A number of scoring systems have been proposed to quantify clinically neurological deficits and hence, define the presence and severity of neuropathy. This approach was originally pioneered by Dyck et al. (15) in the Mayo Clinic who described the neuropathy disability score (Mayo NDS). A comprehensive evaluation of muscular strength in the face, torso and extremities, reflexes of the upper and lower extremities and sensation to pain, vibration, and joint position at the index finger and great toe scored on a scale of
Modified Neuropathy Disability Score
Neuropathy disability score Right Left
128-Hz tuning fork; apex of big toe: Normal = 0
normal = can distinguish vibrating/not Abnormal = 1
Temperature perception on dorsum of the foot Use tuning fork with beaker of ice/warm water
Apply pin proximal to big toe nail just enough to deform the skin; trial pair = sharp, blunt; normal = can distinguish sharp/not sharp
Achilles reflex Present = 0
Present with reinforcement = 1 Absent = 2 NDS Total out of 10
0-4 produces an accurate and reproducible measure of the severity of diabetic neuropathy (16). However, because it should be performed by well-trained neurologist who can accurately evaluate muscle strength and grade the severity of sensory deficits, it renders it a useful research tool but limits its role in daily clinical practice. A modified NDS first described by Young et al. (17) can be performed by a nonspecialist and provides a sum of the sensory and reflex deficits totalling 28. The sensory score is derived from an evaluation of pain (pin prick), touch (cotton wool), cold (tuning fork immersed in icy water), and vibration (128 Hz tuning fork), graded according to the anatomical level at which sensation is impaired (no abnormality , base of toes , midfoot , ankle , mid-leg , knee ). The average of both feet for each modality is calculated and the sum of all four deficits represents the sensory score. The reflex score is derived from the knee and ankle reflexes (normal 0, elicited with reinforcement 1 and absent 2). A score from 1 to 5 represents mild, 6-16 moderate, and 17-28 severe neuropathy. A furthermore simplification of the NDS is provided by a tool which takes only a minute or so to complete and ranges from zero (normal) to 10 (maximum deficit score) indicating a complete loss of sensation to all sensory modalities and absent reflexes (18) (Table 2). Of direct clinical relevance a NDS score of more than 6/10 predicts the risk of foot ulceration better than the monofilament and was found to be second only to past or present history of ulceration (19). Alternative methods to diagnose and stage diabetic neuropathy on an out-patient basis include the Michigan Neuropathy Screening Instrument, which consists of 15 "yes or no" questions for symptoms related to sensation, general asthenia, and peripheral vascular disease in addition to inspection of the foot, assessment of vibration sensation, and ankle reflexes (20). Those with an abnormal Michigan Neuropathy Screening Instrument score undergo a more detailed evaluation, the Michigan Diabetic Neuropathy Score, which involves assessment of vibration perception thresholds, pain,
Toronto Clinical Neuropathy Scoring System
Sensory test scores
Knee reflexes Ankle reflexes
Pinprick Temperature Light touch
Symptom scores: present, 1; absent, 0. Reflex scores: absent, 2; reduced, 1, normal, 0. Sensory test score: abnormal, 1; normal, 0. Total scores range from normal 0 to Maximum of 19.
light touch, 10 g monofilament, and nerve electrophysiology that are scored and graded into normal, mild, moderate, or severe neuropathy. More recently the Toronto clinical scoring system (Table 3) has been validated against neurophysiological and pathological deficits obtained on sural nerve biopsy (21). It is weighted to emphasize sensory symptoms and deficits as opposed to motor deficits, which is a criticism of the original NDS (15). Thus, patients are questioned as to the presence or absence and characteristics (burning, stabbing, or shock-like) of neuropathic pain, numbness, tingling, and weakness in the feet; the presence or absence of similar upper-limb symptoms; and the presence or absence of unsteadiness on ambulation. Sensory testing is performed on the first toe and rated as normal or abnormal while knee and ankle reflexes are graded as normal, reduced, or absent.
The Semmes-Weinstein monofilament, graduated Rydel-Seiffer tuning fork, tactile circumferential discriminator, and Neuropen (Fig. 1) can detect those at risk of ulceration (18). However, their ability to detect mild neuropathy and minimal change is limited and therefore, they should not be used in clinical trials to determine treatment efficacy.
Formal quantitative sensory testing (QST), where the intensity and characteristics of the stimuli are well-controlled, and where the detection threshold is determined in parametric units that can be compared with established "normal" values is essential for accurate quantification of neuropathy. It allows:
1. Serial standardized evaluations at multiple body sites;
2. Accurate control of stimulus characteristics in a wide dynamic range;
3. Assessment of multiple sensory modalities; and
4. Comparison of individual test results with normative databases, and is noninvasive.
The main disadvantages are: (1) lack of objectivity and (2) the examinee's response, which depends on their cooperation and concentration as well as expectations (18). QST measures of vibration using the Biothesiometer or Neurothesiometer
(Fig. 2), thermal and pain thresholds, have proven valuable to identify diabetic patients with subclinical neuropathy (18), track progression (22), and predict those "at risk" for foot ulceration (23). Thus, a consensus subcommittee of the American Academy of Neurology have stated that "QST testing for vibratory and cooling thresholds receives a Class II rating as a diagnostic test. Further, QST is designated as safe, effective, and established, with a type B strength of recommendation. Thus, QST is accepted and has been used as a primary end point in several recent clinical trials of diabetic neuropathy (25,26); however, QST is unacceptable as the sole criteria to define diabetic neuropathy" (24).
Attributes of nerve conduction are reliable, reproducible, and form objective primary outcome measures in trials evaluating pharmaceutical treatment of diabetic peripheral neuropathy. However, they must be performed in triplicate samples and by trained individuals, as a recent study has demonstrated a sixfold difference in the ability to detect polyneuropathy (11.9% by neurologists to 2.4% by podiatrists) (27). Furthermore, maximal nerve conduction velocity (NCV) only reflects a limited aspect of neural activity of a small subset of large diameter and heavily myelinated axons and is insensitive to early functional alterations such as a reduction in Na+/K+ ATPase activity (28). Despite these obvious limitations multiple consensus panels have recommended the inclusion of whole nerve electrophysiology (e.g., NCV, F-waves, sensory,
and/or motor amplitudes) as surrogate measures in multicentre clinical trials of human diabetic neuropathy (29).
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