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Advances in imaging technologies for the assessment of peripheral neuropathies in rheumatoid arthritis

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Abstract

Peripheral neuropathy in patients with rheumatoid arthritis is associated with a maladaptive autoimmune response that may cause chronic pain and disability. Nerve conduction studies are the routine method performed when rheumatologists presume its presence. However, this approach is invasive, may not reveal subtle malfunctions in the early stages of the disease, and does not expose abnormalities in structures surrounding the nerves and muscles, limiting the possibility of a timely diagnosis. This work aims to present a narrative review of new technologies for the clinical assessment of peripheral neuropathy in Rheumatoid Arthritis. Through a bibliographic search carried out in five repositories, from 1990 to 2020, we identified three technologies that could detect peripheral nerve lesions and perform quantitative evaluations: (1) magnetic resonance neurography, (2) functional magnetic resonance imaging, and (3) high-resolution ultrasonography of peripheral nerves. We found these tools can overcome the main constraints imposed by the previous electrophysiologic methods, enabling early diagnosis.

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Abbreviations

PN:

Peripheral neuropathy

RA:

Rheumatoid arthritis

NCS:

Nerve conduction studies

MRI:

Magnetic resonance imaging

MR:

Magnetic resonance

MRN:

Magnetic resonance neurography

SNR:

Signal-to-noise ratio

DWI:

Diffusion-weighted imaging

DTI:

Diffusion tensor imaging

FA:

Fractional anisotropy

fMRI:

Functional magnetic resonance imaging

BOLD:

Blood oxygenation-level dependent

CIDP:

Chronic inflammatory demyelinating polyneuropathy

TNS:

Total neuropathy score

US:

Ultrasound

HRUS:

High-resolution ultrasonography

GSUS:

Greyscale US

DPUS:

Power Doppler US

TNF:

Tumour necrosis factor

References

  1. Reda H, Chin RL (2014) Peripheral neuropathies of rheumatologic disease and gluten-related disorders. Semin Neurol 34(4):413–424. https://doi.org/10.1055/s-0034-1390390

    Article  PubMed  Google Scholar 

  2. Biswas M, Chatterjee A, Ghosh SK, Dasgupta S, Ghosh K, Ganguly PK (2011) Prevalence, types, clinical associations, and determinants of peripheral neuropathy in rheumatoid patients. Ann Indian Acad Neurol 14(3):194–197. https://doi.org/10.4103/0972-2327.85893

    Article  PubMed  PubMed Central  Google Scholar 

  3. Sivri A, Güler-Uysal F (1999) The electroneurophysiological findings in rheumatoid arthritis patients. Electromyogr Clin Neurophysiol 39(7):387–391

    CAS  PubMed  Google Scholar 

  4. Kaeley N, Ahmad S, Pathania M, Kakkar R (2019) Prevalence and patterns of peripheral neuropathy in patients of rheumatoid arthritis. J Family Med Prim Care 8(1):22–26. https://doi.org/10.4103/jfmpc.jfmpc_260_18

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cojocaru M, Cojocaru IM, Silosi I, Vrabie CD, Tanasescu R (2010) Extra-articular Manifestations in Rheumatoid Arthritis. Maedica 5(4):286–291

    PubMed  PubMed Central  Google Scholar 

  6. Bayrak AO, Durmus D, Durmaz Y, Demir I, Canturk F, Onar MK (2010) Electrophysiological assessment of polyneuropathic involvement in rheumatoid arthritis: relationships among demographic, clinical and laboratory findings. Neurol Res 32(7):711–714. https://doi.org/10.1179/016164109x12581096870195

    Article  PubMed  Google Scholar 

  7. Vallat JM, Rabin M, Magy L (2012) Peripheral neuropathies in rheumatic disease—a guide to diagnosis. Nat Rev Rheumatol 8(10):599–609. https://doi.org/10.1038/nrrheum.2012.138

    Article  CAS  PubMed  Google Scholar 

  8. Salaffi F, Giacobazzi G, Di Carlo M (2018) Chronic pain in inflammatory arthritis: mechanisms, metrology, and emerging targets—a focus on the JAK-STAT pathway. Pain Res Manag 2018:8564215. https://doi.org/10.1155/2018/8564215

