sympathetic skin response-a methodof assessing

Journal of Neurology, Neurosurgery, and Psychiatry 1984;47:536-542

Sympathetic skin response-a method of assessingunmyelinated axon dysfunction in peripheralneuropathiesBHAGWAN T SHAHANI, JOHN J-HALPERIN,* PHILIPPE BOULU,t JEFFERY COHENt

From the Laboratories of Clinical Neurophysiology and Neurocytology, Department ofNeurology,Massachusetts General Hospital, Boston, Mass. USA

SUMMARY The sympathetic skin response (SSR) was measured in 33 patients with peripheralneuropathies and in 30 normal control subjects. Abnormalities of the response were correlatedwith clinical, pathologic, and EMG observations. The response was usually absent in axonalneuropathies, but present in demyelinating disorders. Abnormalities of the sympathetic skinresponse did not correlate well with clinical evidence of dysautonomia, but were a reliableindicator of disorders affecting unmyelinated axons.

In the study of disorders of the peripheral nervoussystem, non-invasive electrophysiologic tests havehelped greatly in diagnosis and evaluation; mor-phologic methods have permitted more detailedstudy of biopsied nerve, and have helped to confirmthe validity of newer electrophysiologic methodsthat assess the function of nerve fibres of differentdiameters. However, there remain inherent limita-tions of both morphologic and electrophysiologicmethods. Conventional ultrastructural techniquesare useful for identifying abnormal inclusions orderanged structure of organelles,1 2 but they do notdiscriminate among functional classes of axons.Morphometric methods detect abnormalities ofunmyelinated fibres, but cannot differentiate auton-omic from sensory axons. In contrast, elec-trophysiologic tests permit measurement of sensoryand motor conductions in the same nerve, but studyonly the most rapidly conducting, heavily myeli-nated axons. These non-invasive tests, which evalu-ate nerve conduction velocity by either direct meas-

*Present address, Health Sciences Ctr, SUNY at Stony Brook,Stony Brook, NY.tPresent address, Hopital Beaujon, Clichy, France.*Present address, Mt Sinai Hospital Medical Center, New York,NY.

Address for reprint requests: Dr BT Shahani, ClinicalNeurophysiology Laboratory, Massachusetts General Hospital,Fruit Street, Boston, MA 02114, USA.

Received 18 November 1983. Accepted 2 December 1983

urement or measurement of minimal late responselatency, do not assess the state of slowly conductingmyelinated or unmyelinated fibres.

Collision techniques3-6 help measure the functionof the slower myelinated fibres, but cannot evaluatethe function of unmyelinated fibres. Unmyelinatedaxons produce signals that are of such low amplitudeand are so dispersed that they can only be wellcharacterised by microneurography, which recordsdirectly from unmyelinated axons7'-6 withintraneural needle electrodes. With this method it iseven possible to differentiate between nerve fasci-cles mediating sympathetic control of the intramus-cular vasculature (motor sympathetic activity(MSA)) and those conveying sympathetic impulsesto the cutaneous blood vessels and sweat glands(skin sympathetic activity).7 12-16 (These two classesof sympathetic activity are apparently conveyed byseparate fascicles of unmyelinated axons.) Unfor-tunately, microneurography is time-consuming,requires skilled, experienced operators, and is inva-sive, making routine use impractical.However, the improved understanding of sym-

pathetic activity that has been gained from mic-roneurography has suggested a simple method forassessing autonomic function. Sympathetic skinactivity mediates sudomotor function7 12 15 and asimple technique for assessing sudomotor functionhas been available for decades-the "galvanic skinresponse" (GSR).'7 18 This change in skin resistance(which occurs after emotional or noxious stimuli, ormost prominently, following deep inspiration) istriggered by increased sudomotor activity, mediated

