Archives of Physical Medicine and Rehabilitation
Volume 87, Issue 9 , Pages 1201-1206, September 2006

Reduced Sympathetic Skin Response in the Isolated Spinal Cord of Subjects With Spinal Cord Injury

  • Shin-Liang Pan, MD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, Taipei, Taiwan
    • National Taiwan University College of Medicine, Taipei, Taiwan
    • ,
  • Yen-Ho Wang, MD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, Taipei, Taiwan
    • National Taiwan University College of Medicine, Taipei, Taiwan
    • Corresponding Author InformationReprint requests to Yen-Ho Wang, MD, Dept of Physical Medicine and Rehabilitation, National Taiwan University Hospital, No 7 Chung-Shan South Rd, Taipei 100, Taiwan
    • ,
  • Wen-Hsuan Hou, MD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, Taipei, Taiwan
    • ,
  • Chao-Min Wang, MD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, National Taiwan University Hospital, Taipei, Taiwan
    • ,
  • Tien-Shang Huang, MD

      Affiliations

    • Department of Internal Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei, Taiwan

Article Outline

Abstract 

Pan S-L, Wang Y-H, Hou W-H, Wang C-M, Huang T-S. Reduced sympathetic skin response in the isolated spinal cord of subjects with spinal cord injury.

Objective

To compare the excitability of the sympathetic skin response (SSR) between subjects with spinal cord injury (SCI) and healthy controls with intact supraspinal connection.

Design

Cross-sectional survey.

Setting

Referral center.

Participants

A total of 37 men with traumatic neurologically complete SCI (26 with tetraplegia, 11 with paraplegia) and history of autonomic dysreflexia were included. Twenty age-matched healthy male controls were recruited as the control group. Subjects with SCI were at the mean age ± standard deviation of 36.5±11.0 years (range, 20.1−61.3y) and the mean injury duration was 11.3±9.3 years (range, 1.0−38.1y).

Interventions

Not applicable.

Main Outcome Measures

The SSR tests were grouped into 3 test sets according the stimulation and recording sites: (1) right supraorbital nerve stimulation with left hand recording (SH set); (2) right supraorbital nerve stimulation and left foot recording (SF set); and (3) right posterior tibial nerve stimulation and left foot recording (TF set).

Results

In patients with tetraplegia (n=26), none showed positive SSR in the SH or the SF set, and only 5 (19.2%) showed a positive SSR in the TF set. In subjects with paraplegia (n=11), the positive response rates of SSR were 72.7% for the SH set, 0% for the SF set, and 9.1% for the TF set. Electric stimulation at high intensity (100mA for 1ms) was required to elicit SSR for the TF set in the patients with SCI. The SSR amplitudes in the SH and TF sets were smaller in subjects with SCI than those in controls (SH set, P=.004; TF set, P<.001). The SSR latency in the SH set was longer in patients with SCI (P=.04), whereas the SSR latency in the TF set tended to be shorter in subjects with SCI (P=.09).

Conclusions

The excitability of SSR was reduced in an isolated spinal cord. This suggests that excitability of sympathetic sudomotor response in subjects with an isolated spinal cord is lower than in healthy controls.

Key Words:  Autonomic dysreflexia , Autonomic nervous system , Electric stimulation , Rehabilitation , Spinal cord injuries

 

SPINAL CORD INJURY (SCI) affects both spinal somatic and autonomic function. Various autonomic dysfunctions, including of the cardiovascular system, bladder, and bowel, are associated with complete SCI.1 Autonomic dysreflexia (AD) is a unique sympathetic dysfunction in patients with high-level SCI. The pathophysiology of AD is disconnection of the spinal sympathetic centers from supraspinal control (hypothalamus, brainstem), leading to unopposed and sustained sympathetic outflow below the spinal lesion.2 Patients with SCI at or above the major sympathetic splanchnic outflow, usually about the T6 level, are at risk of developing AD. Clinically, it is characterized by an acute blood pressure increase, headache, sweating, and facial flushing, and is often triggered by nonspecific stimuli below the level of the spinal cord lesion.2, 3 Without prompt treatment, AD with sustained high blood pressure can result in seizure, intracranial hemorrhage, congestive heart failure, and even death.4, 5, 6 The existence of AD suggests that a sympathetic response can be generated within an isolated spinal cord without the contribution of the supraspinal sympathetic reflex center. An evaluation of the sympathetic reflex activity within an isolated spinal cord would be helpful in understanding the neurophysiologic basis of AD.

