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An evaluation of clinical and electrophysiologic tests in nerve injury diagnosis after mandibular sagittal split osteotomy
Int. J. Oral Maxillofac. Surg. 2003; 32: 15–23 doi:10.1054/ijom.2002.0325, available online at http://www.sciencedirect.com
Clinical Paper Orthognathic Surgery
An evaluation of clinical and electrophysiologic tests in nerve injury diagnosis after mandibular sagittal split osteotomy
T. Teerijoki-Oksa, S. Ja¨a¨skela¨inen, K. Forssell, A. Virtanen, H. Forssell Department of Oral and Maxillofacial Surgery and Clinical Neurophysiology, Turku University Central Hospital, Lemminka¨isenkatu 2, 20520 Turku, Finland
T. Teerijoki-Oksa, S. Ja¨a¨skela¨inen, K. Forssell, A. Virtanen, H. Forssell: An evaluation of clinical and electrophysiologic tests in nerve injury diagnosis after mandibular sagittal split osteotomy. Int. J. Oral Maxillofac. Surg. 2003; 32: 15–23. 2003 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Science Ltd. All rights reserved. Abstract. The yield of clinical sensory tests and electrophysiologic tests in the diagnostics of inferior alveolar nerve (IAN) damage after bilateral sagittal split osteotomy (BSSO) was studied. The diagnostic value of these tests was evaluated by comparing the test results to the degree of nerve damage at the end of the operation as documented by means of the intraoperative nerve conduction recording of the IAN. Twenty patients undergoing BSSO were analysed preoperatively and 2 weeks postoperatively. The frequency of the IAN disturbance ranged from 10% to 94% depending on the test method and the test site used. Of the clinical sensory tests, the touch detection threshold (TD) test was the most sensitive and clinically useful test. It also correlated best with the electrophysiologically verified intraoperative nerve damage (R= 0.603, P=0.017 on the right, R= 0.626, P=0.01 on the left). The blink reflex and quantitative cold detection threshold tests were almost as often abnormal as the TD-test, but nerve conduction study (NCS) was the most sensitive (88%) of all clinical and electrophysiologic tests. The frequency of abnormal findings in the electrophysiologic tests indicating IAN injury, 75% on the right side and 90% on the left side, corresponded exactly with the figures of subjective sensory alteration. Almost all electrophysiologic tests showed obvious associations with the objectively verified IAN damage. All tests, except the NCS, showed only moderate sensitivity. Specificity of the tests was generally high, the only exceptions being the TD test and the NCS. To increase the diagnostic accuracy of the testing and to detect different types of damage in different nerve fibre populations, a combination of different sensory and electrophysiologic tests is recommended.
Introduction Bilateral sagittal split osteotomy (BSSO) is known to involve a considerable 0901-5027/03/010015+09 $30.00/0
risk for inferior alveolar (IAN) nerve damage. The actual figures presented in different studies for nerve damage have, however, varied from 0% to 100%30,37.
Key words: inferior alveolar nerve; nerve injury; sensory tests; electrodiagnosis; sagittal split osteotomy; trigeminal nerve. Accepted for publication 29 June 2002
The varying results of the studies are thought to be explained by different follow-up times, different diagnostic methods used, lack of standardization of
2003 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Science Ltd. All rights reserved.
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Table 1. Clinical and electrophysiologic tests for evaluating nerve injury after BSSO Test Brush-stroke directional discrimination (BSD) Touch detection threshold (TD) Grating orientation discrimination (GO) Warm/cold discrimination (W/C) Sharp/blunt discrimination (S/B) Mental nerve blink reflex (BR) Cold detection threshold (CDT) Warm detection threshold (WDT) Heat pain threshold (HPT) Nerve conduction study (NCS)
examination methods, and the way the nerve damage has been defined. In most earlier studies, the diagnosis of IAN disturbance is based on the subjective report of the patient and clinical sensory tests4,6,17,21,40. Since subjective factors on the part of both the patient and the examiner contribute to the results, lack of objectivity is one of the problems associated with the use of clinical examination in the diagnosis of sensory nerve damage8. Furthermore, the diagnostic accuracy of the clinical tests is not precisely known, and there is no knowledge of the relationship between the postoperative test results and the objectively verified presence or absence of intraoperative IAN injury. Only a few studies have compared the results of clinical sensory tests with more objective electrophysiologic tests within the trigeminal distribution, with inconsistent results11,23,30,38, and no consensus on the ideal choice of test methods has been reached. Clinical electrodiagnosis of nerve injuries is based on not only needle EMG, but also on sensory and motor nerve conduction studies18,28, which have also been used for intraoperative monitoring9,13. We have previously developed a method for continuous monitoring of the IAN function during BSSO using nerve conduction recording16,31. The results of our studies indicate that the IAN is injured in almost all patients to various degrees at different stages of the BSSO31. In addition to nerve conduction recording, the electrophysiologic examination of brainstem reflexes, such as the blink reflex, has been shown to be useful in the diagnosis of both peripheral and central lesions within the trigeminal system2,14. To study the function of thin sensory A and C fibres, quantitative psychophysical measurement of warm and cold detection thresholds is used in the extremities29,35, but they have only rarely been applied in the
Sensory afferent fibre
Dependent measure
A-beta A-beta A-beta A-delta and C A-delta A-beta A-delta C C A-beta
Percent correct Minimum detectable force (mN) Minimum spatial period required for discrimination Percent correct Percent correct Latency in ms Degree C for cooling detection Degree C for warming detection Degree C for heat pain detection Latency in ms, amplitude in V
diagnostics of trigeminal nerve lesions30,33,38. The aim of the present study was to evaluate the frequency of early postoperative sensory disturbance after BSSO and to compare the yields of different clinical sensory tests and electrophysiologic tests. In addition, the diagnostic value of these tests was evaluated by comparing the postoperative results to the degree of nerve damage at the end of the operation as documented by means of the intraoperative monitoring of the IAN.
on the left side of the patient. Local anaesthetic was avoided, because the lidocaine–adrenaline solution has been found to cause peripheral slowing of the nerve conduction velocity (NCV) of the IAN. Other details of the surgical procedure and anaesthesia have been described earlier16,31. Subjective sensory disturbance
Twenty consecutive patients undergoing BSSO for correction of mandibular deformity in our hospital were studied. All patients (8 women, 12 men) had mandibular retrognathia. The age of the patients ranged from 17 to 51 years (mean 32.8 years). The Local Ethics Committee of the hospital approved the study protocol, and all patients gave informed consent for participation in the study.
Patients’ subjective symptoms and discomfort connected with the sensory alteration within the IAN distribution were asked about at 2 weeks postoperatively. Patients were asked to indicate the regions with altered sensation (e.g. diminished sensation or paraesthesia) with a yellow pencil, and those with total anaesthesia with a blue pencil on a schematic figure of the face. The area of the affected skin regions (in mm2) was measured from the drawings using a transparent square millimetre sheet. The performed clinical sensory and electrophysiologic tests are summarized in Table 1.
Surgical technique
Clinical sensory tests
The BSSOs were carried out using standard methods for this osteotomy32. On the medial side of the mandibular ramus, the duration of the medial retraction (medial opening) was kept as short as possible, and the compression and stretching of the IAN were kept as light as possible as described in detail earlier31. After completing the splitting of the mandible, the IAN was observed macroscopically and classified into four grades: 1=not exposed, 2=exposed, not manipulated, 3=exposed and manipulated, 4=lacerated. There were no total nerve transsections. The bone fragments were fixed together transbuccally with three bicortical titanium positional screws. Usually, a senior surgeon operated on the right side and a trainee
The testing procedures were explained and demonstrated to the patient before each test. The tests were done while the patient was sitting with his/her eyes closed in a peaceful room. The tests were performed bilaterally at the vermilion border of the lower lip, and on the mental skin region. The clinical sensory tests were performed in all patients preoperatively and 2 weeks postoperatively, with the exception that the chin region was not tested in the first four patients. Tests were always done in the same order and by the same investigator. To reduce bias, the examiner who performed the clinical sensory testing was blinded to the results of the electrophysiologic recordings and vice versa.
