Somatosensory evoked potential monitoring of peripheral nerves

 CHILDREN’S ORTHOPAEDICS

Somatosensory evoked potential monitoring of peripheral nerves during external fixation for limb lengthening and correction of deformity in children M. R. Makarov, M. L. Samchukov, J. G. Birch, A. M. Cherkashin, S. P. Sparagana, M. R. Delgado From Texas Scottish Rite Hospital for Children, Dallas, Texas, United States

 M. R. Makarov, MD, Research Scientist  M. L. Samchukov, MD, Associate Professor of Orthopaedic Surgery  J. G. Birch, MD, FRCS, Professor of Orthopaedic Surgery  A. M. Cherkashin, MD, Assistant Professor of Orthopaedic Surgery  S. P. Sparagana, MD, Pediatric Neurologist  M. R. Delgado, MD, FRCPC, FAAN, Director of Pediatric Neurology, Professor of Neurology Texas Scottish Rite Hospital for Children, 2222 Welborn Street, Dallas, Texas 75019, USA. Correspondence should be sent to Dr M. R. Makarov; e-mail: [email protected] ©2012 British Editorial Society of Bone and Joint Surgery doi:10.1302/0301-620X.94B10. 28913 $2.00 J Bone Joint Surg Br 2012;94-B:1421–6. Received 14 December 2011; Accepted after revision 26 June 2012

We undertook a retrospective analysis of 306 procedures on 233 patients, with a mean age of 12 years (1 to 21), in order to evaluate the use of somatosensory evoked potential (SSEP) monitoring for the early detection of nerve compromise during external fixation procedures for limb lengthening and correction of deformity. Significant SSEP changes were identified during 58 procedures (19%). In 32 instances (10.5%) the changes were transient, and resolved once the surgical cause had been removed. The remaining 26 (8.5%) were analysed in two groups, depending on whether or not corrective action had been performed in response to critical changes in the SSEP recordings. In 16 cases in which no corrective action was taken, 13 (81.2%, 4.2% overall) developed a post-operative neurological deficit, six of which were permanent and seven temporary, persisting for five to 18 months. In the ten procedures in which corrective action was taken, four patients (40%, 1.3% overall) had a temporary (one to eight months) post-operative neuropathy and six had no deficit. After appropriate intervention in response to SSEP changes, the incidence and severity of neurological deficits were significantly reduced, with no cases of permanent neuropathy. SSEP monitoring showed 100% sensitivity and 91% specificity for the detection of nerve injury during external fixation. It is an excellent diagnostic technique for identifying nerve lesions when they are still highly reversible.

Injury to a nerve is an uncommon but troublesome complication of external fixation. The incidence of neurological complications in reports from the early 1990s ranges from 2% to 9% after external fixation involving the lower limb,1,2 and from 7% to 23% after that involving the upper limb.3,4 Subsequent publications have not shown any appreciable improvement in those rates: an incidence of peripheral nerve dysfunction after limb lengthening of 9.3% (76 of 814) was reported by Nogueira, Paley and Bhave5 in 2003; 12 (16%) of these resulted from intra-operative trauma. In 2010, Clement et al6 evaluated radial nerves after external fixation for stabilisation of fractures of the humeral shaft and elbow in 20 cadaver limbs. They found that in nine cases (45%) a pin was placed in close contact with the radial nerve, and in four cases (20%) directly impaled it, confirming the risk of inducing an iatrogenic nerve injury.6 Symptoms of peripheral nerve compromise include sensory disturbances such as paraesthesiae, dysaesthesiae, numbness and pain, and motor deficits ranging from weakness to complete paralysis. Although the use of intraoperative monitoring (IOM) can reduce the incidence of nerve injury, its role in external

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fixation procedures has not been accepted as standard practice. Somatosensory evoked potential (SSEP) monitoring is an established technique for assessing neurological function and is routine practice for many spinal operations.7,8 It has also been shown to reduce the risk of neurological injury in a variety of orthopaedic operations.9-11 We described the use of IOM during the application of an external fixator for limb reconstruction12-14 and found that SSEP monitoring could be used to detect – and often prevent – neurological damage during these procedures. However, the relatively small number of cases in these studies precluded assessment of the specificity or sensitivity of this technique. The aims of this study were to determine the incidence of nerve injury, to evaluate the diagnostic value of IOM in the early detection of nerve compromise during external fixation and to determine whether corrective actions in response to the early detection of nerve injury might prevent or substantially reduce the incidence of neurological complications. In addition, it was hoped that the larger patient population in this study would enable assessment of the specificity and sensitivity of IOM in this situation. 1421

