F-waves persistence in peripheral sensory syndromes

Abstract

Background The distinction between sensory neuronopathies (SN), which is by definition purely sensory, and sensory polyneuropathies (SP) and sensory multineuropathies (SM) is important for etiologic investigation and prognosis estimation. However, this task is often challenging in clinical practice. We hypothesize that F-wave assessment might be helpful, since it is able to detect subtle signs of motor involvement, which are found in SP and SM, but not in SN.

Objective The aim of the present study was to determine whether F-waves are useful to distinguish SN from SP and SM.

Methods We selected 21 patients with SP (12 diabetes mellitus, 4 transthyretin familial amyloid polyneuropathy, 4 others), 22 with SM (22 leprosy), and 26 with SN (13 immune-mediated, 10 idiopathic, 3 others) according to clinical-electrophysiological-etiological criteria. For every subject, we collected data on height and performed 20 supramaximal distal stimuli in median, ulnar, peroneal, and tibial nerves, bilaterally, to record F-waves. Latencies (minimum and mean) and persistences were compared across groups using the Kruskal-Wallis and Bonferroni tests. P-values < 0.05 were considered significant.

Results All groups were age, gender, and height-matched. Overall, there were no significant between-group differences regarding F-wave latencies. In contrast, F-wave persistence was able to stratify the groups. Peroneal F-wave persistence was higher, bilaterally, in the SN group compared to SM and SP (p < 0.05). In addition, F-waves persistence of the ulnar and tibial nerves was also helpful to separate SN from SP (p < 0.05).

Conclusion F-wave persistence of the peroneal nerves might be an additional and useful diagnostic tool to differentiate peripheral sensory syndromes.

Resumo

Antecedentes A distinção entre neuronopatias sensitivas (SN) e polineuropatias sensitivas (SP) e multineuropatias sensitivas (SM) é importante para a investigação etiológica e para o prognóstico. Contudo, esta tarefa é desafiadora na prática clínica. Hipotetizou-se que a avaliação das ondas-F pode ser útil, por ser capaz de detectar envolvimento motor nas SP e SM, mas não nas SN.

Objetivo Determinar se as ondas-F podem ajudar a distinguir entre SN, SP e SM.

Métodos Selecionou-se 21 pacientes com SP (12 diabetes mellitus, 4 ATTR-FAP e 4 com outras neuropatias), 22 com SM (22 hanseníases) e 26 com SN (13 imunomediadas, 10 idiopáticas e 3 com outras neuronopatias), de acordo com critérios clínicos, etiológicos e eletrofisiológicos. Para cada indivíduo, foi aferida a altura e foram aplicados 20 estímulos distais supramáximos nos nervos mediano, ulnar, fibular e tibial, bilateralmente, para registrar as ondas-F. Uma comparação foi feita, por grupo, das latências (mínimas e médias) e persistências pelos testes Kruskal-Wallis e Bonferroni. Valores de p < 0.05 foram considerados estatisticamente significativos.

Resultados Todos os grupos foram pareados por idade, sexo e altura. Não houve diferença estatística significativa entre os grupos quanto às latências das ondas-F. A persistência da onda-F foi capaz de estratificar os grupos, sendo as dos nervos fibulares bilateralmente maiores no grupo SN que nos grupos SM e SP (p < 0.05). Adicionalmente, a persistência das ondas-F dos nervos ulnares e tibiais também foi útil para distinguir SN de SP (p < 0.05).

Conclusão A persistência das ondas-F dos nervos fibulares pode ser uma ferramenta adicional e útil para diferenciar síndromes sensitivas periféricas.

Keywords

Nerve Conduction Studies - Polyneuropathies - Mononeuropathies - Hereditary Sensory and Autonomic Neuropathies

Palavras-chave

Estudos de Condução Nervosa - Polineuropatias - Mononeuropatias - Neuropatias Hereditárias Sensoriais e Autônomas

Authors' Contributions

FDL, ARMM, GSS, MCFJ: wrote the manuscript; FDL, ARMM, GSS, MCFJ: interpreted and analyzed data; FDL, ARMM, MCFJ: designed the research methodology; FDL, ARMM: both authors contributed equally to this article and should be considered co-first authors. All authors performed research, reviewed, and edited the final manuscript.

Support

This study was funded by the São Paulo Research Foundation, (Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP - grants 2013/01766-7 and 13/26410-0).