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Sympathetic skin response-assessment of unmyelinated axon dysfunction in peripheral neuropathies 537by the autonomic nervous system. Closely related tothe GSR is the "sympathetic skin response", achange in the voltage measured from the surface ofthe skin, that is also attributable to sudomotor activ-ity. The mechanism responsible for the sympatheticskin response is not known, but both the sympathe-tic skin response and the GSR seem to be mediatedby the same afferent and efferent pathways.Both sympathetic skin activity"I and the sym-

pathetic skin response'9 have been used in the pastto evaluate autonomic function in patients with sus-pected dysautonomia. Both may be abnormal insuch patients, but neither is invariably abnormal. Inthese patients these tests are most consistentlyabnormal when dysautonomia is associated with asevere peripheral neuropathy."' 19 This suggested tous that the sympathetic skin response might providea simple way to test unmyelinated axon function inperipheral neuropathies. We therefore measuredthe sympathetic skin response in patients withneuropathies, and correlated the observations withclinical, EMG and, pathologic findings.

Methods

In the past 2 years we studied the sympathetic skinresponse in 33 patients being evaluated for peripheralneuropathy (ages 24 to 79 years, mean 56) (table 1). Forsome the test was requested by the referring physicianbecause of the possibility of dysautonomia; in others, it wasperformed as part of the evaluation of suspectedneuropathy. This report includes all patients who had thetest performed during this period. To establish the normalrange, we measured sympathetic skin responses in 30 nor-mal adult volunteers (ages 13 to 62 years, mean 33), noneof whom had any evidence of peripheral neuropathy ordysautonomia. In no subjects were there any adverseeffects of the procedure.

Several factors alter the GSR and sympathetic skinresponse artefactually. The response habituates rapidlyafter repeated stimuli,'7 so stimuli were delivered atirregular time intervals over an extended period of time.All tests were performed with the subject supine andrelaxed in a semi-darkened room, with ambient tempera-ture controlled at 22 to 24°C. Since the response dependson body temperature,20 skin temperature was measuredand if under 32°C, the limbs were warmed. Body tempera-ture (measured orally) was normal in all subjects at thetime of the test.The aim of the study was to devise a test of C fibre

function that could be performed easily in clinical EMGlaboratories. Therefore we did not perform other tests ofautonomic function, or use the more technically demand-ing but standardised sympathetic skin response methodsused in research laboratories studying the autonomic nerv-ous system.2' Rather, we used standard surface EMG discelectrodes (TECA 10 mm diameter stainless steel surfaceelectrodes), applied with commercial electrode paste to:(a) the palm and dorsum of the hand (b) the sole and

Table 1

Diagnosis Pts with Pts withsympathetic skin sympathetic skinresponse present response absent

Diabetes 5 5Alcohol 2 4Refsum's syndrome 1LGB 2MLD 1CMT 1LS plexopathy 1lschaemia 1Hypoparathyroid 1Paraneoplastic 1 1Neurodegenerative 2Tabes dorsalis 1Undiagnosed 2 2Totals 17 16

dorsum of the foot (c) the anterior and posterior surfacesof the upper arm and (d) the patella andl popliteal fossa.The band pass was 0-5-2000 Hz. In each patient, responseswere measured in upper and lower extremities and thestimuli included the following: (a) Deep inspiration. Torecord the diaphragmatic EMG, two surface electrodeswere placed 4 cm apart in the eighth intercostal space, withthe anterior electrode in the anterior axillary line. (b) Elec-trical stimuli: Single square wave pulses of 0-1 msc dura-tion, 10-20 mA intensity, were applied to the skin at thelevel of the wrist or ankle. Each type of stimulus was deli-vered 5-10 times.

Responses were recorded with standard EMGapparatus. The latency and amplitude of each responsewere measured manually. The latency was measured fromthe onset of the stimulus artefact (electrical stimulus) ordiaphragmatic EMG activity to the beginning of theresponse; amplitude was measured peak to peak. Conduc-tion velocity was estimated by recording simultaneously attwo different sites (proximal and distal) in the same limb(electrode separation approximately 70 cm in the leg,50 cm in the arm) following a single electrical stimulus anddividing the distance between the two recording sites bythe difference in latency of the response at the two loca-tions.