The sympathetic skin response (SSR) is a noninvasive method for measuring the reflex activity of sympathetic sudomotor function,7 and has been used to evaluate autonomic dysfunction, such as neurogenic bladder, impotence, and autonomic dysreflexia in subjects with SCI.8, 9, 10, 11 Cerebral cortex,12 brainstem, and medullary reticular formation13, 14 have been proposed as the sites of central reflex center for the SSR. However, there is still controversy about the excitability of the SSR reflex within an isolated spinal cord. It has been reported that, in subjects with complete SCI, electric stimulation below the level of injury can induce a change in skin conductance.15 Stjernberg and Wallin,16, 17 using microneurographic recording from the peroneal nerve in subjects with complete SCI, demonstrated that electric stimulation can elicit sympathetic nerve discharge and the associated vessel contraction and skin conductance change. In addition, they reported that the vasoconstrictor and sudomotor impulses of sympathetic activity were parallel.16, 17 However, Cariga et al18 failed to observe an SSR using electric stimulation below the level of injury in such subjects. Reitz et al19 showed that a foot SSR can be elicited by pudendal nerve stimulation, but not by tibial nerve stimulation. The previous conflicting results may be attributed to the different stimulation methods used and the different study subjects included. Most researchers have used electric stimulation at relative low intensity (only several times the motor threshold).18, 19 Moreover, none of the previous studies were performed on the more homogenous population of patients with SCI and a history of AD. In addition, there have been no reports of the characteristics (eg, amplitude, latency) of the SSR generated within an isolated cord. In this cross-sectional survey, electric stimuli at various intensities were used to elicit an SSR in patients with complete SCI and a history of AD. Our aim was to investigate the excitability of the SSR between subjects with SCI and healthy controls who had intact supraspinal connection.

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Methods 

Participants 

To investigate the SSR in SCI subjects with AD, we recruited patients with (1) complete traumatic SCI with a neurologic level at T6 or above (the neurologic examination was performed according to the international American Spinal Injury Association guidelines20), and (2) a history of AD, defined by characteristic clinical symptoms, including recurrent paroxysmal hypertension (increased systolic blood pressure by 30mmHg as compared with baseline value), headache, and flushing, typically precipitated by urine retention or bowel distension.2 We excluded: (1) patients with a known neuropathy or other systemic diseases that may affect the peripheral or autonomic nervous system (eg, diabetes mellitus, renal failure, heart failure, or cardiac arrhythmia), and (2) patients taking medication, such as α-blockers, β-blockers, or anticholinergic agents, that might affect the autonomic nervous system. To rule out peripheral neuropathy, motor and sensory nerve conduction studies using standard electrophysiologic techniques (motor nerve conduction studies on the median and posterior tibial nerves and sensory nerve conduction studies on the median and sural nerves) were performed on all participants.

We recruited 20 age-matched healthy male subjects as the control group. The study protocol was approved by the Research Ethics Committee of National Taiwan University Hospital. All patients and controls gave written informed consent before testing.

