Disease: Does Double Crush Occur?

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Journal ofNeurology, Neurosurgery, and Psychiatry 1997;62:71-76 71 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.1.71 on 1 January 1997. Downloaded from Entrapment of motor nerves in motor neuron disease: does double crush occur?

Vinay Chaudhry, Lora L Clawson

Abstract This concept has been used to explain the clini- Objective-To investigate whether "dis- cal finding that patients with proximal lesions eased nerves" are more prone to entrap- such as cervical radiculopathies or thoracic out- ment neuropathy than normal nerves. let syndrome are more likely to have distal Nerve conduction studies of human neu- lesions such as median nerve entrapment at the ropathies have shown that electrophysio- wrist (carpal tunnel syndrome) or ulnar nerve logical abnormalities are often most entrapment at the elbow.2-9 Experimentally, prominent at potential sites of nerve Shimpo et al'0 showed that guinea pigs that had entrapment, and entrapments are more a constricting ligature placed proximally in the common in patients with radicu- sciatic nerve developed plantar neuropathy in lopathies-a concept designated as "dou- the ipsilateral foot but not on the contralateral ble crush". As entrapment neuropathies foot. Peripheral nerves also seem to be more commonly occur in otherwise healthy sub- vulnerable to compressive injury in the pres- jects, it is unclear whether this relation is ence of generalised neuropathies such as dia- coincidental or whether peripheral nerves betes or Guillain-Barre syndrome." 12 Hopkins affected by disease are rendered more sus- and Morgan-Hughes'3 were able to show that ceptible to effects of repeated minor guinea pigs with demyelinating neuropathy trauma, traction, or mechanical compres- induced by diphtheria toxin developed com- sion. pressive neuropathies in their footpads sooner Methods-Sequential ulnar nerve conduc- than did healthy animals. tion studies were prospectively performed As well as the increased incidence of a sec- at baseline and at four, eight, and 12 ond lesion in the presence of an already existing month intervals in 16 patients with amy- lesion, double crush syndrome has also been otrophic lateral sclerosis. Ulnar nerve interpreted to mean that two sequential lesions entrapment was defined as a focal reduc- can be additive.'4'6 Therefore, the presence of tion (>10 mIs) in conduction velocity in the one proximal lesion will lessen the nerve's ability across-elbow segment. to withstand additional distal compression. Results-Ulnar sensory and motor nerve Hence, trauma, traction, or mechanical com- fibres showed similar findings of ulnar pression at a potential site of entrapment may

nerve entrapment at baseline and at follow not be sufficient to cause clinically important http://jnnp.bmj.com/ up over the period of the study. Nerves symptoms in healthy subjects, but may do so if with ulnar nerve entrapment showed a sig- that nerve is already affected by another disease nificantly greater reduction in distal motor process. amplitudes than nerves without entrap- Although double crush is an attractive con- ment, even though distal ulnar sensory cept, little clinical data support it. In this study amplitudes remained unchanged. we tested the double crush hypothesis by Conclusions-Motor nerves in motor neu- prospectively studying ulnar nerves in patients ron disease do not seem to be more sus- with amyotrophic lateral sclerosis. Amyotrophic on September 30, 2021 by guest. Protected copyright. ceptible to entrapment at the elbow than lateral sclerosis provides a model in which do healthy sensory nerves, thus casting motor fibres are "diseased" and sensory fibres doubt on the double crush hypothesis. are healthy within the same nerve fibre bundle, Nerves with double pathology (amy- thus allowing comparison of diseased and nor- otrophic lateral sclerosis and ulnar nerve mal fibres at the same site. Firstly, we reasoned entrapment), however, seem to undergo that if the concept of double crush is correct, more rapid axonal loss than do nerves with ulnar motor fibres in patients with amyotrophic single pathology (amyotrophic lateral scle- lateral sclerosis will show a higher incidence of Department of rosis or ulnar nerve entrapment alone). ulnar at the elbow than would the Neurology, Johns neuropathy Hopkins University adjacent ulnar sensory fibres, which do not School ofMedicine, (J7Neurol Neurosurg Psychiatry 1997;62:71-76) have a superimposed pathology but are exposed Baltimore, MD, USA to the same external factors that lead to ulnar V Chaudhry L L Clawson nerve entrapment. Secondly, if the effect of two Keywords: entrapment; double crush; amyotrophic lat- lesions is additive, then ulnar motor nerves that Correspondence to: eral sclerosis; nerve conduction Dr V Chaudhry, Department develop ulnar nerve entrapment will show a ofNeurology, Johns Hopkins Hospital, Pathology 509, greater axonal loss than ulnar motor nerves that Baltimore, MD 21287, USA. The double crush hypothesis states that do not have ulnar nerve entrapment. Lastly, Received 11 March 1996 patients with a proximal peripheral nerve lesion ulnar sensory fibres that have only one lesion and in revised form 22 May 1996 are more susceptible to developing a second will show minimal axonal loss compared with Accepted 16 August 1996 distal lesion along the course of that nerve.' ulnar motor fibres that have two lesions (amy- 72 Chaudhry, Clawson