Publication History

Received: 08 March 2023

Accepted: 12 May 2023

Article published online:
04 October 2023

• References

• 1 Gwathmey KG, Pearson KT. Diagnosis and management of sensory polyneuropathy. BMJ 2019; 365: l1108
• 2 Santos DFD, Mendonça MR, Antunes DE. et al. Revisiting primary neural leprosy: Clinical, serological, molecular, and neurophysiological aspects. PLoS Negl Trop Dis 2017; 11 (11) e0006086
• 3 Damasceno A, França Jr MC, Nucci A. Chronic acquired sensory neuron diseases. Eur J Neurol 2008; 15 (12) 1400-1405
• 4 Creigh PD, Mountain J, Sowden JE. et al. Measuring peripheral nerve involvement in Friedreich's ataxia. Ann Clin Transl Neurol 2019; 6 (09) 1718-1727
• 5 França Jr MC, D'abreu A, Nucci A, Cendes F, Lopes-Cendes I. Prospective study of peripheral neuropathy in Machado-Joseph disease. Muscle Nerve 2009; 40 (06) 1012-1018
• 6 Currò R, Salvalaggio A, Tozza S. et al. RFC1 expansions are a common cause of idiopathic sensory neuropathy. Brain 2021; 144 (05) 1542-1550
• 7 Antoine JC, Robert-Varvat F, Maisonobe T. et al; French Neuromuscular Network FILNEMUS. Identifying a therapeutic window in acute and subacute inflammatory sensory neuronopathies. J Neurol Sci 2016; 361: 187-191
• 8 Garcia RU, Ricardo JAG, Horta CA, Garibaldi SG, Nucci A, França Jr MC. Ulnar sensory-motor amplitude ratio: a new tool to differentiate ganglionopathy from polyneuropathy. Arq Neuropsiquiatr 2013; 71 (07) 465-469
• 9 Zhu DQ, Zhu Y, Qiao K. et al. Proximally evoked soleus H-reflex to S1 nerve root stimulation in sensory neuronopathies (ganglionopathies). Muscle Nerve 2013; 48 (05) 814-816
• 10 Zis P, Hadjivassiliou M, Sarrigiannis PG, Barker ASJE, Rao DG. Rapid neurophysiological screening for sensory ganglionopathy: A novel approach. Brain Behav 2017; 7 (12) e00880
• 11 Rutkove SB, Kothari MJ, Raynor EM, Levy ML, Fadic R, Nardin RA. Sural/radial amplitude ratio in the diagnosis of mild axonal polyneuropathy. Muscle Nerve 1997; 20 (10) 1236-1241
• 12 Overbeek BUH, van Alfen N, Bor JA, Zwarts MJ. Sural/radial nerve amplitude ratio: reference values in healthy subjects. Muscle Nerve 2005; 32 (05) 613-618
• 13 Nobrega JAMI, Pinheiro DS, Manzano GM, Kimura J. Various aspects of F-wave values in a healthy population. Clin Neurophysiol 2004; 115 (10) 2336-2342
• 14 Mesrati F, Vecchierini MF. F-waves: neurophysiology and clinical value. Neurophysiol Clin 2004; 34 (05) 217-243
• 15 Pastore C, Izura V, Geijo-Barrientos E, Dominguez JR. A comparison of electrophysiological tests for the early diagnosis of diabetic neuropathy. Muscle Nerve 1999; 22 (12) 1667-1673
• 16 Jerath NU, Aul E, Reddy CG, Azadeh H, Swenson A, Kimura J. Prolongation of F-wave minimal latency: a sensitive predictor of polyneuropathy. Int J Neurosci 2016; 126 (06) 520-525
• 17 Kohara N, Kimura J, Kaji R. et al. F-wave latency serves as the most reproducible measure in nerve conduction studies of diabetic polyneuropathy: multicentre analysis in healthy subjects and patients with diabetic polyneuropathy. Diabetologia 2000; 43 (07) 915-921
• 18 Camdessanché JP, Jousserand G, Ferraud K. et al. The pattern and diagnostic criteria of sensory neuronopathy: a case-control study. Brain 2009; 132 (Pt 7): 1723-1733
• 19 Preston DC, Shapiro BE. Electromyography and Neuromuscular Disorders: Clinical-Electrophysiologic Correlations. 3th ed. New York: Elsevier Saunders; 2012
• 20 Fisher MA. AAEM Minimonograph #13: H reflexes and F waves: physiology and clinical indications. Muscle Nerve 1992; 15 (11) 1223-1233
• 21 Martinez ARM, Casseb RF, Martins Jr CR, Nucci A, França Jr MC. Sensory neuronopathy heralding human T cell lymphotropic virus type I myelopathy. J Neurovirol 2018; 24 (03) 369-371
• 22 Garbino JA, Heise CO, Marques Jr W. Assessing nerves in leprosy. Clin Dermatol 2016; 34 (01) 51-58
• 23 Smith WC, van Brakel W, Gillis T, Saunderson P, Richardus JH. The missing millions: a threat to the elimination of leprosy. PLoS Negl Trop Dis 2015; 9 (04) e0003658
• 24 Jusić A, Baraba R, Bogunović A. H-reflex and F-wave potentials in leg and arm muscles. Electromyogr Clin Neurophysiol 1995; 35 (08) 471-478
• 25 Martinez ARM, Nunes MB, Nucci A, França Jr MC. Sensory neuronopathy and autoimmune diseases. Autoimmune Dis 2012; 2012: 873587
• 26 Cuppini R, Sartini S, Ambrogini P, Fulgenzi G, Graciotti L. Rat motor neuron plasticity induced by dorsal rhizotomy. Neurosci Lett 1999; 275 (01) 29-32
• 27 Joodaki MR, Olyaei GR, Bagheri H. The effects of electrical nerve stimulation of the lower extremity on H-reflex and F-wave parameters. Electromyogr Clin Neurophysiol 2001; 41 (01) 23-28
• 28 Pourmemari MH, Shiri R. Diabetes as a risk factor for carpal tunnel syndrome: a systematic review and meta-analysis. Diabet Med 2016; 33 (01) 10-16
• 29 Conceição I, González-Duarte A, Obici L. et al. “Red-flag” symptom clusters in transthyretin familial amyloid polyneuropathy. J Peripher Nerv Syst 2016; 21 (01) 5-9
• 30 Oh SJ, Joy JL, Kuruoglu R. “Chronic sensory demyelinating neuropathy”: chronic inflammatory demyelinating polyneuropathy presenting as a pure sensory neuropathy. J Neurol Neurosurg Psychiatry 1992; 55 (08) 677-680
• 31 Sinnreich M, Klein CJ, Daube JR, Engelstad J, Spinner RJ, Dyck PJB. Chronic immune sensory polyradiculopathy: a possibly treatable sensory ataxia. Neurology 2004; 63 (09) 1662-1669