Neuropathic Pain
Introduction
Pain is usually the natural consequence of tissue injury resulting in
approximately forty million medical appointments per year. In general, as the
healing process commences, the pain and tenderness associated with the injury will
resolve. Unfortunately some individuals experience pain without an obvious
injury or suffer protracted pain that persists for months or years after the
initial insult. This pain condition is usually neuropathic in nature and
accounts for a large number of patients presenting to pain clinics with
chronic, nonñmalignant pain. Rather than the nervous system functioning
properly to sound an alarm regarding tissue injury, in neuropathic pain the
peripheral or central nervous systems are malfunctioning and become the cause
of the pain.
Terminology
Acute pain and chronic pain differ in their etiology, pathophysiology,
diagnosis and treatment. Acute pain is selfñlimiting and serves a protective
biological function by acting as a warning of onñgoing tissue damage. It is a
symptom of a disease process experienced in or around the injured or diseased
tissue. Associated psychological symptoms are minimal and are usually limited
to mild anxiety. Acute pain is nociceptive in nature,
and occurs secondary to chemical, mechanical and thermal stimulation of Añdelta
and Cñpolymodal pain receptors.
Chronic pain, on the other hand, serves no protective biological function.
Rather than being the symptom of a disease process, chronic pain is itself a
disease process. Chronic pain is unrelenting and not selfñlimiting and as
stated earlier, can persist for years and even decades after the initial
injury. Chronic pain can be refractory to multiple treatment modalities. If
chronic pain is inadequately treated, associated symptoms can include chronic
anxiety, fear, depression, sleeplessness and impairment of social interaction.
Chronic, nonñmalignant pain is predominately neuropathic in nature and involves
damage either to the peripheral or central nervous systems.
Nociceptive and neuropathic pain
are caused by different neuroñphysiological
processes, and therefore tend to respond to different treatment modalities. Nociceptive pain is mediated by receptors on Añdelta and
Cñfibers which are located in skin, bone, connective tissue, muscle and
viscera. These receptors serve a biologically useful role at localizing noxious
chemical, thermal and mechanical stimuli. Nociceptive
pain can be somatic or visceral in nature. Somatic pain tends to be well
localized, constant pain that is described as sharp, aching, throbbing, or
gnawing. Visceral pain, on the other hand, tends to be vague in distribution,
paroxysmal in nature and is usually described as deep, aching, squeezing and
colicky in nature. Examples of nociceptive pain
include: postñoperative pain, pain associated with trauma, and the chronic pain
of arthritis. Nociceptive pain usually responds to opioids and nonñsteroidal antiñinflammatories
(NSAIDS).
Neuropathic pain, in contrast to nociceptive pain,
is described as "burning", "electric",
"tingling", and "shooting" in nature. It can be continuous
or paroxysmal in presentation. Whereas nociceptive
pain is caused by the stimulation of peripheral of Añdelta and Cñpolymodal pain receptors, by algogenic
substances (eg. histamine bradykinin,
substance P, etc.) neuropathic pain is produced by damage to, or pathological
changes in the peripheral or central nervous systems.
Examples of pathological changes include prolonged peripheral or central
neuronal sensitization, central sensitization related damage to nervous system
inhibitory functions, and abnormal interactions between the somatic and
sympathetic nervous systems. The hallmarks of neuropathic pain are chronic allodynia and hyperalgesia. Allodynia is defined as pain resulting from a stimulus that
ordinarily does not elicit a painful response (eg.
light touch). Hyperalgesia is defined as an increased
sensitivity to a normally painful stimuli. Primary hyperalgesia, caused by sensitization of Cñfibers, occurs
immediately within the area of the injury. Secondary hyperalgesia,
caused by sensitization of dorsal horn neurons, occurs in the undamaged area
surrounding the injury.
Examples of neuropathic pain include: monoradiculopathies,
trigeminal neuralgia, postherpetic neuralgia, phantom
limb pain, complex regional pain syndromes and the various peripheral
neuropathies. Neuropathic pain tends to be only partially responsive to opioid therapy.
Pathophysiology
The mechanisms involved in neuropathic pain are complex and involve both
peripheral and central pathophysiologic phenomenon.
The underlying dysfunction may involve deafferentation
within the peripheral nervous system (eg.
neuropathy), deafferentation within the central
nervous system (eg. postñthalamic stroke) or an
imbalance between the two (eg. phantom limb pain).
Peripheral Mechanisms:
Following a peripheral nerve injury (eg. crush,
stretch, or axotomy) sensitization occurs which is
characterized by spontaneous activity by the neuron, a lowered threshold for
activation and increased response to a given stimulus. Should the injured nerve
be a nociceptor then increased nervous discharge will
equate to increased pain. Following nerve injury Cñfiber nociceptors
can develop new adrenergic receptors and sensitivity, which may help to explain
the mechanism of sympathetically maintained pain.
In addition to sensitization following damaged peripheral nerves, the
formation of ectopic neuronal pacemakers can occur at
various sites along the length of the nerve. Increased densities of abnormal or
dysfunctional sodium channels are thought to be the cause of this ectopic activity.1,2,3 The sodium channels in
damaged nerves differ pharmacologically and demonstrate different
depolarization characteristics.4 This may explain the rationale of
treatment with lidocaine, mexiletine,
phenytoin, carbamazepine,
and tricyclic antidepressants each of which blocks
sodium channels. These ectopic pacemakers can occur
in the proximal stump (eg. neuroma),
in the cell bodies of the dorsal root ganglion, and in focal areas of demylenation along the axon. Neuromas
are composed of abnormal sprouting axons and have a significant degree of
sympathetic innervation.5 Neuromas have
been reported to accumulate sodium channels at their distal ends which can
modulate their sensitivity. They can acquire adrenergic sensitivity, as
indicated by increased pain following injection of norepinephrine
into the neuroma. Neuromas
can also acquire sensitivity to catecholamines, prostanoids and cytokines.6 Novel ion channels
or receptors, not found in normal nerves, appear to be expressed in the
regenerating terminal/axon.4
Further animal investigations suggest that abnormal electrical connections
can occur between adjacent demyelinated axons. These
are referred to as ephapses. "Ephaptic cross talk" may result in the transfer of
nerve impulses from one axon to another. Cross talk between A and C fibers
develops in the dorsal root ganglion.7 Nerve growth trophic factors may be important in the elaboration of
these changes.4 A similar event referred to as "crossed afterdischarge" has also been described whereby
"the sprouts of primary afferents with damaged axons can be made to
discharge at high frequencies by the discharge of other afferents."8
It is also theorized that injured nerves may contain ephapses
between sensory and sympathetic fibers, and such crossñconnections may play a
role in the pathogenesis of sympathetically mediated pain.