Figure 1 Comparison of 12 000 r p=0.0002 14 000 r p=0.0001 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.1.71 on 1 January 1997. Downloaded from baseline (filled squares) andfollow up (open 10 000 H 12 000 - squares) distal evoked H 10 000 1 amplitudes in ulnar to 8000 >: I m ADM (abductor digiti a m¶ CL minimi) and ulnar to FDI E 8000 (first dorsal interosseous) 6000 b~~~[ muscles on the left (L) and E 6000 right (R) sides. There is a 0 4000 0 < 4000 significant reduction in -i cr CMAP amplitude (P 2000 1 values represent 7 b 2000 i comparison of baseline to Ia No I follow up by paired t test). 0 0 Patient No Patient No

| Baseline El Follow up

14 000 p=0.0002 14 000 P=0.0007 12 000 12 000 11 i 5 10 000 5 10 000 11 a 8000 aC 8000 i E m 11 < 6000 I! 0 r-i < 6000 0 C]0 0 LL r- -J 4000 ![ ] 4000 2000 2000 0 III -:il LL 0 III Patient No Patient No

otrophic lateral sclerosis and ulnar nerve (VC) performed the conductions in each entrapment). patient. Supramaximal stimulations were ensured and five responses were averaged for the sensory recordings. Sensory nerve action Patients and methods potential (SNAP) and compound muscle Serial nerve conduction studies were performed action potential (CMAP) amplitudes (peak to at baseline, and at four, eight, and 12 month peak for SNAP; baseline to peak for CMAP) intervals in 16 patients (nine men and seven and conduction velocities were recorded for women) with amyotrophic lateral sclerosis. each segment. Electrophysiologically, ulnar None of the patients had sensory symptoms or nerve entrapment was said to be present if the selective ulnar conduction velocity in the across-the-elbow clinical evidence of neuropathy http://jnnp.bmj.com/ at the elbow. The average age was 54 (range 33 segment was less than that in the below-elbow to 75) years. In each case, bilateral ulnar nerve forearm segment by 10 m/s or more. Data were conduction studies were performed. The stimu- analysed separately for conduction velocity lation sites were the wrist, elbow, above-elbow, reduction in sensory fibres, motor fibres, and and axilla, with the elbow maintained at 1350 both sensory and motor fibres. The baseline flexion. The recording sites for the ulnar motor and follow up measures were analysed by nerve conduction studies were the abductor paired t test. The institutional review board