Material and methods
An evaluation of tests in nerve injury diagnosis Brush-stroke directional discrimination (BSD)
Tactile directional discrimination was tested with a 5 mm wide soft brush, swept manually along a 0.5 cm line on the test area5. Ten pairs of strokes were used, with randomly varying directions to the left or to the right. A twoalternative forced choice design was used in which the patient had to identify the interval containing a stimulus movement from right to left33. When the correct response percentage was above or equal to 80%, the result was considered normal. Touch detection threshold (TD)
Touch detection thresholds were measured using the Semmes–Weinstein Aesthesiometer (Stoelting Co., USA). The different diameter monofilaments bend at different forces to deliver calibrated stimulus intensities. The testing protocol was a simplified modification of that described by E5. Starting with the least-stiff filament (1.65), the filaments were applied perpendicular to the test site in three ascending series until the filament was detected. The patients were warned that stimuli would not be delivered in all trials. The median of these three values was considered the touch detection threshold. The highest preoperative threshold values, 2.83 for the lip and 3.22 for the chin, were chosen for upper normal limits.
Grating orientation discrimination (GO)
Spatial discrimination was tested with square-wave gratings cut into seven acrylic domes, 19 mm in diameter, consisting of parallel bars and grooves of equal widths. The groove widths ranged from 1 mm to 4 mm. The gratings were applied to the test area randomly in either a horizontal or a vertical direction. This process was repeated five times with each grating, starting with the grating having the narrowest grooves. The patient had to report the direction of the grooves. The threshold was determined by the grating with the narrowest grooves that resulted in d80% correct responses. The largest preoperatively detected threshold value, 3 mm, was chosen to represent the normal limit. Due to the almost total inability of the patients to discriminate the direction of the grooves on the chin region preoperatively, we decided to use the test only on the lower lip.
Warm/cold discrimination (W/C)
Warm/cold discrimination was determined with two small test tubes containing water. The temperature of the cold water was 15–20C and that of the warm water 40–45C. The test area was randomly touched with the test tubes 10 times and the patient had to decide whether the stimulus was warm or cold. The result of the test was deemed normal when d80% of the answers were correct. Sharp/blunt discrimination (S/B)
Sharp/blunt discrimination was tested using a mechanical probe with two heads, one sharp and the other blunt. The test area was touched randomly 10 times. The patient had to decide whether the stimulus was sharp or blunt. The result of the test was deemed normal when d80% of the answers were correct.
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vermilion border of the lower lip midway between the midline and the corner of the mouth, the anode lying 1 cm below on each side. The BR responses were recorded with surface electrodes from the eye closing muscles simultaneously on both sides with Viking IV EMG equipment (Nicolet Biomedical Instruments, Madison, WI, USA). The stimulus intensity was adjusted until sufficient to continuously evoke a reflex response, but kept under 30 mA to avoid spread to the neighbouring distributions. Eight single stimuli of 0.2 ms duration were delivered on both the right and the left sides at random intervals of 10 to 30 s. The latencies were measured to the onset of the R2i and R2c components on both sides. Out of eight responses, those with the shortest latencies were selected for analyses and compared to the reference values of our laboratory12.
Electrophysiologic recordings
Quantitative sensory tests (QST)
The patients underwent the mental nerve blink reflex test (BR), nerve conduction study (NCS) of the IAN, and quantitative sensory tests (QST) of the mental nerve distribution on both sides preoperatively and 2 weeks postoperatively. The recordings were made in a quiet, normally lighted and warm room (20– 22C), with the patient lying with his/her eyes open on a bed. Due to technical failure of the equipment, a QST was not performed in two patients preoperatively, and in three patients at 2 weeks postoperatively. In two of these cases, the QSTs were abnormal when tested later at 1 month postoperatively and, in the categorical statistical analyses, these thresholds were classified as abnormal also at the 2-week control. The BR test was not done in one case postoperatively. Intraoperative monitoring of the NCV of the IAN was performed in nineteen cases. Postoperatively, two patients refused the NCS, in fear of possible pain caused by the procedure. All postoperative electrophysiologic tests were performed at the same session.
The cold detection (CDT), warm detection (WDT), and heat pain (HPT) thresholds were separately measured within the mental nerve distribution. The classical method of limits7 was applied. For each threshold, six series of increasing intensities were given, and after deleting the highest and the lowest value, the mean of the remaining four threshold values was calculated to be used as the detection threshold. The thresholds were measured with Thermotest apparatus (Somedic Sales AB, Ho¨rby, Sweden) equipped with a small, hand-held, rectangular probe (816 mm) especially constructed for stimulating the face area. The thermode consisted of four Peltier elements that either cooled or warmed up linearly depending on the direction of the applied electric current changed by a subject-operated switch. The maximal temperature range was set at 10–50C for CDT and WDT, and 10–55C for HPT measurements, the baseline temperature at 30C, and the rate of temperature change at 1C. The intervals between the stimuli varied randomly between 2 and 6 s. Before the testing started, the subjects were instructed to press the switch button immediately they perceived a change in temperature (cooling or warming), and when they felt the warm stimulus to become painful. They were particularly told that the HPT measurement was not intended to test the pain tolerance but to detect the point when the stimulus changes from innocuous warming to noxious heat. The
Mental nerve blink reflex (BR)
The recording of the mental nerve BR has been described in detail earlier12,14,15. The BRs were elicited by electrical stimulation with a small bipolar surface electrode (DantecMedtronic, Skovlunde, Denmark) at 10 mm interelectrode distance. The stimulating cathode was placed on the
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facial skin was wiped with denatured alcohol solution to delete facial grease and make-up before the probe was placed firmly on the skin, at the centre of the small distribution of the mental nerve. On each side, the CDT was always measured first, then the WDT, and last the HPT. The amount of change (in C) from the baseline temperature to the CDT, WDT and HPT was used in further analyses, and compared to the reference values of our laboratory. Nerve conduction study (NCS)
The technique for orthodromic recording13 and intraoperative monitoring16,31 of NCV of the IAN has been described in detail elsewhere. Eight-channel EMG devices (Viking I and IV, Nicolet Biomedical Instruments, Madison, WI, USA) were used for the recordings. A teflon-coated silver wire electrode (Pure silver multistrand, AG7/40T, Leico industries, Inc., USA) was used as the active electrode, and a silver–silver chloride surface electrode as the reference in the operating room. At the outpatient controls, two disposable monopolar needle electrodes (13R12 and 13R31, Dantec-Medtronic, Skovlunde, Denmark) were used for the recording. The active recording electrodes were inserted beneath the zygomatic arch in front of the temporomandibular joint to a depth of about 4.5 cm, to lie near the oval foramen. The electrical stimuli (square-wave pulses with a duration of 0.2 ms) were given at the mental foramen via two disposable monopolar needle electrodes (in the operating room; 13R21 and 13R22 Dantec-Medtronic) or a bipolar surface electrode (at out-patient controls, 13L35, DantecMedtronic). The onset latencies of the responses and the amplitudes from baseline to negative peak were determined from the recordings, and NCV was calculated. These variables were used in the analyses and compared with the reference values of our laboratory13 for normality.
Fig. 1. a and b. Frequency of IAN disturbance as documented by clinical sensory tests on the lip (a) and on the chin region (b) 2 weeks after BSSO (BSD=brush-stroke directional discrimination, TD=touch detection threshold, GO=grating orientation discrimination, W/C=warm/cold discrimination and S/B=sharp/blunt discrimination).
of the operation and the test results at the 2-week control were assessed using the Spearman Correlation Coefficient. All reported P-values are two-sided. Calculations were performed with the SAS software package (version 6.12, SAS Institute, Cary, NC, USA).
Statistical methods
When calculating the specificity and sensitivity of different clinical and electrophysiologic tests, the cases with intraoperative over 50% amplitude decrement of the nerve action potential (NAP) and/or latency over 2 ms were considered indicative of intraoperative nerve damage. The relationship between the nerve conduction parameters at the end
Results
the chin region 2 weeks postoperatively. One of the patients had total anaesthesia of the whole mental nerve distribution on the right side and three on the left side. The mean size of the affected region on the schematic figures of the faces was 124 mm2 on the right side and 135 mm2 on the left side.
Subjective sensory disturbance
The frequencies of IAN disturbances in clinical tests
Preoperatively, none of the patients had clinical sensory IAN disturbances. Fifteen patients (75%) reported some degree of subjective sensory disturbance on the right side and 18 (90%) patients on the left side of the lower lip and/or
In different clinical sensory tests, the frequency of IAN disturbance varied between 10% and 56%. On the lip (Fig. 1a), the GO test showed the highest and the BSD test the lowest percentage of sensory disturbance. In fact, the GO
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An evaluation of tests in nerve injury diagnosis
the left side. In all, different clinical tests indicated higher frequencies of IAN disturbance on the chin region and the left side. There were no subjects with abnormal findings on the lip region and normal findings on the chin region. The frequencies of IAN disturbances in electrophysiologic tests
The different electrophysiologic tests indicated nerve damage in from 29% to 94% of the nerves recorded, NCS showing the highest frequency of injury (Fig. 2). When abnormal response in at least one of the five electrophysiologic tests was considered to indicate IAN injury, the frequencies were 75% on the right side and 90% on the left side. Fig. 2. Frequency of abnormal findings in different electrophysiologic tests 2 weeks after BSSO (BR=blink reflex, CDT=cold detection threshold, WDT=warm detection threshold, HPT=heat pain threshold and NCS=nerve conduction study).
