Prevalence of Ulnar Neuropathy in Patients Receiving Hemodialysis

ORIGINAL CONTRIBUTION Prevalence of Ulnar Neuropathy in Patients Receiving Hemodialysis

Rachel Nardin, MD; Kristine M. Chapman, MD; Elizabeth M. Raynor, MD

Background: Ulnar neuropathy can cause pain, weak- Results: Clinically evident, electrophysiologically con- ness, and sensory changes in the hand and can result in firmed ulnar neuropathy was present in 37 (51%) of the functional impairment. Patients with end-stage renal dis- 73 subjects with both screening and nerve conduction ease receiving hemodialysis may be predisposed to ul- study data available. The true prevalence of ulnar neu- nar neuropathy by factors such as arm positioning dur- ropathy in this cohort was estimated between 41% ing hemodialysis, underlying polyneuropathy, and upper and 60%. extremity vascular access. Conclusions: There is a high prevalence of ulnar neu- Objective: To determine the prevalence of clinically evi- ropathy in patients with end-stage renal disease receiving dent ulnar neuropathy in a cohort of 102 patients with end-stage renal disease receiving hemodialysis. hemodialysis, which has not been previously recognized. The high prevalence of ulnar neuropathy in this popula- Design: All eligible patients in a single dialysis unit were tion suggests that preventative efforts are indicated to pre- screenedforsymptomsandsignsofulnarneuropathy.Those vent this functionally limiting complication. with at least 1 symptom or sign underwent nerve conduction studies to confirm the presence of ulnar neuropathy. Arch Neurol. 2005;62:271-275

LNAR NEUROPATHY CAUSES weakness and sensory changes in the hand and pain in the elbow and distal arm. Untreated ulnar neuropathyU can lead to an ulnar “claw hand” with functional impairment. The ulnar nerve is prone to injury at the elbow, where it is subject to mechanical stretch and compression owing to its location in the ulnar groove. Risk factors for ulnar neuropathy include repetitive flexion of the elbow and sustained external pressure on Figure 1. Typical patient position during dialysis; the the ulnar groove. Individuals with poly- ulnar nerve is vulnerable to compression against the neuropathy appear more likely to de- armrest. velop secondary compressive mononeu- ropathies.1 in the arm. The hemodynamic effects of Patients with end-stage renal disease vascular access or the repeated inflation (ESRD) receiving hemodialysis may be at of a blood pressure cuff during hemodi- increased risk for ulnar neuropathy. They alysis may lead to ischemia of peripheral often have underlying polyneuropathy nerves, increasing their vulnerability to from uremia2,3 or diabetes.1 Patients re- compression.4-7 Lastly, tumoral calcino- Author Affiliations: ceiving hemodialysis spend many hours sis,8 amyloid deposition,9,10 and expanded Department of Neurology, Beth sitting in a dialysis chair with the fore- extracellular fluid volume11 may also affect Israel Deaconess Medical arm typically pronated so that the cubital peripheral nerves in this population. Center, Boston, Mass (Drs Nardin and Raynor); and tunnel is in contact with the flat surface Estimates of the prevalence or inci- Division of Neurology, of the arm rest; this may lead to compres- dence of ulnar neuropathy in the hemo- University of British Columbia, sion of the ulnar nerve (Figure 1). Many dialysis population range from 1% to 19%, Vancouver, British Columbia patients receive hemodialysis through an with the higher figures including asymp- (Dr Chapman). arteriovenous fistula or a synthetic graft tomatic subjects.11,12 Based on our expe-

