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Diabetic Neuropathy: Review of a Surgical Approach to Restore Sensa- tion, Relieve , and Prevent Ulceration and Amputation

A. Lee Dellon, M.D. Baltimore, Maryland

ABSTRACT understand this concept, it is necessary to review the metabolic problems that are present in diabetes that Diabetic neuropathy occurs in a stocking and glove render the nerve susceptible to compression and to distribution consistent with a systemic metabolic disease. consider the relationship between nerve compression Historically, this concept led to the conclusion that and neuropathy. the only role for surgery in a patient with diabetic neuropathy is for treatment of wounds, amputation, or reconstruction of a Charcot foot. This article reviews SUSCEPTIBILITY TO COMPRESSION the basic scientific and clinical research that support the concepts that metabolic neuropathy renders the peripheral nerve susceptible to compression in patients Two metabolic changes occur in the peripheral with diabetes and that decompression of lower extremity nerves of patients with diabetes that render the nerve peripheral nerves in these patients can relieve pain, susceptible to chronic compression. The most critical restore sensation, and prevent ulceration and amputation. is the increased water content within the nerve as the result of glucose being metabolized into sorbitol,21 Key Words: Decompression; Diabetic Neuropathy; which causes the nerve to have an increased volume. Surgery The second metabolic change is a decrease in the slow anterograde component of axoplasmic flow, which INTRODUCTION transports the lipoproteins necessary to maintain and rebuild the nerve. The peripheral nerves cross areas There is a cause for optimism in patients with symp- of anatomic narrowing, such as the carpal tunnel at toms related to diabetic neuropathy. Traditionally, foot the wrist, the cubital tunnel at the elbow, fibular tunnel and ankle surgeons have been asked to treat infec- at the outside of the knee, or the at the tion, heal ulcerations, reconstruct Charcot deformities, ankle, which causes external pressure on the nerve, or amputate the insensate foot. It is now possible to especially when its volume is already increased from consider surgery that can relieve pain and restore sensa- the water content. tion in patients with symptomatic diabetic neuropathy. This increased external pressure increases intraneural This approach can change the natural history of diabetic pressure, decreasing blood flow29 and resulting in a neuropathy by preventing ulceration and amputation. To relative ischemic condition for the peripheral nerve. The neurophysiologic consequences of decreased blood Professor of Plastic Surgery and Neurosurgery, Johns Hopkins University, flow in a peripheral nerve are paresthesias, inter- Baltimore, Maryland Professor of Plastic Surgery, Department of Surgery, University of Arizona, preted generally as numbness or tingling. The chronic Tucson, Arizona pathophysiologic result of increased pressure along a An invited presentation at the American Academy of Orthopaedic Surgeons Specialty Day for the American Academy of Orthopaedic Foot and Ankle peripheral nerve is demyelination. The peripheral nerve Society, February 8, 2003, New Orleans with decreased axoplasmic flow, as in patients with Corresponding Author: A. Lee Dellon, M.D. diabetes, cannot transport sufficient protein structures Institute for Peripheral Nerve Surgery to rebuild itself. Additionally, advanced glycosylation Suite 370, 3333 North Calvert Street end (AGE) products build up within the nerve. Although Baltimore, Maryland 21218 Email: [email protected] biomechanical properties of the peripheral nerve in For information on prices and availability of reprints, call 410-494-4994 X226 patients with diabetes have not been studied yet, the 749 750 DELLON Foot & Ankle International/Vol. 25, No. 10/October 2004 presence of these AGE products within the nerve theo- deformity of the hand. compression at the retically should make the nerve stiffer, decreasing nerve elbow can be decompressed surgically.7,9 Compres- gliding with joint motion. The non-enzymatic binding sion of the radial sensory nerve in the forearm causes of glucose to the collagen within the nerve and in the numbness over the remaining skin surface of the hand, epineurium is the basis for this decreased elasticity. the dorsoradial skin. The radial sensory nerve also can The decreased elasticity in the peripheral nerve and be decompressed surgically.17 Chronic compression of the nerve’s normal physiologic requirement to stretch the median, ulnar, and radial nerves resulting in a glove as it glides across joints increase the stress and strain distribution of numbness would result in symptoms on the peripheral nerve within these areas of known indistinguishable from those in a patient with symp- anatomic narrowing. This increasing tension along the tomatic diabetic neuropathy of the upper extremity. nerve