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M. R. MAKAROV, M. L. SAMCHUKOV, J. G. BIRCH, A. M. CHERKASHIN, S. P. SPARAGANA, M. R. DELGADO

Fig. 1 Intra-operative photograph showing stimulation of the peroneal and posterior tibial nerves at the ankle and somatosensory evoked potential (SSEP) recording in the popliteal fossa area in a patient with external fixation for correction of a proximal tibial deformity. Subdermal electrodes are firmly attached to the skin using transparent self-adhesive surgical dressings.

Fig. 2 Intra-operative photograph showing stimulation of the ulnar, median, and both branches of the radial nerves in a patient with external fixation for correction of deformity. Electrode leads from all four recording sites are taped together to minimise interference with the surgical field.

Patients and Methods We retrospectively analysed IOM data for 306 consecutive external fixation procedures performed on 233 patients between 1992 and 2010. Prior to 1995 an Ilizarov frame (Smith & Nephew, Memphis, Tennessee) was used; thereafter, the procedures were performed using a TrueLok circular fixator (Orthofix, Lewisville, Texas). The mean age of the patients was 12 years (1 to 21) and there were 132 males and 101 females. The fixator was applied to the tibia alone in 156 procedures, the femur alone in 108, the femur and tibia simultaneously in 22, the humerus in five, and the forearm in 15. The application of bilateral or multisegmental frames during a single procedure was considered as a single case with IOM. Following ethical approval the SSEP monitoring data, operation records and medical records of all patients were analysed. We documented the time of the change of the SSEP recording during surgery, corrective action taken, the intra-operative SSEP response to corrective action, and the post-operative manifestations of nerve injury, including its anatomical distribution and possible aetiology. Patients with a post-operative deficit were followed until neurological recovery, or for a minimum of two years in the event of failure of recovery. Intra-operative peripheral nerve monitoring. The protocol of IOM described in our previous publications was closely followed.12-14 In the upper limbs the ulnar, median, and both sensory and motor branches of the radial nerve were stimulated over the distal forearm, and SSEPs were recorded at Erb’s point and the cervical region (Fig. 1). In the lower limbs they were elicited from the popliteal fossa, lumbar, and cervical regions after stimulation of the posterior tibial nerve at the medial malleolus and the peroneal nerve at the dorsal surface of the ankle joint (Fig. 2). All recording sites were found to be of use during the

application of tibial frames, whereas for femoral fixation only the lumbar and cervical sites were useful. The applied electrical stimulus had an intensity ranging from 20 mA to 80 mA, with a pulse width of 0.1 ms to 0.3 ms and a repetition rate of 2.35 to 3.24 stimulations/s. The recording parameters comprised a 30 Hz to 2000 Hz bandpass filter, 100 ms analysis time and 10 μV/division gain. Each SSEP recording was the mean of the responses from 50 to 800 stimuli, depending on the signal-to-noise ratio. The recording and stimulating electrodes were disposable stainless steel needles (Nicolet Biomedical, subsequently Viasys CareFusion, Madison, Wisconsin). The active leads of the electrodes were referenced to inactive leads at a distance of 2 cm. Surgeons inserted sterile electrodes in the operative field, and a neurophysiologist inserted all other electrodes in an aseptic manner. Electrodes placed on the opposite limb served to record SSEP changes resulting from anaesthesia, physiological factors and technical problems. The resulting waveforms were recorded using contemporary models of Cadwell or Axon Workstations. The latest model used was the Cascade/Elite (Cadwell, Kennewick, Washington). Baseline recordings were obtained after the induction of anaesthesia but before any surgical intervention. Stimulation was continued throughout the procedure and these data were compared with the baseline recordings. Body temperature and arterial blood pressure (which exert a moderate influence on SSEP values) were constantly monitored and correlated with the neurophysiological data. Cooperation between the surgeon, the anaesthetist and the neurophysiologist enabled accurate documentation of intra-operative events. Significant changes in the SSEPs were defined as either a reduction in amplitude > 50% or a prolongation of latency > 10% with reference to baseline THE JOURNAL OF BONE AND JOINT SURGERY

