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Published in: Clinical Oral Investigations 8/2017

01-11-2017 | Original Article

Reliability of the nociceptive blink reflex evoked by electrical stimulation of the trigeminal nerve in humans

Authors: Yuri Martins Costa, Lene Baad-Hansen, Leonardo Rigoldi Bonjardim, Paulo César Rodrigues Conti, Peter Svensson

Published in: Clinical Oral Investigations | Issue 8/2017

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Abstract

Objective

The nociceptive blink reflex (nBR) can be useful to investigate trigeminal nociceptive function. The aim of this study was to estimate the reliability of the nBR evoked by electrical stimulation of the three branches of the trigeminal nerve under the following conditions: over time (test-retest and intrarater reliability) and by two examiners (interrater reliability).

Materials and methods

Twenty-one healthy participants were evaluated in two sessions (24 h apart). The nBR was elicited by a so-called “nociceptive-specific” electrode placed over the entry zone of the right supraorbital (V1R), infraorbital (V2R), mental (V3R), and left infraorbital (V2L) nerve. The outcomes were individual electrical sensory (I 0) and pain thresholds (I P); root mean square (RMS), area-under-the-curve (AUC), and onset latencies of R2 responses (determined twice after a recalibration session); and stimulus-evoked pain on a 0–10 numerical rating scale. Intraclass correlation coefficients (ICCs) and Kappa statistics were computed (α = 5%).

Results

ICCs were fair to excellent in 82% of the psychophysical measures (fair 21%, good 31%, excellent 30%) and in 86% of V1R, V2R, and V2L nBR parameters, whereas 52% of V3R showed poor reliability. ICCs for intrarater reliability were fair to good in 70% of measurements (fair 20%, good 50%) and in 75% of interrater measurements after the recalibration (fair 55%, good 20%). All kappa values showed at least fair agreement and the majority of the nBR measures (93%) presented moderate to excellent reliability.

Conclusion

The nBR and its associated psychophysical measures can be considered a sufficiently reliable test.