    Article  PubMed  PubMed Central  Google Scholar 

  9. Courvoisier N, Dougados M, Cantagrel A, Goupille P, Meyer O, Sibilia J, Daures JP, Combe B (2008) Prognostic factors of 10-year radiographic outcome in early rheumatoid arthritis: a prospective study. Arthritis Res Ther 10(5):R106. https://doi.org/10.1186/ar2498

    Article  PubMed  PubMed Central  Google Scholar 

  10. Atzeni F, Cazzola M, Benucci M, Di Franco M, Salaffi F, Sarzi-Puttini P (2011) Chronic widespread pain in the spectrum of rheumatological diseases. Best Pract Res Clin Rheumatol 25(2):165–171. https://doi.org/10.1016/j.berh.2010.01.011

    Article  PubMed  Google Scholar 

  11. Mallik A, Weir AI (2005) Nerve conduction studies: essentials and pitfalls in practice. J Neurol Neurosurg Psychiatry 76(Suppl 2):ii23-31. https://doi.org/10.1136/jnnp.2005.069138

    Article  PubMed  PubMed Central  Google Scholar 

  12. Bromberg MB (2013) An electrodiagnostic approach to the evaluation of peripheral neuropathies. Phys Med Rehabil Clin N Am 24(1):153–168. https://doi.org/10.1016/j.pmr.2012.08.020

    Article  PubMed  Google Scholar 

  13. Chhabra A, Andreisek G, Soldatos T, Wang KC, Flammang AJ, Belzberg AJ, Carrino JA (2011) MR neurography: past, present, and future. AJR Am J Roentgenol 197(3):583–591. https://doi.org/10.2214/ajr.10.6012

    Article  PubMed  Google Scholar 

  14. Magda P, Latov N, Renard MV, Sander HW (2002) Quantitative sensory testing: high sensitivity in small fiber neuropathy with normal NCS/EMG. J Peripher Nerv Syst 7(4):225–228. https://doi.org/10.1046/j.1529-8027.2002.02029.x

    Article  PubMed  Google Scholar 

  15. Casteleyn V, Hahn K, Stenzel W, Siegert E (2019) Peripheral nerve involvement in rheumatic diseases. Z Rheumatol 78(4):339–351. https://doi.org/10.1007/s00393-019-0621-z

    Article  CAS  PubMed  Google Scholar 

  16. Gasparyan AY, Ayvazyan L, Blackmore H, Kitas GD (2011) Writing a narrative biomedical review: considerations for authors, peer reviewers, and editors. Rheumatol Int 31(11):1409–1417. https://doi.org/10.1007/s00296-011-1999-3

    Article  PubMed  Google Scholar 

  17. Schardt C, Adams MB, Owens T, Keitz S, Fontelo P (2007) Utilization of the PICO framework to improve searching PubMed for clinical questions. BMC Med Inform Decis Mak 7:16. https://doi.org/10.1186/1472-6947-7-16

    Article  PubMed  PubMed Central  Google Scholar 

  18. Chapter 6—Magnetic resonance imaging (2011). In: Waldman SD, Campbell RSD (eds) Imaging of Pain. W.B. Saunders Philadelphia, pp. 19–21. https://doi.org/10.1016/B978-1-4377-0906-3.00006-7

  19. Chou ET, Carrino JA (2007) Magnetic resonance imaging. In: Waldman SD (ed) Pain management. W.B. Saunders, Philadelphia, pp. 106–117. https://doi.org/10.1016/B978-0-7216-0334-6.50014-5

  20. Chen Y, Haacke EM, Li J (2019) Peripheral nerve magnetic resonance imaging. F1000Research 8:1803. https://doi.org/10.12688/f1000research.19695.1

    Article  CAS  Google Scholar 

  21. Martinez AR, Nunes MB, Nucci A, França MC Jr (2012) Sensory neuronopathy and autoimmune diseases. Autoimmune Dis 2012:873587. https://doi.org/10.1155/2012/873587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kronlage M, Schwehr V, Schwarz D, Godel T, Heiland S, Bendszus M, Bäumer P (2019) Magnetic resonance neurography : normal values and demographic determinants of nerve caliber and T2 relaxometry in 60 healthy individuals. Clin Neuroradiol 29(1):19–26. https://doi.org/10.1007/s00062-017-0633-5