further decreases blood flow within the nerve.36 This same applies to the lower extremity. Compres- The hypothesis that the peripheral nerves in patients sion of the ’s common peroneal nerve at with diabetes have an increased susceptibility to the lateral aspect of the knee occurs in the fibular tunnel, compression has been tested in the rat model.18 Rats causing paresthesias or pain from the knee to the top were made diabetic by being given streptozotocin. of the foot. The motor component, when completely Silicone bands were placed about the sciatic nerve compressed, results in a ‘‘drop foot,’’ just as complete in these rats and in a group of non-diabetic, age- compression of the motor branch of the at matched rats. Electrophysiology was tested in both the elbow results in a ‘‘drop wrist.’’ More commonly in groups after 6 months of banding, as this had been the lower extremity the long toe extensor is weak, so this demonstrated to be sufficient time to develop elec- toe is positioned lower than the other toes and is weak trophysiologic and histologic changes consistent with on manual muscle testing.33 Decompression of the chronic nerve compression in this model.32 It was common peroneal nerve in this location requires neurol- found that the diabetic rats had a statistically significant ysis by division of the fascial coverings above and below lower conduction velocity and a statistically significant the peroneus longus muscle. Over the dorsum of the lower amplitude for the sciatic nerve measured across foot, the deep peroneal nerve can become entrapped the region of compression than did the non-diabetic between the extensor digitorum brevis and the junction banded rats, confirming that the peripheral nerve has an of the first metatarsal and the cunieform bone.8 This increased susceptibility to chronic nerve compression entrapment is corrected by excision of the tendon of in diabetic rats. this small muscle, which has no functional significance in the foot. Entrapment of the deep peroneal nerve is similar to radial sensory nerve entrapment in the SYMPTOMS OF NEUROPATHY AND COMPRESSION forearm. Tarsal tunnel syndrome in the lower extremity is analogous to in the upper Patients with diabetic neuropathy have symptoms extremity.24,27 To achieve restoration of sensation of all that include sensory complaints of numbness and toes and the plantar aspect of the foot, the medial and tingling, pain, and loss of sensation and motor lateral plantar nerves and the calcaneal nerves must complaints of weakness. The complaints extend to each be released in its own separate tunnel just distal the autonomic system as well and, in the extremi- to the tarsal tunnel. Severe compression of the lateral ties, include loss of sudomotor function, with the skin plantar nerve creates hyperextension at the metatar- becoming dry and thick. The sensory symptoms occur sophalangeal joints, which appear as ‘‘hammer toes’’ in a distribution that has been called ‘‘stocking and in patients with diabetes but are really ‘‘clawed toes’’ glove,’’ with the symptoms being worse in the lower from intrinsic muscle paralysis in the foot. This is similar extremity than the upper extremity. In contrast, a patient to the ‘‘clawed hand’’ that results from intrinsic muscle with single chronic nerve compression has these same paralysis in the hand.30 Relief of paresthesias and pain symptoms but only in the distribution of that partic- in the foot, and often correction of the intrinsic muscle ular nerve. For example, a patient with carpal tunnel wasting, can be accomplished by decompression of syndrome, with compression has the the four medial ankle tunnels.11 Chronic compression of sensory complaints in only the palmar aspect of the the peroneal and tibial nerves would cause a stocking thumb, index, and middle fingers and weakness in the distribution of numbness and symptoms indistinguish- muscles that control part of the thumb’s function.31 able from those in a patient with symptomatic diabetic Chronic compression of the ulnar nerve at the elbow neuropathy of the lower extremity. results in paresthesias in the palmar and dorsal surfaces How can a physician identify compression of a periph- of the ring and little fingers, and weakness of pinch and eral nerve? The most reliable clinical finding of nerve grip strength. Severe ulnar nerve compression causes compression is tenderness of the nerve at the site of intrinsic muscle weakness, which creates a ‘‘claw’’ anatomic narrowing. This sensitivity of the nerve at Foot & Ankle International/Vol. 25, No. 10/October 2004 DIABETIC NEUROPATHY 751 the site of chronic compression may be manifested and an inability to perceive hot water in a bathtub or as simply tenderness of the nerve at that site, but feel the pedals required for driving a car and makes most often it is manifested by a distally-radiating pares- them unsteady when walking down stairs. These same thesia in the distribution of the nerve when the nerve symptoms put a