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 Table 1. Electrophysiologic Criteria Total Hemodialysis Unit Population (N = 102) Ulnar Neuropathy—Any of the Following: 1. Ն10-m/s drop in ulnar MCV across the elbow 2. Ulnar MCV across the elbow Ͻ45 m/s (with a normal median MCV) Not Eligible (n = 12) Screening Interview and Examination (n = 90) 3. Ulnar SNAP Յ12 uV (with a normal median or radial SNAP) 4. Ulnar CMAP Ͻ5 mV (with a normal median CMAP) A. Mild to moderate: ulnar CMAP Ͼ3mV Յ Ͻ Signs or Symptoms No Signs or Symptoms B. Moderate to severe: ulnar CMAP 3mVor ulnar SNAP 5uV of Ulnar Neuropathy (n = 62) of Ulnar Neuropathy (n = 28) with a radial SNAP Ն12 uV Median Neuropathy at the Wrist—Any of the Following: 1. Median DML absent or prolonged in relation to ulnar DML by Ն Complete Incomplete Refused 1.5 ms NCS (n = 45) Data (n = 1) Consent (n = 16) 2. Median DML prolonged in relation to ulnar DML by Ն1msona lumbrical/interosseous study 3. Median SNAP absent (if no polyneuropathy) or prolonged in Figure 2. Study flow diagram. NCS indicates nerve conduction study. relation to ulnar SNAP by Ն1ms A. Mild to moderate: median CMAP Ն 2.5 mV B. Moderate to severe: median CMAP Ͻ2.5 mV or median SNAP ELECTROPHYSIOLOGIC STUDIES Ͻ5 uV with radial SNAP Ն12 uV Polyneuropathy: Board-certified electromyographers performed all NCSs using Radial SNAP amplitude Ͻ12 uV and ulnar + median MCV Ͻ48 m/s a Synergy electromyograph (Oxford Instruments, New York, A. Mild to moderate: best radial SNAP 4.1-12 uV NY). We studied only subjects’ arms with symptoms or signs. B. Moderate to severe: best radial SNAP Յ4uV We performed the following studies: antidromic sensory NCS of the ulnar nerve (recording digit V), the median nerve (re- Abbreviations: CMAP, compound muscle action potential; DML, distal cording digit II), and the superficial radial nerve (recording at motor latency; MCV, motor conduction velocity; SNAP, sensory nerve action the snuff box); and motor NCS of the median nerve (record- potential. ing abductor pollicis brevis) and the ulnar nerve (recording abductor digiti minimi), performed with the elbow in 70° to 90° of flexion. The electromyographer performed a second lumbrical- rience, we hypothesized that the prevalence of ulnar neu- first palmar interosseous comparative study if needed to clarify ropathy in patients receiving hemodialysis is greater than the presence of a median or ulnar nerve lesion at the wrist. previously recognized. Chronic ulnar nerve compres- Table 1 summarizes the electrophysiologic criteria used sion may not cause pain or tingling and thus may be over- to define ulnar neuropathy, median neuropathy, and polyneu- looked until weakness is profound, particularly in pa- ropathy. The criteria we used were stricter than the standard diagnostic criteria used in the BIDMC Electromyography Labo- tients with multiple medical problems. The identification ratory to minimize false-positive diagnoses. of hemodialysis as a risk factor for ulnar neuropathy would have clinical implications because this functionally lim- STATISTICAL ANALYSIS iting complication is potentially preventable. We under- took to determine the prevalence of clinically evident ul- Comparisons of demographic variables between subjects with nar neuropathy in a cohort of patients receiving and without ulnar neuropathy were made using unpaired t tests. hemodialysis. Analysis of the relationship between ulnar neuropathy and subject risk factors used the ␹2 test of significance. All analyses were performed using StatView statistical software (SAS Institute, METHODS Cary, NC).

SUBJECTS RESULTS We studied all patients receiving hemodialysis at Gambro Healthcare in Brookline, Mass, during a 3-week period in SUBJECTS March 2003. We screened all patients for eligibility and in- cluded those older than 18 years receiving hemodialysis for at During the study period, 102 patients received hemodi- least 3 months, who were medically stable and able to give in- alysis at Gambro Healthcare. Figure 2 illustrates the flow formed consent. The Beth Israel Deaconess Medical Center through the study of these individuals. Twelve patients (BIDMC) Committee on Clinical Investigation approved this did not meet inclusion criteria. We screened the remain- protocol, and we obtained written informed consent from all ing 90 subjects for symptoms or signs of ulnar neuropa- subjects. thy. Table 2 summarizes the clinical characteristics of We screened each eligible subject for symptoms or signs sug- this cohort. gestive of ulnar neuropathy. Symptoms of ulnar neuropathy were defined as (1) numbness or tingling in the fifth finger, (2) subjective hand weakness, or (3) pain in the elbow, medial fore- ELECTROPHYSIOLOGIC FINDINGS arm or hand, or fifth digit. We looked for signs of ulnar neuropathy, defined as (1) atrophy of the first dorsal interosseous Of the 90 subjects, 62 (69%) had at least 1 symptom or muscle, (2) weakness of the finger spreaders, or (3) reduced sign suggestive of ulnar neuropathy in 1 or both arms perception of pinprick over the fifth finger compared with the and were thus eligible for NCSs. Complete NCS data were index finger. All subjects with at least 1 symptom or sign were available for 45 (72%) of these 62 subjects. The NCS re- eligible to proceed with nerve conduction studies (NCSs). sults confirmed the suspected ulnar neuropathy in 37