Correlation of different postoperative test results and electrophysiologically verified intraoperative IAN injury
test indicated nerve damage on the right side in two cases, where all other clinical tests showed normal responses: both nerves had shown signs of significant intraoperative nerve damage. In the first case, the NAP of the IAN had totally disappeared during medial preparation of the ramus and did not recover during surgery. There was subjective sensory alteration postoperatively, but the electrophysiologic parameters included in the study were just within the reference limits (the nerve conduction velocity was slow, however). In the other case, a partial nerve laceration occurred during the splitting of the mandible, and the patient had clear subjective sensory disturbance postoperatively with abnormal findings in all other
Patients reporting a larger area of sensory disturbance had more pronounced NAP decrement during the operation compared to patients with more limited postoperative disturbances (right side R= 0.50988 P=0.0306 and left side R= 0.61957 P=0.0047). The detailed results of the correlation analyses between the electrophysiologic grade of intraoperative nerve damage and postoperative clinical sensory and electrophysiologic test results are presented in Table 2. Of the clinical tests, the TD test showed the closest association with the degree of nerve injury at the end of the operation. Other clinical sensory tests yielded significant correlation with the objectively verified nerve damage only occasionally on the chin area. Except for the HPT test, all other
electrophysiologic tests except the WDT and the HPT. When abnormal response in at least one of the five clinical tests of the lip was considered to indicate IAN injury, the frequencies of nerve damage were 45% on the right side and 55% on the left side. On the chin area (Fig. 1b), clinical tests indicated identical incidence of IAN injuries, with the exception that the TD test showed a clearly higher frequency of sensory disturbance. In two cases the TD test was the only clinical test which, in addition to the electrophysiologic tests, indicated nerve injury. When abnormal response in at least one of the four clinical tests was considered to indicate IAN injury, the frequencies were 53% on the right side and 65% on
Table 2. Correlation of different postoperative test results and electrophysiologically verified intraoperative IAN injury BSD lip Intraoperative IAN damage Right side Intraoperative IAN damage
R P R P
Left side
0.227 ns (18) 0.246 ns (19) NAP amplitude
Intraoperative IAN damage Right side Intraoperative IAN damage Left side
R P R P
0.724 0.002 (15) 0.803 0.0002 (16)
BSD chin 0.471 ns (15) 0.715 0.002 (16)
TD lip 0.567 0.014 (18) 0.618 0.005 (19)
Clinical sensory tests TD chin GO lip 0.603 0.017 (15) 0.626 0.01 (16)
Electrophysiologic tests BR CDT WDT 0.481 0.051 (17) 0.703 0.001 (18)
0.589 0.021 (15) 0.522 0.038 (16)
0.74 0.002 (15) 0.619 0.011 (16)
0.566 0.014 (18) 0.353 ns (19)
W/C lip
W/C chin
S/B lip
S/B chin
0.401 ns (18) 0.338 ns (19)
0.516 0.049 (15) 0.580 0.019 (16)
0.322 ns (18) 0.424 ns (19)
0.516 0.049 (15) 0.317 ns (16)
HPT 0.278 ns (15) 0.437 ns (16)
Number of observations in parentheses; R, Spearman correlation coefficient; P, statistical significance; ns, not statistically significant.
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electrophysiologic tests showed a clear association with objectively verified intraoperative IAN damage. Correlation of macroscopic nerve lesions to findings in different sensory tests
During the BSSO, 25 nerves were partly exposed, five were exposed and manipulated, and seven were partially lacerated. The macroscopic appearance of the IAN during the BSSO was not associated with the clinical sensory test results. However, QST threshold values showed significant correlation (CDT R=0.55 P=0.021, WDT R=0.64 P=0.06, HPT R=0.563, P=0.019) with the macroscopic damage of the IAN on the left side. The NCV of the IAN was abnormal in all laceration cases 2 weeks postoperatively. Sensitivity and specificity: Figs 3a, 3b and 4 show the sensitivity and specificity of different clinical sensory and electrophysiologic tests. All tests, except the NCS, showed only moderate sensitivity. On the whole, the electrophysiologic tests were somewhat more sensitive than the clinical tests. On the other hand, the specificity of the tests was generally high, the only exceptions being the TD test on the chin region and the NCS. The four nerves showing false positive findings in the postoperative NCS coincided, however, with subjective complaints of postoperative sensory alteration in the IAN distribution. Discussion In general, the efficacy of diagnostic tests is defined as their ability to indicate the presence or absence of disease. An ideal diagnostic sensory test would always be positive in the presence of nerve injury, and negative in the absence of injury42. However, the relationship between the results of different sensory tests and the actual, objectively verified nerve damage after BSSO (or other trigeminal nerve injuries) has never been studied. So far, only few attempts have been made to elucidate the relationship between macroscopically verified nerve lesions and the diagnostic accuracy of clinical sensory tests in patients with previous nerve injuries and sensory complaints42. In addition, some authors have investigated the association between macroscopic intraoperative events and the incidence of postoperative sensory alteration with inconsistent results6,21,27,36. In this respect, it is of interest that, in this study, the macroscopic grade of intraoperative
Fig. 3. a and b. Sensitivity and specificity of different clinical sensory tests on the lip (a) and on the chin region (b) (abbreviations as in Fig. 1).
nerve damage as reported by the surgeon was not significantly associated with any of the clinical or electrophysiologic tests (with the exception of the QST on the left side), nor with the subjective report of sensory alteration 2 weeks postoperatively. This indicates that seemingly intact nerves may have suffered considerable injury due to compression and stretching, which will go unnoticed without intraoperative monitoring11,16. However, all cases with nerve laceration showed symptoms and signs of nerve injury at postoperative control. To evaluate the occurrence of IAN disturbance in the early postoperative stage after BSSO, the most standardized, and widely used clinical test methods
which can easily be adapted to routine chair-side postoperative follow-up were chosen5,6,17,21,33,41. Spatial resolution was examined using the GO test, because the two-point discrimination test has not been considered reliable5,25,33. Two test sites were used, because the somatosensory characteristics of the vermilion border of the lower lip and the mental skin region are different26, and because other investigators have routinely used both of these regions. All the electrophysiologic tests applied in the study are routinely used to assess peripheral nerve function. The NCS gives detailed information about the conductive properties and number of thick myelinated sensory A fibres9,18.
An evaluation of tests in nerve injury diagnosis
Fig. 4. Sensitivity and specificity of different electrophysiologic tests (abbreviations as in Fig. 2).