Clinical significance

The nBR can be recommended as an electrophysiological technique to assess trigeminal nociceptive function.
Literature
1.
go back to reference Backonja MM, Attal N, Baron R, Bouhassira D, Drangholt M, Dyck PJ, Edwards RR, Freeman R, Gracely R, Haanpaa MH, Hansson P, Hatem SM, Krumova EK, Jensen TS, Maier C, Mick G, Rice AS, Rolke R, Treede RD, Serra J, Toelle T, Tugnoli V, Walk D, Walalce MS, Ware M, Yarnitsky D, Ziegler D (2013) Value of quantitative sensory testing in neurological and pain disorders: NeuPSIG consensus. Pain 154:1807–1819CrossRefPubMed Backonja MM, Attal N, Baron R, Bouhassira D, Drangholt M, Dyck PJ, Edwards RR, Freeman R, Gracely R, Haanpaa MH, Hansson P, Hatem SM, Krumova EK, Jensen TS, Maier C, Mick G, Rice AS, Rolke R, Treede RD, Serra J, Toelle T, Tugnoli V, Walk D, Walalce MS, Ware M, Yarnitsky D, Ziegler D (2013) Value of quantitative sensory testing in neurological and pain disorders: NeuPSIG consensus. Pain 154:1807–1819CrossRefPubMed
2.
go back to reference Kersten P, White PJ, Tennant A (2014) Is the pain visual analogue scale linear and responsive to change? An exploration using Rasch analysis. PLoS One 9:e99485CrossRefPubMedPubMedCentral Kersten P, White PJ, Tennant A (2014) Is the pain visual analogue scale linear and responsive to change? An exploration using Rasch analysis. PLoS One 9:e99485CrossRefPubMedPubMedCentral
4.
go back to reference Kimura J (1989) The blink reflex. In: Kimura J (ed) Book title, 3rd edn. Oxford University Press, New York Kimura J (1989) The blink reflex. In: Kimura J (ed) Book title, 3rd edn. Oxford University Press, New York
6.
go back to reference Ellrich J, Hopf HC (1996) The R3 component of the blink reflex: normative data and application in spinal lesions. Electroencephalogr Clin Neurophysiol 101:349–354CrossRefPubMed Ellrich J, Hopf HC (1996) The R3 component of the blink reflex: normative data and application in spinal lesions. Electroencephalogr Clin Neurophysiol 101:349–354CrossRefPubMed
7.
go back to reference Ellrich J (2000) Brain stem reflexes: probing human trigeminal nociception. News Physiol Sci 15:94–97PubMed Ellrich J (2000) Brain stem reflexes: probing human trigeminal nociception. News Physiol Sci 15:94–97PubMed
8.
go back to reference Kaube H, Katsarava Z, Kaufer T, Diener H, Ellrich J (2000) A new method to increase nociception specificity of the human blink reflex. Clin Neurophysiol 111:413–416CrossRefPubMed Kaube H, Katsarava Z, Kaufer T, Diener H, Ellrich J (2000) A new method to increase nociception specificity of the human blink reflex. Clin Neurophysiol 111:413–416CrossRefPubMed
9.
go back to reference de Tommaso M (2013) Reply to "Activating selectively and reliably nociceptive afferents with concentric electrode stimulation: yes we can! Provided that low stimulus intensities are used!". Clin Neurophysiol 124:424–425CrossRefPubMed de Tommaso M (2013) Reply to "Activating selectively and reliably nociceptive afferents with concentric electrode stimulation: yes we can! Provided that low stimulus intensities are used!". Clin Neurophysiol 124:424–425CrossRefPubMed
10.
go back to reference de Tommaso M, Santostasi R, Devitofrancesco V, Franco G, Vecchio E, Delussi M, Livrea P, Katzarava Z (2011) A comparative study of cortical responses evoked by transcutaneous electrical vs CO(2) laser stimulation. Clin Neurophysiol 122:2482–2487CrossRefPubMed de Tommaso M, Santostasi R, Devitofrancesco V, Franco G, Vecchio E, Delussi M, Livrea P, Katzarava Z (2011) A comparative study of cortical responses evoked by transcutaneous electrical vs CO(2) laser stimulation. Clin Neurophysiol 122:2482–2487CrossRefPubMed
11.
go back to reference Perchet C, Frot M, Charmarty A, Flores C, Mazza S, Magnin M, Garcia-Larrea L (2012) Do we activate specifically somatosensory thin fibres with the concentric planar electrode? A scalp and intracranial EEG study. Pain 153:1244–1252CrossRefPubMed Perchet C, Frot M, Charmarty A, Flores C, Mazza S, Magnin M, Garcia-Larrea L (2012) Do we activate specifically somatosensory thin fibres with the concentric planar electrode? A scalp and intracranial EEG study. Pain 153:1244–1252CrossRefPubMed