digiti minimi (ADM) and the first dorsal approved the protocol and informed consent on September 30, 2021 by guest. Protected copyright. interosseous (FDI) muscles. The recording site was obtained for each patient. for the ulnar sensory nerve conduction studies was the fifth digit. The stimulation and recording sites were all precisely predefined: the stim- Results ulation site at the wrist was 65 mm from the Thirty two ulnar sensory and 64 ulnar motor recording site; below-elbow and above-elbow nerve conduction studies were performed at segments were each 5 cm away from the olecra- baseline. All patients had nerve conduction non process; and the axilla segment was 10 cm studies at baseline and at least one follow up proximal to the above-elbow site. The active study, with the median time from baseline to recording sites for the ADM and FDI were the follow up being eight (range, 4-12) months. midpoint of the hypothenar eminence and the Figure 1 shows baseline and final follow up first metacarpal bone dorsally, respectively; the measurements of CMAP amplitudes for bilat- corresponding reference electrode was placed eral ADM and FDI muscles. In most patients, on the metacarpophalangeal joints of the fifth CMAP amplitudes fell between the time of and the second digits. The recording sites for baseline and follow up examinations, with the the sensory fibres were the distal and proximal average reductions being 25% for the left ADM creases of the fifth digit. Skin temperature was muscle, 20% for the right ADM muscle, 35% recorded in the second digit, and the limb for the left FDI muscle, and 34% for the left heated up when required to bring the recorded FDI muscle. By contrast, ulnar sensory fibres temperature to > 32°C. The same examiner (fig 2) showed no significant change in ampli- Entrapment ofmotor nerves in motor neuron disease: does double crush occur? 73 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.1.71 on 1 January 1997. Downloaded from Figure 2 Comparison of 80 r 80 r baseline (filled squares) |p=1.0 andfoUlow up (open Ip=0.8I squares) distal evoked 70 H 70 H i sensory amplitudes in ulnar to digit 5 on the left (L) 60 H 60 H and right (R) sides. Most m patients show no 50 H 50 e- significant change. I 40 H 40 e- -j0) 0) m m *0._ m i p -J 30 H i 30 H i i 20 H 20

10 10

0 0 Patient No Patient No | Baseline El Follow up

Figure 3 Incidences of focal reductions of > 10 tude, with the average reduction being 2%. mis in conduction velocities These findings established that ulnar motor in the across-elbow segment fibres innervating all four muscles were indeed in only sensory, only a0 50 Baseline motor, and in both sensory "diseased" and undergoing Wallerian-like c = Follow and motor nerve fibres, at (D up degeneration, as shown by progressive reduc- baseline and atfollow up. E 40 C. tion in CMAP amplitudes, whereas the ulnar There was no significant sensory fibres were relatively "healthy" over the differencefrom baseline to ' 30 folow up in the percentage 0) study period. No patient showed evidence of of nerves showing the distal ulnar neuropathy; distal motor latencies finding ofulnar nerve '1220 entrapment. co and sensory conduction velocities in the wrist 0) and second digit segments, were normal in all 4) 10 c patients.

CU At baseline evaluation, ulnar nerve entrapment was found in 22% of sensory nerves, 25% 5 Sensory Motor Sensory of motor nerves, sensory and and 19% in both and motor motor nerves; on follow up evaluation, these numbers were 14% for ulnar sensory nerve entrapment, 19% for ulnar motor nerve entrapment, and 19% for both. These differences http://jnnp.bmj.com/ Figure 4 Thefocal 12 000 14 000 change in conduction 0 0 velocity in the across-elbow 10 000 12 000 0-4 segment (below-elbow * 0 IS I. 10 000 forearm segment - across- 8000 elbow segment) is plotted 5*- 8000 0. against the CMAP 6000 0. * E E amplitude for all recording 6000 _ 0*0*0o %----5-- sites andfor all baseline 4000 ~~** 015' - andfollow up evaluations. 4000 on September 30, 2021 by guest. Protected copyright. Ulnar nerve entrapment is 2000 50 a: defined by a focal 2000 ~~0 I * I: reduction in this segment of 0 > 10 m/s (to the right of 0 the vertical dotted line). I The horizontal dotted line -30 -20 -10 0 10 20 30 -30 -20 0 represents the lower limit of -10 10 20 30 normalfor the CMAP CV (Below elbow-across elbow (m/s) CV (Below elbow-across elbow (m/s) amplitude in our laboratory. 14 000 0*r 20 000 12 000 18 000 . 0 SI 16 000 * I 10 000 a* . 14000 S S x 8000 12 000 0. 0 E 00 6000 E 10000 * 0: < 8000 I0 4000 -* --- w 0 * ---:---Si0 0 6000 2000 -J < 4000 . 2000 0 . *. .t~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~e. . 0 I :^

