|Year : 2016 | Volume
| Issue : 3 | Page : 85-94
Foot neuropathy in rheumatoid arthritis patients: clinical, electrophysiological, and ultrasound studies
Abd El-Samad I El-Hewala1, Samar G Soliman2, Alaa A Labeeb2, Ashraf A Zytoon3, Amira T El-Shanawany MSc 2
1 Department of Rheumatology, Physical Medicine, and Rehabilitation, Faculty of Medicine, Zagazig University, Egypt
2 Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Menoufia University, Egypt
3 Department of Radiology, Faculty of Medicine, Menoufia University, Egypt
|Date of Submission||10-Oct-2015|
|Date of Acceptance||12-Nov-2015|
|Date of Web Publication||7-Sep-2016|
Amira T El-Shanawany
Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Faculty of Medicine, Menoufia University
Source of Support: None, Conflict of Interest: None
Aim This study aimed to evaluate neuropathic foot pain in patients with rheumatoid arthritis (RA) using electrophysiological studies and musculoskeletal ultrasound (MSUS) to address the association between these findings and disease activity. Evaluation of the usefulness of this combination was undertaken.
Design The present study was designed as a cross-sectional study.
Patients and methods A total of 50 RA patients underwent a complete history-taking and rheumatologic examination. According to the cut-off point of Disease Activity Score in 28 joints, patients were divided into two equal groups (25 patients each): active and inactive. In total, 25 healthy individuals were included as controls. Routine tibial and peroneal nerve conduction studies, as well as electromyography of tibialis anterior and abductor hallucis muscles, were carried out. MSUS assessment of the ankle joint and extra-articular portion of the foot complex was also performed.
Results Electrophysiological findings of foot neuropathy were observed in 78% of the patients, irrespective of the disease activity level. In total, 48% of the patients had mononeuropathies of a demyelinating pattern (entrapment neuropathies), whereas the other 30% had symmetrical polyneuropathy with axonal degeneration. Combined distal tibial and peroneal nerve entrapments were reported in 16% of the patients. A positive power Doppler signal and joint erosions showed a highly statistical significant prevalence among the active group in comparison with patients in remission (P ≤ 0.001).
Conclusion Peripheral nerve affection is common in the rheumatoid foot, irrespective of the disease activity status. The most common neuropathies were posterior tarsal tunnel syndrome, peroneal nerve entrapment at the fibular neck, and pure sensory axonal neuropathy. A positive power Doppler signal and bone erosions of the ankle joint, detected by MSUS, were associated with RA disease activity. Electrophysiology was superior to MSUS for the diagnosis of posterior tarsal tunnel syndrome.
Keywords: musculoskeletal ultrasound, neuropathic pain, rheumatoid foot
|How to cite this article:|
El-Hewala ASI, Soliman SG, Labeeb AA, Zytoon AA, El-Shanawany AT. Foot neuropathy in rheumatoid arthritis patients: clinical, electrophysiological, and ultrasound studies. Egypt Rheumatol Rehabil 2016;43:85-94
|How to cite this URL:|
El-Hewala ASI, Soliman SG, Labeeb AA, Zytoon AA, El-Shanawany AT. Foot neuropathy in rheumatoid arthritis patients: clinical, electrophysiological, and ultrasound studies. Egypt Rheumatol Rehabil [serial online] 2016 [cited 2020 Apr 4];43:85-94. Available from: http://www.err.eg.net/text.asp?2016/43/3/85/189640
| Introduction|| |
Rheumatoid arthritis (RA) is a chronic systemic rheumatic inflammatory disorder predominantly affecting synovial joints. The inflammatory response within the joint synovium leads to joint erosion, ligament laxity, and subsequent deformity. In addition, extra-articular manifestations occur in 10–20% of patients, especially those with high titers of rheumatoid factor. Extra-articular pathology includes bursitis, tendonitis, fasciitis, neuritis, and vasculitis ,.
Clinical involvement of the peripheral nervous system may be asymptomatic in the early stages of the rheumatoid disease or may present with a wide variety of symptoms such as pain, paresthesias, and muscle weakness. These symptoms may mimic and overlap with those of arthritis . In presence of severe joint disease, restriction, pain, and deformities, symptoms of neuropathy may be overlooked or overestimated ,.
For persons with RA, the prevalence of foot pain has been reported in varying numbers within the published literature . Although patients with RA complain of foot pain and disability because of foot problems, physicians generally overlook or neglect the feet in routine clinical examination. This is because feet and ankles are not included as part of the Disease Activity Scoring in 28 joints (DAS28) scoring system, which is generally used to assess disease activity and helps to define clinical remission of the disease. Hence, patients in remission may suffer from foot disease activity, as shown in the previous studies .