12.
go back to reference Rehberg B, Baars JH, Kotsch J, Koppe P, von Dincklage F (2012) Comparison of trigeminal and spinal modulation of pain and nociception. Int J Neurosci 122:298–304CrossRefPubMed Rehberg B, Baars JH, Kotsch J, Koppe P, von Dincklage F (2012) Comparison of trigeminal and spinal modulation of pain and nociception. Int J Neurosci 122:298–304CrossRefPubMed
13.
go back to reference Giffin NJ, Kowacs F, Libri V, Williams P, Goadsby PJ, Kaube H (2003) Effect of the adenosine A1 receptor agonist GR79236 on trigeminal nociception with blink reflex recordings in healthy human subjects. Cephalalgia 23:287–292CrossRefPubMed Giffin NJ, Kowacs F, Libri V, Williams P, Goadsby PJ, Kaube H (2003) Effect of the adenosine A1 receptor agonist GR79236 on trigeminal nociception with blink reflex recordings in healthy human subjects. Cephalalgia 23:287–292CrossRefPubMed
14.
go back to reference Baad-Hansen L, List T, Jensen TS, Leijon G, Svensson P (2005) Blink reflexes in patients with atypical odontalgia. J Orofac Pain 19:239–247PubMed Baad-Hansen L, List T, Jensen TS, Leijon G, Svensson P (2005) Blink reflexes in patients with atypical odontalgia. J Orofac Pain 19:239–247PubMed
15.
go back to reference Baad-Hansen L, List T, Kaube H, Jensen TS, Svensson P (2006) Blink reflexes in patients with atypical odontalgia and matched healthy controls. Exp Brain Res 172:498–506CrossRefPubMed Baad-Hansen L, List T, Kaube H, Jensen TS, Svensson P (2006) Blink reflexes in patients with atypical odontalgia and matched healthy controls. Exp Brain Res 172:498–506CrossRefPubMed
16.
go back to reference Kaube H, Katsarava Z, Przywara S, Drepper J, Ellrich J, Diener HC (2002) Acute migraine headache: possible sensitization of neurons in the spinal trigeminal nucleus? Neurology 58:1234–1238CrossRefPubMed Kaube H, Katsarava Z, Przywara S, Drepper J, Ellrich J, Diener HC (2002) Acute migraine headache: possible sensitization of neurons in the spinal trigeminal nucleus? Neurology 58:1234–1238CrossRefPubMed
17.
go back to reference Peddireddy A, Wang K, Svensson P, Arendt-Nielsen L (2009) Blink reflexes in chronic tension-type headache patients and healthy controls. Clin Neurophysiol 120:1711–1716CrossRefPubMed Peddireddy A, Wang K, Svensson P, Arendt-Nielsen L (2009) Blink reflexes in chronic tension-type headache patients and healthy controls. Clin Neurophysiol 120:1711–1716CrossRefPubMed
18.
19.
go back to reference Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, Bouter LM, de Vet HC (2010) The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol 63:737–745CrossRefPubMed Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, Bouter LM, de Vet HC (2010) The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol 63:737–745CrossRefPubMed
20.
go back to reference Katsarava Z, Ellrich J, Diener HC, Kaube H (2002) Optimized stimulation and recording parameters of human 'nociception specific' blink reflex recordings. Clin Neurophysiol 113:1932–1936CrossRefPubMed Katsarava Z, Ellrich J, Diener HC, Kaube H (2002) Optimized stimulation and recording parameters of human 'nociception specific' blink reflex recordings. Clin Neurophysiol 113:1932–1936CrossRefPubMed
21.
go back to reference von Dincklage F, Koppe P, Kotsch J, Baars JH, Rehberg B (2010) Investigation of threshold and magnitude criteria of the nociceptive blink reflex. Clin Neurophysiol 121:945–949CrossRef von Dincklage F, Koppe P, Kotsch J, Baars JH, Rehberg B (2010) Investigation of threshold and magnitude criteria of the nociceptive blink reflex. Clin Neurophysiol 121:945–949CrossRef
22.
go back to reference Blumenthal TD, Cuthbert BN, Filion DL, Hackley S, Lipp OV, van Boxtel A (2005) Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 42:1–15CrossRefPubMed Blumenthal TD, Cuthbert BN, Filion DL, Hackley S, Lipp OV, van Boxtel A (2005) Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 42:1–15CrossRefPubMed
23.