SSR Test Procedure 

We performed electrophysiologic studies with the subject supine. The subject was instructed to relax, but not to fall asleep. The ambient temperature was maintained at 24° to 26°C and the skin temperature at, or higher than, 31°C. A Medelec Synergy electromyographa was used for recordings, using a bandpass of 0.1 to 100Hz, a sensitivity of 0.5 to 2mV per division, and a sweep speed of 1 second per division. The sweep duration of recording was 10 seconds for each response. We used 2-channel SSR recording to record the waveforms generated from the left hand and left foot. In 1 setup, the active electrode was attached to the left palm and the reference electrode to the dorsum of the left hand; in the other, the active and reference electrodes were attached to the left sole and the dorsum of the left foot, respectively. The electric stimuli were applied to either: (1) the right supraorbital nerve at the medial border of the upper margin of the orbit; or (2) the right posterior tibial nerve at the ankle. The grounding electrode was attached to the left forearm. Using supraorbital nerve stimulation, a single square wave pulse of 0.2ms in duration with intensity sufficient to produce a painful sensation was applied. Such stimulation could startle all subjects suddenly and could evoke SSR in all healthy controls. Using tibial nerve stimulation, a single square wave of 0.2ms in duration with intensity sufficient to generate a visible motor response at the foot was used initially; if no SSR could be obtained, the intensity of stimulation was increased to 100mA and the duration to 1.0ms for maximal stimulation. In the pilot study on healthy controls, we found that a slow and consecutive increase in the stimulation intensity may lead to habituation that cannot be completely prevented by random stimulation. Moreover, in the pilot study on SCI subjects, we found that in test sets involving tibial nerve stimulation of the left foot (discussed below), no SSR could be obtained in SCI subjects at motor-threshold intensity. Therefore, when the SSR was unobtainable at low intensity in SCI subjects, the stimulation intensity was increased to 100mA directly. In contrast, the SSRs could be elicited by tibial nerve stimulation in all controls with stimulation intensity sufficient to generate a visible motor response at the foot. The maximal stimulation was never used in the healthy controls. Maximal stimulation (100mA for 1ms) was not applied at the supraorbital nerve because it was intolerable for most subjects. We used stimulation sites contralateral to the recording side, because stimulation at the ipsilateral ankle with high intensity tended to evoke large compound motor action potentials, which might affect the baseline and the subsequent SSR measurement.

In the SSR test, there is a tendency to habituation if the same stimulus is used repeatedly,21, 22 so stimuli were delivered unexpectedly and at irregular intervals of more than 60 seconds to reduce this effect. A flat, smooth baseline was required before applying each stimulus. The amplitude was measured from the negative peak to the positive peak if the waveform was biphasic or from the baseline to the peak if the waveform was monophasic. The largest obtainable SSR amplitude was taken for analysis. Latency was measured from the stimulus to the onset of the first deflection from baseline. The response was considered to be absent if no consistent voltage change occurred using a sensitivity of 50μV per division after 3 trials.

The SSR test results were grouped into 3 sets according to the stimulation and recording sites: (1) right supraorbital nerve stimulation with left hand recording (SH test set); (2) right supraorbital nerve stimulation and left foot recording (SF test set); and (3) right posterior tibial nerve stimulation and left foot recording (TF test set). In SCI subjects, both the SH and the SF test sets consisted of stimulation above the lesion and recording below the lesion. Therefore, positive responses of SSR in these 2 test sets indicate integrity of the supraspinal connection to spinal cord. The TF test set (stimulation and recording below injury level) was used to determine the ability to generate an SSR within an isolated cord in subjects with complete SCI.

Statistical Analysis 

Descriptive statistics were expressed as mean ± standard deviation (SD). We used the Wilcoxon rank-sum test to compare SSR latency and amplitude between patients with SCI and control subjects, stratified by the SH and the TF test sets. All statistical analyses were performed using SAS software.b

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Results 

A total of 37 male subjects with complete SCI were included. The mean age was 36.5±11.0 years (range, 20.1−61.3y) and the duration of injury 11.3±9.3 years (range, 1.0−38.1y). The neurologic level of injury ranged from C3 to T6. All patients had a typical history of AD. Twenty healthy male volunteers (mean age, 38.7±12.1y; range, 22.2−61.1y) constituted the control group. The demographic and clinical characteristics of subjects with SCI and controls are presented in table 1. Reference values for the SSR latency and amplitude were determined in the control group (table 2). Valid SSR waveforms were obtained for the SH, SF, and TF test sets in all healthy subjects. The SSR response could be elicited by pain threshold stimulation in the SH and SF test sets and by motor threshold stimulation in the TF test sets. Figure 1A shows typical SSR waveforms for the SH, SF, and TF test sets from a control subject.

