Impaired small fiber conduction in patients with Fabry disease: a neurophysiological case–control study
Tóm tắt
Fabry disease is an inborn lysosomal storage disorder which is associated with small fiber neuropathy. We set out to investigate small fiber conduction in Fabry patients using pain-related evoked potentials (PREP). In this case–control study we prospectively studied 76 consecutive Fabry patients for electrical small fiber conduction in correlation with small fiber function and morphology. Data were compared with healthy controls using non-parametric statistical tests. All patients underwent neurological examination and were investigated with pain and depression questionnaires. Small fiber function (quantitative sensory testing, QST), morphology (skin punch biopsy), and electrical conduction (PREP) were assessed and correlated. Patients were stratified for gender and disease severity as reflected by renal function. All Fabry patients (31 men, 45 women) had small fiber neuropathy. Men with Fabry disease showed impaired cold (p < 0.01) and warm perception (p < 0.05), while women did not differ from controls. Intraepidermal nerve fiber density (IENFD) was reduced at the lower leg (p < 0.001) and the back (p < 0.05) mainly of men with impaired renal function. When investigating A-delta fiber conduction with PREP, men but not women with Fabry disease had lower amplitudes upon stimulation at face (p < 0.01), hands (p < 0.05), and feet (p < 0.01) compared to controls. PREP amplitudes further decreased with advance in disease severity. PREP amplitudes and warm (p < 0.05) and cold detection thresholds (p < 0.01) at the feet correlated positively in male patients. Small fiber conduction is impaired in men with Fabry disease and worsens with advanced disease severity. PREP are well-suited to measure A-delta fiber conduction.
Tài liệu tham khảo
Schiffmann R: Fabry disease. Pharmacol Ther. 2009, 122: 65-77. 10.1016/j.pharmthera.2009.01.003.
Laaksonen SM, Roytta M, Jaaskelainen SK, Kantola I, Penttinen M, Falck B: Neuropathic symptoms and findings in women with Fabry disease. Clin Neurophysiol. 2008, 119: 1365-1372. 10.1016/j.clinph.2008.02.004.
Liguori R, Di Stasi V, Bugiardini E, Mignani R, Burlina A, Borsini W, Baruzzi A, Montagna P, Donadio V: Small fiber neuropathy in female patients with fabry disease. Muscle Nerve. 2010, 41: 409-412. 10.1002/mus.21606.
Torvin Moller A, Winther Bach F, Feldt-Rasmussen U, Rasmussen A, Hasholt L, Lan H, Sommer C, Kolvraa S, Ballegaard M, Staehelin Jensen T: Functional and structural nerve fiber findings in heterozygote patients with Fabry disease. Pain. 2009, 145: 237-245. 10.1016/j.pain.2009.06.032.
Üçeyler N, He L, Schönfeld D, Kahn AK, Reiners K, Hilz MJ, Breunig F, Sommer C: Small fibers in Fabry disease: baseline and follow-up data under enzyme replacement therapy. J Peripher Nerv Syst. 2011, 16: 304-314. 10.1111/j.1529-8027.2011.00365.x.
Burlina AP, Sims KB, Politei JM, Bennett GJ, Baron R, Sommer C, Torvin Moller A, Hilz MJ: Early diagnosis of peripheral nervous system involvement in Fabry disease and treatment of neuropathic pain: the report of an expert panel. BMC Neurol. 2011, 11: 61-10.1186/1471-2377-11-61.
Kaube H, Katsarava Z, Kaufer T, Diener H, Ellrich J: A new method to increase nociception specificity of the human blink reflex. Clin Neurophysiol. 2000, 111: 413-416. 10.1016/S1388-2457(99)00295-3.
Katsarava Z, Ayzenberg I, Sack F, Limmroth V, Diener HC, Kaube H: A novel method of eliciting pain-related potentials by transcutaneous electrical stimulation. Headache. 2006, 46: 1511-1517. 10.1111/j.1526-4610.2006.00446.x.