go back to reference Ellrich J, Treede RD (1998) Characterization of blink reflex interneurons by activation of diffuse noxious inhibitory controls in man. Brain Res 803:161–168CrossRefPubMed Ellrich J, Treede RD (1998) Characterization of blink reflex interneurons by activation of diffuse noxious inhibitory controls in man. Brain Res 803:161–168CrossRefPubMed
24.
go back to reference Rosner B (2006) Fundementals of biostatistics. Thomson Brooks/Cole, Duxbury Rosner B (2006) Fundementals of biostatistics. Thomson Brooks/Cole, Duxbury
25.
go back to reference Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRefPubMed Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRefPubMed
26.
go back to reference Mouraux A, Iannetti GD, Plaghki L (2010) Low intensity intra-epidermal electrical stimulation can activate Adelta-nociceptors selectively. Pain 150:199–207CrossRefPubMed Mouraux A, Iannetti GD, Plaghki L (2010) Low intensity intra-epidermal electrical stimulation can activate Adelta-nociceptors selectively. Pain 150:199–207CrossRefPubMed
27.
go back to reference Romaniello A, Valls-Sole J, Iannetti GD, Truini A, Manfredi M, Cruccu G (2002) Nociceptive quality of the laser-evoked blink reflex in humans. J Neurophysiol 87:1386–1394CrossRefPubMed Romaniello A, Valls-Sole J, Iannetti GD, Truini A, Manfredi M, Cruccu G (2002) Nociceptive quality of the laser-evoked blink reflex in humans. J Neurophysiol 87:1386–1394CrossRefPubMed
28.
go back to reference Jaaskelainen SK (1995) Electrophysiological study of blink reflex in humans: differences in mental and supraorbital nerves. Acta Physiol Scand 154:143–150CrossRefPubMed Jaaskelainen SK (1995) Electrophysiological study of blink reflex in humans: differences in mental and supraorbital nerves. Acta Physiol Scand 154:143–150CrossRefPubMed
29.
go back to reference Jaaskelainen SK (1995) Blink reflex with stimulation of the mental nerve. Methodology, reference values, and some clinical vignettes. Acta Neurol Scand 91:477–482CrossRefPubMed Jaaskelainen SK (1995) Blink reflex with stimulation of the mental nerve. Methodology, reference values, and some clinical vignettes. Acta Neurol Scand 91:477–482CrossRefPubMed
30.
go back to reference Cruccu G, Sommer C, Anand P, Attal N, Baron R, Garcia-Larrea L, Haanpaa M, Jensen TS, Serra J, Treede RD (2010) EFNS guidelines on neuropathic pain assessment: revised 2009. Eur J Neurol 17:1010–1018CrossRefPubMed Cruccu G, Sommer C, Anand P, Attal N, Baron R, Garcia-Larrea L, Haanpaa M, Jensen TS, Serra J, Treede RD (2010) EFNS guidelines on neuropathic pain assessment: revised 2009. Eur J Neurol 17:1010–1018CrossRefPubMed
31.
go back to reference Ongerboer de Visser BW, Moffie D (1979) Effects of brain-stem and thalamic lesions on the corneal reflex: an electrophysiological and anatomical study. Brain 102:595–608CrossRefPubMed Ongerboer de Visser BW, Moffie D (1979) Effects of brain-stem and thalamic lesions on the corneal reflex: an electrophysiological and anatomical study. Brain 102:595–608CrossRefPubMed
32.
go back to reference de Vet HCT, Terwee CB, Mokkink LB, Knol DK (2011) Measurement in medicine: a practical guide. Cambridge University Press, SuffolkCrossRef de Vet HCT, Terwee CB, Mokkink LB, Knol DK (2011) Measurement in medicine: a practical guide. Cambridge University Press, SuffolkCrossRef
33.
go back to reference Forssell H, Jaaskelainen S, Tenovuo O, Hinkka S (2002) Sensory dysfunction in burning mouth syndrome. Pain 99:41–47CrossRefPubMed Forssell H, Jaaskelainen S, Tenovuo O, Hinkka S (2002) Sensory dysfunction in burning mouth syndrome. Pain 99:41–47CrossRefPubMed
34.
go back to reference Forssell H, Tenovuo O, Silvoniemi P, Jaaskelainen SK (2007) Differences and similarities between atypical facial pain and trigeminal neuropathic pain. Neurology 69:1451–1459CrossRefPubMed Forssell H, Tenovuo O, Silvoniemi P, Jaaskelainen SK (2007) Differences and similarities between atypical facial pain and trigeminal neuropathic pain. Neurology 69:1451–1459CrossRefPubMed
35.