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Subjects With Subjects Without All Eligible Subjects Ulnar Neuropathy Ulnar Neuropathy Characteristic (n = 90) (n = 37) (n = 36) Age, mean (range), y 61.2 (25-96) 63.4 (39-88) 54.8 (25-96) Male 39 (43) 16 (43) 17 (47) Female 51 (57) 21 (57) 19 (53) Duration of hemodialysis treatment, 53.9/42 (3-240) 39.9/30 (4-120) 62.8/54 (3-240) mean/median (range), mo Known polyneuropathy 23 (26) 9 (24) 9 (25) Diabetes 48 (53) 22 (59) 15 (41) Duration of diabetes, mean (range), y 22 (2-50) 22.3 (2-50) 16.5 (2-47) Current vascular access Arteriovenous fistula 35 (39) 9 (24): 12 arms 19 (53): 42 arms (9 ipsilateral; 3 contralateral) (18 ipsilateral; 24 contralateral) Arteriovenous graft 24 (27) 16 (51): 22 arms 3 (8): 16 arms (11 ipsilateral; 11 contralateral) (8 ipsilateral; 8 contralateral) Central access 31 (34) 12 (32): 18 arms 14 (39): 36 arms BMI, mean (range) NA 27.3 (16.7-59.6) 25.0 (16.8-34.5)

Abbreviation: BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters); NA, data not available for enough of the subjects to report. *Data are given as number (percentage) unless otherwise specified.

Table 3. Electrophysiologic Findings in the 52 Subjects’ Arms Meeting Criteria for Ulnar Neuropathy*

Total Met Criterion 1 Met Criterion 2 Met Criterion 3 Met Criterion 4 Had Coexistent PN 1 Criterion met 29 13 2 6 8 21 Ͼ1 Criterion met 23 22 11 13 7 5

Abbreviation: PN, polyneuropathy. *Data are given as number of arms. Criterion 1 indicates Ն10 m/s drop in ulnar motor conduction velocity (MCV) across the elbow; criterion 2, ulnar MCV across the elbow Ͻ45 m/s (with a normal median MCV); criterion 3, ulnar SNAP Յ12 uV (with a normal median or radial SNAP); criterion 4, ulnar CMAP Ͻ5mV (with a normal median CMAP).

(82%) of these 45 subjects and in 52 (72%) of the 72 sub- erate ulnar neuropathies, 28 (72%) were localized to the jects’ arms studied. Twenty-two subjects had unilateral elbow compared with 7 (54%) of the moderate to severe and 15 had bilateral ulnar neuropathy. ulnar neuropathies. Table 3 summarizes the electrophysiologic findings Of the 45 subjects who underwent NCSs, 24 (53%) in the 52 arms diagnosed as having ulnar neuropathy. had evidence for a median neuropathy at the wrist (6 Twenty-three met more than 1 criterion for ulnar neu- [25%] of which were severe); 19 (42%) had concomi- ropathy. In the remaining 29, a single criterion was met, tant ulnar and median neuropathies; 20 (44%) had evi- most often criterion 1 (focal slowing of motor conduc- dence for polyneuropathy affecting the upper extremi- tion velocity [MCV] across the elbow). In 25 of these 29 ties, which was mild to moderate in 16 subjects and severe arms, additional abnormalities involving the ulnar nerve in 4; and 17 (45%) of the subjects with an ulnar neu- were present, which did not meet established criteria; this ropathy also had polyneuropathy. One patient had an is- was most often owing to the coexistent presence of poly- chemic monomelic neuropathy. neuropathy. In 19 of these 25 arms, the ulnar sensory amplitude was low, but criterion 3 was not met because the CLINICAL FINDINGS median and radial sensory amplitudes were also abnor- mal. In 3 additional arms, ulnar MCV across the elbow was Of subjects with an electrophysiologically confirmed ul- abnormally slow, but criterion 2 was not met because the nar neuropathy, 26 (71%) had signs of ulnar neuropa- median MCV was slow as well. This left 4 arms in which thy and 23 (62%) had symptoms. Figure 3 illustrates there was no second, confirmatory abnormality for ulnar the distribution of symptoms and signs in arms with ul- neuropathy; 1 had only slowing of MCV across the el- nar neuropathy. Objective weakness of finger spreaders bow, and the rest had only low ulnar sensory amplitudes. was the most common symptom or sign and was pres- Ulnar neuropathy was mild to moderate in 39 (75%) ent in a higher proportion of arms with moderate to se- of the affected arms and moderate to severe in 13 (25%). vere ulnar neuropathy (12 [92%]) than with mild to mod- The ulnar neuropathy was localized at the elbow in 34 erate ulnar neuropathy (29 [74%]). (65%) and was nonlocalized in 17 (33%). One subject In 8 of the 45 subjects with symptoms or signs of ul- had a lesion at both the elbow and forearm. No subject nar neuropathy for whom electrophysiologic data were had an ulnar neuropathy at the wrist. Of the mild to mod- available, NCSs did not confirm ulnar neuropathy. Of