Neurogenic inflammation is a useful model for
understanding pain and hyperalgesia.9 Neurogenic
inflammation and the cascade of events following neural injury have been
described.10 Inflammatory neuropeptides
(substance P) and prostaglandins (PGE2) may be released from primary afferent nociceptors and sympathetic postganglionic neurons
respectively,9,11 activating nearby receptors and triggering a
process of spreading activation. These mechanisms may explain the clinical
response of some neuropathic pain patients to topical nonsteroidal
antiñinflammatory drugs, lidocaine, and capsaicin.9
The connective tissue sheath around peripheral nerves is innervated by the nervi nervorum.
Injury, compression, and inflammation of the sheath may cause pain.12
In cancer patients, pain associated with tumor compression of neural structures
is clinically indistinguishable from nonñmalignant neuropathic pain.9
This nervi nervorum related
pain may resolve following tumor resection or treatment of tumor induced
inflammation.9 Antiñinflammatory medications (NSAIDs
and corticosteroids) have been shown to be effective in certain neuropathic
pain conditions. The mechanism of pain relief may be decreased edema at the
tumor or injury site.9 However these
medications also have membranes stabilizing effects and central analgesic
effects. Therefore it is extremely difficult to distinguish primary
tumorñassociated inflammation and involvement of the nervi nervorum from other
mechanisms of neuropathic pain.9
Central Mechanisms:
Following a peripheral nerve injury, anatomical and neuroñchemical
changes can occur within the central nervous system (CNS) that can persist long
after the injury has healed.13 This "CNS plasticity" may
play an important role in the evolution of chronic, neuropathic pain. As is the
case in the periphery, sensitization of neurons can occur within the dorsal
horn following peripheral tissue damage and this is characterized by an
increased spontaneous activity of the dorsal horn neurons, a decreased
threshold and an increased responsivity to afferent
input, and cell death in the spinal dorsal horn.14,15,16,17
In the nonñinjured state, A beta fibers (large myelinated
afferents) penetrate the dorsal horn, travel ventrally, and terminate in lamina
III and deeper. C fibers (small unmyelinated
afferents) penetrate directly and generally terminate no deeper than lamina II.
However, after peripheral nerve injury there is a prominent sprouting of large
afferents dorsally from lamina III into laminae I and II.20 After
peripheral nerve injury, these large afferents gain access to spinal regions
involved in transmitting high intensity, noxious signals, instead of merely
encoding low threshold information.18
Significant alterations have been shown in the dorsal horn ipsilateral to the injury. The mechanisms are likely
related to the barrage of afferent impulses or the factors transported from the
lesion site.4,9,21 Studies have revealed that peripheral nerve
injury may lead to increased mRNA for specific neurotransmitters (e.g.
substance P), differential temporal expression of mRNA and receptors,22
decreased levels of opiod binding sites,23,24,25
appearance of immediate early gene products (e.g. cñfos),26,27
of which the significance is that peripheral nerve injury is causing changes in
the cell's synthesis of products, and alterations in the relative levels of neuropeptides/neuromodulators (e.g. increased galanin and VIP and reductions in sP
and CGRP).4
Several forms of thermal or tactile hyperalgesia
may involve the intercellular and intracellular messengers nitric oxide and arachidonic acid and metabolites.28,29,30 Cyclooxygenase inhibition appears to suppress tactile
allodynia.4 Blockade of activation of protein kinase C has been
shown to prevent behavioral neuropathic manifestations.31,32 Protein
kinase C removes the voltage gating of the NMDA receptor, allowing activation
of the receptor by glutamate.4 Protein kinase C may also modulate
sodium channels.33
The injured axon may release factors which may be transported in a
retrograde or orthograde fashion to initiate changes
important to the development of a pain state.4,34 Thermal hyperalgesia has been prevented in the Bennett model of
nerve injury by blocking axonal transport bidirectionally
with colchicine.2,35 It has been shown also that colchicine
blocks orthograde transport of tachykinins
which may explain its ability to induce prolonged reductions in sciatic neurogenic extravasation at
concentrations that spare Cñfiber nociceptor
function.34
Repetitive noxious stimulation of unmyelinated
Cñfibers can result in prolonged discharge of dorsal horn cells. This
phenomenon which is termed "windñup", is a
progressive increase in the number of action potentials elicited per stimulus
that occurs in dorsal horn neurons.36 Repetitive episodes of "windñup"
may precipitate longñterm potentiation (LTP), which
involves a long lasting increase in the efficacy of synaptic transmission. Where "windñup" is thought to last only minutes, LTP by
definition, lasts at least one hour and maybe even months. Both "windñup"
and LTP are believed to be part of the sensitization process involved in many
chronic pain states.
Animal studies suggest that expansion of receptive fields may also occur following tissue injury. Therefore, any peripheral
stimulation would activate a greater number of dorsal horn cells because of an
increased overlap of their receptive fields.
Evidence suggests that excessive nociceptive input
to the dorsal horn can have excitotoxic consequences
resulting in the death of inhibitory interneurons. This inhibition may
contribute to spinal hyperñexcitability.
The allodynia and hyperalgesia
associated with neuropathic pain may be best explained by: 1) the development
of spontaneous activity of afferent input 2) the sprouting of large primary efferents (eg. Añbeta
fibers from lamina 3 into lamina 1 and 2), 3) sprouting of sympathetic efferents into neuromas and
dorsal root and ganglion cells, 4) elimination of intrinsic modulatory
systems and 5) up regulation of receptors in the dorsal horn which mediate excitatory
processes.