SOMATOSENSORY EVOKED POTENTIAL MONITORING OF PERIPHERAL NERVES DURING EXTERNAL FIXATION FOR LIMB LENGTHENING

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306 procedures (233 patients)

Normal SSEPs 248

Abnormal SSEPs 58

Required corrective action

No PND 248

Late PND 10

Resolved at surgery

Action not performed 16

Action performed 10

No PND 3

No PND 6

PND 13

Permanent 6

Transient 7

Tourniquet 30

PND 4

Permanent 0

(5 to 18 months)

Osteotomy* 2

Transient 4 (1 to 8 months)

Fig. 3 Flow diagram showing the results of intra-operative monitoring (*, acute manipulation of bone segments during osteotomy; SSEPs, somatosensory evoked potentials; PND, peripheral nerve deficit).

values, these being the parameters used in IOM of the spinal cord.7,8 Data analysis. The sensitivity, specificity and predictive values of positive and negative tests were calculated based on the following classification of IOM outcomes: True positive: SSEPs decreased to below critical values, correlating with either post-operative neurological deficit or return to acceptable limits following corrective surgical manipulation. False positive: SSEP decrease reached critical values but could not be related to a surgical event, with no neurological impairment identified post-operatively. True negative: SSEPs remained consistent with baseline values and no new neurological deficit was noted postoperatively. False negative: New neurological deficit was found postoperatively, but no significant waveform changes were noted intra-operatively. VOL. 94-B, No. 10, OCTOBER 2012

Statistical analysis. The incidence and severity of neurological complications in patients with and without corrective manipulations were compared using statistical analysis. To determine whether the means of two samples were significantly different, Student’s t-test was used, assuming unequal variances in the groups. Fisher’s exact test was used in the analysis of contingency data where sample sizes were small. A p-value < 0.05 was considered statistically significant.

Results During the course of 306 procedures there were 58 instances (19%) of significant SSEP change (Fig. 3). Of these, in 32 (10.5%) the changes were transient and resulted from tourniquet inflation (n = 30) or manipulation of bone segments (n = 2). The surgeon was informed, and after deflating the tourniquet or completion of the osteotomy, the waveform abnormalities promptly resolved without post-operative sequelae. The remaining 26 instances (8.5%) of significant

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Table I. Aetiology and outcome of neuropathies resulting from external fixation procedures (n = 17) Mechanism of nerve injury/diagnosis

Nerve affected

Site of injury/corrective action

Neuropathy*

Duration (mths)

Nerve impingement by wire or half-pin (n = 5) Achondroplasia Fibular hemimelia Lisfranc fracture Fibular hemimelia Post-traumatic femoral shortening

Peroneal Peroneal Peroneal Peroneal Peroneal

Distal tibial half pin/replaced Distal tibial wire/replaced Proximal tibial wire/replaced with half pin Proximal tibial wire/no correction Distal femoral pin/no correction

S S-M S M S-M

1 6 8 > 2 years 18

Acute deformity correction (n = 4) Fibular hemimelia Type IV tibial deficiency Achondroplasia Radial dysplasia

Peroneal Peroneal Peroneal Radial

Femoral varus correction/no action Foot equinus correction/degree reduced Tibial varus correction/no action Clubhand correction/no action

M M M S-M

> 2 years 6 6 6

Nerve retraction for osteotomy (n = 3) Fibular hemimelia Blount’s disease Post-traumatic tibial growth arrest

Peroneal Peroneal Peroneal

Fibular osteotomy/no action Fibular & tibial osteotomy/no action Fibular osteotomy/no action

M S M

> 2 years 5 12

Pressure by haematoma (n = 1) Post-traumatic humeral shortening

Ulnar / radial

Vein perforation at distal humerus by wire/ no frame adjustment

S/M

3 / 18

Prolonged tourniquet time (n = 1) Type IV tibial deficiency

Peroneal

Tourniquet on femur for 2 hrs/no action

M

5

Unknown cause (n = 3) Achondroplasia Achondroplasia Achondroplasia

Peroneal Peroneal Peroneal

Proximal tibial osteotomy?/no action One of proximal tibial wires?/no action Proximal tibial osteotomy?/no action