patient at risk for ulcer, infection, is gently percussed (positive Tinel sign).5 If a systemic and amputation. Currently no medication is available cause exists for the nerve dysfunction, there should be for the symptoms of sensory loss, and this general no localizing sign along the course of the peripheral inability to treat the symptoms of neuropathy creates a nerve. However, if the neuropathy causes the nerve sense of hopelessness in many patients with diabetic to be susceptible to nerve compression, there can neuropathy, leading to depression and a sense of futility. be superimposed compression of the peripheral nerve Against this background, the concept that relief of in addition to the underlying neuropathy. Traditionally, symptoms of diabetic neuropathy by decompression electrodiagnostic testing has been used to make the of superimposed peripheral nerve compressions was diagnosis of peripheral nerve compression, neuropathy, introduced as a source of optimism for this difficult or nerve root compression. Often, however, the periph- clinical problem.6 eral neuropathy is so advanced that no conduction is measurable in the peripheral nerve. Also, the conduction Operative Treatment velocity and amplitude may be so reduced already that If the presence of a constricting structure causes identification of a superimposed nerve compression in symptoms of neuropathy in a patient with diabetes, a patient with neuropathy is not possible technically. then the absence of such a structure should mean In these situations, physical examination is critical in that symptoms of neuropathy do not occur. This making this distinction. hypothesis has been tested in the streptozotocin- induced diabetic rat model, a study first published TREATMENT in 1994.15 In that model, it was first demonstrated that a neuropathic walking track pattern occurred in Nonoperative rats with diabetes. A group of rats with serum glucose Laboratory tests can identify patients with diabetes levels of 400 was followed for one year (about half a and those who are not maintaining glycemic control. rat’s lifetime). Half of these rats with streptozotocin- Unfortunately, even patients maintaining strict glycemic induced diabetes had decompression of the tarsal control, with frequent daily monitoring of their blood tunnel before the onset of diabetes, and the other glucose, may develop the symptoms of neuropathy. half were not treated. Both groups were followed for The treatment of symptoms of neuropathy in a patient one year with walking track analysis. The group without with diabetes, in addition to the maintenance of a tarsal tunnel had walking track patterns that were glycemic control, relies on a combination of non- the same as weight-matched non-diabetic rats, while narcotic and narcotic neuropathic pain medications. the diabetic rats with intact tarsal tunnels developed a The classic triad of neuropathic medications includes progressive neuropathic walking track patterns. Without Tegretol (carbamazepine, Norvartis Pharmaceuticals, an anatomic site of narrowing, even the rats with poorly- East Hanover, NJ), Dilantin (phenytoin sodium, Parke- controlled diabetes did not develop evidence of diabetic Davis, New York, NY), and Elavil (amitriptyline neuropathy in the feet, suggesting that even if the hydrochloride, Mylan Pharmaceuticals, Morgantown, underlying metabolic neuropathy could not be corrected WV). Many patients are unable to tolerate the side medically, it might be possible to treat the symptoms effects of Tegretol, and Dilantin often is not effec- related to superimposed chronic nerve compressions by tive. Because many patients with neuropathy have decompression of the peripheral nerve. This research trouble sleeping, Elavil, the side effect of which is model also has been applied to the neuropathy related most commonly drowsiness, is often the most effec- to the chemotherapeutic drug cisplatin.40 That study tive of these three. Currently, Neurontin (gabapenin, extended the observations made in the diabetic rat Parke-Davis, New York, NY) has become the drug of model in that decompression of the tarsal tunnel in rats choice for the treatment of the symptoms of neuropathy. with cisplatin neuropathy restored normal walking track Many patients do not tolerate the doses required of patterns. These results were independently confirmed non-narcotic neuropathic pain medications or simply by a group of investigators23 using the identical cannot accept the decrease in cognitive function these model who reported that peripheral nerve function drugs induce. improved in diabetic rats when there was no tarsal For many patients with neuropathy the problem is tunnel compression present and additional functional not pain or paresthesias but the loss of sensation in improvement, as determined by walking track, analysis, their feet which causes them to have a loss of balance, resulted from opening the epineurium. 752 DELLON Foot & Ankle International/Vol. 25, No. 10/October 2004