Table 1. Demographic and Clinical Characteristics of Subjects With SCI and Healthy Controls
VariablesSCI (n=37)Controls (n=20)P⁎
Age (y)36.5±11.038.7±12.1.483
Body height (cm)169.5±4.7171.1±4.5.213
Duration of injury (y)11.3±9.3NA
Neurologic level of injury
C31NA
C48NA
C57NA
C69NA
C71NA
T31NA
T41NA
T55NA
T64NA

NOTE. Values are mean ± SD.

Abbreviation: NA, not applicable.

⁎ Student t test.

Table 2. Reference Values of the SSR Latency and Amplitude From the Control Group (n=20)
Test SetSSR Parameter
Latency (s)Amplitude (mV)
SH1.46±0.176.09±2.81
SF1.94±0.273.16±1.66
TF1.98±0.253.63±1.84

Note. Values are mean ± SD.

Abbreviations: SF, supraorbital stimulation, foot recording; SH, supraorbital nerve stimulation, hand recording; TF, tibial nerve stimulation, foot recording.

  • View full-size image.
  • Fig 1. 

    SSR waveforms of the SH, SF, and TF test sets obtained from (A) a control subject and (B) a patient with paraplegia. Abbreviations: SF, supraorbital nerve stimulation, foot recording; SH, supraorbital nerve stimulation, hand recording; TF, tibial nerve stimulation, foot recording.

Of the subjects with tetraplegia (n=26; level of injury, C3-7), none exhibited an SSR in the SH and the SF test sets (table 3). Because the site of stimulation was the supraorbital nerve in these 2 test sets, the absence of an SSR suggests disconnection of the efferent pathways from the supraspinal SSR reflex center to the palm and foot through the spinal cord. Of the subjects with paraplegia (n=11; level of injury, T3-6), most (72.7% [8/11]) gave a positive SSR in the SH test set, but none gave a recordable SSR in the SF test set (see table 3). The absence of an SSR in the SF test set again indicates disconnection of the efferent tracts from the supraspinal center to the foot. Figure 1B shows SSR waveforms obtained in various test sets from a patient with paraplegia.

Table 3. SSR Response Rate of Various Test Sets in Subjects With SCI
Test SetTetraplegia (n=26)Paraplegia (n=11)Total SCI Subjects (n=37)
SH0(0.0)8(72.7)8(21.6)
SF0(0.0)0(0.0)0(0.0)
TF5(19.2)1(9.1)6(16.3)

NOTE. Values are n (%). Stimulation at high intensity (100mA for 1ms) was required in TF test set.

In patients with complete SCI, the presence of an SSR using stimulation and recording below the level of injury indicated that an SSR could be generated within an isolated spinal cord. In the present study, most subjects showed no SSR in the TF (sole of foot recording using tibial nerve stimulation) test set. Of the tetraplegic subjects (n=26), only 5 (19.2%) gave an SSR in the TF test set (see table 3). It should be pointed out that, for the control group, SSR could be obtained in the TF test set by electric stimulation at the motor threshold. In contrast, for the whole group of SCI subjects, no SSR could be elicited in the TF test set by electric stimulation at the motor threshold and it was necessary to use maximal stimulation (100mA for 1ms). The lower SSR response rate and higher stimulation intensity required in the TF test set suggests that there is a higher threshold for generating an SSR within an isolated spinal cord. Of the subjects with paraplegia (n=11), only 1 gave an SSR response in the TF test set, and again this could only be elicited by maximal stimulation. This indicates a high threshold and poor SSR reflex activity within the isolated spinal cord.