    Article  PubMed  Google Scholar 

  23. Hargreaves BA, Worters PW, Pauly KB, Pauly JM, Koch KM, Gold GE (2011) Metal-induced artifacts in MRI. AJR Am J Roentgenol 197(3):547–555. https://doi.org/10.2214/ajr.11.7364

    Article  PubMed  PubMed Central  Google Scholar 

  24. Chhabra A, Madhuranthakam AJ, Andreisek G (2018) Magnetic resonance neurography: current perspectives and literature review. Eur Radiol 28(2):698–707. https://doi.org/10.1007/s00330-017-4976-8

    Article  PubMed  Google Scholar 

  25. Bendszus M, Wessig C, Solymosi L, Reiners K, Koltzenburg M (2004) MRI of peripheral nerve degeneration and regeneration: correlation with electrophysiology and histology. Exp Neurol 188(1):171–177. https://doi.org/10.1016/j.expneurol.2004.03.025

    Article  PubMed  Google Scholar 

  26. Filler AG, Howe FA, Hayes CE, Kliot M, Winn HR, Bell BA, Griffiths JR, Tsuruda JS (1993) Magnetic resonance neurography. Lancet 341(8846):659–661. https://doi.org/10.1016/0140-6736(93)90422-d

    Article  CAS  PubMed  Google Scholar 

  27. Dailey AT, Tsuruda JS, Filler AG, Maravilla KR, Goodkin R, Kliot M (1997) Magnetic resonance neurography of peripheral nerve degeneration and regeneration. Lancet 350(9086):1221–1222. https://doi.org/10.1016/s0140-6736(97)24043-2

    Article  CAS  PubMed  Google Scholar 

  28. Chhabra A, Lee PP, Bizzell C, Soldatos T (2011) 3 Tesla MR neurography—technique, interpretation, and pitfalls. Skeletal Radiol 40(10):1249–1260. https://doi.org/10.1007/s00256-011-1183-6

    Article  PubMed  Google Scholar 

  29. Stoll G, Wilder-Smith E, Bendszus M (2013) Imaging of the peripheral nervous system. Handb Clin Neurol 115:137–153. https://doi.org/10.1016/b978-0-444-52902-2.00008-4

    Article  PubMed  Google Scholar 

  30. Husarik DB, Saupe N, Pfirrmann CW, Jost B, Hodler J, Zanetti M (2009) Elbow nerves: MR findings in 60 asymptomatic subjects—normal anatomy, variants, and pitfalls. Radiology 252(1):148–156. https://doi.org/10.1148/radiol.2521081614

    Article  PubMed  Google Scholar 

  31. Deshmane A, Gulani V, Griswold MA, Seiberlich N (2012) Parallel MR imaging. J Magn Reson Imaging 36(1):55–72. https://doi.org/10.1002/jmri.23639

    Article  PubMed  PubMed Central  Google Scholar 

  32. Chhabra A, Zhao L, Carrino JA, Trueblood E, Koceski S, Shteriev F, Lenkinski L, Sinclair CD, Andreisek G (2013) MR neurography: advances. Radiol Res Pract 2013:809568. https://doi.org/10.1155/2013/809568

    Article  PubMed  PubMed Central  Google Scholar 

  33. Andersson G, Orädd G, Sultan F, Novikov LN (2018) In vivo diffusion tensor imaging, diffusion kurtosis imaging, and tractography of a sciatic nerve injury model in rat at 9.4 T. Sci Rep 8(1):12911. https://doi.org/10.1038/s41598-018-30961-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Zhu LH, Zhang ZP, Wang FN, Cheng QH, Guo G (2019) Diffusion kurtosis imaging of microstructural changes in brain tissue affected by acute ischemic stroke in different locations. Neural Regen Res 14(2):272–279. https://doi.org/10.4103/1673-5374.244791