The BR studies the same trigeminal sensory fibres and, in addition, their central connections within the brainstem2,18. The QST is the only clinically available quantitative method for evaluation of the thinly myelinated A and the unmyelinated C fibres29,35. These electrophysiologic techniques are able to verify different types of nerve damage that may occur due to compression, stretching, laceration, and ischaemia during BSSO. In the present study, the degree of nerve damage at the end of the BSSO operation, as documented by means of the intraoperative monitoring of the IAN, was used as ‘the gold standard’. The 2-week time point was chosen for postoperative investigation in order to avoid testing during the time when swelling and pain are most severe. However, postoperative oedema can cause compression, which increases or even gives rise to nerve dysfunction during the immediate postoperative period20. A limitation of the present study is the possibility that the status of the nerve may have changed during the 2-week period, as was actually indicated by four cases where the NCV of the IAN was normal at the end of the operation but abnormal 2 weeks postoperatively, with corresponding subjective sensory alteration. In three additional cases, the NCV of the IAN was abnormal at the end of the operation but normal 2 weeks postoperatively, indicating that the intraoperative dysfunction of the IAN was probably mainly caused by mild compression or ischaemia from which the
nerve can recover even in a few hours19. These probable regenerative and degenerative processes weaken ‘the gold standard’ of this study, and thus influence the calculated sensitivity and specificity values, especially those of the most accurate TD test and NCS. In general, however, the NAP amplitude at 2 weeks correlated well with the NAP amplitude at the end of the operation. In addition to direct orthodromic recording of the NCV of the IAN, also trigeminal somatosensory evoked potentials (TSEP) have been applied to study the function of the IAN in patients with postoperative nerve damage11,23,24. In all these studies inconstant middle-latency waveforms have been utilized. The reliability of these TSEPs-components has, however, been questioned2,9. In addition, cortical SEP may overlook peripheral nerve damage because of central amplification of the responses10. The frequencies of the IAN disturbances ranged widely, depending on the test method and the test site used, as reported in many other studies6,11,17,21, 33,40 . The most sensitive clinical tests were the GO and TD tests, a finding which is in agreement with earlier reports1,34,33,38. Other clinical tests were much less sensitive, e.g. the W/C test showed considerably less thin fibre dysfunction compared to the quantitative CDT and WDT tests. The clinical utility of the TD test in particular is greatly emphasized by the good correlation of this test with the electrophysically verified intraoperative nerve damage. In agreement with earlier observations25,
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the use of the GO test had to be limited to the vermilion region because the patients were mostly not able to discriminate the direction of the grooves when tested on the chin region. In addition, the recorded threshold values at 2 weeks were inconsistent in six cases, showing lower values at 2 weeks despite the fact that according to by other measures, nerve damage had occurred. Thus, the clinical usefulness of the GO test can be considered somewhat questionable. Clinical sensory tests indicated a slightly higher percentage of IAN nerve damage on the chin compared to the lip region. The fact that no subjects with abnormal findings on the lip region had normal findings on the chin region, whereas several patients with abnormal sensitivity on the chin region had normal test results on the lip indicates that testing on the vermilion border might not add to the information obtained. The subjective sensory disturbances corresponded with the aforementioned; the chin region was more frequently affected compared to the lip. The good correlation of many of the clinical sensory tests performed on the chin region with the intraoperatively verified nerve damage supports the use of the chin as the test site when diagnosing nerve injuries connected to BSSO operations. The frequencies of the electrophysiologic tests indicating IAN injury, 75% on the right side and 90% on the left side, corresponded exactly with the figures of subjective sensory disturbance. Electrophysiologic tests were, on average, slightly more sensitive than the clinical sensory tests. Of the individual tests, the NCS yielded the highest frequencies of nerve injury. The WDT and HPT test results indicated lower frequencies than the BR and CDT tests. This difference may be due to the nature of nerve damage connected with BSSO operation; the main type of injury was compression of the nerve31. Compression causes more damage to myelinated A and A fibres than to unmyelinated C fibres19. All electrophysiologic tests except the HPT test, correlated well with the objectively verified nerve injury, thus supporting their clinical use. The poorer correlation of the HPT test can be due to the wide normal range of pain detection thresholds22,39 that may be related to the more subjective nature of HPT. All tests showed high specificity, and thus false positive results were exceptional, associated mainly with NCS and the TD test on the chin region. This can
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be due to their good sensitivity to detect possible further injury of the nerve caused by postoperative events. In general, the sensitivity of the clinical tests was rather low, especially, the BSD, W/C and S/B tests often gave false negative results. The BSD, W/C and S/B tests can thus be considered rather crude and insensitive chair-side methods, especially as regards the diagnosis of the less severe nerve injuries that mainly occurred in the present study. The material in this study may have consisted of minor nerve damage in comparison with damage connected with BSSO in general, as we have already modified our operation technique e.g. by using refined instruments for medial retraction during subperiosteal preparation, by exerting as light compression as possible on the nerve trunk with the retractor, and by trying to keep the total duration of the medial soft tissue retraction as short as possible16,31. Additionally, we were able to reduce nerve damage in these patients by means of continuous intraoperative monitoring of the IAN. The clinical neurophysiologist could warn the surgeon of a threatening IAN injury during the medial retraction, splitting or fixation16,31. Of the electrophysiologic tests, the NCS showed high sensitivity, whereas the sensitivity of the BR, CDT and WDT tests was only slightly higher than that of the clinical TD and GO tests. The moderate sensitivity of electrophysiologic and clinical tests can be due to the fact that different tests measure different nerve fibres and, thus, their sensitivity in different types of nerve injury can vary, e.g. the BR test is more sensitive to demyelinating compression injuries, and the QST tests to laceration injuries causing partial axonal damage. To increase the diagnostic sensitivity, a combination of different tests is mandatory. To conclude, the frequency of nerve injury at the early postoperative stage after BSSO varied widely, depending on the test and the test site used. The most sensitive and clinically useful clinical sensory test was the TD test, which gives quantitative data that may be used in the follow-up of recovery. The electrophysiologic NCS and QST tests increase the diagnostic sensitivity and add to the diagnostic accuracy by detecting different types of damage in different nerve fibre populations. Acknowledgment. The study was supported by a grant from the Finnish Association for the Study of Pain.
References 1. C RL, S RG, H SW. Assessment of recovery from injury to inferior alveolar and mental nerves. Oral Surg Oral Med Oral Pathol 1987: 64: 519–526. 2. C W. Conduction velocity of the human inferior alveolar nerve: a preliminary report. J Oral Maxillofac Surg 1995: 53: 1300–1023. 3. C G, A R, I M, I P, R A, M M. Mandibular nerve involvement in diabetic polyneuropathy and chronic inflammatory demyelinating polyneuropathy. Muscle Nerve 1998: 21: 1673–1679. 4. C LL, T BD, C GM, B RA, K SD, R JD. A comparison of questionnaire versus monofilament assessment of neurosensory deficit. J Oral Maxillofac Surg 1996: 54: 454–459. 5. E GK. Comprehensive clinical evaluation of perioral sensory function. Oral Maxillofac Surg Clin North Am 1992: 4: 503–526. 6. F KL, H TJ, P KJ, B MJ. Neurosensory recovery following the mandibular bilateral sagittal split osteotomy. J Oral Maxillofac Surg 1995: 53: 1300–1306. 7. F H, L U, S WG. Method for quantitative estimation of thermal thresholds in patients. J Neurol Neurosurg Psychiatry 1976: 39: 1071–1075. 8. G GE, E BN. Clinical neurosensory testing: Practical applications. J Oral Maxillofac Surg 1989: 47: 1074–1078. 9. H CM J. Cranial nerve monitoring. Syllabus for Course F, annual meeting of the American Association of Electrodiagnostic Medicine, Orlando, FL, October 1998: 23–31. 10. H CM J. Somatosensory evoked potentials. In: Daube JR, ed.: Clinical Neurophysiology. Philadelphia: F.A. Davis Company 1996: 157–170. 11. J DL, W LM. Intraoperative recording of trigeminal evoked potentials during orthognathic surgery. Int J Adult Orthod Orthognath Surg 1990: 5: 167–174. 12. J¨ ¨ ¨ S. Blink reflex with stimulation of the mental nerve. Methodology, reference values, and some clinical vignettes. Acta Neurol Scand 1995: 91: 477–482. 13. J¨ ¨ ¨ SK. A new technique for recording sensory conduction velocity of the inferior alveolar nerve. Muscle Nerve 1999: 22: 455–459. 14. J¨ ¨ ¨ SK, P JK. Clinical application of the blink reflex with stimulation of the mental nerve in lesion of the inferior alveolar nerve. Neurology 1994: 44: 2356–2361.