Histories were reviewed for symptoms of autonomic dys-function (orthostatic dizziness or syncope, altered gastro-intestinal function, or altered perspiration). Examinationsincluded tests of postural changes in pulse and blood pres-sure, pulse response to Valsalva, qualitative assessment ofskin temperature and sweating, and pupillary responses.

All patients had conventional motor and sensory con-duction and late response studies, and EMG with concen-tric needle electrodes. In these tests, limb skin temperaturewas maintained at a minimum of 32°C. Usual criteria wereemployed to divide patients into those with demyelinatingneuropathies and those with axonal disease. Findings of (1)slowed conduction velocity (reduced to less than 60% ofnormal); (2) asynchronous, prolonged duration compoundmuscle action potential (CMAP); (3) prolonged distallatencies; (4) absence of sensory nerve action potentials;and (5) low persistence and prolonged latency of lateresponses suggested a primarily demyelinating process.Conversely, the presence of (1) reduced amplitude CMAP;


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(2) reduced amplitude compound nerve action potentials;(3) relatively normal conduction velocity; (4) mild pro-longation (by less than 25% of normal) and normal persis-tence of late responses; and (5) abnormal spontaneousEMG activity (fibrillations and positive sharp waves) sug-gested an axonopathy.

In eight of the 33 patients, a sural nerve was biopsied. A6 cm specimen was taken so that the distal end of theexcised nerve was about 5 cm proximal to the lateral mal-leolus. Teased fibre preparations were performed on allbiopsies.' Portions of each biopsy were fixed in 1-25%glutaraldehyde, 1% paraformaldehyde, postfixed withosmium tetroxide, embedded in epon and sectioned forstudy by light and electron microscopy. Quantitativestudies were performed on representative EMG photo-montages, printed at a final magnification of 7000x. Datawere collected using a Graf/pen digitiser, a PDP 11/23computer, and software developed in our laboratoryspecifically for this purpose. Four nerves were studied within vitro electrophysiologic methods.22

Results

NORMAL CONTROLSThe sympathetic skin response was present in alllimbs of all normal subjects. In each subject theresponse amplitude varied from test to test, despiteefforts to limit habituation. The shapes of theresponses were similar in the arms and legs, but theamplitude (figs 1 and 2, table 2) was consistentlygreater in the hand than in the foot (p < 0-01, Stu-dent' s 2 tailed t test) and was greater when triggeredby deep inspiration than by electrical stimulation(p < 0.01). The sympathetic skin response latency(fig 3) correlated well with the subject's height andwas consistently longer in the leg than in the arm(1.88 + 0 11 vs 1-39 + 0O07, mean + SD, p < 0-005Student' s 1 tailed t test). Estimates of unmyelinated

]05 mV

H

5OOmsF

Fig 1 Example ofthe sympathetic skin response recordedsimultaneously in the hand (H) and foot (F) ofa controlsubject, following deep inspiration. Uppermost tracing is thediaphragmatic EMG activity. Upward pointing arrowsindicate the onset ofthe response.

Shahani, Halperin, Boulu, Cohen

A

500 ms

B~

Fig 2 Sympathetic skin response recorded in the proximalarm (A) and in the hand (H) ofthe same limb, following anelectrical stimulus. Downward pointing arrows indicate thestimulus, and upward pointing arrows demonstrate the onsetofthe response.

axon conduction velocity (five normal subjects)were 1-57 + 0*11 in the arm and 1.02 + 0-07 m/s. inthe leg (p < 0-01, 2 tailed t test) corresponding wellwith previous estimates from sympathetic skin activ-ity measurements,'0 13 4 and with expectations forunmyelinated fibres.

