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Published in: Experimental Brain Research 2/2012

01-06-2012 | Research Article

Tissue characteristics during temporal summation of pressure-evoked pain

Authors: Sara Finocchietti, Lars Arendt-Nielsen, Thomas Graven-Nielsen

Published in: Experimental Brain Research | Issue 2/2012

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Abstract

Temporal summation due to repeated pain stimulation of deep somatic structures is facilitated in chronic musculoskeletal pain. In this study, the relation between repeated pressure-induced pain and stress/strain distribution within the deep tissue was evaluated to understand whether tissue characteristics may change during repeated stimulation. This information is important for interpret the pain-evoked responses. The muscle pain intensity was recorded on a 10-cm visual analogue scale (VAS) during ten computer-controlled pressure stimulations (3-s interstimulus interval) at pain threshold intensity. The experimental data validated computer models describing the stress/strain time relationship in the deep tissue during pressure stimulation. VAS scores increased progressively with 2.5 ± 0.7 cm during the ten stimuli (P < 0.02) in contrast to the tissue indentation assessed by ultrasound, which was non-significantly changing leading to a mean of 3.4 ± 0.4 mm. The principal stress peaked in the skin was reduced to 16 % in the underlying muscle tissue and not different during the ten stimuli. The peak principal strain in adipose tissue was 0.12; in muscle tissue, it was 0.108 during the first stimulus and increased by 16 % in the tenth stimulus. In a model of a one-stimulus paradigm, it was found that a VAS increase of 2.5 cm required a 47 % increase in muscle strain. These findings show that the increase in muscle strain during repeated pressure stimulations is not sufficient to explain the VAS increase; the temporal summation of deep-tissue pain evoked by repetitive pressure stimulations is not likely to be fully explained by peripheral tissue changes.
Literature
go back to reference Arendt-Nielsen L (1997) Induction and assessment of experimental pain from human skin, muscle, and viscera. in: Proceedings of the 8th World Congress on Pain, IASP Press, Seattle, pp 393–425 Arendt-Nielsen L (1997) Induction and assessment of experimental pain from human skin, muscle, and viscera. in: Proceedings of the 8th World Congress on Pain, IASP Press, Seattle, pp 393–425
go back to reference Arendt-Nielsen L, Brennum J, Sindrup S, Bak P (1994) Electrophysiological and psychophysical quantification of temporal summation in the human nociceptive system. Eur J Appl Physiol Occup Physiol 68:266–273PubMedCrossRef Arendt-Nielsen L, Brennum J, Sindrup S, Bak P (1994) Electrophysiological and psychophysical quantification of temporal summation in the human nociceptive system. Eur J Appl Physiol Occup Physiol 68:266–273PubMedCrossRef
go back to reference Arendt-Nielsen L, Nie H, Laursen MB, Laursen BS, Madeleine P, Simonsen OH, Graven-Nielsen T (2010) Sensitization in patients with painful knee osteoarthritis. Pain 149:573–581 Arendt-Nielsen L, Nie H, Laursen MB, Laursen BS, Madeleine P, Simonsen OH, Graven-Nielsen T (2010) Sensitization in patients with painful knee osteoarthritis. Pain 149:573–581
go back to reference Ashina S, Jensen R, Bendtsen L (2003) Pain sensitivity in pericranial and extracranial regions. Cephalalgia 23:456–462PubMedCrossRef Ashina S, Jensen R, Bendtsen L (2003) Pain sensitivity in pericranial and extracranial regions. Cephalalgia 23:456–462PubMedCrossRef
go back to reference Cua AB, Wilhelm KP, Maibach HI (1990) Elastic properties of human skin: relation to age, sex, and natomical region. Arch Dermatol Res 282:283–288 Cua AB, Wilhelm KP, Maibach HI (1990) Elastic properties of human skin: relation to age, sex, and natomical region. Arch Dermatol Res 282:283–288