Sommer C, Richter H, Rogausch JP, Frettloh J, Lungenhausen M, Maier C: A modified score to identify and discriminate neuropathic pain: a study on the German version of the neuropathic pain symptom inventory (NPSI). BMC Neurol. 2011, 11: 104-10.1186/1471-2377-11-104.
Bouhassira D, Attal N, Fermanian J, Alchaar H, Gautron M, Masquelier E, Rostaing S, Lanteri-Minet M, Collin E, Grisart J, Boureau F: Development and validation of the Neuropathic Pain Symptom Inventory. Pain. 2004, 108: 248-257. 10.1016/j.pain.2003.12.024.
Von Korff M, Ormel J, Keefe FJ, Dworkin SF: Grading the severity of chronic pain. Pain. 1992, 50: 133-149. 10.1016/0304-3959(92)90154-4.
Radloff LS: The CES-D: a self-report symptom scale to detect depression in the general population. Appl Psychol Meas. 1977, 3: 385-401.
Lacomis D: Small-fiber neuropathy. Muscle Nerve. 2002, 26: 173-188. 10.1002/mus.10181.
Schiffmann R, Warnock DG, Banikazemi M, Bultas J, Linthorst GE, Packman S, Sorensen SA, Wilcox WR, Desnick RJ: Fabry disease: progression of nephropathy, and prevalence of cardiac and cerebrovascular events before enzyme replacement therapy. Nephrol Dial Transplant. 2009, 24: 2102-2111. 10.1093/ndt/gfp031.
Tahir H, Jackson LL, Warnock DG: Antiproteinuric Therapy and Fabry Nephropathy: Sustained Reduction of Proteinuria in Patients Receiving Enzyme Replacement Therapy with Agalsidase-beta. J Am Soc Nephrol. 2007, 18: 2609-2617. 10.1681/ASN.2006121400.
Vedder AC, Linthorst GE, Houge G, Groener JE, Ormel EE, Bouma BJ, Aerts JM, Hirth A, Hollak CE: Treatment of Fabry disease: outcome of a comparative trial with agalsidase alfa or beta at a dose of 0.2 mg/kg. PLoS ONE. 2007, 2: e598-10.1371/journal.pone.0000598.
Kimura J: Electrodiagnosis in diseases of nerve and muscle: Principles and practice. Third edition edn. 2001, New York: Oxford University Press
Rolke R, Baron R, Maier C, Tölle TR, Treede RD, Beyer A, Binder A, Birbaumer N, Birklein F, Botefur IC: Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): standardized protocol and reference values. Pain. 2006, 123: 231-243. 10.1016/j.pain.2006.01.041.
Magerl W, Krumova EK, Baron R, Tolle T, Treede RD, Maier C: Reference data for quantitative sensory testing (QST): refined stratification for age and a novel method for statistical comparison of group data. Pain. 2010, 151: 598-605. 10.1016/j.pain.2010.07.026.
Üçeyler N, Zeller D, Kahn AK, Kewenig S, Kittel-Schneider S, Schmid A, Casanova-Molla J, Reiners K, Sommer C: Small fibre pathology in patients with fibromyalgia syndrome. Brain. 2013, 10.1093/brain/awt053.
Üçeyler N, Kafke W, Riediger N, He L, Necula G, Toyka KV, Sommer C: Elevated proinflammatory cytokine expression in affected skin in small fiber neuropathy. Neurology. 2010, 74: 1806-1813. 10.1212/WNL.0b013e3181e0f7b3.
Lauria G, Cornblath DR, Johansson O, McArthur JC, Mellgren SI, Nolano M, Rosenberg N, Sommer C: European Federation of Neurological S: EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur J Neurol. 2005, 12: 747-758. 10.1111/j.1468-1331.2005.01260.x.
Biegstraaten M, Binder A, Maag R, Hollak CE, Baron R, van Schaik IN: The relation between small nerve fibre function, age, disease severity and pain in Fabry disease. Eur J Pain. 2011, 15: 822-829. 10.1016/j.ejpain.2011.01.014.