Evaluation mainstays of the rheumatoid foot include both electrophysiological and imaging techniques . Musculoskeletal ultrasound (MSUS) is an attractive method of imaging because of its low cost, absence of harmful radiation, and rapidity of imaging. Compared with standard radiography, ultrasonography (US) is shown to be superior at detecting joint erosions early in the course of the disease. In addition, it can study tendon involvement, which often accompanies and in some cases precedes the evidence of the disease at the joint level ,.
This study aimed to evaluate neuropathic foot pain in patients with RA using electrophysiological studies and MSUS to address the association between these findings and disease activity. Electrophysiology was used to assess the peripheral electrophysiological changes in the rheumatoid feet, whereas MSUS was used to assess bone erosions and synovitis in these patients. Evaluation of the usefulness of this combination was undertaken.
| Patients and methods|| |
After the approval of the protocol from our ethical committee and after providing detailed information to the patients as regards the aim and procedures of the study, 50 patients with RA having neuropathic pain in their feet gave their consent and were then enrolled in this study. The patients were recruited from the Physical Medicine & Rehabilitation Clinic, Menoufia University Hospitals.
RA was diagnosed according the 2010 ACR/EULAR criteria for classification of RA . Characteristics of neuropathic pain described by the patients included in the study were burning; painful, cold sensations or electric shocks possibly associated with tingling, pins, and needles; numbness; or itching .
Patients were excluded if they had diabetes mellitus, L5 and S1 radiculopathies, space occupying lesions at the tarsal tunnel, foot trauma and fractures, congenital or post-traumatic foot deformity, varicose veins and deep venous thrombosis, severe obesity by BMI or lower limb edema. Moreover, patients with peripheral neuromyopathy or arthritis due to systemic or local disease ‘other than RA’ or drug-induced were not included in our study.
According to the cut-off point of the DAS28 , the patients were divided into two groups: group I (active RA) and group II (inactive RA). Group III constituted the healthy controls, 25 in number.
All the patients were subjected to a detailed history-taking. Assessment of foot function was carried out using the Swindon Foot and Ankle Questionnaire (SFAQ), which is a simply worded 10-point foot-and-ankle screening questionnaire with diagrams for rapid screening in routine rheumatology outpatients . Assessment of functional disability was performed using the Stanford Health Assessment Questionnaire Disability Index (HAQ-DI), which consists of eight questions regarding the limitations that the patients experience in performing daily physical activities .
Complete rheumatologic examination was carried out for every participant, including neurological examination of the four extremities with special emphasis on excluding upper motor neuron lesions or lesions affecting any part of the lower motor neuron pathway other than the peripheral nerves. Moreover, saphenous neuropathy, sciatic neuropathy and proximal affection of tibial, and common peroneal nerves were excluded.
In this study, the Medical Research Council grading scale (0–5) was used for muscle strength assessment ; muscle weakness was assumed to be present if any muscle in the lower limb has a score less than 5. Abnormal muscle mass index indicated muscle wasting . Eliciting Tinel’s sign was considered as an objective clinical sign for possible tibial or peroneal nerve entrapments ,. In addition, superficial sensations using a pinprick were examined and an altered pinprick response was used to infer a possible neuropathic pain .
All 50 patients along with the controls were tested by the Neuropack M1 electromyograph (EMG) apparatus (Nihon Kohden, Tokyo, Japan). Nerve conduction (motor and sensory) studies were conducted on bilateral medial plantar, lateral plantar, deep peroneal, superficial peroneal, and sural nerves. Needle EMG was also performed bilaterally on the tibialis anterior and abductor hallucis muscles. This was done as described in a study by Kim and colleagues ,,,,,,,. Findings were presented as the mean value of both sides.
It was proposed that abnormal sural and/or peroneal sensory responses along with any abnormalities in the plantar nerves were likely secondary to a polyneuropathy . Diagnosis of posterior tibial nerve entrapment at the ankle was based on measuring the distal motor latency and distal sensory latency of both medial and lateral plantar nerves as well as their compound muscle action potential and sensory nerve action potential amplitudes. Calculated cut-off points of the electrophysiological parameters were used. It was proposed that the affection of any parameter of the electrophysiological study reflects pathologic affection of the related nerve ,. Finally, diagnosis of peroneal nerve entrapment at the fibular neck was based on certain neurophysiological criteria:
- Demyelinating lesion,
- Compound muscle action potential axonal damage,
- Mixed involvement (conduction block plus axonal damage), and
- Sensory nerve action potential axonal loss ,,.