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 evidence of both ulnar and median neuropathies, 15 (80%) 100 were diabetic; this combination was more likely in dia- ␹2 90 betic than in nondiabetic subjects ( , P=.007). 83 There was no significant association between any cur- 80 rent or prior vascular access in the affected arm and an ulnar neuropathy (␹2, P=.88). When grafts and fistulas 70 were examined separately in the 146 arms screened for ulnar neuropathy, there was a significant association be- 60 52 tween an ulnar neuropathy and an ipsilateral function- 2 50 48 ing graft (␹ , P=.03) but not an ipsilateral functioning 44 fistula (␹2, P=.85).

Subjects’ Arms, % 40

30 29 COMMENT

19 20 Our results confirm that there is a high prevalence of ul- 10 nar neuropathy in patients with ESRD and receiving hemodialysis. Thirty-seven subjects (51%) met both clini- 0 Weakness Atrophy Reduced Numbness Hand Pain in the cal and electrophysiologic criteria for ulnar neuropathy, of Finger of Dorsal Pinprick or Tingling Weakness Elbow, with the true prevalence of clinically evident ulnar neu- Spreaders Interossei Sensation in Digit V Medial Hand, in Digit V or Digit V ropathy in this cohort estimated between 41% and 60%. Our decision to diagnose ulnar neuropathy based on Physical Examination Findings Subjective Symptoms a single ulnar NCS abnormality raises the possibility of Figure 3. Distribution of signs and symptoms in the 72 subjects’ arms with overdiagnosis. However, we believe that the false- electrophysiologically confirmed ulnar neuropathy. positive rate was low for the following reasons: (1) most arms (15/29) diagnosed as having ulnar neuropathy by a single criterion showed slowing of ulnar MCV across these subjects, 1 had a median neuropathy and 2 had both the elbow (ie, criterion 1 or 2; this is an accepted diag- median neuropathy and polyneuropathy. The remain- nostic criterion with specificity reported at Ն95%)13 and ing 5 subjects had normal NCS results. (2) all but 3 of the 14 arms which met only criterion 3 or 4 (ie, low ulnar sensory or motor amplitudes) had a PREVALENCE OF ULNAR NEUROPATHY second, internally consistent abnormality in the ulnar nerve that did not meet criteria, usually owing to the pres- Of the 90 eligible patients in this cohort, 73 were both ence of coexistent polyneuropathy. screened for ulnar neuropathy and had confirmatory NCS This study suggests that the prevalence of ulnar neu- data available. Clinically evident, electrophysiologically ropathy in patients receiving hemodialysis is higher than confirmed ulnar neuropathy was present in 37 subjects previously recognized. Prior studies of prevalence were (51%). Because 17 patients with signs or symptoms of retrospective reviews of only cases that came to medical ulnar neuropathy refused NCSs or had incomplete data, attention or reports of ulnar neuropathies found inci- we cannot calculate the true prevalence of clinically evi- dentally in studies of carpal tunnel syndrome. To our dent ulnar neuropathy in this cohort. We estimate, how- knowledge, this is the first study to screen an entire co- ever, that the true prevalence of ulnar neuropathy in this hort of patients specifically for ulnar neuropathy. population lies between 41% and 60% (assuming first that The factors responsible for the high incidence of ulnar all 17 subjects did not have an electrophysiologically con- neuropathy in this population are unknown. Male sex and firmed ulnar neuropathy and then that all did). high or low body mass index, which are risk factors in other populations, were not risk factors.14,15 In contrast to prior RISK FACTORS FOR ULNAR NEUROPATHY findings, diabetes was not an independent risk factor, nor was it clearly associated with more severe ulnar neuropa- There were no statistically significant differences in demo- thies.16 Amyloidosis, tumoral calcinosis, and edema could graphic variables between patients with and without ul- have played a role in individual subjects; we did not as- nar neuropathy except for the duration of dialysis. Sub- sess for these potential risk factors. jects without ulnar neuropathy were receiving dialysis The correlation between an ulnar neuropathy and an significantly longer than those with ulnar neuropathy ipsilateral graft, as opposed to an ipsilateral fistula or cen- (mean of 62.8 months vs 39.9 months; unpaired t test, tral venous access, suggests that nerve ischemia may be a P=.01). Of all subjects, 48 (53%) had diabetes, with a contributing factor. The hemodynamics of grafts differs from mean duration of 22 years. However, subjects with dia- that of fistulas because blood flow through a graft is more betes were no more likely to have an ulnar neuropathy likely to ultimately decline.17 In addition, grafts are usu- than those without (␹2, P=.20), nor was the duration of ally reserved for subjects whose native blood vessels are in- diabetes significantly longer in those with ulnar neu- adequate for a fistula or who have failed fistula placement, ropathy (unpaired t test, P=.15). There was no signifi- in whom the potential for nerve ischemia may be higher. cant correlation between diabetes and the severity of ul- The localization of most ulnar nerve lesions to the el- nar neuropathy. Of the cases with electrophysiologic bow supports the hypothesis that external compression