15. J¨ ¨ ¨ SK, P JK, L R. The mental blink reflex in the diagnosis of lesions of the inferior alveolar nerve following orthognathic surgery of the mandible. Br J Oral Maxillofac Surg 1996: 34: 87–95. 16. J¨ ¨ ¨ SK, T-O T, F K, V¨ ¨ K, P JK, F H. Intraoperative monitoring of the inferior alveolar nerve during mandibular sagittal-split osteotomy. Muscle Nerve 2000: 23: 368–375. 17. K ND, B SB, S DP. Recovery of neurosensory function following orthognathic surgery. J Oral Maxillofacial Surg 1990: 48: 124–134. 18. K J. Anatomy and physiology of the peripheral nerve. In: Electrodiagnosis in Diseases of the Nerve and Muscle: Principles and Practice. Philadelphia: F.A. Davis Company 1989: 55–77. 19. K DG, H AR. Nerve Injuries. Operative Results for Major Nerve Injuries, Entrapments, and Tumours. Philadelphia: W.B. Saunders Company 1995: 41–53. 20. L AK, B FY-S, J RK, P LH, Y CD. Delayed onset facial nerve dysfunction following acoustic neuroma surgery. Am J Otology 1995: 16: 758–764. 21. L JI, G-M OT. Sensory impairment following sagittal split osteotomy for correction of mandibular retrognathism. Int J Adult Ortod Orthognath Surg 1991: 6: 161–167. 22. M D, Dˇ M. Quantitative assessment of thermal and pain sensitivity. J Neurol Sci 1994: 127: 164–169. 23. N K, U K, M N, T S, Y E, O H. The assessment of trigeminal sensory nerve paraesthesia after sagittal split osteotomy: modified somatosensory evoked potentials recording method. J Craniomaxillofac Surg 1997: 25: 97–101. 24. N K, U T, T S, T D, Y E. Somatosensory-evoked potential to evaluate the trigeminal nerve after sagittal split osteotomy. Oral Surg Oral Med Oral Pathol Oral Endod 2001: 91: 146–152. 25. P, E GK, K DG. Utility of square-wave gratings to assess perioral spatial acuity. J Oral Maxillofac Surg 1997: 55: 593–601. 26. R EM, E GK. Perioral somesthetic sensibility: Do the skin of the lower face and the midface exhibit comparable sensitivity? J Oral Maxillofac Surg 1990: 48: 1181–1190. 27. R PP. Observations of the recovery of sensation following inferior alveolar nerve injuries. Br J Oral Maxillofac Surg 1988: 26: 177–189. 28. R LR. Traumatic injury to peripheral nerves. Muscle Nerve 2000: 23: 863–873. 29. S S, F T, E ML. Neurophysiological studies of thin
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myelinated (A delta) and unmyelinated (C) fibers: application to peripheral neuropathies. Neurophysiol Clin 2000: 30: 27–42. S-M S, K H, O R, N FW. A prospective electromyographic and computer-aided thermal sensitivity assessment of nerve lesions after sagittal split osteotomy and Le Fort I osteotomy. J Oral Maxillofacial Surg 2001: 59: 128–139. doi:10.1053/joms. 2001.20480. T-O T, J¨ ¨ ¨ S, F K, F H, V¨ ¨ K, T T, V A. Risk factors of nerve injury during mandibular sagittal split osteotomy. Int J Oral Maxillofac Surg 2002: 31: 33–39. doi:10.1054/ ijom.2001.0157. T BC, W RP J. Mandibular ramus surgery. In: Proffit WR, White RP. Jr, eds: Surgical-Orthodontic Treatment. St. Louis: Mosby 1991: 264–282. B R, J KA. Psychophysical study of the mechanisms of sensory recovery following nerve injury in humans. Brain 1994: 117: 149–167.
34. S JE, Z M, N GJ, T WJ. A comparative study of normal sensibility of the inferior alveolar nerve and the infraorbital nerve. Oral Surg Oral Med Oral Pathol 1989: 67: 255–257. 35. V R, O JL. Quantitative somatosensory thermotest. A key method for functional evaluation of small caliber afferent channels. Brain 1992: 115: 893–913. 36. W A, B H, K L. Inferior alveolar nerve function after sagittal split osteotomy of the mandible: correlation with degree of intraoperative nerve encounter and other variables in 496 operations. Br J Oral Maxillofac Surg 1998: 36: 429–433. 37. W A. On inferior alveolar nerve function after sagittal split osteotomy of the mandible. Thesis. Stockholm: 1999: 11. 38. W A, E L, B U. Neurosensory function after sagittal split osteotomy of the mandible: A comparison between subjective evaluation and objective assessment. Int J Adult Orthod Orthognath Surg 1999: 14: 268–275.
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39. Y D, S E, Z R, H JA. Heat pain thresholds. Normative data and repeatability. Pain 1995: 60: 329–332. 40. Y L, K J, O K. Comparison of different tests assessing neurosensory disturbances after bilateral sagittal split osteotomy. Int J Oral Maxillofac Surg 1998: 27: 417–421. 41. Z JR, E GK. A contemporary approach to the clinical evaluation of trigeminal nerve injuries. Oral Maxillofac Surg Clin North Am 1992: 4: 353–366. 42. Z JR, M RA, G JM, M M, D LF. The accuracy of clinical neurosensory testing for nerve injury diagnosis. J Oral Maxillofac Surg 1998: 56: 2–8.
Address: Tuija Teerijoki-Oksa Department of Oral and Maxillofacial Surgery Turku University Central Hospital Lemminka¨isenkatu 2, 20520 Turku, Finland E-mail: [email protected]
Clinical Paper Orthognathic Surgery
An evaluation of clinical and electrophysiologic tests in nerve injury diagnosis after mandibular sagittal split osteotomy
T. Teerijoki-Oksa, S. Ja¨a¨skela¨inen, K. Forssell, A. Virtanen, H. Forssell Department of Oral and Maxillofacial Surgery and Clinical Neurophysiology, Turku University Central Hospital, Lemminka¨isenkatu 2, 20520 Turku, Finland
T. Teerijoki-Oksa, S. Ja¨a¨skela¨inen, K. Forssell, A. Virtanen, H. Forssell: An evaluation of clinical and electrophysiologic tests in nerve injury diagnosis after mandibular sagittal split osteotomy. Int. J. Oral Maxillofac. Surg. 2003; 32: 15–23. 2003 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Science Ltd. All rights reserved. Abstract. The yield of clinical sensory tests and electrophysiologic tests in the diagnostics of inferior alveolar nerve (IAN) damage after bilateral sagittal split osteotomy (BSSO) was studied. The diagnostic value of these tests was evaluated by comparing the test results to the degree of nerve damage at the end of the operation as documented by means of the intraoperative nerve conduction recording of the IAN. Twenty patients undergoing BSSO were analysed preoperatively and 2 weeks postoperatively. The frequency of the IAN disturbance ranged from 10% to 94% depending on the test method and the test site used. Of the clinical sensory tests, the touch detection threshold (TD) test was the most sensitive and clinically useful test. It also correlated best with the electrophysiologically verified intraoperative nerve damage (R= 0.603, P=0.017 on the right, R= 0.626, P=0.01 on the left). The blink reflex and quantitative cold detection threshold tests were almost as often abnormal as the TD-test, but nerve conduction study (NCS) was the most sensitive (88%) of all clinical and electrophysiologic tests. The frequency of abnormal findings in the electrophysiologic tests indicating IAN injury, 75% on the right side and 90% on the left side, corresponded exactly with the figures of subjective sensory alteration. Almost all electrophysiologic tests showed obvious associations with the objectively verified IAN damage. All tests, except the NCS, showed only moderate sensitivity. Specificity of the tests was generally high, the only exceptions being the TD test and the NCS. To increase the diagnostic accuracy of the testing and to detect different types of damage in different nerve fibre populations, a combination of different sensory and electrophysiologic tests is recommended.
Introduction Bilateral sagittal split osteotomy (BSSO) is known to involve a considerable 0901-5027/03/010015+09 $30.00/0
risk for inferior alveolar (IAN) nerve damage. The actual figures presented in different studies for nerve damage have, however, varied from 0% to 100%30,37.
Key words: inferior alveolar nerve; nerve injury; sensory tests; electrodiagnosis; sagittal split osteotomy; trigeminal nerve. Accepted for publication 29 June 2002
The varying results of the studies are thought to be explained by different follow-up times, different diagnostic methods used, lack of standardization of
2003 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Science Ltd. All rights reserved.
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Table 1. Clinical and electrophysiologic tests for evaluating nerve injury after BSSO Test Brush-stroke directional discrimination (BSD) Touch detection threshold (TD) Grating orientation discrimination (GO) Warm/cold discrimination (W/C) Sharp/blunt discrimination (S/B) Mental nerve blink reflex (BR) Cold detection threshold (CDT) Warm detection threshold (WDT) Heat pain threshold (HPT) Nerve conduction study (NCS)
examination methods, and the way the nerve damage has been defined. In most earlier studies, the diagnosis of IAN disturbance is based on the subjective report of the patient and clinical sensory tests4,6,17,21,40. Since subjective factors on the part of both the patient and the examiner contribute to the results, lack of objectivity is one of the problems associated with the use of clinical examination in the diagnosis of sensory nerve damage8. Furthermore, the diagnostic accuracy of the clinical tests is not precisely known, and there is no knowledge of the relationship between the postoperative test results and the objectively verified presence or absence of intraoperative IAN injury. Only a few studies have compared the results of clinical sensory tests with more objective electrophysiologic tests within the trigeminal distribution, with inconsistent results11,23,30,38, and no consensus on the ideal choice of test methods has been reached. Clinical electrodiagnosis of nerve injuries is based on not only needle EMG, but also on sensory and motor nerve conduction studies18,28, which have also been used for intraoperative monitoring9,13. We have previously developed a method for continuous monitoring of the IAN function during BSSO using nerve conduction recording16,31. The results of our studies indicate that the IAN is injured in almost all patients to various degrees at different stages of the BSSO31. In addition to nerve conduction recording, the electrophysiologic examination of brainstem reflexes, such as the blink reflex, has been shown to be useful in the diagnosis of both peripheral and central lesions within the trigeminal system2,14. To study the function of thin sensory A and C fibres, quantitative psychophysical measurement of warm and cold detection thresholds is used in the extremities29,35, but they have only rarely been applied in the
Sensory afferent fibre
Dependent measure
A-beta A-beta A-beta A-delta and C A-delta A-beta A-delta C C A-beta
Percent correct Minimum detectable force (mN) Minimum spatial period required for discrimination Percent correct Percent correct Latency in ms Degree C for cooling detection Degree C for warming detection Degree C for heat pain detection Latency in ms, amplitude in V
diagnostics of trigeminal nerve lesions30,33,38. The aim of the present study was to evaluate the frequency of early postoperative sensory disturbance after BSSO and to compare the yields of different clinical sensory tests and electrophysiologic tests. In addition, the diagnostic value of these tests was evaluated by comparing the postoperative results to the degree of nerve damage at the end of the operation as documented by means of the intraoperative monitoring of the IAN.