Dutsch M, Marthol H, Stemper B, Brys M, Haendl T, Hilz MJ: Small fiber dysfunction predominates in Fabry neuropathy. J Clin Neurophysiol. 2002, 19: 575-586. 10.1097/00004691-200212000-00011.
Low M, Nicholls K, Tubridy N, Hand P, Velakoulis D, Kiers L, Mitchell P, Becker G: Neurology of Fabry disease. Intern Med J. 2007, 37: 436-447. 10.1111/j.1445-5994.2007.01366.x.
Luciano CA, Russell JW, Banerjee TK, Quirk JM, Scott LJ, Dambrosia JM, Barton NW, Schiffmann R: Physiological characterization of neuropathy in Fabry's disease. Muscle Nerve. 2002, 26: 622-629. 10.1002/mus.10236.
Scott LJ, Griffin JW, Luciano C, Barton NW, Banerjee T, Crawford T, McArthur JC, Tournay A, Schiffmann R: Quantitative analysis of epidermal innervation in Fabry disease. Neurology. 1999, 52: 1249-1254. 10.1212/WNL.52.6.1249.
Maag R, Binder A, Maier C, Scherens A, Toelle T, Treede RD, Baron R: Detection of a characteristic painful neuropathy in Fabry disease: a pilot study. Pain Med. 2008, 9: 1217-1223. 10.1111/j.1526-4637.2008.00470.x.
Schepers RJ, Ringkamp M: Thermo receptors and thermo sensitive afferents. Neurosci Biobehav Rev. 2010, 34: 177-184. 10.1016/j.neubiorev.2009.10.003.
Kakigi R, Endo C, Neshige R, Kuroda Y, Shibasaki H: Estimation of conduction velocity of A delta fibers in humans. Muscle Nerve. 1991, 14: 1193-1196. 10.1002/mus.880141209.
Lefaucheur JP, Ahdab R, Ayache SS, Lefaucheur-Menard I, Rouie D, Tebbal D, Neves DO, Ciampi de Andrade D: Pain-related evoked potentials: a comparative study between electrical stimulation using a concentric planar electrode and laser stimulation using a CO2 laser. Neurophysiol Clin. 2012, 42: 199-206. 10.1016/j.neucli.2011.12.003.
Müller D, Obermann M, Koeppen S, Kavuk I, Yoon MS, Sack F, Diener HC, Kaube H, Katsarava Z: Electrically evoked nociceptive potentials for early detection of diabetic small-fiber neuropathy. Eur J Neurol. 2010, 17: 834-841. 10.1111/j.1468-1331.2009.02938.x.
Obermann M, Katsarava Z, Esser S, Sommer C, He L, Selter L, Yoon MS, Kaube H, Diener HC, Maschke M: Correlation of epidermal nerve fiber density with pain-related evoked potentials in HIV neuropathy. Pain. 2008, 138: 79-86. 10.1016/j.pain.2007.11.009.
Valeriani M, Mariotti P, Le Pera D, Restuccia D, De Armas L, Maiese T, Vigevano F, Antuzzi D, Zampino G, Ricci R, Tonali P: Functional assessment of A delta and C fibers in patients with Fabry's disease. Muscle Nerve. 2004, 30: 708-713. 10.1002/mus.20174.
Kaye EM, Kolodny EH, Logigian EL, Ullman MD: Nervous system involvement in Fabry's disease: clinicopathological and biochemical correlation. Ann Neurol. 1988, 23: 505-509. 10.1002/ana.410230513.
Park S, Kim JA, Joo KY, Choi S, Choi EN, Shin JA, Han KH, Jung SC, Suh SH: Globotriaosylceramide leads to K(Ca)3.1 channel dysfunction: a new insight into endothelial dysfunction in Fabry disease. Cardiovasc Res. 2011, 89: 290-299. 10.1093/cvr/cvq333.
The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2377/13/47/prepub