-30 -20 -10 0 10 20 30 -30 -20 -10 0 10 20 30 CV (Below elbow-across elbow (m/s) CV (Below elbow-across elbow (m/s) 74 Chaudhry, Clawson J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.1.71 on 1 January 1997. Downloaded from Figure 5 Reduction in M Ulnar nerves analyse these data, although analysis evoked amplitudes in without entrapment using abductor digiti minimi W Ulnar nerves with entrapment ulnar motor nerve entrapment gave similar (ADM), first dorsal 60 results. For both ADM and FDI recordings, interosseous (FDI), and the nerves with entrapment showed a greater sensory (digit 2) nerves a, reduction in CMAP amplitudes than did non- with entrapment and in 5 nerves without entrapment. entrapped ulnar nerves. By contrast, the ulnar A significantly greater a. 4 sensory fibres with ulnar nerve entrapment did reduction in motor E amplitudes (FDI and m not show a difference in SNAP amplitudes ADM) wasfound in c compared with those ulnar sensory fibres not nerves with a finding of showing a finding of ulnar nerve entrapment. In entrapment. 0 0 patients who had unilateral entrapment shown = 20 by electrophysiology, we compared side to side a) cc differences in amplitude (fig 6). In the same patients, the sides showing the ulnar nerve entrapment had significantly greater reductions 0 l in CMAP amplitudes than the sides without ADM FDI Sensory ulnar nerve entrapment. Again, the sensory fibres did not show comparable differences in SNAP amplitudes between the two sides. were not significant (fig 3), indicating that fre- Figure 7 illustrates this point for one patient in quency of ulnar nerve entrapment does not whom this difference was most prominent. The increase with progressive reduction in CMAP left ulnar nerve showed a 31 % reduction in amplitudes. These data were further analysed conduction velocity across the elbow segment to determine whether CMAP amplitudes corre- at the eight month study. In the right ulnar lated with change in conduction velocity in the nerve no reduction in conduction velocity was across-elbow segment. Differences in conduc- detected in the across-elbow segment. Between tion velocity between the forearm segment and the eighth and 12th month periods, a precipi- the across-elbow segment were plotted against tous reduction (99%) in CMAP amplitude was the CMAP amplitudes, at baseline and all fol- detected on the left side. At baseline the left low up evaluations, for all four muscles (fig 4). ulnar nerve had a relatively normal CMAP Change in conduction velocity in the across- amplitude compared with that of the right ulnar elbow segment did not correlate with CMAP nerve, which had already undergone axonal amplitudes, again confirming that loss of ampli- degeneration. Side to side differences in SNAP tude did not result in ulnar nerve entrapment. amplitudes in this patient were minimal. To test the second part of the hypothesis- that two sequential lesions can add to each other's effects-we compared the percentage Discussion reductions in amplitude for sensory and motor The initial hypothesis of double crush syn- fibres in the entrapped ulnar nerves with those drome was based on the increased incidence of of the non-entrapped ulnar nerves (fig 5). As carpal tunnel syndrome or ulnar nerve entrap- reduction in sensory conduction velocity in the ment in patients with cervical radiculopathy.2

across-elbow segment is considered the most Although nerve entrapment seemed well docu- http://jnnp.bmj.com/ sensitive indicator of ulnar nerve entrapment,'7 mented electrophysiologically, the presence or we used ulnar sensory nerve entrapment to distribution of radiculopathy was not. Other