PATIENTSThe sympathetic skin response was absent in 16 ofthe 33 patients. In one other patient a response wasobtained in the hands but not the legs; in no otherinstance was a response seen in one limb but notothers. In this same patient, a response was recordedafter electrical stimulation but not after deep inspi-ration. In no other patient was a response elicitableby one class of stimulus but not by others. Whenresponses were obtained, the sympathetic skinresponse amplitudes varied widely and did not differsignificantly from controls (fig 3).The presence or absence of sympathetic skin

response did not correlate with symptoms suggestingdysautonomia. In only four of the 33 patients were

Table 2 Sympathetic skin response amplitude (mcV):

Nonnal controls:following inspiration-hand 1193 ± 522foot 822 ± 421

following electric stim.-hand 806 + 322foot 640 + 276

Patients:following inspiration-hand 1119 ± 536foot 1000 ± 666

Sympathetic skin response amplitude (mean ± standard deviation).In normal controls, the amplitude of the response in the hand isconsistently greater than in the foot (p < 0-01, Student's 2 tailed ttest). In addition, in normals the amplitude following inspiration isgreater than following an electrical stimulus (p < 0-01, 2 tailed ttest). The difference between controls and patients is notsignificant.


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Sympathetic skin response-assessment of unmyelinated axon dysfunction in peripheral neuropathies 53925 -

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Fig 3 Sympathetic skin response latency following deepinspiration, as a function ofheight. Responses measured inthe hand ofnormal subjects (*), the hand ofthose patients inwhom a response was elicitable (+); the foot ofcontrolsubjects (x), and the foot ofpatients (0). The lowerregression line (-4 is a least squares fit to the latency in thehands ofnormal subjects. The upper regression line (. .) isa least squares fit to the latency in controls' feet.

there symptoms or physical findings suggestive ofdisordered autonomic function. In three patientsthese symptoms were prominent and sympatheticskin response was preserved. Of the 16 patients withno sympathetic skin response, only one had suchsymptoms. In contrast, absence of the sympatheticskin response did correlate with the "stocking-glove" neuropathy (affecting all modalities equally)

Table 3

Sympathetic skin Sympathetic skinresponse present response absent(n = 17) (n = 16)

Sx of dysautonomia 3 1EMG/NCT: (n = 33)*

primarily axonal 5 13mixed 3 3primarily demyelinating 9 0

Pathology: (n = 8)teased fibre-

axonal 1/5 1/3demyelinating 3/5 0/3mixed 1/5 2/3

quantitation-tunmyelinated

decreased 2/5 3/3myelinated decreased 5/5 3/3

In vitro hysiology (n = 4)Aalopn'adecreased 4/4A delta decreased 3/4C decreased 0/4

*Correlation of absence of sympathetic skin response to axonalneuropathy significant at the p < 0-005 level, Chi 2).tLower limits of normal, unmyelinated 28,000 mm2 of fasciclecross section, myelinated 7500. Patients with decreased numbers ofunmyelinated axons were all < 23,000.

seen in all but one of these 16 patients.All patients had prolonged or absent responses.

Two had normal sensory conductions; three hadnormal motor conductions. Of the 17 patients withpreserved sympathetic skin response, nine had elec-trophysiologic findings of a demyelinatingneuropathy; in five the tests implied an axonal pro-cess. In three, the findings suggested a mixeddemyelinating and axonal disorder (table 3). In con-trast, 13 of the 16 patients with no sympathetic skinresponse had abnormalities consistent with anaxonopathy; in the other three, the tests suggested amixed process.

These electrophysiologic findings suggested thatabsence of sympathetic skin response was associatedwith axonal disorders. To test this statistically, it wasnecessary first to consider those patients who hadfindings suggestive of disorders affecting both axonsand myelin. We grouped these patients in a mannerthat would bias the conclusions against ourhypothesis. In patients with preserved sympatheticskin response, we considered those with mixedfindings to have an axonal process. In those with nosympathetic skin response, we combined thepatients with mixed abnormalities with those withdemyelinating disorders. Despite this grouping, therelationship was still significant (p < 0-01, Chi).Of the eight patients with sural nerve biopsies, the

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Axons/sq mm(xlOOO)

nl 2 3 4 5Axon diameter

Fig 4 Distribution ofunmyelinated axon size. In eachhistogram, axon diameter is plotted on the X axis. Thenumber on the Y axis is, for each diameter range, thenumber ofaxons permm ofnerve fascicle cross section. Theupper graph is ofa biopsy from a patient in whom thesympathetc skin response was absent. The overall density(axonslmm) ofunmyelinated axons was 21,900,(abnormally low). The lower graph is ofa biopsy from apatent in-whom the sympathetic skin response waspreserved. The overall density ofunmyelinated axons was33,400 (normal).