go back to reference Teerijoki-Oksa T, Jaaskelainen SK, Forssell K, Forssell H (2004) Recovery of nerve injury after mandibular sagittal split osteotomy. Diagnostic value of clinical and electrophysiologic tests in the follow-up. Int J Oral Maxillofac Surg 33:134–140CrossRefPubMed Teerijoki-Oksa T, Jaaskelainen SK, Forssell K, Forssell H (2004) Recovery of nerve injury after mandibular sagittal split osteotomy. Diagnostic value of clinical and electrophysiologic tests in the follow-up. Int J Oral Maxillofac Surg 33:134–140CrossRefPubMed
36.
go back to reference Topka H, Hallett M (1992) Perioral reflexes in orofacial dyskinesia and spasmodic dysphonia. Muscle Nerve 15:1016–1022CrossRefPubMed Topka H, Hallett M (1992) Perioral reflexes in orofacial dyskinesia and spasmodic dysphonia. Muscle Nerve 15:1016–1022CrossRefPubMed
37.
go back to reference Baad-Hansen L, Pigg M, Yang G, List T, Svensson P, Drangsholt M (2015) Reliability of intra-oral quantitative sensory testing (QST) in patients with atypical odontalgia and healthy controls—a multicentre study. J Oral Rehabil 42:127–135CrossRefPubMed Baad-Hansen L, Pigg M, Yang G, List T, Svensson P, Drangsholt M (2015) Reliability of intra-oral quantitative sensory testing (QST) in patients with atypical odontalgia and healthy controls—a multicentre study. J Oral Rehabil 42:127–135CrossRefPubMed
38.
go back to reference Pigg M, Baad-Hansen L, Svensson P, Drangsholt M, List T (2010) Reliability of intraoral quantitative sensory testing (QST). Pain 148:220–226CrossRefPubMed Pigg M, Baad-Hansen L, Svensson P, Drangsholt M, List T (2010) Reliability of intraoral quantitative sensory testing (QST). Pain 148:220–226CrossRefPubMed
39.
go back to reference Rolke R, Baron R, Maier C, Tolle TR, Treede RD, Beyer A, Binder A, Birbaumer N, Birklein F, Botefur IC, Braune S, Flor H, Huge V, Klug R, Landwehrmeyer GB, Magerl W, Maihofner C, Rolko C, Schaub C, Scherens A, Sprenger T, Valet M, Wasserka B (2006) Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): standardized protocol and reference values. Pain 123:231–243CrossRefPubMed Rolke R, Baron R, Maier C, Tolle TR, Treede RD, Beyer A, Binder A, Birbaumer N, Birklein F, Botefur IC, Braune S, Flor H, Huge V, Klug R, Landwehrmeyer GB, Magerl W, Maihofner C, Rolko C, Schaub C, Scherens A, Sprenger T, Valet M, Wasserka B (2006) Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): standardized protocol and reference values. Pain 123:231–243CrossRefPubMed
40.
go back to reference Kottner J, Audige L, Brorson S, Donner A, Gajewski BJ, Hrobjartsson A, Roberts C, Shoukri M, Streiner DL (2011) Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. J Clin Epidemiol 64:96–106CrossRefPubMed Kottner J, Audige L, Brorson S, Donner A, Gajewski BJ, Hrobjartsson A, Roberts C, Shoukri M, Streiner DL (2011) Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. J Clin Epidemiol 64:96–106CrossRefPubMed
41.
go back to reference Giffin NJ, Katsarava Z, Pfundstein A, Ellrich J, Kaube H (2004) The effect of multiple stimuli on the modulation of the 'nociceptive' blink reflex. Pain 108:124–128CrossRefPubMed Giffin NJ, Katsarava Z, Pfundstein A, Ellrich J, Kaube H (2004) The effect of multiple stimuli on the modulation of the 'nociceptive' blink reflex. Pain 108:124–128CrossRefPubMed
42.
go back to reference Jaaskelainen SK, Forssell H, Tenovuo O (1999) Electrophysiological testing of the trigeminofacial system: aid in the diagnosis of atypical facial pain. Pain 80:191–200CrossRefPubMed Jaaskelainen SK, Forssell H, Tenovuo O (1999) Electrophysiological testing of the trigeminofacial system: aid in the diagnosis of atypical facial pain. Pain 80:191–200CrossRefPubMed
Metadata
Title
Reliability of the nociceptive blink reflex evoked by electrical stimulation of the trigeminal nerve in humans
Authors
Yuri Martins Costa
Lene Baad-Hansen
Leonardo Rigoldi Bonjardim
Paulo César Rodrigues Conti
Peter Svensson
Publication date
01-11-2017
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 8/2017
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-016-2042-6

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