Figure 6 Side to side 100 r D o comparison of reduction in 100 F sensory nerve action

potential (SNAP) and A on September 30, 2021 by guest. Protected copyright. muscle action 80 K | p=0.01 compound D DL potential (CMAP) E 80 H amplitudes in nerves with and without entrapment. Q0 C 60 K E El z Cn 60 K 0- C c0. V C: 40 K 0 -. C.) 40 K a) 0 a) m 20 AL iL~~ X,,,-s"~~~~~~~~-1 -0 20 A

o A A A A

0 2 4 6 8 10 12 1 2 3 4 5 6 No of ulnar motor NCS No of ulnar sensory NCS (wrist-ADM and wrist-FDI) (wrist-digit 2)

-o Side with entrapment - - Side without entrapment Entrapment ofmotor nerves in motor neuron disease: does double crush occur? 75 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.1.71 on 1 January 1997. Downloaded from Figure 7 Comparison of 4000 Baseline nerve distribution; hence, a finding of ulnar the CMAP amplitude in abductor digiti minimi 3500 FouLr months nerve entrapment by nerve conduction studies (ADM) andfirst dorsal ._ Eight mornths was classified as subclinical. m 1 ) m-, n t he interosseous (FDI) on the 33JUUt _ I~L II|IUI ILI lb The presence of amyotrophic lateral sclerosis > d left (L) side with those on II35000 produces an additional insult selectively to the the right (R) side, in a UCL I23000 motor component of ulnar nerve fibres. If the patient with ulnar nerve ;:2 entrapment only on the left concept of double crush were correct, focal side. Progressive reduction reductions in motor conduction velocities in the in CMAP amplitude 1500 occurred only on the left elbow segment should have occurred with pro- side (the side with 1000 gression of amyotrophic lateral sclerosis. entrapment), even though However, motor nerves in motor neuron dis- the starting amplitude was 500 ease did not seem to be any more susceptible to lower on the right side. 0 L ADM R ADV L FDI RFDI entrapment at the elbow than were sensory nerves, thus casting doubt on the first part of the double crush hypothesis. clinical studies of double crush had pitfalls in The second part of the hypothesis states that that they either lacked a rigorous definition of two sequential lesions may add to each other's the two lesions or they failed to include a con- effects. Although motor axonal loss was trol population and to exclude the possibility undoubtedly occurring over time in these that the findings were due to the chance occur- patients with amyotrophic lateral sclerosis, rence of two common entities.' 4 7 Furthermore, ulnar nerve entrapment was not by itself pro- cervical radiculopathies (usually C5-C6) may ducing significant axonal loss, as distal sensory affect different fibre populations than entrap- amplitudes were preserved. And yet, motor ments (usually C8-T1) and should not cause axonal loss occurred more rapidly in patients sensory fibres to undergo axonal degeneration. with ulnar nerve entrapment than in those with- Similarly, studies reporting the coexistence of out entrapment. In the same patients, in whom thoracic outlet syndrome with a distal compres- a unilateral ulnar nerve entrapment was found, sive neuropathy lacked objective evidence ofthe the side with entrapment had greater axonal two lesions and failed to compare their patients loss than did the contralateral side without with a control population.589 Although some ulnar nerve entrapment. Figure 6 best illus- experimental models of compressive neuropa- trates this. Although the baseline CMAP ampli- thy are purported to prove the double crush tude was lower for the right side (suggesting syndrome, none of these is an accurate model greater motor axonal loss due to amyotrophic of clinical human entrapment neuropa- lateral sclerosis), after one year the amplitudes thy. 101415 18-20 The entity of double-crush syn- were lower on the left, presumably because drome, therefore, remains controversial.62' 22 there was additional entrapment. Thus one Our prospective study had strict definitions lesion by itself would not have produced that for the two "lesions". All patients in this study injury but the presence of two lesions together were diagnosed as having amyotrophic lateral resulted in greater axonal loss. sclerosis based strictly on the criteria of the El The electrophysiological finding of ulnar Escorial World Federation of Neurology.2' nerve entrapment is frequent because the ulnar

