and left of Th1–S2 dermatomes.

Conformity to normal statistical distribution of the thresholds values of thermal and pain sensitivities from heat was estimated using the Kolmogorov and Smirnov criteria. Their arithmetic mean (M) and the standard error of mean (m) as well as the occurrence frequency (ν) of lack of thermal (thermoanesthesia) and lack of pain (thermoanalgesia) sensation as a percentage ratio of the number of observations for thermoanesthesia (n1) and thermoanalgesia (n2), respectively, to the total number of observations in the analyzed sample (N) were calculated:

(1)

where ni is the number of observations of the i-th parameter.

The error (Sν) was calculated from the occurrence frequency as

(2)

The statistical significance of the differences in the esthesiometric parameters between the compared groups with normal distribution was assessed using Student’s t-test (p < 0.05). For a small sample, a nonparametric Mann–Whitney U-test was used (p < 0.05). The significance of changes in the occurrence frequency of thermoanesthesia and thermoanalgesia was evaluated using the z-test of the difference in proportions. The data obtained were mathematically processed using Microsoft Excel 2010 with the Attestat add-on [24].

IONM was performed using the ISIS IOM system (Inomed Medizintechnik GmbH, Germany). We have described its implementation scheme in detail in a previous study [25]. The reactions of MEPs registered during monitoring were ranked according to the scale we previously developed [25] from 0 (preservation at the time of testing of the form, amplitude, and time parameters of MEPs close to initial ones) to 7 (complete disappearance of MEPs without signs of restoration by the time of surgery completion). During subsequent testing, the rank estimate was either maintained at the same level (relative to previous MEP dynamics) or increased or decreased depending on the ability of the somatic motor system to transmit the excitation wave from the motor cortex to the muscle indicator. The changes in MEP rankings during surgery characterized the reaction type of the somatic motor system to surgery. We identified five stable combinations of ranks corresponding to five types of spinal tract reactions to surgical aggression [25]. The occurrence frequency was calculated by equation (1), and its error was calculated by equation (2) for each type of reaction
identified.

Results

Analysis of the thermal and pain sensitivity parameters determined that the preoperative average values of thresholds of thermal (Figure 1a) and pain (Figure 1b) sensitivity (at symmetrical right and left test points) were similar (p > 0.05) and increased unidirectionally with insignificant variation in the caudal direction (from the Th1 dermatome to the S2 dermatome).

 

Fig. 1. Thresholds of (a) thermal sensitivity and (b) pain sensitivity in Th1–S2 dermatomes before treatment (columns: white — the right test points; gray — the left test points) and after treatment (lines: solid — the right test points; dashed — the left test points). Black columns are normal threshold values

 

Comparing the sensitivity thresholds in patients with normal values (Figure 1) revealed that the thermal sensitivity threshold in the Th3 dermatome increased by 2°C–7°C (average 5.3°C ± 1.2°C, p < 0.05) and that the pain sensitivity in the Th5–Th6 dermatomes increased by 2°C–8°C (average 4.3°C ± 0.7°C, p < 0.05).

The occurrence frequency of thermoanesthesia and thermoanalgesia is presented in Figure 2. The preoperative bilateral differences of this indicator were, as a rule, insignificant. Thermoanesthesia (Figure 2a) was more pronounced (before treatment 27%–56%, after treatment 22%–58%) than thermoanalgesia (before treatment 0%–2%, after treatment 0%–8%) (Figure 2b). The distribution of thermoanesthesia was more or less even across all tested dermatomes, with a slight tendency to increase in the caudal direction, whereas that of thermoanalgesia was uneven and occurred randomly (Figure 2b).

 

Fig. 2. Occurrence frequency of (a) thermoanesthesia and (b) thermoanalgesia before treatment (columns: white — the right test points; gray — the left test points) and after treatment (lines: solid — the right test points; dashed — the left test points)

 

Before surgery, but after anesthetic induction and the offset of action of the muscle relaxant, baseline MEPs were obtained to assess the degree of change in the control responses during surgery. In three cases, the initial responses showed unstable shapes and characteristics; in two cases, basic MEPs could not be obtained; and in one case, they were observed only in the leads on the left and had low amplitude.