Recent animal studies have shown that dynamic and static hyperalgesia
are probably mediated by different mechanisms,37
tactile allodynia and hyperalgesia
are likely mediated by different mechanisms38,39 and repetitive
thermal and mechanical stimuli are likely processed in different ways.40,41
On a cellular level, the central nervous system plastic changes appear to be
associated with enhanced neurotransmission via the NMDA receptor. Under the
appropriate conditions, appropriate Cñfiber stimulation can activate dorsal
horn interñneurons, causing them to release excitatory amino acids (eg. aspartate and glutamate),
which will excite wide dynamic range (WDR) neurons via the NMDA receptor. Hanai found that the C fiber response to stimulation of the
superficial peroneal nerve consisted of three
components: early, middle, and late.42 The separation into three
components was found to be caused by asynchronous volleys in three different
classes of C fibers in the superficial peroneal
nerve.42 The phenomenon of wind up was observed to occur always in
the late component, frequently in the middle component and to a far lesser
extent in the early component.42 The NMDA antagonist, MK801
significantly suppressed the middle and late components of the C fiber
response, although the effect on the early component was insignificant.42
NMDA receptor activation triggers a cascade of events leading to sensitization
of dorsal horn wide dynamic range neurons then ensues. There is a significant
increase in intracellular calcium and activation of protein kinases
and phophorylating enzymes. NMDA receptor stimulation
will also increase the production of spinal phospholipase
and induce the production of nitric oxide synthetase.
The prostaglandins and nitric oxide which are subsequently produced and
released into the extracellular milieu can facilitate further release of
excitatory amino acids and neuropeptides from primary
afferent pain fibers. The NMDA receptor antagonists ketamine and dextromethorphan can
block this cascade of events which contribute to sensitization.
Management of Neuropathic Pain
Early recognition and aggressive management of neuropathic pain is critical
to successful outcome. Oftentimes, multiple treatment modalities are provided
by an interdisciplinary management team. Numerous treatment modalities are
available and include systemic medication, physical modalities (eg. physical rehabilitation), psychological modalities (eg. behavior modification, relaxation training), invasive
procedures (eg. triggerñpoint injections, epidural
steroids, sympathetic blocks), spinal cord stimulators, intrathecal
morphine pump systems and various surgical techniques (eg.
dorsal root entry zone lesions, cordotomy and sympathectomy). It should be noted that caution is warranted
regarding the use of neuroablative techniques. Such
approaches may produce deaffrentation and exacerbate
the underlying neuropathic mechanisms. The focus of this review will be on
pharmacological interventions.
As previously mentioned, most neuropathic pain responds poorly to NSAIDS and
opioid analgesics. The mainstay of
treatment are predominantly the tricyclic
antidepressants (TCA's), the anticonvulsants and the
systemic local anesthetics. Other pharmacological agents that have proven
efficacious include the corticosteroids, topical therapy with substance P depletors, autonomic drugs and NMDA receptor antagonists.
The TCA's have been successfully used for the
treatment of neuropathic pain for some 25 years. The mechanism of action for
the alleviation of neuropathic pain is thought to be due to the inhibition of
reñuptake of serotonin and norepinephrine within the
dorsal horn,49 however, other possible
mechanisms of action include alphañadrenergic blockade, sodium channel effects
and NMDA receptor antagonism.
Amitriptyline is the prototypical tertiary amine.
Other tertiary amines include imipramine, doxepine, clomipramine and trimipramine. Unlike the dosing regimen utilized for the
treatment of depression doses of TCA's for treatment
of neuropathic pain are considerably less. The typical dosing schedule for amitriptyline may be simply 10 mg orally at bedtime with a
gradual escalation every three days, in 10 mg increments, to a maximum to 30 to
50 mg orally at bedtime. Furthermore, the onset analgesia usually occurs over
several days versus the two weeks that are required for the onset of the
antidepressant effects of the drugs.
The side effect profile of the TCA's include sedation and anticholinergic
effects. Since these side effects are more prominent with the tertiary amines
prudence would dictate the use of a secondary amine such as nortriptyline
or desipramine, particularly in the elderly
population who are more sensitive to the side effects.
The recently introduced selective serotonin reuptake inhibitors (SSRI's) have not proven to be as effective against
neuropathic pain as anticipated. Fluoxetine (Prozac)
only appears to relieve pain in patients with coñmorbid depression. Paroxetine (Paxil) has found some
utility in the treatment of chronic, daily headaches. In general, the SSRI's are partially effective in the treatment of diabetic
neuropathy, but not to the extent of the TCA's. Venlafaxine (Effexor) may have
some analgesic effects since, like the TCA's, it inhibits the reuptake of both serotonin and norepinephrine. Its side effect profile is similar to the
other SSRI's and can include agitation, insomnia, or
somnolence, gastrointestinal distress and inhibition of sexual functioning. Anticholinergic side effects are less bothersome than with
the TCA's.
The antiñconvulsant medications can be
particularly effective treatment for neuropathic pain that is described as
burning and lancinating in nature. Commonly used
medications in this category include phenytoin, carbamazepine, valproic acid, clonazepam, and gabapentin.
Carbamazepine has proven to be particularly
effective against glossopharyngeal neuralgia, post
herpetic neuralgia, trigeminal neuralgia, and diabetic neuropathies. Should carbamazepine prove ineffective, it can be replaced with phenytoin. Unlike the other anticonvulsants, valproic acid has found some success in treating migraine
headaches. The combination of an anticonvulsant with a TCA can be synergistic.
The mechanism of action of the anticonvulsant medications is thought to
involve membrane stabilization. Evidence also suggests that some of the agents,
such as carbamazepine and phenytoin
can depress both segmental and descending excitatory pathways in the CNS and at
the same time facilitate inhibitory mechanisms. For example, carbamazepine has been shown to inhibit the electrical C
and A fiber evoked neuronal responses of spinal nerve ligated rats.50 Valproic
acid, on the other hand, has been reported to increase gammañamino butyric acid
(GABA) levels in the substantia nigra
and corpus striatum. Gabapentin, which we will be
discussing subsequently, reportedly increases extracellular GABA levels
throughout the brain, including the thalamus and causes the release of GABA
from glial cells. However it is unlikely that Gabapentin increases GABAergic
tone because neither GABAa nor GABAb
antagonists reverse the analgesic effects of Gabapentin.48
Because of the significant risks of the blood dyscrasias
and liver dysfunction, baseline and periodic monitoring of blood chemistries
and liver function tests are highly recommended when prescribing phenytoin, carbamazepine, or valproic acid.
Although clonazepam, a benzodiazepine, is usually
used for the treatment of petite mal and myoclonic
seizures, it has been successfully utilized to treat the lancinating
and pain associated with phantom limb pain.51 Its mechanism of
action may be associated with its reputed ability to enhance the inhibitory
action of GABA within the CNS, and also possibly secondary to increased
serotonin levels.