on the left side of the patient. Local anaesthetic was avoided, because the lidocaine–adrenaline solution has been found to cause peripheral slowing of the nerve conduction velocity (NCV) of the IAN. Other details of the surgical procedure and anaesthesia have been described earlier16,31. Subjective sensory disturbance
Twenty consecutive patients undergoing BSSO for correction of mandibular deformity in our hospital were studied. All patients (8 women, 12 men) had mandibular retrognathia. The age of the patients ranged from 17 to 51 years (mean 32.8 years). The Local Ethics Committee of the hospital approved the study protocol, and all patients gave informed consent for participation in the study.
Patients’ subjective symptoms and discomfort connected with the sensory alteration within the IAN distribution were asked about at 2 weeks postoperatively. Patients were asked to indicate the regions with altered sensation (e.g. diminished sensation or paraesthesia) with a yellow pencil, and those with total anaesthesia with a blue pencil on a schematic figure of the face. The area of the affected skin regions (in mm2) was measured from the drawings using a transparent square millimetre sheet. The performed clinical sensory and electrophysiologic tests are summarized in Table 1.
Surgical technique
Clinical sensory tests
The BSSOs were carried out using standard methods for this osteotomy32. On the medial side of the mandibular ramus, the duration of the medial retraction (medial opening) was kept as short as possible, and the compression and stretching of the IAN were kept as light as possible as described in detail earlier31. After completing the splitting of the mandible, the IAN was observed macroscopically and classified into four grades: 1=not exposed, 2=exposed, not manipulated, 3=exposed and manipulated, 4=lacerated. There were no total nerve transsections. The bone fragments were fixed together transbuccally with three bicortical titanium positional screws. Usually, a senior surgeon operated on the right side and a trainee
The testing procedures were explained and demonstrated to the patient before each test. The tests were done while the patient was sitting with his/her eyes closed in a peaceful room. The tests were performed bilaterally at the vermilion border of the lower lip, and on the mental skin region. The clinical sensory tests were performed in all patients preoperatively and 2 weeks postoperatively, with the exception that the chin region was not tested in the first four patients. Tests were always done in the same order and by the same investigator. To reduce bias, the examiner who performed the clinical sensory testing was blinded to the results of the electrophysiologic recordings and vice versa.
Material and methods
An evaluation of tests in nerve injury diagnosis Brush-stroke directional discrimination (BSD)
Tactile directional discrimination was tested with a 5 mm wide soft brush, swept manually along a 0.5 cm line on the test area5. Ten pairs of strokes were used, with randomly varying directions to the left or to the right. A twoalternative forced choice design was used in which the patient had to identify the interval containing a stimulus movement from right to left33. When the correct response percentage was above or equal to 80%, the result was considered normal. Touch detection threshold (TD)
Touch detection thresholds were measured using the Semmes–Weinstein Aesthesiometer (Stoelting Co., USA). The different diameter monofilaments bend at different forces to deliver calibrated stimulus intensities. The testing protocol was a simplified modification of that described by E5. Starting with the least-stiff filament (1.65), the filaments were applied perpendicular to the test site in three ascending series until the filament was detected. The patients were warned that stimuli would not be delivered in all trials. The median of these three values was considered the touch detection threshold. The highest preoperative threshold values, 2.83 for the lip and 3.22 for the chin, were chosen for upper normal limits.
Grating orientation discrimination (GO)
Spatial discrimination was tested with square-wave gratings cut into seven acrylic domes, 19 mm in diameter, consisting of parallel bars and grooves of equal widths. The groove widths ranged from 1 mm to 4 mm. The gratings were applied to the test area randomly in either a horizontal or a vertical direction. This process was repeated five times with each grating, starting with the grating having the narrowest grooves. The patient had to report the direction of the grooves. The threshold was determined by the grating with the narrowest grooves that resulted in d80% correct responses. The largest preoperatively detected threshold value, 3 mm, was chosen to represent the normal limit. Due to the almost total inability of the patients to discriminate the direction of the grooves on the chin region preoperatively, we decided to use the test only on the lower lip.
Warm/cold discrimination (W/C)
Warm/cold discrimination was determined with two small test tubes containing water. The temperature of the cold water was 15–20C and that of the warm water 40–45C. The test area was randomly touched with the test tubes 10 times and the patient had to decide whether the stimulus was warm or cold. The result of the test was deemed normal when d80% of the answers were correct. Sharp/blunt discrimination (S/B)
Sharp/blunt discrimination was tested using a mechanical probe with two heads, one sharp and the other blunt. The test area was touched randomly 10 times. The patient had to decide whether the stimulus was sharp or blunt. The result of the test was deemed normal when d80% of the answers were correct.
17
vermilion border of the lower lip midway between the midline and the corner of the mouth, the anode lying 1 cm below on each side. The BR responses were recorded with surface electrodes from the eye closing muscles simultaneously on both sides with Viking IV EMG equipment (Nicolet Biomedical Instruments, Madison, WI, USA). The stimulus intensity was adjusted until sufficient to continuously evoke a reflex response, but kept under 30 mA to avoid spread to the neighbouring distributions. Eight single stimuli of 0.2 ms duration were delivered on both the right and the left sides at random intervals of 10 to 30 s. The latencies were measured to the onset of the R2i and R2c components on both sides. Out of eight responses, those with the shortest latencies were selected for analyses and compared to the reference values of our laboratory12.
Electrophysiologic recordings
Quantitative sensory tests (QST)
The patients underwent the mental nerve blink reflex test (BR), nerve conduction study (NCS) of the IAN, and quantitative sensory tests (QST) of the mental nerve distribution on both sides preoperatively and 2 weeks postoperatively. The recordings were made in a quiet, normally lighted and warm room (20– 22C), with the patient lying with his/her eyes open on a bed. Due to technical failure of the equipment, a QST was not performed in two patients preoperatively, and in three patients at 2 weeks postoperatively. In two of these cases, the QSTs were abnormal when tested later at 1 month postoperatively and, in the categorical statistical analyses, these thresholds were classified as abnormal also at the 2-week control. The BR test was not done in one case postoperatively. Intraoperative monitoring of the NCV of the IAN was performed in nineteen cases. Postoperatively, two patients refused the NCS, in fear of possible pain caused by the procedure. All postoperative electrophysiologic tests were performed at the same session.