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Fig 5 Electron micrographs ofrepresentative regions ofnerve fascicles from a patient with thesympathetic skin response present (a) (unmyelinated axon density 31,900 axons/mm) and sympatheticskin response absent (b) (unmyelinated axon density 17,100). In (a) most Schwann cellprocesses (arrows)enclose unmyelinated axons (u). In (b) most Schwann cell processes (arrows) do not envelope axons, butinstead wrap around each other or around bundles ofcollagen fibrils. In (b) the amount ofendoneurialcollagen is increased. Only three unmyelinated axons (u) are seen in (b) compared to twelve in (a).(Magnification x 12 000).

sympathetic skin response was absent in three. Ofthe five with preserved sympathetic skin response,teased fibre preparations demonstrated segmentaldemyelination in three, predominantly segmentaldemyelination but with some evidence of anaxonopathy in one, and primarily axonal degenera-tion in one. This last patient had an unusual clinicalpicture suggesting a patchy lumbosacral plexopathythat spared some parts of the nerve while affectingothers (presumably sparing enough axons to pre-serve the reflex). Of the three patients with no sym-pathetic skin response, teased fibre preparationswere consistent with an axonopathy in all threealthough two also had some evidence of mild seg-mental demyelination (commensurate with thatdescribed in some axonopathies.)23 In four biopsiedpatients with sympathetic skin response, in vitroelectrophysiologic testing was performed. In all, Cfibre function was preserved while A alpha and Adelta functions were markedly decreased.

Quantitative morphometric studies confirmedthat the absent sympathetic skin response correlatedbest with disorders of unmyelinated axons (figs 4

and 5). All three patients with absent sympatheticskin response had decreased numbers of unmyeli-nated fibres (17-22,000/m) (table 3). Of the fivepatients with preserved sympathetic skin response,three had normal numbers of unmyelinated fibresand significantly decreased numbers of myelinatedaxons. Of the other two, one patient had an uniquemultisystem degenerative disorder, decreased num-bers of myelinated and unmyelinated fibres(18 500), and symptoms of dysautonomia. In thispatient, there was prominent segmental demyelina-tion, and the decreased number of unmyelinatedfibres probably reflected an increase in endoneurialconnective tissue (decreasing the number ofaxons/mm of fascicle cross section). The last patientwas the woman with a patchy plexopathy, withdecreased numbers of both myelinated andunmyelinated axons (18 000) in some fascicles butnot others. It is likely that more proximally, someautonomic trunks were partially spared by such aprocess, preserving the sympathetic skin response.The very small sample size precluded a valid

statistical comparison of these two groups. How-

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Sympathetic skin response-assessment of unmyelinated axon dysfunction in peripheral neuropathies 541ever, the pathologic and in vitro physiologic findings(table 3) qualitatively support the conclusions basedon EMGs. The sympathetic skin response wasabsent in patients with axonopathies that severelyaffected unmyelinated axons, and was preservedwhen these fibres were spared. The pathologicfindings correlated better with the presence orabsence of sympathetic skin response than with clin-ical evidence of dysautonomia. Of the five biopsiedpatients with sympathetic skin response present andpathology suggesting a demyelinating or mixed pro-cess, three had prominent symptoms of disorderedsympathetic and para-sympathetic function. Two ofthese had decreased numbers of unmyelinated fibresin the sural nerve, one did not. Of the three biopsiedpatients with no sympathetic skin response, nonehad symptoms of disordered autonomic function,and all had decreased numbers of unmyelinatedaxons.