Musculoskeletal ultrasound testing
A commercially available real-time scanner (Hitachi Medical Systems, Tokyo, Japan) was used for the US examination using a multilinear high-frequency (10 MHz) linear array transducer. The patients underwent systematic multiplanar, bilateral and dynamic gray-scale US and Power Doppler ultrasound (PDUS) assessments of the ankle joint and the extra-articular portion of foot complex, as described by Riente et al. .
The ankle joint was evaluated in both transverse and longitudinal planes, regarding three criteria: synovitis, power Doppler (PD) signal, and erosions.
Joint synovitis, which was detected by gray-scale US, was defined as the presence of synovial hypertrophy and/or intra-articular effusion. Active synovitis was defined as intra-articular synovitis detected with PD signal . Intra-articular PD activity was evaluated using a semiquantitative four-grade scale of 0–3 ,. According to OMERACT guidelines, joint erosion was defined as intra-articular discontinuity of the bone surface, which was visible in two perpendicular planes . Erosions were recorded as either present or absent.
Diagnosis of tarsal tunnel syndrome (TTS) was based on detection of anatomically relevant changes of the tarsal tunnel, associated with RA, mainly signs of active inflammation affecting soft tissue within the tunnel: tenosynovitis/synovial hypertrophy with or without effusion, tendinitis, paratenonitis, as well as bursitis with effusion and/or synovial hypertrophy .
The current study faced multiple technical considerations for sonography of the posterior tibial and deep peroneal nerves at their tunnels as a 10 MHz probe was used, whereas superficially located nerves such as the median nerve, ulnar nerve, peroneal and tibial nerves should be examined with transducers of 15–18 MHz .
Statistical analyses were performed with SPSS 20 for Windows (SPSS Inc., Chicago, Illinois, USA). For continuous variables, Mann–Whitney U-test or independent-sample Student’s t-test was used for comparison between two groups. For comparison between three groups, one-way ANOVA test or Kruskal–Wallis test was used. For categorical variables, χ2-test was used. In addition, bivariate regression analysis (r-test) was performed to assess the independent association between the nerve conduction study (NCS)/EMG variables and disease activity in each patient group. A P-value of less than or equal to 0.05 was considered statistically significant and a P- value of less than or equal to 0.001 was considered highly statistically significant.
| Results|| |
Demographic and clinical characteristics
A total of 50 patients and 25 controls were enrolled in the present study. Demographic data are presented in [Table 1]. It shows that there was a significant prevalence of muscle weakness and wasting among patients in group I when compared with group II patients. An altered pinprick response, in the form of mechanical allodynia and/or hyperalgesia/hypoalgesia, showed no significant relationship between this deficit and disease activity (P > 0.05). It was found in 37 (74%) patients; 30 (60%) patients showed a bilateral deficit, whereas the other seven (14%) patients showed a unilateral deficit.
Finally, there was a highly significant prevalence of increased SFAQ and Stanford HAQ-DI scores (P = 0.001) among patients in group I when compared with group II patients [Table 1].
Nerve conduction studies and needle electromyography findings
[Table 2] compares NCSs parameters among the studied groups (groups I, II, and III), which revealed significant (P ≤ 0.05) to a highly significant (P ≤ 0.001) changes in the motor and sensory nerve studies regarding mean values of distal latency, amplitude, and conduction velocity in RA patients compared with healthy indivisuals.
[Table 3] displaying results of the needle EMG in the studied muscles reveals that the motor unit action potentials (MUAPs) showed a significant (P ≤ 0.05) to a highly significant (P ≤ 0.001) reduction in the duration and amplitude among the patients in comparison with the controls. It also shows a highly significant increased proportions of spontaneous activity recorded from abductor hallucis muscle in patients compared with controls (P ≤ 0.001). However, the intrinsic foot muscles commonly show increased insertional activity and occasionally fibrillation potentials associated with large, long-duration MUAPs, as one would expect in a neurogenic lesion. Such findings are not unusual in normal indivisuals without symptoms, however, and are thought to be due to everyday wear and tear of the feet .