Diagnosis and staging confidence limit of pressure for the patient to discrimi- Over the past 20 years, an approach to the selection nate two different points, then the nerve does not have of patients for decompression of peripheral nerves has normal function but does not yet have axonal loss. been developed; it begins with the measurement of If the distance at which one from two points can be peripheral nerve function to stage the degree of nerve distinguished is 9 mm, then axonal loss has occurred.38 impairment.13 A model developed for staging the degree Two-point discrimination is to the neurosensory testing of nerve impairment in patients with chronic nerve of peripheral nerve function as amplitude is to electro- compression without neuropathy has been found to be diagnostic testing. In terms of prognosis, if the pressure valid in patients with neuropathy. Since 1989, peripheral threshold is abnormal but two-point discrimination is nerve function has been evaluated with computer- still present, then the prognosis for recovery is one that assisted sensory motor testing. While vibrometry is is relatively fast. However, if no two-point discrimina- useful for evaluating a single patient and comparing that tion is present, then recovery will occur over the course patient to a group of patients, vibrometry does not help of a year as the nerve regenerates at the rate of one identify a specific nerve that requires decompression. inch per month, assuming that nerves in people with The reason for this is that vibration travels as a wave, diabetes regenerate at the same rate nerves in people and if it is not perceived well in the index finger, for without diabetes. instance, it is difficult to ascertain if the cause is a The most valid prognostic sign of a good result from lesion of the median nerve or of the radial nerve. decompression of a nerve in a person with diabetes Similarly, if the vibration is not perceived well in the and symptoms of neuropathy is the presence of a big toe, it is difficult to determine if the tibial or positive Tinel sign. This test is done by tapping the peroneal nerve is affected. The Semmes-Weinstein region of known anatomic tightness, such as the tarsal monofilament number 5.07 (10 gm of force) may be tunnel, with the examiner’s finger (not with a percussion useful in identifying an individual with diabetes who hammer). A ‘‘positive’’ test occurs when the patient can has lost protective sensation and is therefore at risk feel a radiating sensation, painful or not, into the territory of ulceration in the foot.1,19,20,25,26,34,35,37 The filament supplied by that nerve, e.g. the arch of the foot, the heel, represents a cutaneous pressure threshold of greater or the big toe. The simple perception by the patient that than 90 gm/mm2. At this advanced stage of chronic a thumping occurred is not a positive sign. Tapping nerve compression, the patient has lost two-point over several ‘‘control’’ sites, areas of skin without a discrimination and has severe axonal loss, and surgical known anatomic region of compression beneath them, intervention will probably not restore sensation and should be done. The common peroneal nerve at the relieve pain.12 fibular head often is just tender, and distally radiating In contrast, it has been found that the Pressure- sensations do not occur. Tenderness of this nerve is Specified Sensory DeviceTM (PSSD) (Sensory Manage- sufficient to suggest entrapment at this location. In my ment Services, LLC, Baltimore, Maryland) can identify experience with patients with diabetic neuropathy, when the earliest degree of chronic nerve compression by a superimposed nerve compression is identified by a measuring the pressure required to distinguish one positive Tinel sign, there is an 80% chance of a good to from two points touching the skin. Normative values excellent result in terms of pain relief and restoration of for the Pressure-Specified Sensory DeviceTM (PSSD) sensation to the feet.14 have been reported in the upper extremity for patients with carpal and cubital tunnel syndrome,16 as well as Results of surgical decompression in the lower extremity for patients with tarsal tunnel Since 1992,10 several studies have evaluated the syndrome.39 The PSSD is at least as sensitive as tradi- results of decompression of peripheral nerves in tional electrodiagnostic studies,38 it is not invasive nor patients with diabetes. These studies have been painful, and no electric shocks are used. The PSSD reviewed, and their patient populations regrouped to documents the presence of neuropathy by recording permit comparison of nerve-specific results. These a symmetrical sensory loss in both the peroneal and results are presented in Table 1 for carpal tunnel decom- tibial nerves (medial plantar, medial calcaneal, deep and pression, in Table 2 for cubital tunnel decompression, superficial peroneal nerves). Depending on the stage of and in Table 3 for tarsal tunnel decompression. the neuropathy, the patient can be referred for a surgical Decompression of the median nerve in the carpal consultation, i.e. when axonal loss is documented by tunnel in patients with diabetes gives excellent relief of abnormal two-point discrimination. As an example, the sensory symptoms in about 95% and good results in 99% confidence limit for two-point discrimination in the 5%, with 95% of the patients recovering useful two- hallux pulp is 8 mm in someone older than 45 years of point discrimination.10,2 These results are what one age.39 If the PSSD measurement is 8 mm of static two- would expect after carpal tunnel decompression in point discrimination but requires more than the 99% patients without diabetes.31 Foot & Ankle International/Vol. 25, No. 10/October 2004 DIABETIC NEUROPATHY 753