Discussion

The sympathetic skin response was readily elicitablein normal subjects. With double recording techni-ques, it was possible to derive an estimate of conduc-tion velocity for unmyelinated axons, which agreedwith that derived by microneurography insudomotor fibres." In patients with neuropathies,the response amplitude and latency remained in thenormal range, so long as the sympathetic skinresponse was present. Therefore the sympatheticskin response could only be considered definitelyabnormal when absent. Using this criterion alone,we could subdivide our patients into two groups-those with and those without sympathetic skinresponse. (A third sub-group consisted of onepatient who had a response in one limb but notothers. This observation suggests that the techniquecould be used to assess isolated lesions of unmyeli-nated axons, but this has not yet been pursuedfurther.) When we then subdivided patients intothose with electrophysiologic evidence ofaxonopathies and those with demyelination, axonaldisorders correlated strongly with absence of sym-pathetic skin response. Conversely, those with pre-dominantly demyelination had intact sympatheticskin responses. These findings were substantiated bymorphologic findings in sural nerve biopsies.Absence of sympathetic skin response correlatedbest with disorders that preferentially affectedunmyelinated axons.

Abnormalities of sympathetic skin response didnot correlate with clinical evidence ofdysautonomia. In previous studies of sympatheticskin activity and sympathetic skin response, the cor-relation between abnormalities of these tests and

dysautonomia was weak. In contrast, most studiesfound a relationship between abnormalities of thesetests and abnormal autonomic function when the lat-ter was associated with a severe peripheralneuropathy." '9 This lack of correlation betweenclinical evidence of dysautonomia and abnormalitiesof this test of sympathetic function initially seemssurprising. However, the sympathetic skin responsespecifically tests the skin sympathetic fibre-not theparasympathetic fibres or the motor sympatheticfibres, that mediate many of the clinical symptoms ofdysautonomia. It is a common clinical observationthat sudomotor function is disordered in peripheralneuropathies, such as diabetic neuropathy,24 evenwhen there is no evidence of other abnormalities ofautonomic function. It seems likely that a diffuse,"dying back" type of peripheral neuropathy wouldaffect many small, distal sudomotor fibres andthereby alter sympathetic skin activity long beforeother sympathetic or parasympathetic fibres weredamaged sufficiently to cause orthostatic hypoten-sion or other signs of dysautonomia. For this reason,sympathetic skin response is a better marker ofperipheral neuropathies than of dysautonomia. Wethen conclude that the sympathetic skin response-as performed in this study-can document axonalpathology, especially when unmyelinated axons areinvolved, but does not assess autonomic function.Three recent studies25-27 have suggested that the

sural nerve contains few sympathetic fibres. Ourobservations bear on this data in two ways. First, inone of the three biopsied patients with prominentsymptoms of autonomic nervous system dysfunc-tion, there were no abnormalities of unmyelinatedaxons in the sural nerve, as also observed insome28 29but not aII30 31 previously published reportsof sural nerve biopsies in dysautonomia. In contrast,three patients with marked abnormalities ofunmyelinated axons in the sural nerve had no symp-toms of dysautonomia. We take this as further evi-dence that, in a broader sample of patients thanreported in previous studies, the sural nerve prob-ably does not contain many sympathetic fibres. Onthe other hand, we noted the frequent occurrence ofboth abnormalities of unmyelinated axons in thesural nerve, and absence of the sympathetic skinresponse. Therefore the sympathetic skin responseis absent in diseases in which small unmyelinatedaxons of many types-sensory and autonomic-aredamaged.The sympathetic skin response can be recorded

with commonly available EMG equipment. It maybe present when conventional motor and sensoryconduction and late response studies demonstrategross abnormalities, or absent when these tests arenormal. These findings suggest that recording the


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sympathetic skin response is a new and usefulmethod of evaluating a part of the peripheral nerv-ous system-small unmyelinated C fibres-that can-not be assessed by the studies currently performedin clinical EMG laboratories.

The authors gratefully acknowledge the technicalassistance of Mr L Cherkas and Mrs H Goolsby.This work was supported in part by NIH post-doctoral fellowship NS06638 (Dr J Halperin). Sym-pathetic skin response in peripheral neuropathies.

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