[Table 4] of bivariate correlation analyses between the nerve study parameters or MUAP parameters on one side and DAS28 on the other side showed insignificant results (P > 0.05), except for the distal sensory latency and sensory nerve action amplitude of the medial plantar response, being significant in group II patients (P ≤ 0.05). However, this significant finding cannot be relied upon on the basis of the few obtainable plantar sensory responses, and thus being a marked limitation in this study.
|Table 4 Correlation coefficients (r) between Disease Activity Score in 28 joints and nerve conduction study/electromyographic results, in the patients' groups|
Click here to view
[Table 5] shows the prevalence of the electrophysiological patterns in the patient’s groups. Out of 50 patients, 39 (78%) had different types of peripheral neuropathy, 24 (48%) had mononeuropathies of demyelinating pattern (entrapment neuropathies), and 15 (30%) had symmetrical polyneuropathy with axonal degeneration.
|Table 5 Prevalence of the electrophysiological patterns and findings in the patients' groups (n = 50)|
Click here to view
[Figure 1] shows the prevalence of electrophysiological findings of peripheral neuropathy in the patients’ groups. The most common type of neuropathy which was observed was pure sensory axonal neuropathy (24% of the patients) followed by tibial nerve entrapment at posterior tarsal tunnel ‘posterior TTS’ (20% of the patients), combined entrapments of posterior tibial nerve at the ankle and peroneal nerve at fibular neck (16% of the patients), peroneal nerve entrapment at fibular neck (12% of the patients), and finally sensorimotor axonal neuropathy (6% of the patients). None of the studied cases showed deep peroneal nerve entrapment at the ankle, pure motor axonal neuropathy or mononeuritis multiplex.
|Figure 1: The prevalence of electrophysiological findings of peripheral neuropathy in the patients' groups (n = 50).|
Click here to view
[Table 6] shows that posterior tibial nerve entrapment at the ankle was reported in 18 (36%) patients; 10 (20%) patients showed an isolated tibial nerve affection and eight (16%) patients had an associated peroneal nerve entrapment at the fibular neck. It also reveals that peroneal nerve entrapment at the fibular neck was reported in 14 cases (28% of cases); six cases had an isolated peroneal nerve affection and eight cases had an associated posterior tibial nerve entrapment at the ankle.
|Table 6 Frequency of affection of the plantar and peroneal nerves in posterior tibial and peroneal entrapments in the patients' groups (n = 50)|
Click here to view
Musculoskeletal ultrasound findings
[Figure 2] and [Figure 3] show the results of PDUS and joint erosion assessment of the ankle joint, respectively. There was a highly statistically significant prevalence of positive ankle PD signal and joint erosions among group I patients in comparison with group II patients (P ≤ 0.001).
|Figure 2: Power Doppler findings in the patients' groups (n = 50). RA, rheumatoid arthritis|
Click here to view
|Figure 3: Joint erosions in the patients' groups (n = 50). RA, rheumatoid arthritis|
Click here to view
The comparison between electrophysiological and ultrasonograhic diagnoses of posterior tarsal tunnel syndrome
This comparison, as displayed in [Table 7], revealed statistically significant results (P < 0.05), according to which electrophysiology could detect the syndrome in 18 (36%) patients, whereas MSUS could detect the syndrome in only eight (16%) patients.
|Table 7 Comparison between electrophysiological and ultrasound diagnoses of posterior tarsal tunnel syndrome|
Click here to view
| Discussion|| |
The present study showed that females and males constituted 92 and 8%, respectively, in both the patients’ groups, whereas female to male ratio was 80 to 20%, respectively, in the control group. This emphasizes the higher prevalence of RA in females than in males, whereas the sex ratio is typically around 3 : 1 ,.
There was a significant prevalence of muscle weakness among the active RA group when compared with the inactive one (P ≤ 0.05). There was a significant positive association (P ≤ 0.05) between the disease activity score and isometric muscle strength, which was measured with the validated Muscle Strength Index ,. Muscle weakness is generally attributed to a reflex response to pain, joint deformation or disuse, extra-articular manifestations of the disease and/or psychological factors .
Similarly, there was a significant prevalence of muscle wasting among the active RA patients when compared with the inactive group (P ≤ 0.05). This confirms what other authors found that DAS28 score is negatively correlated with the lean body cell mass ,.
Mechanical allodynia and/or hyperalgesia/hypoalgesia were assumed to be pathognomonic of neuropathic pain . In our study, an altered pinprick response was found in 30 (60%) patients bilaterally and in seven (14%) patients unilaterally.
A highly significant SFAQ scoring (P ≤ 0.001) was encountered more among the active patients than among the inactive ones. This disagrees with the study conducted by Waller et al. , which reported that the SFAQ did not correlate with DAS28. However, a limitation of both studies, Waller’s research and the present study, is that feet and ankles are not included as part of the DAS28 scoring system.
Similarly, a highly significant HAQ-DI was encountered more among the active patients than among the inactive ones (P ≤ 0.001). Keeping-up with our results, previous studies found a significant correlation between HAQ-DI and DAS28 in RA patients ,,, suggesting that functional incapacity is most associated with disease activity in early RA .