Gabapentin (Neurontin),
1ñ(aminomethyl) cyclohexaneñacetic
acid, is an antiñepileptic drug which was introduced in 1993 and was originally
approved for the treatment of partial seizures with or without secondary
generalization. Recently, however, reports have documented its efficacy in the
treatment of various neuropathic pain states such as complex regional pain
syndrome, deafferentation neuropathy of the face, postherpetic neuralgia, sciatic type pain, and HIVñrelated
neuropathy.52 The effective dose range is 30ñ300 mg/kg (systemic)
and >37.5 mg/kg (IT).48 Gabapentin is
reportedly completely ineffective in altering threshold responses to acute nociceptive stimuli at doses up to 300 mg/kg.53ñ56
Presently the mechanism of action as either an anticonvulsant or an analgesic
is unknown. The antinociceptive effects are likely to
be due to actions within the spinal cord, because 1000 times the IT dose is
required to produce equianalgesic effects when given
intraperitoneally.53,57 Gabapentin
binds to the alpha 2 delta calcium channel subunit.48 However, the
relationship between binding at this site and the analgesic properties of gabapentin have not been determined. The NMDA receptor
complex may be a potential spinal locus for neuropathic pain relief
, but it has not been conclusively found that this is the major site of
action.48 Gabapentin has a relatively
benign side effect profile and is well tolerated if dosing proceeds in a
gradually escalating manner. It has few if any drug interactions and is
primarily renally excreted. Although expensive, it
does not require the routine monitoring of blood chemistries and liver
functions tests like carbamazepine and phenytoin. To date, little evidence suggests the efficacy
of felbamate or lamotrogine
in the treatment of neuropathic pain. Further investigation is necessary.
The systemic local anesthetics which are commercially available include lidocaine, tocainide, and mexiletine. The assumed mechanism of action to effect analgesia is the acute blocking of sodium channels. Phenytoin, carbamazepine and tricyclic antidepressants also act as sodium channel
blockers. Following the use of the TCA's and
anticonvulsants, local anesthetics tend to be third line drugs. Lidocaine has proven effective for noncancer
patients58 but not for those with cancer.59 In cancer
patients tumor involvement of nervi nervorum with "nociceptive
neuropathic pain" (as discussed earlier) may represent a different
mechanism with variable response to therapy.9 The predictive value
of lidocaine in determining the expected benefits of
drugs such as mexilitene remains important in
allowing us to move more efficiently through therapeutic trials.9
Recent studies have suggested that the duration and pattern of spontaneous
discharge is dependent on the level and kinetics of Na+ slow channel inactivation.60
Slow inactivation of voltageñgated ion channels could be major factors in the
induction and treatment of neuropathic pain.60 QXñ314, a positively
charged lidocaine derivative which is frequently
assumed to be membrane impermeant, has recently been
shown to acutely block Na+ channels at nerve injury sites in rats.61
We avoid the use of tocainide because of unacceptable
side effects which include blood dyscrasis and
pulmonary fibrosis. Dosing of mexiletine is begun at
150 mg po qd and is slowly
escalated by 150 mg q 72 hours to a maximum of 10 mg/kg/day as tolerated.62
The only absolute contraindication to the use of mexiletine is preñexisting second or third degree AV block
or known allergy to the medication.
Autonomic drugs which are proven beneficial in the treatment of neuropathic
pain include the alphañ2 agonists (eg. Clonidine) and
alphañ1 antagonists (eg. prazosin,
terazosin). The role of the 2 adrenergic
system in neuropathic pain has been studied using various pharmacologic
interventions and animal models.63 In animal studies, alpha 2
adrenergic agonists produce analgesia by actions in the periphery, supraspinal CNS, and in the spinal cord.64
Spaulding et al studies in mice suggested a primary spinal site of action.65
Clonidine is believed to produce analgesia at the
spinal level in part through stimulation of cholinergic interneurons in the
spinal cord. This cholinergic mediation of analgesia, as reflected by CSF
acetylcholine concentration is activated by intrathecal,
but not IV, injection of clonidine.66 However, clonidine
has been shown to produce analgesia to experimental pain stumuli
after systemic67 and epidural68 injection. Yet, clinical
studies of systemic clonidine for analgesia have
yielded conflicting results.64 Alpha 2 adrenergic agonists produce
sedation and reduced blood pressure in addition to analgesia small doses (ie 50 mg) clonidine may reduce
blood pressure more after an intrathecal than IV
injection.64 Clonidine has also been shown
to potentiate the neuropathic pain relieving action
of NMDA antagonist MKñ801 while preventing its neurotoxic
and hyperactivity side effects.69 Clonidine
is available in several different dosage forms and can be administered orally,
transdermally70 or spinally. Conversely, systemic Dexmedetomidine, another alpha 2 adrenergic agonist, has
been shown neither to prevent nor attenuate neuropathic pain behavior in rats.63
Dexmedetomidine has affinity to all three alpha 2ñ
adrenergic subtypes.71 The role of the different subtypes of alpha 2
adrenoreceptors is unclear. Subtypeñselective alpha
2ñadrenergic agonists are needed for further studies.
Several other pharmacological treatments which have proven beneficial in the
treatment of neuropathic pain include the corticosteroids, and capsaicin cream.
Corticosteroids are believed to provide longñterm pain relief because of their
ability to inhibit the production of phospholipaseñAñ2
and through membrane stabilizing effects, hence their utility for epidural
steroid injections.1 Topical capsaicin cream (Zostrix,
0.025% and 0.075%) is a substance P depletor, and has
on occasion provided relief for both acute herpetic neuralgia (shingles) and
postñherpetic neuralgia. Capsaicin is known for its selectivity for and effect
on Cñfiber nociceptors and heat receptors.72
Studies have shown its ability to trigger membrane depolarization and to open
non selective cation channels,73 which may
be either reversible or lytic. Capsaicin is theorized
to cause a neurotoxic cellular degeneration of
primary afferent nociceptors.74 Basically, exposure to capsaicin
results in activation, desensitization, and under certain conditions, the
destruction of lightly myelinated or unmyelinated primary afferent fibers.75 A recent
preliminary study proposes a clinical role for topical capsaicin at doses of
5%ñ10% in patients with intractable pain.72 A recent animal study
suggests that an orally bioavailable capsaicin
analogue, civamide (cisñ8ñmethylñNñvanillylñ6ñnonenamide) possessed
analgesic activity with respect to several noxious stimuli, including nerve
injuryñinduced tactile allodynia.39 Compliance may be a problem with
this medication, since it needs to be applied 4ñ5 times a day for several weeks
before any significant benefit is appreciated and it has intense initial
burning effects.76 A recent study demonstrated that if famciclovior (Famvir) is
administered within 72 hours of the onset of the vesicles of shingles then
damage to peripheral nerves can be minimized and therefore, the subsequent pain
of postñherpetic neuralgia attenuated.77 The dose of famciclovior is 500 mg orally, three times a day for seven
days.77
If a chronic neuropathic pain condition is already well established,
treatment is more difficult. Sensitization (eg. "windñup") is presumed to have already
occurred, so the ideal medication would include an NMDA receptor antagonist.