The cold detection (CDT), warm detection (WDT), and heat pain (HPT) thresholds were separately measured within the mental nerve distribution. The classical method of limits7 was applied. For each threshold, six series of increasing intensities were given, and after deleting the highest and the lowest value, the mean of the remaining four threshold values was calculated to be used as the detection threshold. The thresholds were measured with Thermotest apparatus (Somedic Sales AB, Ho¨rby, Sweden) equipped with a small, hand-held, rectangular probe (816 mm) especially constructed for stimulating the face area. The thermode consisted of four Peltier elements that either cooled or warmed up linearly depending on the direction of the applied electric current changed by a subject-operated switch. The maximal temperature range was set at 10–50C for CDT and WDT, and 10–55C for HPT measurements, the baseline temperature at 30C, and the rate of temperature change at 1C. The intervals between the stimuli varied randomly between 2 and 6 s. Before the testing started, the subjects were instructed to press the switch button immediately they perceived a change in temperature (cooling or warming), and when they felt the warm stimulus to become painful. They were particularly told that the HPT measurement was not intended to test the pain tolerance but to detect the point when the stimulus changes from innocuous warming to noxious heat. The
Mental nerve blink reflex (BR)
The recording of the mental nerve BR has been described in detail earlier12,14,15. The BRs were elicited by electrical stimulation with a small bipolar surface electrode (DantecMedtronic, Skovlunde, Denmark) at 10 mm interelectrode distance. The stimulating cathode was placed on the
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facial skin was wiped with denatured alcohol solution to delete facial grease and make-up before the probe was placed firmly on the skin, at the centre of the small distribution of the mental nerve. On each side, the CDT was always measured first, then the WDT, and last the HPT. The amount of change (in C) from the baseline temperature to the CDT, WDT and HPT was used in further analyses, and compared to the reference values of our laboratory. Nerve conduction study (NCS)
The technique for orthodromic recording13 and intraoperative monitoring16,31 of NCV of the IAN has been described in detail elsewhere. Eight-channel EMG devices (Viking I and IV, Nicolet Biomedical Instruments, Madison, WI, USA) were used for the recordings. A teflon-coated silver wire electrode (Pure silver multistrand, AG7/40T, Leico industries, Inc., USA) was used as the active electrode, and a silver–silver chloride surface electrode as the reference in the operating room. At the outpatient controls, two disposable monopolar needle electrodes (13R12 and 13R31, Dantec-Medtronic, Skovlunde, Denmark) were used for the recording. The active recording electrodes were inserted beneath the zygomatic arch in front of the temporomandibular joint to a depth of about 4.5 cm, to lie near the oval foramen. The electrical stimuli (square-wave pulses with a duration of 0.2 ms) were given at the mental foramen via two disposable monopolar needle electrodes (in the operating room; 13R21 and 13R22 Dantec-Medtronic) or a bipolar surface electrode (at out-patient controls, 13L35, DantecMedtronic). The onset latencies of the responses and the amplitudes from baseline to negative peak were determined from the recordings, and NCV was calculated. These variables were used in the analyses and compared with the reference values of our laboratory13 for normality.
Fig. 1. a and b. Frequency of IAN disturbance as documented by clinical sensory tests on the lip (a) and on the chin region (b) 2 weeks after BSSO (BSD=brush-stroke directional discrimination, TD=touch detection threshold, GO=grating orientation discrimination, W/C=warm/cold discrimination and S/B=sharp/blunt discrimination).
of the operation and the test results at the 2-week control were assessed using the Spearman Correlation Coefficient. All reported P-values are two-sided. Calculations were performed with the SAS software package (version 6.12, SAS Institute, Cary, NC, USA).
Statistical methods
When calculating the specificity and sensitivity of different clinical and electrophysiologic tests, the cases with intraoperative over 50% amplitude decrement of the nerve action potential (NAP) and/or latency over 2 ms were considered indicative of intraoperative nerve damage. The relationship between the nerve conduction parameters at the end
Results
the chin region 2 weeks postoperatively. One of the patients had total anaesthesia of the whole mental nerve distribution on the right side and three on the left side. The mean size of the affected region on the schematic figures of the faces was 124 mm2 on the right side and 135 mm2 on the left side.
Subjective sensory disturbance
The frequencies of IAN disturbances in clinical tests
Preoperatively, none of the patients had clinical sensory IAN disturbances. Fifteen patients (75%) reported some degree of subjective sensory disturbance on the right side and 18 (90%) patients on the left side of the lower lip and/or
In different clinical sensory tests, the frequency of IAN disturbance varied between 10% and 56%. On the lip (Fig. 1a), the GO test showed the highest and the BSD test the lowest percentage of sensory disturbance. In fact, the GO
19
An evaluation of tests in nerve injury diagnosis
the left side. In all, different clinical tests indicated higher frequencies of IAN disturbance on the chin region and the left side. There were no subjects with abnormal findings on the lip region and normal findings on the chin region. The frequencies of IAN disturbances in electrophysiologic tests
The different electrophysiologic tests indicated nerve damage in from 29% to 94% of the nerves recorded, NCS showing the highest frequency of injury (Fig. 2). When abnormal response in at least one of the five electrophysiologic tests was considered to indicate IAN injury, the frequencies were 75% on the right side and 90% on the left side. Fig. 2. Frequency of abnormal findings in different electrophysiologic tests 2 weeks after BSSO (BR=blink reflex, CDT=cold detection threshold, WDT=warm detection threshold, HPT=heat pain threshold and NCS=nerve conduction study).
Correlation of different postoperative test results and electrophysiologically verified intraoperative IAN injury
test indicated nerve damage on the right side in two cases, where all other clinical tests showed normal responses: both nerves had shown signs of significant intraoperative nerve damage. In the first case, the NAP of the IAN had totally disappeared during medial preparation of the ramus and did not recover during surgery. There was subjective sensory alteration postoperatively, but the electrophysiologic parameters included in the study were just within the reference limits (the nerve conduction velocity was slow, however). In the other case, a partial nerve laceration occurred during the splitting of the mandible, and the patient had clear subjective sensory disturbance postoperatively with abnormal findings in all other
Patients reporting a larger area of sensory disturbance had more pronounced NAP decrement during the operation compared to patients with more limited postoperative disturbances (right side R= 0.50988 P=0.0306 and left side R= 0.61957 P=0.0047). The detailed results of the correlation analyses between the electrophysiologic grade of intraoperative nerve damage and postoperative clinical sensory and electrophysiologic test results are presented in Table 2. Of the clinical tests, the TD test showed the closest association with the degree of nerve injury at the end of the operation. Other clinical sensory tests yielded significant correlation with the objectively verified nerve damage only occasionally on the chin area. Except for the HPT test, all other
electrophysiologic tests except the WDT and the HPT. When abnormal response in at least one of the five clinical tests of the lip was considered to indicate IAN injury, the frequencies of nerve damage were 45% on the right side and 55% on the left side. On the chin area (Fig. 1b), clinical tests indicated identical incidence of IAN injuries, with the exception that the TD test showed a clearly higher frequency of sensory disturbance. In two cases the TD test was the only clinical test which, in addition to the electrophysiologic tests, indicated nerve injury. When abnormal response in at least one of the four clinical tests was considered to indicate IAN injury, the frequencies were 53% on the right side and 65% on
Table 2. Correlation of different postoperative test results and electrophysiologically verified intraoperative IAN injury BSD lip Intraoperative IAN damage Right side Intraoperative IAN damage
R P R P
Left side
0.227 ns (18) 0.246 ns (19) NAP amplitude
Intraoperative IAN damage Right side Intraoperative IAN damage Left side
R P R P
0.724 0.002 (15) 0.803 0.0002 (16)
BSD chin 0.471 ns (15) 0.715 0.002 (16)
TD lip 0.567 0.014 (18) 0.618 0.005 (19)
Clinical sensory tests TD chin GO lip 0.603 0.017 (15) 0.626 0.01 (16)
Electrophysiologic tests BR CDT WDT 0.481 0.051 (17) 0.703 0.001 (18)
0.589 0.021 (15) 0.522 0.038 (16)
0.74 0.002 (15) 0.619 0.011 (16)
0.566 0.014 (18) 0.353 ns (19)
W/C lip
W/C chin
S/B lip
S/B chin
0.401 ns (18) 0.338 ns (19)
0.516 0.049 (15) 0.580 0.019 (16)
0.322 ns (18) 0.424 ns (19)
0.516 0.049 (15) 0.317 ns (16)
HPT 0.278 ns (15) 0.437 ns (16)
Number of observations in parentheses; R, Spearman correlation coefficient; P, statistical significance; ns, not statistically significant.