During surgery, practically all variants of MEP changes were observed relative to the baseline: from a moderate decrease and instability in shape and characteristics to a significant decrease until complete disappearance. By analyzing the IONM protocols, all indicated variants of MEP changes were categorized into the five stable combinations of ranks identified earlier, the frequency of which is presented in Table 1.

 

Table 1. Reaction types (I–V) of the spinal tracts to surgical correction of spinal deformities

Type	Combinations of ranks	Number of observations	Occurrence frequency (ν), %	Risk of neurologic complications
I	0, 1, 2	28	44.4 ± 6.26	Absence of risk
II	0–3, 4a	8	12.7 ± 4.19	Minimum risk
III	0–3, 4a, 5	11	17.5 ± 4.60	Low risk
IV	0–3, 4b, 5, 6	10	15.9 ± 4.60	Average risk
V	0–3, 4b, 5, 6, 7	6	9.5 ± 4.00	High risk

Note: The occurrence frequency was calculated by equation (1) without taking into account two observations with an initial lack of response (N = 63 − 2), and its error (Sν) was calculated by equation (2).

 

Table 1 shows that the use of MEP technology for surgical correction of spinal deformities is accompanied by a low risk of developing neurological complications. When reaction types IV and V were identified, due to timely measures (transposition of screws, administration of glucocorticoids, partial discharge of traction loads to the spinal cord), in most cases, the motor functions of patients remained at a level corresponding to the preoperative level. In one case (of six cases), after having a type V reaction, the patient underwent repeated surgery (discharge of traction loads). In three cases (4.8%), there were electromyography (EMG) signs of spinal cord root irrigation, such as short-term outbreaks of spontaneous EMG in the corresponding leads, which subsided as a result of corrective action by the surgeons.

Postoperative control esthesiometric examination showed that compared with the baseline, changes in the average thermal and pain sensitivity thresholds (Figure 1) vary insignificantly (p > 0.05). The nature of their distribution along the spine and the degree of bilateral differences (p > 0.05) were retained. The postoperative occurrence frequency of thermoanesthesia varies ambiguously (Figure 2a). In the upper thoracic region, these changes are multidirectional. For the Th3 dermatome, the decrease in this parameter is statistically significant on the left (p < 0.05). Starting from the Th6 dermatome, there is a distinct increase in the postoperative occurrence frequency of thermoanesthesia compared with the baseline. In the lumbar region, changes in this parameter can be considered insignificant. Figure 2b shows that the manifestations of thermoanalgesia are more uneven than the local loss of thermal sensation; however, after surgery, the occurrence frequency of thermoanalgesia in the analyzed sample increases significantly in the lower part of the thoracic spine, as in the case of thermoanesthesia.

The entire patient sample was divided into four groups (Figure 3), depending on the type of reaction of the spinal tracts to surgery.

 

Fig. 3. Thresholds of thermal and pain sensitivity before treatment (columns: light gray, thermal threshold; dark gray, pain threshold) and after treatment (lines: dashed, thermal threshold; solid, pain threshold) for different reaction types of the spinal tracts to surgery. (a) Group 1 (type I), (b) group 2 (types II and III), (c) group 3 (type IV), and (d) group 4 (type V)

 

Group 1 (Figure 3a) included patients who did not show changes in MEPs during surgery (reaction type I). Group 2 (Figure 3b) comprised patients with reversible changes in MEPs during surgery (reaction types II and III). Group 3 (Figure 3c) included patients with reaction type IV; their MEP range decreased to the critical level and remained the same after surgery. Group 4 (Figure 3d) patients showed long-term disappearance of MEPs during surgery. Postoperative examination of patients with reaction types I–IV showed that changes in the mean values of thermal and pain sensitivity thresholds were statistically insignificant compared with the baseline (p > 0.05); for reaction type V (group 4), the small sample size and high variability (much higher than other reaction types) did not enable us to reliably estimate the significance of changes in thermal sensitivity thresholds after surgery. Moreover, the thresholds of pain sensitivity due to heat changed unreliably.