Two agents are currently available. Ketamine is an injectable anesthetic that nonñcompetitively antagonizes
NMDA receptors.78 Although it has proven beneficial in the treatment
of neuropathic pain, side effects tend to be unacceptable.79 NMDA
receptor antagonists are known to induce psychomimetic
reactions in adult humans and induce behavioral disturbances such as learning
and memory impairments, sensorimotor disturbances,
stereotypical behavior and hyperactivity and pathomorphological
changes in neurons of the posterior cingulate/retrosplenial
(PC/RS) cortex of the adult rat.69 Recent animal studies have
reported that preemptive intrathecal ketamine delayed mechanical hyperalgesia
but did not prevent it.41 Also, a case report suggests that epidural
administration of a "very low dose" of Ketamine
is sufficient to block activated NMDA receptors and is an effective choice for
the management of neuropathic pain without undesirable side effects.80
We occasionally will prescribe dextromethorphan, a
readily available overñtheñcounter antitussive, to
supplement the medication regimen of some of our patients with neuropathic
pain. Like Ketamine, it is a nonñcompetitive
antagonist at the NMDA receptor. However in humans, doses may be so high that
unacceptable side effects occur. MK801, an antagonist for the NñmethylñDñaspartate receptor for glutamate, has been shown to reverse
mechanical hyperalgesia in streptozotocin/diabetic
rats81 and conversely to have no effect on tactile allodynia in nerveñinjured rats.82 Amantadine, an antiviral and anti Parkinsonian
agent, was shown to act as a nonñcompetitive NMDA antagonist.83
Unlike other NMDA antagonists amantadine is
clinically available for chronic use in humans and its level of toxicity is
low. Case reports84 and a preliminary double
blind, controlled trial85 show that acute administration of amantadine significantly reduces surgical neuropathic pain
in cancer patients. Investigational NMDA receptor antagonists are
currently undergoing clinical trials.
Activation of NMDA receptors leads to calcium entry into the cell and
initiates a series of central sensitization. This sensitization may be blocked
not only with NMDA receptor antagonists, but also with calcium channel blockers
that prevent Ca2+ entry into cells. A double blind study revealed that epidural
verapamil and bupivacaine
reduced the amount of self administered post op analgesic versus epidural bupivacaine alone. The authors suggest that epidural verapamil may prevent central sensitization by surgical
trauma.86
Clinical experience with the use of opioids for
chronic nonñmalignant pain which is neuropathic in character suggests that
there may be a subñpopulation of chronic pain patients who may clearly benefit
from maintenance with opioid analgesics.87
Many studies have shown that neuropathic pain is only slightly responsive or
not responsive at all to opioid treatments.88
Yet others have shown that neuropathic pain responds to high doses of opioids.89ñ91
Portenoy has stated that opioid
responsiveness is partly a matter of dosage and that satisfactory outcomes can
be obtained following dose escalation to an endpoint determined by either
adequate analgesia or intolerable side effects. Benedetti et al suggest that postop neuropathic pair responds to opioid,
opioid responsiveness of neuropathic pain is partly a
matter of dosage and higher doses of opioids that are
necessary to relieve neuropathic pain may be not a characteristic of
neuropathic pain per se but a general feature related to the individual.88
A randomized doubleñblind activeñplaceboñcontrolled crossover trial suggested
that fentanyl may relieve nonñcancer neurapathic pain by its intrinsic analgesic effect.92
The indiscriminate prescribing of chronic opioids,
seductive hypnotics and muscle relaxants, however, is without justification,
especially if patients are not experiencing decreased pain and increased
function.
Agents that may soon be available for the treatment of neuropathic pain
include: 1) butylñparañaminobensoate
(ButambenÆ), an ester local anesthetic, 2) bupivacaine microspheres,and 3) SNXñIII, a selective calcium channel blocker.
Nicotinic acetylcholine receptor agonists such as ABTñ594, which may also prove
efficacious, are in preliminary research stages. Animal studies have revealed
the following as potential therapies in neuropathic pain 1) electroconvulsive
treatment93 2) intrathecal injection of chromaffin cells94ñ96 3) inrathecal
injection of Nitric oxide synthase inhibitor
LñNññGñnitro arginine methyl ester (LñNAME)97 4) intrathecal
neostigmine.98 A clinically available agent which is currently being
investigated for the treatment of neuropathic pain is levodopa.99
Conclusion:
Clearly, numerous pharmacological agents are available for the treatment of neuropathic pain. The definitive drug therapy has however remained elusive. Oftentimes triple drug therapy with tricyclic antidepressants, antiñconvulsants and a systemic local anesthetic is necessary. Occasionally, there is the patient who requires chronic opioid therapy in conjunction with the above medications. When patients fail systemic treatments implantable systems, such as a spinal cord stimulator, or intrathecal morphine pumps are available. Recently, the spinal cord stimulator has been shown to attenuate the augmented dorsal horn release of excitatory amino acids via a GABAergic mechanism in rats.100 Rarely, surgical intervention is required.
References:
1. Devor M, et al, Corticosteroids suppress ectopic neuronal discharge in experimental neurons. Pain
22:127-137, 1985.
2. Devor M, Govrin - Lippmann R: Axoplasmic transport
block reduces ectopic impulse generation in injured
peripheral nerves. Pain 16:73-85, 1983.
3.
England JD, Gamboni F, Levinson SR. Immunocytochemical localization of sodium channels form
along demyelinated axons. Brain
Research 1991; 548:334-337.
4. Yaksh TL, Chaplan SR. Physiology
and pharmacology of neuropathic pain. Anesthesiology Clinics of
5.