Table 4 shows the comparison of SSR latency and amplitude in SCI subjects and control subjects. In the SH test set, the latency was significantly longer in the subjects with SCI (P=.04) and the amplitude smaller (P=.004). In the TF test set, the amplitude in the subjects with SCI was lower than in control subjects (P<.001). It should be noted that the latency of TF in the subjects with SCI (n=6) tended to be shorter than in controls, although no statistical significance was found (P=.09).

Table 4. Comparison of SSR Latency and Amplitude in the SH and TF Test Sets Between SCI Subjects and Controls
SHTF
SSR ParameterSCI (n=8)Controls (n=20)SCI (n=6)Controls (n=20)
Latency (s)1.58±0.13⁎1.46±0.171.78±0.191.98±0.25
Amplitude (mV)2.07±1.73⁎6.09±2.810.38±0.30⁎3.63±1.84

NOTE. Values are mean ± SD.

⁎ P<.05 (Wilcoxon rank-sum test).

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Discussion 

The purpose of the present study was to evaluate the ability of an isolated spinal cord to generate an SSR by means of electric stimulation and to evaluate sympathetic sudomotor reflex activity in SCI subjects with AD. The presence of an SSR in the SH test set was considered evidence of intact efferent tracts from the supraspinal SSR center to the palm. Similarly, its presence in the SF set was considered evidence of intact efferent pathways from the supraspinal center to the foot. Because we included only subjects with complete SCI, all patients with tetraplegia showed a negative SSR in the SH and SF sets and all subjects with paraplegia showed a negative SSR in the SF set. This provides evidence that the spinal cord below the injury level is isolated from its supraspinal reflex center in subjects with complete SCI and a history of AD.

In the TF test set, the electric stimulation was delivered below the level of injury and the SSR was also recorded below the lesion. The SSR in the TF test set therefore represented the sympathetic sudomotor reflex activity within an isolated spinal cord. As shown in table 3, most (84%) subjects gave no SSR even at maximal stimulation intensity in the TF test set. Only 6 of 37 (16%) subjects gave an SSR generated from an isolated cord. Moreover, in these 6 subjects, none of the SSR responses obtained in the TF set could be elicited by relative low stimulation intensity (motor threshold stimulation, ≈15 to 40mA for 0.2ms), and maximal electric stimulation (100mA for 1ms) was required to induce an SSR. In contrast, all control subjects gave an SSR in the TF test set and this could be elicited at relatively low stimulation intensity (motor threshold). In addition, the maximum SSR amplitudes in the TF test set for the 6 subjects with complete SCI were significantly lower than those in the control subjects. Thus, compared with a spinal cord with an intact supraspinal connection, the SSR reflex activity within an isolated cord has a higher threshold for stimulation and a lower response amplitude. It has been reported that no SSR can be obtained in an isolated cord by electric stimulation.18 Reitz et al19 also reported that an SSR could not be elicited in an isolated cord by electric stimulation of the tibial nerve. However, these 2 studies only used stimulation of relatively low intensity. Because a higher electric stimulation intensity at the tibial nerve was required to generate a foot SSR from an isolated cord in the present study, stimulation at a lower intensity may have resulted in no SSR being seen in previous studies. This shows that, although an isolated spinal cord can generate an SSR without the contribution from the supraspinal reflex center (eg, brainstem), the threshold to elicit an SSR is higher in an isolated spinal cord than in healthy controls. This indicates the sympathetic sudomotor reflex activity in an isolated spinal cord is lower than that in healthy controls with intact supraspinal connection. Although there was no significant difference in body height between SCI subjects and controls, we found that the latency of SSR in the TF test set for subjects with SCI tended to be shorter than that in control subjects. It has been proposed that supraspinal locations, such as cerebral cortex and brainstem, are reflex centers for the SSR in subjects with intact supraspinal connection.12, 13, 14 For SSR evoked from a reflex in an isolated spinal cord without the contribution of a long-distance reflex arc traveling between the spinal cord and supraspinal center, the time required to generate SSR would be shorter. This may explain why the TF latency of SCI subjects tended to be shorter than that of healthy controls.