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electrophysiologic tests showed a clear association with objectively verified intraoperative IAN damage. Correlation of macroscopic nerve lesions to findings in different sensory tests
During the BSSO, 25 nerves were partly exposed, five were exposed and manipulated, and seven were partially lacerated. The macroscopic appearance of the IAN during the BSSO was not associated with the clinical sensory test results. However, QST threshold values showed significant correlation (CDT R=0.55 P=0.021, WDT R=0.64 P=0.06, HPT R=0.563, P=0.019) with the macroscopic damage of the IAN on the left side. The NCV of the IAN was abnormal in all laceration cases 2 weeks postoperatively. Sensitivity and specificity: Figs 3a, 3b and 4 show the sensitivity and specificity of different clinical sensory and electrophysiologic tests. All tests, except the NCS, showed only moderate sensitivity. On the whole, the electrophysiologic tests were somewhat more sensitive than the clinical tests. On the other hand, the specificity of the tests was generally high, the only exceptions being the TD test on the chin region and the NCS. The four nerves showing false positive findings in the postoperative NCS coincided, however, with subjective complaints of postoperative sensory alteration in the IAN distribution. Discussion In general, the efficacy of diagnostic tests is defined as their ability to indicate the presence or absence of disease. An ideal diagnostic sensory test would always be positive in the presence of nerve injury, and negative in the absence of injury42. However, the relationship between the results of different sensory tests and the actual, objectively verified nerve damage after BSSO (or other trigeminal nerve injuries) has never been studied. So far, only few attempts have been made to elucidate the relationship between macroscopically verified nerve lesions and the diagnostic accuracy of clinical sensory tests in patients with previous nerve injuries and sensory complaints42. In addition, some authors have investigated the association between macroscopic intraoperative events and the incidence of postoperative sensory alteration with inconsistent results6,21,27,36. In this respect, it is of interest that, in this study, the macroscopic grade of intraoperative
Fig. 3. a and b. Sensitivity and specificity of different clinical sensory tests on the lip (a) and on the chin region (b) (abbreviations as in Fig. 1).
nerve damage as reported by the surgeon was not significantly associated with any of the clinical or electrophysiologic tests (with the exception of the QST on the left side), nor with the subjective report of sensory alteration 2 weeks postoperatively. This indicates that seemingly intact nerves may have suffered considerable injury due to compression and stretching, which will go unnoticed without intraoperative monitoring11,16. However, all cases with nerve laceration showed symptoms and signs of nerve injury at postoperative control. To evaluate the occurrence of IAN disturbance in the early postoperative stage after BSSO, the most standardized, and widely used clinical test methods
which can easily be adapted to routine chair-side postoperative follow-up were chosen5,6,17,21,33,41. Spatial resolution was examined using the GO test, because the two-point discrimination test has not been considered reliable5,25,33. Two test sites were used, because the somatosensory characteristics of the vermilion border of the lower lip and the mental skin region are different26, and because other investigators have routinely used both of these regions. All the electrophysiologic tests applied in the study are routinely used to assess peripheral nerve function. The NCS gives detailed information about the conductive properties and number of thick myelinated sensory A fibres9,18.
An evaluation of tests in nerve injury diagnosis
Fig. 4. Sensitivity and specificity of different electrophysiologic tests (abbreviations as in Fig. 2).
The BR studies the same trigeminal sensory fibres and, in addition, their central connections within the brainstem2,18. The QST is the only clinically available quantitative method for evaluation of the thinly myelinated A and the unmyelinated C fibres29,35. These electrophysiologic techniques are able to verify different types of nerve damage that may occur due to compression, stretching, laceration, and ischaemia during BSSO. In the present study, the degree of nerve damage at the end of the BSSO operation, as documented by means of the intraoperative monitoring of the IAN, was used as ‘the gold standard’. The 2-week time point was chosen for postoperative investigation in order to avoid testing during the time when swelling and pain are most severe. However, postoperative oedema can cause compression, which increases or even gives rise to nerve dysfunction during the immediate postoperative period20. A limitation of the present study is the possibility that the status of the nerve may have changed during the 2-week period, as was actually indicated by four cases where the NCV of the IAN was normal at the end of the operation but abnormal 2 weeks postoperatively, with corresponding subjective sensory alteration. In three additional cases, the NCV of the IAN was abnormal at the end of the operation but normal 2 weeks postoperatively, indicating that the intraoperative dysfunction of the IAN was probably mainly caused by mild compression or ischaemia from which the
nerve can recover even in a few hours19. These probable regenerative and degenerative processes weaken ‘the gold standard’ of this study, and thus influence the calculated sensitivity and specificity values, especially those of the most accurate TD test and NCS. In general, however, the NAP amplitude at 2 weeks correlated well with the NAP amplitude at the end of the operation. In addition to direct orthodromic recording of the NCV of the IAN, also trigeminal somatosensory evoked potentials (TSEP) have been applied to study the function of the IAN in patients with postoperative nerve damage11,23,24. In all these studies inconstant middle-latency waveforms have been utilized. The reliability of these TSEPs-components has, however, been questioned2,9. In addition, cortical SEP may overlook peripheral nerve damage because of central amplification of the responses10. The frequencies of the IAN disturbances ranged widely, depending on the test method and the test site used, as reported in many other studies6,11,17,21, 33,40 . The most sensitive clinical tests were the GO and TD tests, a finding which is in agreement with earlier reports1,34,33,38. Other clinical tests were much less sensitive, e.g. the W/C test showed considerably less thin fibre dysfunction compared to the quantitative CDT and WDT tests. The clinical utility of the TD test in particular is greatly emphasized by the good correlation of this test with the electrophysically verified intraoperative nerve damage. In agreement with earlier observations25,
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the use of the GO test had to be limited to the vermilion region because the patients were mostly not able to discriminate the direction of the grooves when tested on the chin region. In addition, the recorded threshold values at 2 weeks were inconsistent in six cases, showing lower values at 2 weeks despite the fact that according to by other measures, nerve damage had occurred. Thus, the clinical usefulness of the GO test can be considered somewhat questionable. Clinical sensory tests indicated a slightly higher percentage of IAN nerve damage on the chin compared to the lip region. The fact that no subjects with abnormal findings on the lip region had normal findings on the chin region, whereas several patients with abnormal sensitivity on the chin region had normal test results on the lip indicates that testing on the vermilion border might not add to the information obtained. The subjective sensory disturbances corresponded with the aforementioned; the chin region was more frequently affected compared to the lip. The good correlation of many of the clinical sensory tests performed on the chin region with the intraoperatively verified nerve damage supports the use of the chin as the test site when diagnosing nerve injuries connected to BSSO operations. The frequencies of the electrophysiologic tests indicating IAN injury, 75% on the right side and 90% on the left side, corresponded exactly with the figures of subjective sensory disturbance. Electrophysiologic tests were, on average, slightly more sensitive than the clinical sensory tests. Of the individual tests, the NCS yielded the highest frequencies of nerve injury. The WDT and HPT test results indicated lower frequencies than the BR and CDT tests. This difference may be due to the nature of nerve damage connected with BSSO operation; the main type of injury was compression of the nerve31. Compression causes more damage to myelinated A and A fibres than to unmyelinated C fibres19. All electrophysiologic tests except the HPT test, correlated well with the objectively verified nerve injury, thus supporting their clinical use. The poorer correlation of the HPT test can be due to the wide normal range of pain detection thresholds22,39 that may be related to the more subjective nature of HPT. All tests showed high specificity, and thus false positive results were exceptional, associated mainly with NCS and the TD test on the chin region. This can
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be due to their good sensitivity to detect possible further injury of the nerve caused by postoperative events. In general, the sensitivity of the clinical tests was rather low, especially, the BSD, W/C and S/B tests often gave false negative results. The BSD, W/C and S/B tests can thus be considered rather crude and insensitive chair-side methods, especially as regards the diagnosis of the less severe nerve injuries that mainly occurred in the present study. The material in this study may have consisted of minor nerve damage in comparison with damage connected with BSSO in general, as we have already modified our operation technique e.g. by using refined instruments for medial retraction during subperiosteal preparation, by exerting as light compression as possible on the nerve trunk with the retractor, and by trying to keep the total duration of the medial soft tissue retraction as short as possible16,31. Additionally, we were able to reduce nerve damage in these patients by means of continuous intraoperative monitoring of the IAN. The clinical neurophysiologist could warn the surgeon of a threatening IAN injury during the medial retraction, splitting or fixation16,31. Of the electrophysiologic tests, the NCS showed high sensitivity, whereas the sensitivity of the BR, CDT and WDT tests was only slightly higher than that of the clinical TD and GO tests. The moderate sensitivity of electrophysiologic and clinical tests can be due to the fact that different tests measure different nerve fibres and, thus, their sensitivity in different types of nerve injury can vary, e.g. the BR test is more sensitive to demyelinating compression injuries, and the QST tests to laceration injuries causing partial axonal damage. To increase the diagnostic sensitivity, a combination of different tests is mandatory. To conclude, the frequency of nerve injury at the early postoperative stage after BSSO varied widely, depending on the test and the test site used. The most sensitive and clinically useful clinical sensory test was the TD test, which gives quantitative data that may be used in the follow-up of recovery. The electrophysiologic NCS and QST tests increase the diagnostic sensitivity and add to the diagnostic accuracy by detecting different types of damage in different nerve fibre populations. Acknowledgment. The study was supported by a grant from the Finnish Association for the Study of Pain.
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Address: Tuija Teerijoki-Oksa Department of Oral and Maxillofacial Surgery Turku University Central Hospital Lemminka¨isenkatu 2, 20520 Turku, Finland E-mail: [email protected]