Table 1: Results of peripheral nerve decompression in diabetic neuropathy:

MEDIAN NERVE: CARPAL TUNNEL SYNDROME Study Recurrence Number Subjective results Two-point discrim

Nerves Patients Excellent Good Excellent Good of ulcer

Dellon, 199236,10 44 34 96% 2% 96% 4% 0% Aszmann et al., 20002 8 7 88% 12% 88 12% 0%

Table 2: Results of peripheral nerve decompression in diabetic neuropathy:

ULNAR NERVE: CUBITAL TUNNEL SYNDROME Study Strength Number Subjective results Two-point discrim

Nerves Patients Excellent Good Excellent Good Excellent Good

Dellon, 199236,10 11 8 82% 18% 82% 9% 54% 36% Aszmann et al., 20002 7 6 72% 28% 42% 44% n.a n.a.

n.a. = not available

Table 3: Results of peripheral nerve decompression in diabetic neuropathy:

POSTERIOR : TARSAL TUNNEL SYNDROME

Study Number Preoperative Results Recurrent Nerves Patients Ulcers Amput Improved Ulceration

Dellon, 199235,10 31 22 0 0 pain 85% 0% 2PD 72% Wieman and Patel, 199541 33 26 13 0 pain 92% 7% 2PD 72% ulcer 83% Chaffe4 2000 58 36 11 6 pain 86% 0% touch 50% ulcer n.a. Aszmann et al., 20002 16 12 0 0 2PD 69% 0% Wood and Wood, 200342 33 33 0 0 pain 90% 0% 2PD 67% Biddinger and Amend, 20043 22 15 0 0 pain 86% 0% 2PD 80%