NCSs parameters among the studied groups represented the preliminary changes of neuropathic lesions in RA patients, which were previously reported in the literature in the form of significant affection of nerve study parameters of the median, ulnar, peroneal, and posterior tibial nerves in RA patients compared with controls ,,.
Regarding the needle EMG findings in this study, the reduction of MUAP duration and amplitude, associated with polyphasia, is suggestive of a state of early reinnervation following severe denervation, or it may suggest a concomitant myopathy. Many ,, case–controlled studies that involved EMG examination of different muscles in RA patients had been conducted previously. The studied muscles showed neuropathic interference pattern, definite signs of neuropathy or definite signs of denervation .
In general, findings confirm the prevalence of neuropathy in RA. This was in agreement with the studies conducted by Olney , Kadhim et al. , and Agarwal et al. , which concluded that neuropathies are common in patients with diffuse connective tissue diseases.
Accordingly, the current study assumes that there is no relationship between rheumatoid neuropathy and disease activity status. In agreement with our results, previous research work stated that rheumatoid neuropathy occurs irrespective of the disease activity level ,,. High disease activity was not stated as a predictor of rheumatoid vasculitis . Moreover, entrapment neuropathies are associated with mechanical nerve compression as a result of local joint changes, including swelling of soft tissues, synovitis, tenosynovitis, bone erosions joint deformity or rheumatoid nodules ,,. Moreover, there is no correlation between compression neuropathies and the level of acute phase reactants .
The prevalence of rheumatoid neuropathy vary among previous studies ,,,,,. The electrophysiological findings of mild distal symmetric pure sensory and combined sensorimotor axonal neuropathies contribute to the clinical presentation of distal sensory neuropathy (DSN). This emphasizes the prevalence of DSN in RA patients. Rheumatoid diseases are one of the most common causes of DSN .
An important observation provided by the current study was the coexistence of posterior tibial nerve entrapment at the ankle and peroneal nerve entrapment at the fibular neck. According to our knowledge, no previous studies have addressed this issue.
In this study, the electrophysiological diagnosis of posterior TTS was encountered in 18 (36%) patients. Baylan’s study examined 48 RA patients for the presence of posterior TTS and found that 11 (25%) patients had a definite delay in the distal motor latency of the tibial nerve . Moreover, Ibrahim et al.  documented the electrodiagnosis of posterior TTS in 28 out of the 30 feet of RA patients.
The electrophysiological findings of peroneal nerve entrapment at the fibular neck may be due to the compression of the nerve by a ganglion, rheumatoid nodule, an extension of synovial hypertrophy from the knee or even a large knee osteophyte . Data about incidence and prevalence of peroneal neuropathy in rheumatoid knees are insufficient. An increased peroneal neuropathy at the fibular head has been reported in RA .
Lateral plantar nerve was found to be more affected than medial plantar nerve in the patients with TTS. It was previously stated that the lateral plantar nerve is probably affected earlier than the medial plantar one . In another study performed on RA patients, none of the patients showed isolated medial plantar nerve affection .
Similarly, none of the patients who were diagnosed with peroneal nerve entrapment at the fibular neck showed isolated superficial peroneal nerve lesion. It was reported that the superficial peroneal nerve is usually less involved than is the deep peroneal nerve . The most likely explanation was the selective vulnerability of different nerve fascicles to injury, which leads to differing degree of damage to individual fascicles within the common peroneal nerve .
A positive PD signal and joint erosions are considered to be associated with diseased activity on the basis of their prevalence in the active patients when compared with the inactive ones (P ≤ 0.001). Keeping-up with our results, a previous study displayed similar ankle PD findings . The microstructural bone changes associated with development of bone erosions in RA seem to be closely related to disease activity. Explanation for this finding was that disease activity is closely associated to presence of hypervascularity (PD changes), further contributing to the development of erosions and other forms of structural damage .