Chung K, Kim HJ, Na HS, et al: Abnormalities of sympathetic innervation
in the area of an injured peripheral nerve in a rat model of neuropathic pain. Neurosci Lett 162:85-88,1993.
6. Devor M. Neuropathic pain
and injured nerve - peripheral mechanisms. Br Med Bull 47: 619-630, 1991.
7. Devor M, Wall PD: Cross - excitation in dorsal root ganglia
of nerve - injured and intact rats. J Neurophysiol
64: 1733-1746, 1990.
8.
Bennett, GF, Neuropathic pain. In Textbook of Pain, P.D. Wall and R. Melzack (ed.), Churchill
9.
Allen R. Neuropathic Pain: Mechanisms and Clinical Assessment. Assessment and
Treatment of Cancer Pain, Progress in Pain Research and Management, Vol. 12
(1998) 159-173.
10.
Fields HL. Pain.
11.
Levine JD, Fields HL, Basbaum AI. Peptides
and the primary afferent nociceptor. J Neurosci 1993; 13:2273-2286.
12.
Asbury AK, Fields HL. Pain due to peripheral nerve damage; an
hypothesis. Neurology 1984; 34:1587-1590.
13. Tasker RR. Central Pain Syndromes.
In Principles and Practice of Pain Management,
14.
Johnson BW, Parris WCV. Mechanisms of Neuropathic Pain.
In Current Review of Pain, Raj PP,
(ed.) Current Medicine, 1994.
15.
Cameron AA, Cliffer KD, Dougherty PM, et al: Changes
in lectin, GAP-43 and neuropeptide
staining in the rat dorsal horn following experimental peripheral neuropathy. Neurosci Lett 131:249-252, 1991.
16.
Garrison CJ, Dougherty PM, Kajander KC, et al:
Staining of glial fibrillary
acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve
constriction injury. Brain Res 565:1-7, 1991.
17.
Sugimoto T, Bennett GJ, Kajander KC. Transsynaptic degeneration in the superficial dorsal horn
after sciatic nerve injury: Effects of a chronic constriction injury, transection and strychnine. Pain 42:205-213, 1990.
18.
Todd AJ, Sullivan AC. Light microscope study of the coexistence of GABA-like
and glycine-like immunoreactivities
in the spinal cord of the rat. J Comp Neurol
296:496-505, 1990.
19.
Fields HL, Basbaum AI. Central
nervous system mechanisms of pain modulation. In: Wall PD, Melzack R (Eds). Textbook of
Pain, 3rd ed.
20. Yaksh TL: The spinal pharmacology of facilitation of
afferent processing evoked by high-threshold afferent input of the post injury
pain state Curr Opin Neurol Neurosurg 6:250-256, 1993.
21. Woolf CL, Chong MS. Preemptive
analgesia: treating postoperative pain by preventing the establishment of
central sensitization. Anesth. Analg. 1993; 77:362-379.
22.
Ito Y, Yamamoto M, Li M, Doyu M, Tanaka F, Mutch T, Mitsuma T, Sobue G. Differential temporal expression of mRNAs for ciliary neutotrophic factor
(CNTF), leukemia inhibitory factor (LIF), interleukin-6 (IL-6), and their
receptors (CNTFR , LIFR , IL-6R and gp130) in injured peripheral nerves. Brain
Research 793 (1998) 321-327.
23. Besse D, Lombard MC, Besson
JM: Time related decreases in mu and delta opioid receptors in the superficial dorsal horn of the rat
spinal cord following a large unilateral dorsal rhizotomy.
Brain Res 578:115-127, 1992.
24. Besse D, Lombard MC, Perrot
S, etal: Regulation of opioid
binding sites in the superficial dorsal horn of the rat spinal cord following
loose ligation of the sciatic nerve: Comparison with
sciatic nerve section and lumbar dorsal rhizotomy.
Neuroscience 50:921-933, 1992.
25.
Stevens CW, Kajander KC, Bennett GJ, et al: Bilateral
and differential changes in spinal mu, delta and
kappa opioid binding in rats with a painful,
unilateral neuropathy. Pain 46:315-326, 1991.
26.
Presley RW, Menetry D, Levine JD, et al, Systemic
morphine suppresses noxious stimulus-evoked Fos protein-like immuno
reactivity in the rat spinal cord. J Neurosci
10:323-335, 1990.
27. Tolle TR, Castro-Lopes JM,
28. Coderre TJ, Yashpal K.
Intracellular messengers contributing to persistent nociception
and hyperalgesia induced by L-glutamate and substance
P in rat formalin pain model. Eur J Neurosci 6:1328-1334, 1994.
29. Malmberg AB, Basbaum AI. Partial
sciatic nerve injury in the mouse as a model of neuropathic pain: behavioral
and neuroanatomical correlates. Pain 76 (1998)
215-222.
30. Malmberg AB, Yaksh TL: Spinal
nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception
in the formalin test in rats. Pain 54:291-300, 1993.
31. Ahlgren SC, Levine JD: Protein Kinase C inhibitors decrease
hyperalgesia and C fiber hyperexcitability
in the streptozotocin - diabietic
rat. J Neurophysiol 72: 684-692, 1994.
32. Yashpal K, Pitcher GM, Parent A, et al: Noxious thermal and
chemical stimulation induce increases in 3H-phorbol 12, 13-dibutyrate binding
in spinal cord dorsal horn as well as persistent pain and hyperalgesia,
which is reduced by inhibition of protein kinase C. J Neuroscience
15:3263-3272, 1995.
33. Thio CL, Sontheimer H: Differential
modulation of TTX-sensitive and TTX-resistant Na+ channels in spinal cord astrocytes following activation of protein kinase C. J Neurosci 13:4889-4897, 1993.
34. Kingery WS, Guo TZ, Poree LR, Maze M. Colchicine
treatment of the sciatic nerve reduces neurogenic extravasation, but does not affect nociceptive
thresholds or collateral sprouting in neuropathic or normal rats. Pain 74
(1998) 11-20.
35.
Yamamoto T, Yaksh TL: Effects of colchicine
applied to the peripheral nerve on the thermal hyperalgesia
evoked with chronic nerve constriction. Pain 55:227-233, 1993.
36. Pockett S. Spinal cord sympathetic plasticity and chronic
pain. Anesth. Annalg., 80:173-179, 1995.