    Article  PubMed  PubMed Central  Google Scholar 

  35. Ohana M, Moser T, Moussaouï A, Kremer S, Carlier RY, Liverneaux P, Dietemann JL (2014) Current and future imaging of the peripheral nervous system. Diagn Interv Imaging 95(1):17–26. https://doi.org/10.1016/j.diii.2013.05.008

    Article  CAS  PubMed  Google Scholar 

  36. Martín Noguerol T, Barousse R, Gómez Cabrera M, Socolovsky M, Bencardino JT, Luna A (2019) Functional MR neurography in evaluation of peripheral nerve trauma and postsurgical assessment. Radiographics 39(2):427–446. https://doi.org/10.1148/rg.2019180112

    Article  PubMed  Google Scholar 

  37. Heckel A, Weiler M, Xia A, Ruetters M, Pham M, Bendszus M, Heiland S, Baeumer P (2015) Peripheral nerve diffusion tensor imaging: assessment of axon and myelin sheath integrity. PLoS ONE 10(6):e0130833. https://doi.org/10.1371/journal.pone.0130833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Gersing AS, Cervantes B, Knebel C, Schwaiger BJ, Kirschke JS, Weidlich D, Claudi C, Peeters JM, Pfeiffer D, Rummeny EJ, Karampinos DC, Woertler K (2020) Diffusion tensor imaging and tractography for preoperative assessment of benign peripheral nerve sheath tumors. Eur J Radiol 129:109110. https://doi.org/10.1016/j.ejrad.2020.109110

    Article  PubMed  Google Scholar 

  39. Simon NG, Kliot M (2014) Diffusion weighted MRI and tractography for evaluating peripheral nerve degeneration and regeneration. Neural Regen Res 9(24):2122–2124. https://doi.org/10.4103/1673-5374.147941

    Article  PubMed  PubMed Central  Google Scholar 

  40. Jambawalikar S, Baum J, Button T, Li H, Geronimo V, Gould ES (2010) Diffusion tensor imaging of peripheral nerves. Skeletal Radiol 39(11):1073–1079. https://doi.org/10.1007/s00256-010-0974-5

    Article  PubMed  Google Scholar 

  41. Bäumer P, Pham M, Ruetters M, Heiland S, Heckel A, Radbruch A, Bendszus M, Weiler M (2014) Peripheral neuropathy: detection with diffusion-tensor imaging. Radiology 273(1):185–193. https://doi.org/10.1148/radiol.14132837

    Article  PubMed  Google Scholar 

  42. Khalil C, Budzik JF, Kermarrec E, Balbi V, Le Thuc V, Cotten A (2010) Tractography of peripheral nerves and skeletal muscles. Eur J Radiol 76(3):391–397. https://doi.org/10.1016/j.ejrad.2010.03.012

    Article  CAS  PubMed  Google Scholar 

  43. Sánchez-González J, Luna A (2012) DWI at 3 T: advantages, disadvantages, pitfalls, and advanced clinical applications. Diffusion MRI outside the brain. Springer, Berlin, pp 51–73

    Chapter  Google Scholar 

  44. Agarwal A, Chandra A, Jaipal U, Bagarhatta M, Mendiratta K, Goyal A, Kumar R, Mangalhara N (2019) Can imaging be the new yardstick for diagnosing peripheral neuropathy?—a comparison between high resolution ultrasound and MR neurography with an approach to diagnosis. Insights Imaging 10(1):104. https://doi.org/10.1186/s13244-019-0787-6

    Article  PubMed  PubMed Central  Google Scholar 

  45. Pérez-Neri I, González-Aguilar A, Sandoval H, Pineda C, Ríos C (2020) Therapeutic potential of ultrasound neuromodulation in decreasing neuropathic pain: clinical and experimental evidence. Curr Neuropharmacol. https://doi.org/10.2174/1570159x18666200720175253

    Article  PubMed  Google Scholar 

  46. Dou Z, Yang L (2019) The application of functional magnetic resonance imaging in neuropathic pain. In: Medical imaging-principles and applications. IntechOpen, UK

  47. Matthews PM, Jezzard P (2004) Functional magnetic resonance imaging. J Neurol Neurosurg Psychiatry 75(1):6–12

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Brown GG, Perthen JE, Liu TT, Buxton RB (2007) A primer on functional magnetic resonance imaging. Neuropsychol Rev 17(2):107–125. https://doi.org/10.1007/s11065-007-9028-8