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 at the ulnar groove plays a role because the nerve is most is some evidence that they have reduced its incidence.14 superficial and vulnerable to compression there. An un- The improved survival of hemodialysis patients and the expected finding, however, was the longer duration of shortage of kidney transplants for the growing ESRD dialysis in subjects without ulnar neuropathy. Patient po- population has increased the length of time spent receiv- sition, degree of arm flexion, or the degree of uremia may ing hemodialysis, making the recognition and preven- affect the development of ulnar neuropathy more than tion of functionally limiting complications such as ul- duration of dialysis; we did not specifically analyze these nar neuropathy increasingly important. Greater awareness factors in this study. of the high prevalence of ulnar neuropathy in patients Almost half the subjects studied electrophysiologi- receiving hemodialysis should lead to changes in dialy- cally met our criteria for a generalized polyneuropathy sis delivery and more vigilant screening for this compli- affecting the upper limbs. We did not study lower limbs, cation. These measures should reduce the incidence of and therefore this is probably an underestimate of the ulnar neuropathy in this population. prevalence of polyneuropathy in this population. We did not assess for polyneuropathy in subjects without symp- Accepted for Publication: May 6, 2004. toms or signs of ulnar neuropathy, but the presence and/or Correspondence: Rachel Nardin, MD, Beth Israel Dea- severity of polyneuropathy may be a risk factor for ul- coness Medical Center, 330 Brookline Ave, Boston, MA nar neuropathy in this population as well. 02215 ([email protected]). A median neuropathy was present in 33 (46%) of arms Author Contributions: Study concept: Raynor. Study ini- studied. Because signs and symptoms of median neuropa- tiation and protocol design: Nardin and Raynor. Acquisi- thy were not screening criteria for electrophysiologic test- tion of data: Nardin, Chapman, and Raynor. Analysis of ing, this does not represent the true prevalence of me- data and drafting the manuscript: Nardin and Chapman. dian neuropathy in this population. Nonetheless, the many Interpretation of results and revision of the manuscript: Nar- concomitant ulnar and median neuropathies (19 sub- din, Chapman, and Raynor. jects [42%]) supports an underlying vulnerability of the peripheral nerves in this population to compression. This finding confirms that of Delmez et al,11 who found both REFERENCES ulnar and median nerve involvement in 31% of patients receiving chronic hemodialysis. 1. Mulder DW, Lambert EH, Bastron JA, Sprague RG. 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