M M M

> 2 years > 2 years > 2 years

* S, sensory deficit; M, motor deficit

SSEP changes were analysed in two groups, depending on whether or not corrective action was undertaken. Of 16 instances in which no corrective action was taken, there was a neurological deficit in the immediate post-operative period in 13 (81.2%, 4.2% overall). Most of these (ten of 13) occurred early in our experience with IOM, when the importance of SSEP changes was not fully recognised. In seven of these 13 patients post-operative neuropathy was transient, persisting for five to eight months, and in six it was permanent. The remaining three patients in this group were asymptomatic. Therefore, 13 cases were defined as true positive and three as false positive. In the latter three cases, SSEP abnormalities occurred after retraction of a nerve or application of the tourniquet for osteotomy during the final 20 minutes of surgery, so that there was not enough time to observe recovery of the waveform. In the ten patients in whom intra-operative corrective action was taken, four (40%, 1.3% overall) had a postoperative peroneal nerve deficit, which resolved over a period of 1 to 8 months and six had no neurological dysfunction post-operatively. Four of the six patients without post-operative neuropathy showed SSEP recovery in response to corrective manipulation and were considered true positives, whereas the two with no SSEP recovery by the end of surgery were considered false positives.

Based on four instances of post-operative neuropathy in the patients in whom a corrective manipulation was undertaken and 13 instances of nerve injury without corrective actions, the incidence of post-operative nerve compromise was estimated to be 5.5% (17 of 306). The presumptive aetiology of neurological damage in these cases, and their post-operative outcome, is shown in Table I. The difference in the incidence of post-operative neurological complications between these two groups was found to be significant (p = 0.04, Fisher’s exact test). The difference in duration of transient neuropathy between groups did not reach significance (p = 0.09, Student’s t-test). However, the data groups of (1, 6, 6 and 8 months) and (5, 5, 6, 6, 12, 18 and 18 months) suggests the possibility that longer-lasting neuropathy may occur if corrective action is not taken. Ten patients (3.3%) with true negative results of IOM were asymptomatic post-operatively but subsequently developed a peripheral neuropathy during the course of distraction or correction of deformity. The peroneal nerve was involved in eight and the radial and saphenous nerves in one patient each. The symptoms were sensory in nine patients and motor in one, and showed complete resolution after cessation of limb lengthening, reversal of deformity correction, or pin revision. An estimation of the efficacy of IOM during external fixation is presented in Table II. The sensitivity of IOM to THE JOURNAL OF BONE AND JOINT SURGERY

SOMATOSENSORY EVOKED POTENTIAL MONITORING OF PERIPHERAL NERVES DURING EXTERNAL FIXATION FOR LIMB LENGTHENING

Table II. Sensitivity and specificity of somatosensory evoked potential (SSEP) monitoring during external fixation procedures in relation to clinical evidence of nerve compromise (n = 306). SSEP monitoring showed 100% sensitivity and 91% specificity relative to clinical results Clinical results SSEP results

Positive

Negative

Total

Positive

53

5

58

Negative Total

0 53

248 253

248 306

identify patients with a new neurological deficit after external fixation was 100%, with a specificity of 91%. Therefore, the positive and negative predictive values were 100% and 91%, respectively.

Discussion Avoiding iatrogenic nerve injury is a priority of every external fixation procedure. IOM helps to achieve this aim by tracking the physiological integrity of peripheral nerves throughout the procedure and by alerting the surgeon to nerve compromise before irreversible damage has occurred. In our study intra-operative alerts in response to critical SSEP alterations were issued 26 times, but appropriate corrective measures were taken only in ten cases. The decision not to take corrective action was due primarily to our developing experience with IOM. During early cases the surgeon was uncertain of the significance of the changes, as the criteria for critical SSEP changes were adopted from experience with spinal cord monitoring, without confirmation of their clinical significance for peripheral nerves. The most important limitation, however, was our inexperience in appreciating the temporal relationship between changes in the SSEP recordings and particular surgical events. This resulted in failure to identify a precise mechanism of nerve injury in a few cases. Subsequently, we realised that significant SSEP changes do not necessarily occur immediately after the causative event, and some may be delayed. Moreover, critical changes might develop after the surgeon team had performed several steps that could have caused the event, and the he or she may have been uncertain of the proper corrective action to take. With time, our understanding of the particular surgical manoeuvres that can be responsible for nerve injury improved and our surgical protocols have been modified accordingly. In particular, we operate without a tourniquet whenever possible. When a tourniquet is used, baseline SSEPs are acquired prior to tourniquet inflation. The tourniquet is released and removed as soon as is feasible, and the recovery of SSEP responses after its release is closely monitored. Critical wire and half-pin placement is performed early in the procedure to give additional time to monitor nerve function. All VOL. 94-B, No. 10, OCTOBER 2012