Due to the small sample size of groups 3 and 4, comparing the occurrence frequencies of thermoanesthesia and thermoanalgesia, depending on the reaction type of the spinal tracts to surgical aggression for each dermatome, was not helpful because it was for the entire sample (Figure 2). The preoperative occurrence frequency of thermoanesthesia (Figure 4a) varied significantly in the compared groups; the intergroup differences were most likely random, but they showed a slight tendency to increase in patients with reaction type V compared with those with reaction type I. The overall postoperative occurrence frequency of thermoanesthesia was 14.3% higher (p < 0.05) than that before surgery. In three groups of four patients, it increased by 44.5% (type I), 23.6% (type IV), and 30.3% (type V) (p < 0.05) compared with the baseline. This increase was the most pronounced in patients with reaction type V and was the highest at 68% after surgery.

 

Fig. 4. Frequency distribution of (a) thermoanesthesia and (b) thermoanalgesia (1) before and (2) after surgery, depending on the type of reaction of the spinal tracts. *reliability of the difference between the indicators and preoperative level, p < 0.05

 

The preoperative occurrence frequency of thermoanalgesia (Figure 4b) varied significantly in the compared groups. Although intergroup differences were most likely random, there was a slight tendency to increase from reaction type I (0% in the absence of thermoanalgesia, 28 patients, 532 dermatomes, 1064 measurements) to reaction type V (4.3%, 6 patients, 114 dermatomes, 228 measurements).

The overall postoperative occurrence frequency of thermoanalgesia was 160% higher (p ≤ 0.05) than that before surgery. In three groups of four patients, it increased compared with the baseline: in group 1, thermoanalgesia appeared in 0.5% of dermatomes; in group 2, it increased by 4.5 times; and in group 4, it increased by 86% (p ≤ 0.05). This increase was the most pronounced for patients with reaction type V and was the highest at 8% after surgery.

The preoperative occurrence frequency of thermoanalgesia increased monotonically from patients with reaction type I to those with reaction type V. After surgical correction of spinal deformities, the total frequency ν(T2) increased compared with the baseline. In this case, the intergroup differences among patients with reaction type I–IV (groups 1–3) were less pronounced compared with patients with reaction type V (group 4). Patients with reaction types IV and V (groups 3 and 4) (Table 2), on average, did not significantly differ from patients with reaction types I–III (groups 1 and 2) in age, magnitude of deformity of the primary curve, degree of deformity correction, and intraoperative blood loss volume.

 

Table 2. Characteristics of patients with different reaction types (I–V) of spinal tracts to surgical correction of spinal deformities

Indicators	Reaction types of spinal tracts
	Types I, II, and III (n = 47)	Type IV (n = 10)	Type V (n = 6)
Age, years	15.3 ± 0.9	19.1 ± 2.1	14.2 ± 1.7
Magnitude of deformity of the primary curve, °	78.4 ± 4.1	86.7 ± 5.4	80.0 ± 14.9
Degree of correction of the primary curve, %	62.0 ± 3.5	57.6 ± 10.1	63.8 ± 4.5
Number of patients with congenital scoliosis, n (%)	19 (41 %)	2 (20 %)	1 (16 %)
Number of patients with kyphotic deformities, n (%)	9 (19 %)	2 (20 %)	–
Preoperative neurological disorders, n (%)	7 (15 %)	3 (33 %)	3 (50 %)
Intraoperative hemorrhage, mL	502.1 ± 52.2	671.3 ± 164.1	730.0 ± 228.2
Number of decompressions, revisions, n (%)	1 (2.1 %)	1 (10 %)	1 (16 %)
Number of osteotomies, n (%)	6 (13 %)	1 (10 %)	–

 

The proportion of patients with congenital scoliosis and kyphotic deformity, who underwent osteotomy, was greater in groups 1 and 2 (reaction types I–III). In group 4 (reaction type V), there were no patients with kyphotic deformity, and osteotomy was not performed. From the entire sample of patients, only one patient (group 3, reaction type IV) had an intraoperative complication associated with unstable hemodynamics and blood loss. The percentage of patients with neurological disorders before surgery was greater in groups 3 and 4 (reaction types IV and V) than in groups 1 and 2 (reaction types I–III).

The results showed that changes in the state of thermal and pain sensitivities of patients before and after surgical correction of spinal deformities correspond to the proposed scale of the reaction types of the spinal tracts to surgery. This relationship is more pronounced in postoperative tests of pain sensitivity thresholds (thermoanalgesia). This suggested that for these patients, the prevailing possible risk factor in surgical correction of spinal deformities is preoperative dysfunction of the spinal tracts. Further study of the state of preoperative thermal and pain sensitivities will enable researchers to assess the possible risks of neurological complications.