37. Gottrup H, Nielsen J, Arendt-Nielsen
L, Jensen TS. The relationship between sensory thresholds and
mechanical hyperalgesia in nerve injury. Pain
75 (1998), 321-329.
38.
Jett MF, McGuirk J, Waligora
D, Hunter JC. The effects of mexiletine,
desipramine and fluoxetine
in rat models involving central sensitization. Pain 69 (1997) 161-169.
39. Hua XY, Chen P, Hwang J, Yaksh
TL. Antinociception induced by civamide,
an orally active capsaicin analogue. Pain (1997) 313-322.
40. Attal N, Brasseur L, Chauvin M, Bouhassira D. A case of pure dynamic mechano-allodynia
due to a lesion of the spinal cord: pathophysiological
considerations. Pain 75 (1998) 399-404.
42. Hanai F. C Fiber responses of wide dynamic range neurons in
the spinal dorsal horn. Clinical Orthopaedics and
Related Research No. 349(1998), pp 256-267.
43. Yaksh TL: Pharmacology of the Pain Processing System In:
44. Yezierski RP, Liu S, Ruenes GL, Kajander KJ, Brewer
KL. Excitotoxic
spinal cord injury: behavioral and morphological characteristics of a central
pain model. Pain 75 (1998) 141-155.
45. Jasmin L, Kohan L, Franssen M, Janni G, Goff JR. The cold plate as a test of nociceptive behaviors: description and application to the
study of chronic neuropathic and inflammatory pain models. Pain 75 (1998)
367-382.
46. Malmberg AB, Yaksh TL: The effect
of morphine on formalin-evoked behavior and spinal release of excitatory amino
acids and prostaglandin E2 using microdialysis in
conscious rats. Br J Pharmacol 114:1069-1075, 1995.
47. Yaksh TL. Behavioral and autonomic correlates of the
tactile evoked allodynia produced by spinal glycine inhibition: Effects of modulatory
receptor systems and excitatory amino antagonists. Pain 37 (1989) 111-123.
48. Gillin S, Sorkin L. Gabapentin reverses the allodynia
produced by the administration of anti-GD2 ganglioside,
an immunotherapeutic drug. Anesth Analg
1998;86:111-116.
49. Goodkind K, et al, On the putative
efficacy of antidepressants in chronic benign pain syndromes: an update. Pain
Forum 4:237-247, 1995.
50.
Chapman V, Suzuki R, Chamarette HLC, Rygh LJ, Dickenson AH. Effects of systemic carbamazepine and gabapentin on
spinal neuronal responses in spinal nerve ligated
rats. Pain 75 (1998) 261-272.
51. Bartusch, SL, et al, Clonazepam
for the Treatment of Lancinating Phantom Limb Pain.
12:59-62, 1996.
52. Rosner H, et al, Gabapentin
Adjunct Therapy in Neuropathic Pain States. 12:56-58, 1996.
53.
Xiao W-H, Bennett GJ. Gabapentin has an anti-nociceptive effect mediated via a spinal site of action in
a rat model of painful peripheral neuropathy. Analgesia 1997;
2:267-273.
54. Hunter JC, Goas KR,
Hedley LR, et al. The effect of novel anti-epileptic drugs in rat experimental models
of acute and chronic pain. Eur J Pharmaco 1997; 324:153-160.
55.
Singh L, Field MJ, Ferris P, et al. The anti-epileptic agent gabapentin possesses anxiolytic-like
and antinociceptive actions that are reversed by
D-serine. Psychopharmacology 1996; 127:1-9.
56. Stanfa LC, Singh L, Williams RG, Dickerson AH. Gabapentin, ineffective in normal rats, markedly reduces
C-fiber evoked responses after inflammation. Neuroreport 1997; 8:587-590.
57. Hwang JH, Yaksh TL. The effect of intrathecal
gabapentin on tactile-evoked allodynia
in a surgically-induced neuropathic pain model in the rat. Reg Anesth 1997; 22:249-256.
58. Rowbotham MC, Reisner-Keller LA,
Fields HL. Both intravenous lidocaine and morphine
reduce the pain of post herpetic neuralgia. Neurology 1991;41:1024-1028.
59. Bruera E, Ripamonti C, Brennis C, Macmillan K, Hanson J. A
randomized double-blind crossover trial of intravenous lidocaine
in the treatment of neuropathic pain. J Pain Symptom Manage 1992;
7(3):138-140.
60.
Elliott JR. Slow Na+ channel inactivation and bursting discharge in a simple
model axon: implications for neuropathic pain. Brain Research 754 (1997)
221-226.
61. Omana-Zapata I, Khabbaz MA,
Hunter JC, Bley KR. QX-314 inhibits ectopic nerve activity associated with neuropathic pain.
Brain Research 771 (1997) 228-237.
62.
Glazer S, Portenoy RK, Systemic local anesthetics in
pain control, J. Pain Sympt Mgmt 6:30-39, 1991.
63. Kontinen VK, Paananen S, Kalso E. The effects of the - 2
-adrenergic agonist, Dexmedetomidine, in the Spinal
Nerve Ligation Model of Neuropathic Pain. Anesth Analg 1998;86:355-360.
64. Eisenach JC, Hood DD, Curry R. Intrathecal,
but not intravenous, clonidine reduces experimental
thermal or capsaicin-induced pain and hyperalgesia in
normal volunteers. Anesth Analg 1998; 87:591-596.
65.
Spaulding TC, Venafro JJ, MaMG,
Fielding, S. The dissociation of the antinociceptive
effect of clonidine from supraspinal
structures. Neuro pharamacol 1979; 18:103-105.
66.
De Kock M, Eisenach J, Tong
C, et al. Analgesic doses of intrathecal but not
intravenous clonidine increase acetylcholine in
cerebrospinal fluid in humans. Anesth Analg 1997; 84:800-803.
67. Porchet HC, Piletta P, Dayer P. Pharmacokinetics pharmacodynamic
modeling of the effects of clonidine on pain
threshold, blood pressure, and salivary flow. Eur J Clin
Pharmac 1992; 42:655-661.
68. Eisenach J, Detweiler D, Hood D. Hemodynamic and analgesic actions of epidurally
administered clonidine. Anesthesiology
1993; 78:277-287.
69. Jevtovic-Todorovic V, Wozniak DF, Powell S, Nardi A, Olney JW. Clonidine potentiates the neuropathic pain-relieving action of MK-801
while preventing its neurotoxic and hyperactivity
side effects. Brain Research 781 (1998) 202-211.