go back to reference Diehl B, Hoheisel U, Mense S (1993) The influence of mechanical stimuli and of acetylsalicylic acid on the discharges of slowly conducting afferent units from normal and inflamed muscle in the rat. Exp Brain Res 92:431–440PubMedCrossRef Diehl B, Hoheisel U, Mense S (1993) The influence of mechanical stimuli and of acetylsalicylic acid on the discharges of slowly conducting afferent units from normal and inflamed muscle in the rat. Exp Brain Res 92:431–440PubMedCrossRef
go back to reference Finocchietti S, Nielsen M, Mørch CD, Arendt-Nielsen L, Graven-Nielsen T (2011a) Pressure-induced muscle pain and tissue biomechanics: a computational and experimental study. Eur J Pain 15(1):36–44PubMedCrossRef Finocchietti S, Nielsen M, Mørch CD, Arendt-Nielsen L, Graven-Nielsen T (2011a) Pressure-induced muscle pain and tissue biomechanics: a computational and experimental study. Eur J Pain 15(1):36–44PubMedCrossRef
go back to reference Finocchietti S, Mørch CD, Arendt-Nielsen L, Graven-Nielsen T (2011b) Effects of adipose thickness and muscle hardness on pressure pain sensitivity. Clin J Pain 27:735–745 Finocchietti S, Mørch CD, Arendt-Nielsen L, Graven-Nielsen T (2011b) Effects of adipose thickness and muscle hardness on pressure pain sensitivity. Clin J Pain 27:735–745
go back to reference Gennisson JL, Baldeweck T, Tanter M, Catheline S, Fink M, Sandrin L, Cornillon C, Querleux B (2004) Assessment of elastic parameters of human skin using dynamic elastography. IEEE Trans Ultrason Ferroelect Freq Contr 51(8):80–988CrossRef Gennisson JL, Baldeweck T, Tanter M, Catheline S, Fink M, Sandrin L, Cornillon C, Querleux B (2004) Assessment of elastic parameters of human skin using dynamic elastography. IEEE Trans Ultrason Ferroelect Freq Contr 51(8):80–988CrossRef
go back to reference Graven-Nielsen T, Mense S, Arendt-Nielsen L (2004) Painful and non-painful pressure sensations from human skeletal muscle. Exp Brain Res 159:273–283PubMedCrossRef Graven-Nielsen T, Mense S, Arendt-Nielsen L (2004) Painful and non-painful pressure sensations from human skeletal muscle. Exp Brain Res 159:273–283PubMedCrossRef
go back to reference Johansson T, Meier P, Blickhan R (2000) A finite-element model for the mechanical analysis of skeletal muscles. J Theor Biol 206:131–149PubMedCrossRef Johansson T, Meier P, Blickhan R (2000) A finite-element model for the mechanical analysis of skeletal muscles. J Theor Biol 206:131–149PubMedCrossRef
go back to reference Kauer M, Vuskovic V, Dual J, Szekely G, Bajka M (2002) Inverse finite element characterization of soft tissues. Med Image Anal 6:275–287PubMedCrossRef Kauer M, Vuskovic V, Dual J, Szekely G, Bajka M (2002) Inverse finite element characterization of soft tissues. Med Image Anal 6:275–287PubMedCrossRef
go back to reference Koltzenburg M, Handwerker HO (1994) Differential ability of human cutaneous nociceptors to signal mechanical pain and to produce vasodilatation. J Neurosci 14:1756PubMed Koltzenburg M, Handwerker HO (1994) Differential ability of human cutaneous nociceptors to signal mechanical pain and to produce vasodilatation. J Neurosci 14:1756PubMed
go back to reference Lautenbacher S, Kunz M, Strate P, Nielsen J, Arendt-Nielsen L (2005) Age effects on pain thresholds, temporal summation and spatial summation of heat and pressure pain. Pain 115:410–418PubMedCrossRef Lautenbacher S, Kunz M, Strate P, Nielsen J, Arendt-Nielsen L (2005) Age effects on pain thresholds, temporal summation and spatial summation of heat and pressure pain. Pain 115:410–418PubMedCrossRef
go back to reference Mendell LM (1966) Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 16:316–332PubMedCrossRef Mendell LM (1966) Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 16:316–332PubMedCrossRef