In AD, autonomic nerve discharge is elicited by various stimuli below the level of injury in patients with SCI at the mid-thoracic level or above. It has been regarded as an increased autonomic response and was initially described as autonomic “hyperreflexia.”1, 23, 24, 25 However, Mizushima et al26 found that baseline plasma norepinephrine levels in SCI subjects are significantly lower than in healthy subjects. Moreover, it has been reported that patients with high SCI have hypersensitive vascular α-adrenoceptors.27 Similar adrenergic hyper-reactivity in arteries was also reported in a recent animal study.28 These findings indicate that the neuroendocrine pathogenesis of AD may be attributable to low baseline sympathetic activity and increased adrenoreceptor sensitivity. In the present study, all included subjects with SCI who had a history of AD showed lower reflex activity of sympathetic sudomotor response than healthy controls. In addition, none of the tested SCI subjects had clinical symptoms of AD during maximal electric stimulation at 100mA for 1ms, an intensity that would be very painful to persons without SCI. The common precipitating factors for AD are bladder overdistension, stool impaction, and pressure ulcers.2 These precipitating factors are relatively long-lasting stimuli and are highly nociceptive under normal physiologic conditions in healthy persons. It appears that short-duration electric stimulation cannot elicit AD effectively. This study shows that SCI subjects with a history of AD do not have increased sympathetic reflex activity, but, in fact, have decreased activity in terms of the SSR. We therefore hypothesize that the AD might not result from increased sympathetic nerve reflex; indeed, the baseline reflex activity of an isolated cord is decreased and the reflex threshold is higher than normal. Nevertheless, once a long-lasting nociceptive stimulus exceeds the reflex threshold, it will initiate a reflex sympathetic discharge and, because inhibitory control from the supraspinal center is lacking in subjects with SCI, this discharge will be sustained, leading to the clinical symptoms of AD.

In subjects with paraplegia, because the intraspinal pathway is intact from the supraspinal center to the cervical cord, it might be expected that an intact SSR would be recorded at the hand by stimulation of the supraorbital nerve; however, we found that the latency was longer and the amplitude smaller in the SH test set. Moreover, in the SH test set, no SSR could be elicited in 3 of the 11 subjects with paraplegia. Normell29 reported that sympathetic and sensory function after SCI may differ in level by 1 to 2 dermatomes. Although the neurologic level of SCI was at the thoracic level, as defined by somatic sensorimotor function, it is possible that the extent of sympathetic nerve dysfunction does not always parallel that of somatic nerve dysfunction. Thus, sympathetic output to the upper extremities may still be affected in subjects with paraplegia.

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Conclusions 

This study assessed the excitability of SSR in patients with complete SCI and history of AD. When we applied both stimulation and recording below the level of injury (TF test set), reduced SSR responses were found. This indicates that SSR reflex activity is decreased in an isolated spinal cord. However, because SSR testing only provides information regarding sudomotor responses, further studies on the sympathetic vasomotor reflex activity in an isolated spinal cord will be necessary to provide comprehensive evidences for elucidating the pathophysiology of AD.

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  • a Medelec Synergy, Oxford Instruments Measurement Systems, 945 Busse Rd, Elk Grove Village, IL 60007.
  • b Release 8.2; SAS Institute Inc, 100 SAS Campus Drive, Cary, NC 27513.

 Supported by the National Science Council of the Republic of China (grant no. NSC 94-2314-B-002-085).No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated.

PII: S0003-9993(06)00524-7

doi:10.1016/j.apmr.2006.05.027

Archives of Physical Medicine and Rehabilitation
Volume 87, Issue 9 , Pages 1201-1206, September 2006

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