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surgical steps with the highest likelihood of inducing nerve injury are performed in sequence, with sufficient interval between them to allow time to confirm the integrity of peripheral nerves. The importance of responding to critical changes in SSEP recordings during surgery was recognised when patients were analysed in two groups, depending on whether or not corrective action was taken. No cases of permanent neuropathy were documented in the group where intraoperative corrective action was undertaken. Moreover, proper corrective manipulation reduced the incidence of post-operative neuropathy by half, and appeared to result in a more rapid resolution of the symptoms than in the group where no such action was taken (one to eight months versus five to 18 months), although this difference did not reach statistical significance. In our study SSEP monitoring was highly sensitive but less specific. The high sensitivity can be attributed to the mixed and tightly packed arrangement of motor and sensory fibres in peripheral nerves, making isolated injury to only motor or sensory fibres highly unlikely. The lower specificity may be due to the fact that, in contrast to spinal surgery, during which IOM usually continues throughout wound closure until at least 60 minutes after correction,15,16 external fixation procedures often do not last long enough to detect recovery of transient SSEP changes. In four of the five false positive cases in our study, surgery ended within 20 minutes after significant SSEP changes. As none of these patients had a post-operative neuropathy, we may assume that recovery of the waveform occurred later. Nonetheless, the results were classified as false positives, which affected specificity. Ideally, IOM should be continued longer in such cases, and sufficient time should be given to observe recovery of the SSEP recordings. The overall rate of neurological complications in our study was 8.8% (27 of 306), including 17 patients with a peripheral neuropathy in the immediate post-operative period and ten with a neuropathy developing during the course of limb lengthening. This rate is comparable to an incidence of 9.3% reported by Nogueira et al.5 Based on the analysis of 814 limb lengthening procedures, they showed a predominance of peripheral neuropathies resulting from distraction rather than from surgery itself (7.8% vs 1.5%). In our experience, it was the reverse (3.3% vs 5.5%). The higher incidence of intra-operative nerve compromise in our study was apparently due to more precise assessment of nerve function provided by IOM and the ability to detect impending nerve injury at a subclinical level. This may have helped to lower the rate of delayed neuropathies developing during subsequent treatment. We agree with the observation of Nogueira et al5 that the nerve can be irritated during distraction, and may eventually be compromised because of tethering or impingement by hardware. It is unclear whether IOM can detect wires and pins in close proximity to a nerve, but our results suggest that optimal placement of the frame was achieved in our

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patients, reducing the possibility of acute traction of the nerves or delayed pressure from a pin on nerves during subsequent limb lengthening or correction of deformity. Patients with congenital anomalies had a greater risk of iatrogenic nerve injury in our study; this may be due to an aberrant course of the nerves in these cases, something that is difficult to predict in patients with severe limb abnormalities. Similarly, the application of external fixators to the upper limb, especially the forearm, is particularly challenging owing to the high density of neurovascular structures, and this may explain why these procedures are not commonly performed. The use of IOM will increase confidence in performing the external correction of upper limb deformities safely. Some peripheral nerves appear to be more prone than others to injury during external fixation procedures. In our study, acute nerve injury primarily involved branches of the peroneal nerve (n = 15). Five of these patients had achondroplasia, the incidence of peroneal nerve injury in patients with achondroplasia being 33% (five of 15). Surgical correction of short stature is always associated with a high incidence of peroneal nerve dysfunction. Correll et al17 reported a 35% incidence of foot drop after limb reconstructive surgery in 26 patients with short stature. Prevot et al18 described 12 instances (46%) of transient peroneal nerve palsy resulting from bilateral frame application and limb lengthening in 26 patients with achondroplasia. A comparable incidence of peripheral nerve injury (48%) was reported by Nogueira et al5 in their series of patients (55 of 115) with skeletal dysplasia. It is clear that patients with short stature have an inherent risk for neurological complications during limb reconstruction. IOM may help to reduce these risks by providing early diagnosis of nerve damage and allowing appropriate corrective manipulation during the operation. In conclusion, the use of SSEP monitoring during external fixation procedures proved helpful in identifying potential peripheral nerve injury. The early detection of nerve compromise was possible in many instances, resulting in appropriate corrective action, adequate recovery of the response, and no post-operative nerve dysfunction. In cases with actual nerve injuries, appropriate corrective action reduced the severity of the neurological deficit and may have shortened the duration of the neuropathy. IOM is particularly recommended during those procedures where a significant risk of neurological injury is anticipated. These procedures may include, but are not limited to, acute

deformity correction, the use of external fixation on the upper limbs, patients with achondroplasia, distorted anatomy (such as congenital deformities), and excessive soft tissue rigidity from scarring, particularly if significant manipulation at the osteotomy site is expected. The authors thank E. V. Allen, MS, and P. Rampy, MS, for skilful technical assistance during IOM, and R. Browne, PhD, for his help with statistical analysis. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