go back to reference Miller K, Chinzei K, Orssengo G, Bednarz P (2000) Mechanical properties of brain tissue in vivo: experiment and computer simulation. J Biomech 33:1369–1376PubMedCrossRef Miller K, Chinzei K, Orssengo G, Bednarz P (2000) Mechanical properties of brain tissue in vivo: experiment and computer simulation. J Biomech 33:1369–1376PubMedCrossRef
go back to reference Nie H, Arendt-Nielsen L, Andersen H, Graven-Nielsen T (2005) Temporal summation of pain evoked by mechanical stimulation in deep and superficial tissue. J Pain 6:348–355PubMedCrossRef Nie H, Arendt-Nielsen L, Andersen H, Graven-Nielsen T (2005) Temporal summation of pain evoked by mechanical stimulation in deep and superficial tissue. J Pain 6:348–355PubMedCrossRef
go back to reference Nie HL, Graven-Nielsen T, Arendt-Nielsen L (2009) Spatial and temporal summation of pain evoked by mechanical pressure stimulation. Eur J Pain 13:592–599PubMedCrossRef Nie HL, Graven-Nielsen T, Arendt-Nielsen L (2009) Spatial and temporal summation of pain evoked by mechanical pressure stimulation. Eur J Pain 13:592–599PubMedCrossRef
go back to reference Nielsen J, Arendt-Nielsen L (1998) The importance of stimulus configuration for temporal summation of first and second pain to repeated heat stimuli. Eur J Pain 2:329–341PubMedCrossRef Nielsen J, Arendt-Nielsen L (1998) The importance of stimulus configuration for temporal summation of first and second pain to repeated heat stimuli. Eur J Pain 2:329–341PubMedCrossRef
go back to reference Noordenbos W (1959) Pain. Problems pertaining to the transmission of nerve impulses which give rise to pain. Elsevier, Amsterdam Noordenbos W (1959) Pain. Problems pertaining to the transmission of nerve impulses which give rise to pain. Elsevier, Amsterdam
go back to reference Price DD (1972) Characteristics of second pain and flexion reflexes indicative of prolonged central summation. Exp Neurol 37:371–387PubMedCrossRef Price DD (1972) Characteristics of second pain and flexion reflexes indicative of prolonged central summation. Exp Neurol 37:371–387PubMedCrossRef
go back to reference Price DD, Bennett GJ, Rafii A (1989) Psychophysical observations on patients with neuropathic pain relieved by a sympathetic block. Pain 36:273–288PubMedCrossRef Price DD, Bennett GJ, Rafii A (1989) Psychophysical observations on patients with neuropathic pain relieved by a sympathetic block. Pain 36:273–288PubMedCrossRef
go back to reference Sarlani E, Greenspan JD (2002) Gender differences in temporal summation of mechanically evoked pain. Pain 97:163–169PubMedCrossRef Sarlani E, Greenspan JD (2002) Gender differences in temporal summation of mechanically evoked pain. Pain 97:163–169PubMedCrossRef
go back to reference Sarlani E, Grace EG, Reynolds MA, Greenspan JD (2004) Sex differences in temporal summation of pain and aftersensations following repetitive noxious mechanical stimulation. Pain 109:115–123PubMedCrossRef Sarlani E, Grace EG, Reynolds MA, Greenspan JD (2004) Sex differences in temporal summation of pain and aftersensations following repetitive noxious mechanical stimulation. Pain 109:115–123PubMedCrossRef
go back to reference Simons DG, Mense S (1998) Understanding and measurement of muscle tone as related to clinical muscle pain. Pain 75:1–17 Simons DG, Mense S (1998) Understanding and measurement of muscle tone as related to clinical muscle pain. Pain 75:1–17
go back to reference Staud R, Vierck CJ, Cannon RL, Mauderli AP, Price DD (2001) Abnormal sensitization and temporal summation of second pain (wind-up) in patients with fibromyalgia syndrome. Pain 91:165–175PubMedCrossRef Staud R, Vierck CJ, Cannon RL, Mauderli AP, Price DD (2001) Abnormal sensitization and temporal summation of second pain (wind-up) in patients with fibromyalgia syndrome. Pain 91:165–175PubMedCrossRef