    Article  PubMed  Google Scholar 

  49. Boland EG, Selvarajah D, Hunter M, Ezaydi Y, Tesfaye S, Ahmedzai SH, Snowden JA, Wilkinson ID (2014) Central pain processing in chronic chemotherapy-induced peripheral neuropathy: a functional magnetic resonance imaging study. PLoS ONE 9(5):e96474. https://doi.org/10.1371/journal.pone.0096474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Moisset X, Bouhassira D (2007) Brain imaging of neuropathic pain. Neuroimage 37(Suppl 1):S80-88. https://doi.org/10.1016/j.neuroimage.2007.03.054

    Article  PubMed  Google Scholar 

  51. Endo T, Spenger C, Hao J, Tominaga T, Wiesenfeld-Hallin Z, Olson L, Xu XJ (2008) Functional MRI of the brain detects neuropathic pain in experimental spinal cord injury. Pain 138(2):292–300. https://doi.org/10.1016/j.pain.2007.12.017

    Article  PubMed  Google Scholar 

  52. Li J, Zhang W, Wang X, Yuan T, Liu P, Wang T, Shen L, Huang Y, Li N, You H, Xiao T, Feng F, Ma C (2018) Functional magnetic resonance imaging reveals differences in brain activation in response to thermal stimuli in diabetic patients with and without diabetic peripheral neuropathy. PLoS ONE 13(1):e0190699. https://doi.org/10.1371/journal.pone.0190699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yeh CH, Caswell K, Pandiri S, Sair H, Lukkahatai N, Campbell CM, Stearns V, Van de Castle B, Perrin N, Smith TJ, Saligan LN (2020) Dynamic brain activity following auricular point acupressure in chemotherapy-induced neuropathy: a pilot longitudinal functional magnetic resonance imaging study. Glob Adv Health Med 9:2164956120906092. https://doi.org/10.1177/2164956120906092

    Article  PubMed  PubMed Central  Google Scholar 

  54. Baumgärtner U, Iannetti GD, Zambreanu L, Stoeter P, Treede RD, Tracey I (2010) Multiple somatotopic representations of heat and mechanical pain in the operculo-insular cortex: a high-resolution fMRI study. J Neurophysiol 104(5):2863–2872. https://doi.org/10.1152/jn.00253.2010

    Article  PubMed  PubMed Central  Google Scholar 

  55. Hsieh ST (2010) Pathology and functional diagnosis of small-fiber painful neuropathy. Acta Neurol Taiwan 19(2):82–89

    PubMed  Google Scholar 

  56. Borsook D, Becerra L (2007) Phenotyping central nervous system circuitry in chronic pain using functional MRI: considerations and potential implications in the clinic. Curr Pain Headache Rep 11(3):201–207. https://doi.org/10.1007/s11916-007-0191-7

    Article  PubMed  Google Scholar 

  57. Fomberstein K, Qadri S, Ramani R (2013) Functional MRI and pain. Curr Opin Anesthesiol 26(5):588–593. https://doi.org/10.1097/01.aco.0000433060.59939.fe

    Article  Google Scholar 

  58. Hofbauer RK, Olausson HW, Bushnell MC (2006) Thermal and tactile sensory deficits and allodynia in a nerve-injured patient: a multimodal psychophysical and functional magnetic resonance imaging study. Clin J Pain 22(1):104–108. https://doi.org/10.1097/01.ajp.0000149798.93498.7c

    Article  PubMed  Google Scholar 

  59. Padua L, Liotta G, Di Pasquale A, Granata G, Pazzaglia C, Caliandro P, Martinoli C (2012) Contribution of ultrasound in the assessment of nerve diseases. Eur J Neurol 19(1):47–54. https://doi.org/10.1111/j.1468-1331.2011.03421.x

    Article  CAS  PubMed  Google Scholar 

  60. Di Pasquale A, Morino S, Loreti S, Bucci E, Vanacore N, Antonini G (2015) Peripheral nerve ultrasound changes in CIDP and correlations with nerve conduction velocity. Neurology 84(8):803–809. https://doi.org/10.1212/wnl.0000000000001291