On comparing electrophysiological and US diagnoses of posterior TTS, electrophysiological studies were able to detect more cases of posterior TTS (P < 0.05). Electrophysiology could detect the syndrome in 18 (36%) patients, whereas MSUS could detect the syndrome only in eigth (16%) patients. Similar findings were reported by Ibrahim et al.  who investigated for posterior TTS in 30 rheumatoid feet. Electrophysiologically, they could detect 28 (93.3%) patients, whereas by MSUS only 10 (33.3%) patients could be detected. This supports the evidence that electrophysiology is the test of choice for confirming the diagnosis of posterior TTS in 90–100% of cases ,,,,,,.
| Conclusion|| |
Peripheral nerve affection is common in the rheumatoid foot, irrespective of the disease activity status. The most common neuropathies were posterior TTS, peroneal nerve entrapment at the fibular neck, and pure sensory axonal neuropathy. A positive PD signal and bone erosions of the ankle joint, detected by MSUS, were associated with RA disease activity. Electrophysiology was superior to MSUS for the diagnosis of posterior TTS.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Loveday DT, Jackson GE, Geary NPThe rheumatoid foot and ankle: current evidenceFoot Ankle Surg20121894102
Ibrahim I, Medani S, El-Hameed M, Imam M, Shaaban MTarsal tunnel syndrome in patients with rheumatoid arthritis, electrophysiological and ultrasound studyAlexandria J Med20134995104
Agarwal V, Singh R, Wiclaf Chauhan S, Tahlan A, Ahuja C et al.
A clinical, electrophysiological, and pathological study of neuropathy in rheumatoid arthritisClin Rheumatol200727841844
Biswas M, Ghosh S, Ghosh K, Chatterjee A, Dasgupta S, Ganguly PPrevalence, types, clinical associations, and determinants of peripheral neuropathy in rheumatoid patientsAnn Indian Acad Neurol201114194197
Kerry R, Holt G, Stockley IThe foot in chronic rheumatoid arthritis: a continuing problemFoot19944201203
Borman PFoot problems in a group of patients with rheumatoid arthritis: an unmet need for foot careOpen Rheumatol J20126290295
Wakefield R, Gibbon W, Conaghan P, O’Connor P, McGonagle D, Pease C et al.
The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: a comparison with conventional radiographyArthritis Rheum20004327622770
Aletaha D, Neogi T, Silman A, Funovits J, Felson D, Bingham C et al.
Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiativeArthritis Rheum20106225692581
Berker E, Dinçer NChronic pain and rehabilitationAgri2005171016
Fransen J, Creemers MCW, Van Riel PLCMRemission in rheumatoid arthritis: agreement of the disease activity score (DAS28) with the ARA preliminary remission criteriaRheumatol J20044312521255
Waller R, Manuel P, Williamson LThe Swindon foot and ankle questionnaire: is a picture worth a thousand words?ISRN Rheumatol 2012201218
Stanford Patient Education Research Center. Stanford HAQ 8-Item Disability Scale2015Last accessed on 2015 Sep 20Available athttp://patienteducation.stanford.edu/research/haq8.html
Barohn RJWyngaarden JB, Smith LHMuscle diseasesCecil text of medicine1982PhiladelphiaSaundersP2013P2043
Rocha OMD, Batista ADAP, Maestá N, Burini RC, Laurindo IMMSarcopenia in rheumatoid cachexia: definition, mechanisms, clinical consequences and potential therapiesRev Bras Reumatol200949288301
Montagna P, Liguori RThe motor Tinel sign: a useful sign in entrapment neuropathy?Muscle Nerve200023976978
Chung T, Yen J, Ou T, Liu H, Tsai WPrevalence of neuropathic pain in patients with rheumatoid arthritisFormosan J Rheumatol2009231924
Kim W, Kim H, Bluementhal F, Joynt RAntidromic sensory nerve conduction studies of medial and lateral plantar nerves in normalsElectromyogr Clin Neurophysiol199333289294
Buschbacher R, Prahlow NManual of nerve conduction studies2006New York, NYDemos
Preston D, Shapiro BPreston D, Shapiro BArtefacts and technical factorsElectromyography and neuromuscular disorders20133rd edPhiladelphiaElsevier7189
Preston D, Shapiro BPreston D, Shapiro BBasic nerve conduction studiesElectromyography and neuromuscular disorders20133rd edPhiladelphiaElsevier1935
Preston D, Shapiro BPreston D, Shapiro BRoutine lower extremity nerve conductionElectromyography and neuromuscular disorders20133rd edPhiladelphiaElsevier115124
Preston D, Shapiro BPreston D, Shapiro BTarsal tunnel syndromeElectromyography and neuromuscular disorders20133rd edPhiladelphiaElsevier365372
Preston D, Shapiro BPreston D, Shapiro BBasic overview of electromyographyElectromyography and neuromuscular disorders20133rd edPhiladelphiaElsevier125128
Preston D, Shapiro BPreston D, Shapiro BAnatomy for needle electromyographyElectromyography and neuromuscular disorders20133rd edPhiladelphiaElsevier174190
Kaplan P, Kernahan JTarsal tunnel syndrome: an electrodiagnostic and surgical correlationJ Bone Joint Surg1981639699
Aprile I, Tonali P, Caliandro P, Pazzaglia C, Foschini M, Di Stasio E et al.