70.
Ziegler D, Lynch SA, Muir J, et al, Transdermal clonidine vs placebo in painful
diabetic neuropathy. Pain 48:403-408, 1992.
71.
Mac Donald E, Scheinin M. Distribution and
pharmacology of alpha 2-adrenoreceptors in the central nervous system. J Physiol pharmacol
1995; 46:241-258.
72.
Robbins WR, Staats PS, Levine J, et al. Treatment of
intractable pain with topical large-dose capsaicin: preliminary report. Anesth Analg 1998;86:579-583.
73.
Dray A. Mechanism of action of capsaicin - like molecules on sensory neurons. Life Sci 1992; 51:1759-1765.
74. Chung JM,
75. Holzer P. Capsaicin: cellular targets, mechanisms of
action, and selectivity for thin sensory neurons. Pharmacol
Review, 43 (1991) 143-201.
76.
Cotton P. Compliance problems, placebo effect cloud trials of topical analg. JAMA 1990;264:13-14.
77. Tyring S, Barbarsh RA, et al, Famciclovir for the treatment of acute herpes zoster:
effects on acute disease and post-herpetic neuralgia. Arch. Inern.
Med. 123:89-96, 1995.
78.
Mao J, Price DD, Hayes RL, et al, Intrathecal
treatment with dextrorphan or ketamine
potently reduces pain related behaviors in a rat model of mononeuropathy.
Brain 5:164-168, 1993.
79.
Dickenson AH, NMDA receptor antagonists as analgesics. In Progress in Pain
Research and Management, vol. 1, Fields, HL, Liebeskind,
JC (ed.), IASP Press,
80.
Takahashi H,
81. Malcangio M,
82. Wegert S, Ossipov MH, Nichols ML,
et al. Differential activities of intrathecal MK-801
or morphine to alter responses to thermal and mechanical stimuli in normal or
nerve-injured rats. Pain 71 (1997) 56-64.
83. Kohrenhuber J, Quack G, Danysz W,
Jellinger K, Danielczyk W, Gsell W and Riederer P.
Therapeutic brain concentration of the NMDA antagonist Amantadine,
Neuropharmacology, 34 (1995) 713-721.
84.
Eisenberg E, Pud D. Can patients with chronic neuropathic
pain be cured by acute administration of the NMDA receptor antagonist amantadine? Pain 74 (1998) 337-339.
85. Pud D, Eisenberg E, Spitzer A, et al. The NMDA receptor
antagonist amantadine reduces surgical neuropathic
pain in cancer patients: a double blind, randomized, placebo controlled trial.
Pain 75 (1998) 349-354.
86. Choe H, Kim JS, Ko
SH, Kim DC, Han YJ, Song HS. Epidural verapamil
reduces analgesic consumption after lower abdominal surgery. Anesth Analg 1998;86:786-90.
87.
Stein C. Opioid treatment of Chronic Non-malignant
Pain. Anesth. Analg. 84:912-914, 1997.
88.
Benedetti F, Vighetti S, Amanzio
M, et al. Dose-response relationship of opioids in nociceptive and neuropathic postoperative pain. Pain 74
(1998) 205-211.
89. Jadad AR, Carroll D, Glynn CJ, Moore RA and McQuay, HJ. Morphine responsiveness of chronic pain: double
blind randomised crossover study with
patient-controlled analgesia. Lancet, 339 (1992) 1367-1371.
90. Portenoy RK and Foley KM. Chronic use of opioid analgesics in non-malignant pain: report of 38
cases. Pain 25 (1986) 171-186.
91. Portenoy RK, Foley KM and
Inturrisi CE. The nature of opioid responsiveness and its
implications for neuropathic pain: new hypotheses derived from studies of opioid infusions. Pain 43 (1990) 273-286.
92. Dellemijn P, Vanneste J. Randomised double-blind active-placebo-controlled crossover
trial of intravenous fentanyl in neuropathic pain. Lancet 1997; 349: 753-758.
93.
Shibata M, Wakisaka S, Inoue T, et al. The effect of electroconvulsive treatment on thermal hyperalgesia and mechanical allodynia
in a rat model of peripheral neuropathy. Anesth
Analg 1998;86:584-587.
94.
Brewer K, Yezierski RP. Effects of
adrenal medullary transplants on pain-related
behaviors following excitotoxic spinal cord injury.
Brain Research 798, 1998, pp 83-92.
95. Decosterd I, Buchser E, Gilliard N, Saydoff J, Zurn AD, Aebischer P. Intrathecal implants of bovine chromaffin
cells alleviate mechanical allodynia
in a rat model of neuropathic pain. Pain 76 (1998) 159-166.
96.
Yu W, Hao JX, Saydoff J, Haegeeerstrand A. Long term alleviation of allodynia-like behaviors by intrathecal
implantation of bovine chromaffin cells in rats with
spinal cord injury. Pain 74 (1998) 115-122.
97.
Wong CS, Cherng CH, Tung
CS. Intrathecal administration of excitatory amino
acid receptor antagonists or nitric oxide synthase
inhibitor reduced autotomy behavior in rats. Anesth Analg 1998;87:605-608.
98. Lavand'homme P, Pan HL,
99. Ertas M, Sagduyu A, Arac N, Uludag B, Ertekin C. Use of levodopa to
relieve pain from painful symmetrical diabetic polyneuropathy.
Pain 75 (1998) 257-259.
100.
Cui JG, O'Connor WT, Ungerstedt U, Linderoth B, Meyerson BA. Spinal
cord stimulation attenuates augmented dorsal horn release of excitatory amino
acids in mononeuropathy via a GABAergic
mechanism. Pain 73 (1997) 87-95.
101. Sindrup SH, Gram LF, Brosen K, Eshoj O, Mogensen EF. The
selective serotonin reuptake inhibitor paroxetine is
effective in the treatment of diabetic neuropathy symptoms. Pain 42 (1990) 135
- 144.
102. Rowbotham M, Harden N, Stacey B, Bernstein P, Magnus-Miller
L. Gabapentin for the Treatment of Postherpetic Neuralgia. JAMA 280 (1998) 1837 - 1842.
103. Backonja M, Beydoun A, Edwards
KR, et al. Gabapentin for the Symptomatic Treatment
of Painful Neuropathy in Patients with Diabetes Mellitus. JAMA 280 (1998) 1831
- 1836.
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