    Article  PubMed  Google Scholar 

  61. Wilder-Smith EP, Rajendran K, Therimadasamy AK (2009) High-resolution ultrasonography for peripheral nerve diagnostics: a guide for clinicians involved in diagnosis and management of peripheral nerve disorders. World Scientific, Singapore

    Book  Google Scholar 

  62. Moritz T, Prosch H, Pivec CH, Sachs A, Pretterklieber ML, Kriechbaumer L, Happak W, Bodner G (2014) High-resolution ultrasound visualization of the subcutaneous nerves of the forearm: a feasibility study in anatomic specimens. Muscle Nerve 49(5):676–679. https://doi.org/10.1002/mus.24064

    Article  PubMed  Google Scholar 

  63. Chavez-Lopez MA, Hernandez-Diaz C, Moya C, Pineda C, Ventura-Rios L, Moller I, Naredo E, Espinosa R, Pena A, Rosas-Cabral A, Filippucci E (2013) Inter- and intra-observer agreement of high-resolution ultrasonography and power Doppler in assessment of joint inflammation and bone erosions in patients with rheumatoid arthritis. Rheumatol Int 33(1):173–177. https://doi.org/10.1007/s00296-011-2297-9

    Article  PubMed  Google Scholar 

  64. Gallardo E, Noto Y, Simon NG (2015) Ultrasound in the diagnosis of peripheral neuropathy: structure meets function in the neuromuscular clinic. J Neurol Neurosurg Psychiatry 86(10):1066–1074. https://doi.org/10.1136/jnnp-2014-309599

    Article  PubMed  Google Scholar 

  65. Blanch S, Demondion X, Bard H, Montet X, Martinoli C (2007) Échographie du nerf médian. Rev rhum (Ed française) 74(4):376–383

    Google Scholar 

  66. Üçeyler N, Schäfer KA, Mackenrodt D, Sommer C, Müllges W (2016) High-resolution ultrasonography of the superficial peroneal motor and sural sensory nerves may be a non-invasive approach to the diagnosis of vasculitic neuropathy. Front Neurol 7:48. https://doi.org/10.3389/fneur.2016.00048

    Article  PubMed  PubMed Central  Google Scholar 

  67. El-Karabaty H, Hetzel A, Galla TJ, Horch RE, Lücking CH, Glocker FX (2005) The effect of carpal tunnel release on median nerve flattening and nerve conduction. Electromyogr Clin Neurophysiol 45(4):223–227

    CAS  PubMed  Google Scholar 

  68. Ginn SD, Cartwright MS, Chloros GD, Walker FO, Yoon JS, Brown ME, Wiesler ER (2007) Ultrasound in the diagnosis of a median neuropathy in the forearm: case report. J Brachial Plex Peripher Nerve Inj 2:23. https://doi.org/10.1186/1749-7221-2-23

    Article  PubMed  PubMed Central  Google Scholar 

  69. Cartwright MS, Chloros GD, Walker FO, Wiesler ER, Campbell WW (2007) Diagnostic ultrasound for nerve transection. Muscle Nerve 35(6):796–799. https://doi.org/10.1002/mus.20761

    Article  PubMed  Google Scholar 

  70. Peer S, Harpf C, Willeit J, Piza-Katzer H, Bodner G (2003) Sonographic evaluation of primary peripheral nerve repair. J Ultrasound Med 22(12):1317–1322. https://doi.org/10.7863/jum.2003.22.12.1317

    Article  PubMed  Google Scholar 

  71. Chhabra A, Subhawong TK, Andreisek G (2012) Magnetic resonance neurography of tunnels—part I: upper extremity nerves. In: Magnetic resonance neurography. pp. 37

  72. Beekman R, Van Der Plas JP, Uitdehaag BM, Schellens RL, Visser LH (2004) Clinical, electrodiagnostic, and sonographic studies in ulnar neuropathy at the elbow. Muscle Nerve 30(2):202–208. https://doi.org/10.1002/mus.20093