Italian multicentre study of peroneal mononeuropathy: multiperspective follow-upNeurol Sci2009303744
Weiss LWeiss L, Silver J, Weiss JInjury to peripheral nervesEasy EMG20041st edEdinburghButterworth-Heinemann8186
Masakado Y, Kawakami M, Suzuki K, Abe L, Ota T, Kimura AClinical neurophysiology in the diagnosis of peroneal nerve palsyKeio J Med2008578489
Riente L, Delle Sedie A, Iagnocco A, Filippucci E, Meenagh G, Valesini G et al.
Ultrasound imaging for the rheumatologist V. ultrasonography of the ankle and footClin Exp Rheumatol200624493498
Naredo E, Collado P, Cruz A, Palop M, Cabero F, Richi P et al.
Longitudinal power Doppler ultrasonographic assessment of joint inflammatory activity in early rheumatoid arthritis: predictive value in disease activity and radiologic progressionArthritis Rheum200757116124
Brown A, Quinn M, Karim Z, Conaghan P, Peterfy C, Hensor E et al.
Presence of significant synovitis in rheumatoid arthritis patients with disease-modifying antirheumatic drug-induced clinical remissionArthritis Rheum20065437613773
Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus M, D’Agostino MA et al.
Musculoskeletal ultrasound including definitions for ultrasonographic pathologyJ Rheumatol20053224852487
Koenig R, Pedro M, Heinen C, Schmidt T, Richter H, Antoniadis G et al.
High-resolution ultrasonography in evaluating peripheral nerve entrapment and traumaNeurosurg Focus200926E13
Wolfe AMThe epidemiology of rheumatoid arthritis: a review. I. SurveysBull Rheum Dis196819518523
Kvien T, Uhlig T, Ødegård S, Heiberg MEpidemiological aspects of rheumatoid arthritis: the sex ratioAnn N Y Acad Sci20061069212222
Stucki G, Schönbächler J, Brühlmann P, Mariacher S, Stoll T, Michel BDoes a muscle strength index provide complementary information to traditional disease activity variables in patients with rheumatoid arthritis?J Rheumatol19942122002205
Stucki G, Bruhlmann P, Stucki S, Michel BIsometric muscle strength is an indicator of self-reported physical functional disability in patients with rheumatoid arthritisRheumatology199837643648
Willer BEffects of creatine supplementation on muscle weakness in patients with rheumatoid arthritisRheumatology200039293298
Engvall I, Elkan A, Tengstrand B, Cederholm T, Brismar K, Hafström ICachexia in rheumatoid arthritis is associated with inflammatory activity, physical disability, and low bioavailable insulin-like growth factorScand J Rehabil Med200837321328
Chen Y, Chen H, Hsieh C, Hsieh T, Lan J, Chen DA close association of body cell mass loss with disease activity and disability in Chinese patients with rheumatoid arthritisClinics20116612171222
Welsing P, Van Gestel A, Swinkels H, Kiemeney L, Van Riel PThe relationship between disease activity, joint destruction, and functional capacity over the course of rheumatoid arthritisArthritis Rheum20014420092017
Boyd T, Bonner A, Thorne C, Boire G, Hitchon C, Haraoui B et al.
The relationship between function and disease activity as measured by the HAQ and DAS28 varies over time and by rheumatoid factor status in early inflammatory arthritis (EIA). Results from the CATCH CohortOpen Rheumatol J201375863
Nunez-Cornejo Piquer C, Nunez-Cornejo Palomares C, Ivorra Cortes J, Grau E, Chalmeta Verdejo I, Molina Almela C et al.
AB0230 relationship between HAQ, DAS28 and radiological damage with functional capacity of the hand in rheumatoid arthritisAnn Rheum Dis201473879880
Bekkelund S, Torbergsen T, Omdal R, Husby G, Mellgren SNerve conduction studies in rheumatoid arthritisScand J Rheumatol199625287292
Kadhim A, Abdul-Kareem A, Hamdan FPeripheral neuropathy in rheumatoid arthritis: a clinical and neurophysiological studyIraqi J Med Sci20032376382
Sulaiman M, Sulaiman S, Majdal HNerve conduction and electromyography in rheumatoid arthritis patients: a case–control studyAnn Coll Med Mosul2012384451
Bekkelund S, Torbergsen T, Husby G, Mellgren SMyopathy and neuropathy in rheumatoid arthritis. A quantitative controlled electromyographic studyJ Rheumatol19992623482351
Abdullah Q, Rasool M, Qader TAssessment of neurophysiologic changes and disease activity in patients with chronic rheumatoid arthritisJordan Med J201347131141
Olney RNeuropathies associated with connective tissue diseaseSemin Neurol1998186372
Nadkar M, Agarwal R, Samant R, Chhugani S, Idgunji S, Iyer S et al.