go back to reference Staud R, Cannon RC, Mauderli AP, Robinson ME, Price DD, Vierck CJ (2003) Temporal summation of pain from mechanical stimulation of muscle tissue in normal controls and subjects with fibromyalgia syndrome. Pain 102:87–95PubMedCrossRef Staud R, Cannon RC, Mauderli AP, Robinson ME, Price DD, Vierck CJ (2003) Temporal summation of pain from mechanical stimulation of muscle tissue in normal controls and subjects with fibromyalgia syndrome. Pain 102:87–95PubMedCrossRef
go back to reference Takahashi K, Taguchi T, Itoh K, Okada K, Kawakita K, Mizumura K (2005) Influence of surface anesthesia on the pressure pain threshold measured with different-sized probes. Somatosens Mot Res 22:299–305PubMedCrossRef Takahashi K, Taguchi T, Itoh K, Okada K, Kawakita K, Mizumura K (2005) Influence of surface anesthesia on the pressure pain threshold measured with different-sized probes. Somatosens Mot Res 22:299–305PubMedCrossRef
go back to reference Torisu T, Wang K, Svensson P, Laat AD, Tanaka M, Shimada A, Ikoma A, Murata H, Arendt-Nielsen L (2010) Effects of eccentric jaw exercise on temporal summation in jaw-closing muscles of healthy subjects. Eur J Pain 14:719–724PubMedCrossRef Torisu T, Wang K, Svensson P, Laat AD, Tanaka M, Shimada A, Ikoma A, Murata H, Arendt-Nielsen L (2010) Effects of eccentric jaw exercise on temporal summation in jaw-closing muscles of healthy subjects. Eur J Pain 14:719–724PubMedCrossRef
go back to reference Tran HV, Charleux F, Rachik M, Ehrlacher A, Tho MC (2007) In vivo characterization of the mechanical properties of human skin derived from MRI and indentation techniques. Comput Methods Biomech Biomed Eng 10:401–407CrossRef Tran HV, Charleux F, Rachik M, Ehrlacher A, Tho MC (2007) In vivo characterization of the mechanical properties of human skin derived from MRI and indentation techniques. Comput Methods Biomech Biomed Eng 10:401–407CrossRef
go back to reference Treede RD, Rolke R, Andrews K, Magerl W (2002) Pain elicited by blunt pressure: neurobiological basis and clinical relevance. Pain 98:235–240 (Amsterdam)PubMedCrossRef Treede RD, Rolke R, Andrews K, Magerl W (2002) Pain elicited by blunt pressure: neurobiological basis and clinical relevance. Pain 98:235–240 (Amsterdam)PubMedCrossRef
go back to reference Vierck CJ Jr, Cannon RL, Fry G, Maixner W, Whitsel BL (1997) Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. J Neurophysiol 78:992PubMed Vierck CJ Jr, Cannon RL, Fry G, Maixner W, Whitsel BL (1997) Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. J Neurophysiol 78:992PubMed
go back to reference Wall PD, Woolf CJ (1984) Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat. J Physiol 356:443–458PubMed Wall PD, Woolf CJ (1984) Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat. J Physiol 356:443–458PubMed
go back to reference Woolf CJ, Thompson SWN (1991) The induction and maintenance of central sensitization is dependent on N-methyl-d-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain 44:293–299PubMedCrossRef Woolf CJ, Thompson SWN (1991) The induction and maintenance of central sensitization is dependent on N-methyl-d-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain 44:293–299PubMedCrossRef
go back to reference Wright A, Graven-Nielsen T, Davies I, Arendt-Nielsen L (2002) Temporal summation of pain from skin, muscle and joint following nociceptive ultrasonic stimulation in humans. Exp Brain Res 144:475–482PubMedCrossRef Wright A, Graven-Nielsen T, Davies I, Arendt-Nielsen L (2002) Temporal summation of pain from skin, muscle and joint following nociceptive ultrasonic stimulation in humans. Exp Brain Res 144:475–482PubMedCrossRef
Metadata
Title
Tissue characteristics during temporal summation of pressure-evoked pain
Authors
Sara Finocchietti
Lars Arendt-Nielsen
Thomas Graven-Nielsen
Publication date
01-06-2012
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 2/2012
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-012-3085-9

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