    Article  PubMed  Google Scholar 

  73. Pál E, Fülöp K, Tóth P, Deli G, Pfund Z, Janszky J, Komoly S (2020) Small fiber neuropathy: clinicopathological correlations. Behav Neurol 2020:8796519. https://doi.org/10.1155/2020/8796519

    Article  PubMed  PubMed Central  Google Scholar 

  74. Lauria G, Merkies IS, Faber CG (2012) Small fibre neuropathy. Curr Opin Neurol 25(5):542–549. https://doi.org/10.1097/WCO.0b013e32835804c5

    Article  CAS  PubMed  Google Scholar 

  75. Hoeijmakers JG, Faber CG, Lauria G, Merkies IS, Waxman SG (2012) Small-fibre neuropathies—advances in diagnosis, pathophysiology and management. Nat Rev Neurol 8(7):369–379. https://doi.org/10.1038/nrneurol.2012.97

    Article  CAS  PubMed  Google Scholar 

  76. Camdessanché JP, Jousserand G, Ferraud K, Vial C, Petiot P, Honnorat J, Antoine JC (2009) The pattern and diagnostic criteria of sensory neuronopathy: a case–control study. Brain 132(Pt 7):1723–1733. https://doi.org/10.1093/brain/awp136

    Article  PubMed  PubMed Central  Google Scholar 

  77. Lauria G, Sghirlanzoni A, Lombardi R, Pareyson D (2001) Epidermal nerve fiber density in sensory ganglionopathies: clinical and neurophysiologic correlations. Muscle Nerve 24(8):1034–1039. https://doi.org/10.1002/mus.1107

    Article  CAS  PubMed  Google Scholar 

  78. Jusufović E, Sinanović O, Zukić S, Burina A, Džinić Jusufović Z, Šakić A (2018) Multifocal motor neuropathy: case reports. Acta Clin Croat 57(3):581–587. https://doi.org/10.20471/acc.2018.57.03.23

    Article  PubMed  PubMed Central  Google Scholar 

  79. Nobile-Orazio E (2001) Multifocal motor neuropathy. J Neuroimmunol 115(1–2):4–18. https://doi.org/10.1016/s0165-5728(01)00266-1

    Article  CAS  PubMed  Google Scholar 

  80. Van Asseldonk JT, Franssen H, Van den Berg-Vos RM, Wokke JH, Van den Berg LH (2005) Multifocal motor neuropathy. Lancet Neurol 4(5):309–319. https://doi.org/10.1016/s1474-4422(05)70074-0

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Medical Engineering Research, Instituto Nacional de Rehabilitación Luis Guillermo Ibarra Ibarra, Mexico City, Mexico

    Josefina Gutiérrez

  2. Sociomedical Research Unit, Instituto Nacional de Rehabilitación Luis Guillermo Ibarra Ibarra, Mexico City, Mexico

    Hugo Sandoval

  3. Department of Neurochemistry, Instituto Nacional de Neurología y Neurocirugía Manuel Velasco Suarez, Mexico City, Mexico

    Iván Pérez-Neri

  4. Directorate General, Instituto Nacional de Neurología y Neurocirugía Manuel Velasco Suarez, Mexico City, Mexico

    Antonio Arauz

  5. Neurological Emergency Service, Instituto Nacional de Neurología y Neurocirugía Manuel Velasco Suarez, Mexico City, Mexico

    Juan Carlos López-Hernández

  6. Division of Musculoskeletal and Rheumatic Disorders, Instituto Nacional de Rehabilitación Luis Guillermo Ibarra Ibarra, Calzada México-Xochimilco 289, Col. Arenal de Guadalupe, Alcaldía Tlalpan, 14389, Mexico City, Mexico

    Carlos Pineda

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CP, HS, IPN AA, JCLH and JG has been involved in writing, compiling and revising the manuscript critically to suit publication standards. All authors read and approved the final version of manuscript.

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Gutiérrez, J., Sandoval, H., Pérez-Neri, I. et al. Advances in imaging technologies for the assessment of peripheral neuropathies in rheumatoid arthritis. Rheumatol Int 41, 519–528 (2021). https://doi.org/10.1007/s00296-020-04780-5

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  • DOI: https://doi.org/10.1007/s00296-020-04780-5

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