Neuropathy in rheumatoid arthritisJ Assoc Physicians India200149217220
Khedr E, Herdan O, Khalifa H, Ali A, El Fetoh N, El-Hammady D et al.
Clinical and subclinical neuropsychiatric abnormalities in rheumatoid arthritis patientsEgypt Rheumatol Rehabil2015421118
Turesson C, Matteson EVasculitis in rheumatoid arthritisCurr Opin Rheumatol2009213540
Aktekin L, Gözlükaya H, Bodur H, Borman P, Köz ÖPeripheral neuropathy in rheumatoid arthritis patients;an electroneurophysiological studyTurk J Rheumatol2009246264
Ramos-Remus C, Duran-Barragan S, Castillo-Ortiz JBeyond the jointsClin Rheumatol201131112
Rubin D, Daube JNerve conduction studiesAminoff's Electrodiagnosis in Clinical Neurology20126th edPhiladelphiaSaunders/Elsevier289326
Herbison GJ, Teng C, Martin JH, Ditunno JFJrCarpal tunnel syndrome in rheumatoid arthritisAm J Phys Med19735268
Fleming A, Dodman S, Crown J, Corbett MExtra-articular features in early rheumatoid arthritisBMJ1976112411243
Lanzillo B, Pappone N, Crisci C, Di Girolamo C, Massini R, Caruso GSubclinical peripheral nerve involvement in patients with rheumatoid arthritisArthritis Rheum19984111961202
Bayrak A, Durmus D, Durmaz Y, Demir İ, Canturk F, Onar MElectrophysiological assessment of polyneuropathic involvement in rheumatoid arthritis: relationships among demographic, clinical and laboratory findingsNeurol Res201032711714
Sim M, Kim D, Yoon J, Park D, Kim YAssessment of peripheral neuropathy in patients with rheumatoid arthritis who complain of neurologic symptomsAnn Rehabil Med201438249255
Oh SNeuropathies of the footClin Neurophysiol2007118954980
Baylan S, Paik S, Barnert A, Ko K, Yu J, Persellin RPrevalence of the tarsal tunnel syndrome in rheumatoid arthritisRheumatology198120148150
Helliwell PHelliwell PClinical features of the foot in rheumatoid arthritisThe foot and ankle in rheumatoid arthritis20071st edEdinburghChurchill Livingstone/Elsevier5774
Nakano KEntrapment neuropathy from Baker's cystJAMA1978239135b135b
Katirji BPeroneal neuropathyNeurol Clin199017567591
Sourkes M, Stewart JCommon peroneal neuropathy: a study of selective motor and sensory involvementNeurology19914110291029
Soliman S, Korah T, Hammoda G, Mousa WSignificance of serum levels of angiopoietin-2 and its relationship to Doppler ultrasonographic findings in rheumatoid arthritis patientsEgypt Rheumatol2014361520
Naredo E, Möller I, Cruz A, Carmona L, Garrido JPower Doppler ultrasonographic monitoring of response to antitumor necrosis factor therapy in patients with rheumatoid arthritisArthritis Rheum20085822482256
Oh SJ, Sarala PK, Kuba T, Elmore RSTarsal tunnel syndrome: electrophysiological studyAnn Neurol19795327330
Oh SJ, Kim HS, Ahmad BKThe near-nerve sensory nerve conduction in tarsal tunnel syndromeJ Neurol Neurosurg Psychiatry1985489991003
Galardi G, Amadio S, Maderna L, Meraviglia M, Brunati L, Conte G et al.
Electrophysiologic studies in tarsal tunnel syndromeAm J Phys Med Rehabil199473193198
Mondelli M, Giannini F, Reale FClinical and electrophysiological findings and follow-up in tarsal tunnel syndromeElectroencephalogr Clin Neurophysiol1998109418425
Mondelli M, Morana P, Padua LAn electrophysiological severity scale in tarsal tunnel syndromeActa Neurol Scand2004109284289
Patel AT, Gaines K, Malamut R, Park TA, Toro DR, Holland N et al.
Usefulness of electrodiagnostic techniques in the evaluation of suspected tarsal tunnel syndrome: an evidence based reviewMuscle Nerve200532236240
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]