The results of anterior submuscular transposition of with this type of ulnar nerve surgery for moderate to the ulnar nerve at the elbow, using the musculofascial severe ulnar nerve compression.31 Recovery of motor lengthening technique, in patients with diabetes gives function is not as good, with just 55% of patients excellent relief of sensory symptoms in about 77% recovering normal grip strength and 40% recovering and good results in 22%. Approximately 95% of normal pinch strength. patients recover useful two-point discrimination.10,2 The results of decompression of the tibial nerve and its These results are similar to the non-diabetic population medial and lateral plantar and calcaneal branches at the 754 DELLON Foot & Ankle International/Vol. 25, No. 10/October 2004 four medial ankle tunnels are determined by restoration be restored by decompressing the peripheral nerves. of sensation to the sole of the foot and relief of pain in the In contrast, if sensibility testing can be done earlier in foot. In five reported studies,36 – 39,41 in which the same patients with symptoms of neuropathy in the feet, then surgical technique was used for decompression, pain the ability to restore sensation (two-point discrimination) was relieved in 86% of patients and 72% recovered can be offered at an earlier stage, resulting in recovery useful two-point discrimination.2,4,10,41,42 Two studies of closer to normal sensation. included patients with a history of ulceration, and the Decompression of the median nerve in the carpal percentage of patients having relief of pain was the tunnel has a higher success rate than decompression same in these patients; however, many recovered only of the tibial nerve in the tarsal tunnel (Table 1 versus protective sensation (no two-point discrimination).4,41 Table 3) because patients usually seek care earlier for In 62 patients in this combined series who had never hand problems than for feet problems.37,40 This earlier had an ulcer or amputation, none reported an ulceration presentation of patients with hand problems may be or amputation during the followup period. In the 24 related to the general pessimism that accompanies the patients who had a previous ulcer or amputation, one teaching that diabetic neuropathy is ‘‘progressive and (4%) reported a recurrent ulceration during the follow- irreversible.’’ The observation that patients who have up period of observation. A recent report,42 confirmed had restoration of sensation to their feet through decom- that 76% of 33 patients with symptoms of diabetic pression of peripheral nerves have not developed ulcers neuropathy and positive Tinel signs had recovered good or had an amputation suggests that the natural history to excellent sensation in their feet, and 90% achieved of diabetic neuropathy can perhaps be changed.42 To good to excellent pain relief. effect this change, clinicians responsible for the care The ability to restore sensation to the feet of a of patients with diabetes need to measure sensibility in patient with diabetes holds the promise of prevention the foot, evaluate the foot for the presence of a Tinel of ulceration and amputation. We have been able to sign over known sites of peripheral nerve compres- follow for a mean of 4.5 years a group of patients sion, and refer patients to surgeons trained in lower with diabetes who have only had a unilateral set of extremity peripheral nerve decompression techniques. If peripheral nerves decompressed. Of the 49 patients in this concept can be introduced into clinical practice, the the series, there were no ulcerations or amputations frequency of foot ulcerations and amputations should of the lower extremities that had the peripheral nerve decrease significantly. Theoretically, recovery of sensi- decompressions. In contrast, in the legs that were bility in the foot should improve balance and reduce the not decompressed, there were 10 ulcerations and 4 number of falls with their associated fractures in this 28 amputations. This difference is significant (p <.001). group of patients. Indications for surgical decompression of a peripheral DISCUSSION nerve in the lower extremity of a patient with symptoms of diabetic neuropathy are 1) presence of pain unre- The realization that peripheral nerves in patients lieved by neuropathic pain medication in a patient with with diabetes are susceptible to compression can good glycemic control, even with a negative Tinel sign, offer a new source of optimism for patients who and 2) presence of symptoms of numbness, pares- suffer from symptoms of neuropathy.19 Over the past thesias, and loss of sensation in a patient with good 20 years, progressing from clinical observations37 to glycemic control and a positive Tinel sign. Criteria crit- basic science research,20 and then back to clinical ical for the success of surgery include the absence treatment of patients with diabetes and symptomatic of edema in the foot, a sufficient vascular supply as lower extremity neuropathy,40 experience has been judged by the presence of palpable pulses and supple- gained that can now be translated into the regular mented with segmental arterial pressure measurements, care of patients with diabetes. Independent surgical a medical condition acceptable for general anesthesia centers have reported essentially the same findings: or spinal anesthesia, a body weight less than 300 decompression of the tibial nerve and its branches at pounds, patient compliance with post-operative care the ankle and foot relieves pain and restores sensation instructions. Postoperative care includes placement of in about 80% of patients.37 – 41 a bulky, supportive, soft dressing that will permit imme- As with the treatment of most diseases, the earlier diate ambulation with a walker. This should allow the a patient receives treatment, the better the chances tibial nerve to glide in the tarsal tunnel but not tear out are that symptoms can be alleviated. With regard to the sutures. The sutures in the ankle are maintained diabetic neuropathy, once a patient has developed for 3 weeks, while the patient is permitted ambulation an ulceration, it is clear that sufficient sensory axons within the confines of the house. When the sutures are have degenerated and only protective sensation can removed, rehabilitation often is facilitated by walking in Foot & Ankle International/Vol. 25, No. 10/October 2004 DIABETIC NEUROPATHY 755 water each day in a rehabilitation pool. Bilateral simul- 22. 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