Discussion

The results indicated that preoperatively, the state of thermal and pain sensitivities in patients with spinal deformities of different etiologies indicates a violation of the innervation status of the corresponding receptive fields on the skin. They are expressed to the greatest extent for dermatomes associated with the vertex of a spinal deformity, but are not localized within their limits, which correspond to earlier
studies [26].

Surgical correction of spinal deformities has little effect on the average magnitude of the absolute values of thermal and pain sensitivity thresholds, but leads to a significant increase in the occurrence frequencies of thermoanesthesia and thermoanalgesia. In most patients in our sample, the deformity vertices and, therefore, the focus of surgical aggression were localized in the lower part of the thoracic spine, suggesting that thermoanesthesia and thermoanalgesia are mostly expressed in this region.

We found a correlation between the severity of violations in the perception of temperature and pain from heat and the reaction type of the spinal tracts to surgical aggression (Figure 4). This correlation corresponds to the conclusion made earlier on the relationship between the reaction type of the somatic motor system, the level of risk of development and reversibility of postoperative neurologic complications, and the severity of the final motor deficiency [25, 27].

Many studies have identified the following possible causes of neurological complications in surgery for spinal deformities: (i) congenital scoliosis, (ii) scoliosis with hyperkyphosis, (iii) deformity angle >90°, (iv) combined methods of surgery, (v) revision surgery, (vi) reduction of perfusion of the spinal cord due to hypotension or significant blood loss and vascular embarrassment, and (vii) preoperative neurologic impairment [8, 9, 14]. Procedures associated with a higher risk include osteotomy and kyphosis correction [7, 9, 28].

Analysis of the possibility of a connection between the seven causes of neurological complications in surgery for spinal deformities and the reaction types of the somatic motor system to surgery revealed that preoperative violation of the spinal tract function is the prevailing factor for increased risk of iatrogenic disorders, which is consistent with the results of other studies [29].

Conclusion

Changes in the state of thermal and pain sensitivity before and after surgical correction of spinal deformities are correlated with the proposed scale of the reaction types of the spinal tracts to surgical aggression. This relationship is more pronounced in postoperative tests of pain sensitivity thresholds. Consequently, preoperative determination of significant manifestation of thermoanalgesia can be considered a sign requiring increased attention from the surgeon and the neurophysiologist conducting IONM.

Information about the contribution of each author

E.N. Shchurova: collection and processing of material for esthesiometry, analysis of obtained data and literature, writing the text.

M.S. Saifutdinov: conception, study design, collection and processing of material for intraoperative monitoring of MEP, analysis of data obtained, writing the article text.

S.O. Riabykh: collection and processing of material for the treatment and evaluation of the clinical status of patients, analysis of the data obtained, writing the article text.

Funding and conflict of interest

The authors declare no conflict of interest related to the publication of this article. The research was supported by the Ilizarov Russian Research Center of Restorative Traumatology and Orthopedics.

About the authors

Elena N. Shchurova

Ilizarov Scientific Center for Restorative Traumatology and Orthopaedics

Author for correspondence.
Email: elena.shurova@mail.ru
SPIN-code: 6919-1265

Doctor of Biological Sciences, a leading researcher Scientific-and-Clinical Laboratory of Deformity Correction and Limb Lengthening.

 

Russian Federation, 6, M.Ulianova St., Kurgan, 640005

Marat S. Saifutdinov

Ilizarov Scientific Center for Restorative Traumatology and Orthopaedics

Email: maratsait@yandex.ru

Doctor of Biological Sciences, a leading researcher Scientific Clinical-and Experimental Laboratory of Axial Skeletal Pathology and Neurosurgery, Group of clinical neurophysiology

.

 

Russian Federation, 6, M.Ulianova St., Kurgan, 640005

Sergei O. Ryabykh

Ilizarov Scientific Center for Restorative Traumatology and Orthopaedics

Email: rso_@mail.ru

MD,Head of the Laboratory of Axial Skeletal Pathology and Neurosurgery

 

 

Russian Federation, 6, M.Ulianova St., Kurgan, 640005

References

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