References 1. Atar D, Lehman WB, Grant AD, et al. Treatment of complex limb deformities in children with the Ilizarov technique. Orthopedics 1991;14:961–967. 2. Pouliquen JC, Glorion C, Ceolin JL, Langlais J, Pauthier F. Upper metaphyseal lengthening of the tibia by callotasis: forty seven cases in children and adolescents. J Pediatr Orthop 1993;2:49–56. 3. Cattaneo R, Villa A, Catagni MA, Bell D. Lengthening of the humerus using the Ilizarov technique: description of the method and report of 43 cases. Clin Orthop Relat Res 1990;250:117–124. 4. Villa A, Paley D, Catagni MA, Bell D, Cattaneo R. Lengthening of the forearm by the Ilizarov technique. Clin Orthop Relat Res 1990;250:125–137. 5. Nogueira MP, Paley D, Bhave A. Nerve lesions associated with limb-lengthening. J Bone Joint Surg [Am] 2003;85-A:1502–1510. 6. Clement H, Pichler W, Tesch NP, Heidari N, Grechenig W. Anatomical basis of the risk of radial nerve injury related to the technique of external fixation applied to the distal humerus. Surg Radiol Anat 2010;32:221–224. 7. Malhotra NR, Shaffrey CI. Intraoperative electrophysiological monitoring in spine surgery. Spine (Phila Pa 1976) 2010;35:2167–2179. 8. Nuwer MR, Emerson RG, Galloway G, et al. Evidence-based guideline update: intraoperative spinal monitoring with somatosensory and transcranial electrical motor evoked potentials. J Clin Neurophysiol 2012;29:101–108. 9. Arrington ED, Hochschild DP, Steinagle TJ, Mongan PD, Martin SL. Monitoring of somatosensory and motor evoked potentials during open reduction and internal fixation of pelvis and acetabular fractures. Orthopedics 2000;23:1081–1083. 10. Farrell CM, Springer BD, Haidukewych GJ, Morrey BF. Motor nerve palsy following primary total hip arthroplasty. J Bone Joint Surg [Am] 2005;87-A:2619–2625. 11. Warrender WJ, Oppenheimer S, Abboud JA. Nerve monitoring during proximal humeral fracture fixation: what have we learned? Clin Orthop Relat Res 2011;469:2631–2637. 12. Makarov MR, Delgado MR, Birch JG, Samchukov ML. Intraoperative SSEP monitoring during external fixation procedures in the lower extremities. J Pediatr Orthop 1996;16:155–160. 13. Makarov MR, Delgado MR, Birch JG, Samchukov ML. Monitoring peripheral nerve function during external fixation of upper extremities. J Pediatr Orthop 1997;17:663–667. 14. Makarov MR, Samchukov ML, Birch JG, et al. Acute deformity correction of lower extremities under SSEP-monitoring control. J Pediatr Orthop 2003;23:470–477. 15. Kelleher MO, Tan G, Sarjeant R, Fehlings MG. Predictive value of intraoperative neurophysiological monitoring during cervical spine surgery: a prospective analysis of 1055 consecutive patients. J Neurosurg Spine 2008;8:215–221. 16. Thuet ED, Winscher JC, Padberg AM, et al. Validity and reliability of intraoperative monitoring in pediatric spinal deformity surgery: a 23-year experience of 3436 surgical cases. Spine (Phila Pa 1976) 2010;35:1880–1886. 17. Correll J. Surgical correction of short stature in skeletal dysplasias. Acta Paediatr Scand 1991;377:143–148. 18. Prévot J, Guichet JM, Leneveu E, Kuhnast M. Bilateral lengthening of short lower limbs: 26 cases treated with the Ilizarov method. Chirurgie 1994-1995;120:360– 367 (in French).

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