More importantly, these patients were docu- sensory and ulnar motor nerve fibres are http://jnnp.bmj.com/ mented as having lower motor neuron lesions exposed to external pressures at the elbow; in in the C8-T1 distribution, as evidenced by pro- addition, because of their more superficial loca- gressive loss of motor amplitudes in the ulnar tion, sensory fibres are more susceptible. innervated muscles of the hand. The adjacent However, segmental demyelination caused by travelling sensory fibres of the ulnar nerve ulnar nerve entrapment may not be of sufficient remained normal over the period of the study, severity to result in distal axonal loss. An addi- as shown by preserved distal SNAP amplitudes. tional insult, a second lesion (the double crush), on September 30, 2021 by guest. Protected copyright. The second lesion was strictly defined by a may be necessary to produce the axonal loss focal reduction of > 10 m/s in nerve conduc- and perhaps make a subclinical entrapment tion velocity across the elbow. No patient had into a clinical one. any other definable lesion along the course of Arguably, motor neuron disease with ulnar the nerve (such as distal ulnar neuropathy) nerve entrapment does not represent a true except for ulnar nerve entrapment. All patients "double crush", as the effect on nerve of motor had sequential evaluations on both anns, thus neuron loss may not be the same as a proximal serving as their own internal controls. compressive lesion. However, as outlined in the The elbow is often a site of minor trauma or initial report by Upton and McComas,' any traction to the ulnar nerve, so that "subclinical" proximal nerve lesion that causes axonal dys- ulnar nerve entrapment is not uncommon even function distally should produce the phenome- in healthy subjects. This was evident from our non of "double crush" when a second study, in which 22% of the subjects had ulnar compressive lesion is added. Some ofthe exper- nerve entrapment by sensory nerve conduction imental models of peripheral neuropathy asso- studies. The sensory amplitudes remained ciated with entrapment neuropathy have also unchanged over the period of the study, despite called this paradigm "double crush".'014518-20 focal reductions in velocity across the elbow, One advantage of our model is that in chronic confirming that the focal demyelinating change degenerating diseases such as amyotrophic lat- was not severe enough to cause axonal loss. eral sclerosis, the distal effects of a proximal Additionally, none of the patients had sensory "lesion" presumably occur over a long period of or motor symptoms or signs limited to the ulnar time; therefore, the affected motor fibres pre- 76 Chaudhry, Clawson J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.1.71 on 1 January 1997. Downloaded from sumably remain "diseased", rather than suffer- 9 Narkas AO. The role of thoracic outlet syndrome in double an acute insult crush syndrome. 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The effect of local pres- conclusion, this electrophysiological study sure in diphtheritic neuropathy. .7 Neurol Neurosurg supports the notion that motor nerves with two Psychiatry 1969;32:614-23. insults undergo greater axonal loss 14 Nemoto K, Matsumoto N, Tazaki K-i, Horiuchi Y, than do Uchinishi K-i, Mori Y. An experimental study on nerves with one, but that the presence of one the "double crush" hypothesis. _7 Hand Surg 1987;12A: 552-9. insult does not necessarily predispose a nerve to 15 Seiler WA, Schlegel R, MacKinnon SE, Dellon AL. a second lesion. Double crush syndrome: experimental model in the rat. Surgical Forum 1983;34:596-8. 16 MacKinnon SE. Double and multiple "crush" syndromes. Hand Clinics 1992;8:369-90. 1 Lishman WA, Russell WR. The brachial neuropathies. 17 Raynor EM, Shefner JM, Preston DC, Logigian EL. Lancet 1961;ii:941-6. Sensory and mixed nerve conduction studies in the evalu- 2 Upton ARM, McComas AJ. 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World Neurology 1990;5:12. http://jnnp.bmj.com/ on September 30, 2021 by guest. Protected copyright.