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1 Cover Page The handle holds various files of this Leiden University dissertation Author: Schilder, Janneke Title: Motor dysfunction in complex regional pain syndrome : studies on objective measures Issue Date:
2 CHAPTER 1 General introduction and aims 9
3 CHAPTER 1 Current understandings in complex regional pain syndrome (CRPS) Clinical characteristics CRPS is characterized by pain in combination with sensory, autonomic, trophic and motor abnormalities. Typically, patients with CRPS present after minor or moderate tissue injury (e.g. a wrist fracture). A distinction is made between CRPS type I, in which there is no evidence of a nerve lesion, and type II, in which there is. In the acute phase, the injured limb is usually extreme painful, red, warm (although sometimes it quickly becomes cold) and swollen [1]. Other features, which are also confined to the injured limb but not to the distribution of a specific nerve or nerve root, include allodynia and hyperalgesia, changes in sweating, changes in hair and nail growth, and muscle weakness [2]. Mechanical and thermal hyperalgesia are frequently present in CRPS [3-5]. As the disorder persists (chronic CRPS), pain does not subside but often spreads, voluntary motor control is reduced in some patients, hyperpathia might occur, and negative sensory signs as hypoesthesia, -algesia, and -thermesthesia can develop [4-5]. Thus, CRPS seems to be characterized by a mixture of noxious sensations (positive symptoms) and sensory loss (negative symptoms) [4]. Over months, the warm limb often becomes cold. Dystonia, tremor, and myoclonus might also develop. Activity of the limb typically exacerbates signs and symptoms. Over time, clinical features spread proximally [7] and can even emerge on the opposite or ipsilateral limb [8,9]. Diagnosis of CRPS The diagnosis of CRPS is made on the basis of clinical criteria. Several diagnostic criteria sets have been developed over time, like those described by Veldman [1], those endorsed by the International Association for the Study of Pain (IASP) [10], and the recently validated Budapest criteria [11]. Although the Budapest criteria have a higher specificity than the IASP criteria [11], the latter will be used in some studies in this thesis as the Budapest criteria were yet to be published and validated when those studies were conducted. 10
4 GENERAL INTRODUCTION AND AIMS The IASP criteria include [10]: 1. The presence of an initiating noxious event or a cause of immobilization 2. Continuing pain, allodynia or hyperalgesia with which the pain is disproportionate to any inciting event 3. Evidence at some time of edema, changes in skin blood flow or abnormal sudomotor activity in the region of the pain 4. Absence of a condition that would otherwise account for the degree of pain and dysfunction For the diagnosis of CRPS, criteria 2-4 must be fulfilled. Epidemiology A recent Dutch population-based study [12] found an estimated overall incidence rate of CRPS of 26.2 per 100,000 person-years (95% CI ), whereas another study from the USA found an incidence rate of 5.5 per 100,000 person-years [13]. However, it should be noted that these incidence rates are based on the IASP (i.e., Merskey & Bogduk) criteria and that the IASP has meanwhile formally accepted the Budapest criteria as the diagnostic standard. The latter are stricter, which indicates that if current diagnostic standards would have been applied, the incidence rate would have been considerably lower. Women are affected 3-4 times more often than men. CRPS may occur at all ages but the highest number is found between years. The arm is affected in about 60% of cases and the leg in about 40% [12]. Resolution rate differs greatly between studies, ranging from 74% in the first year [13] to 36% within 6 years [14]. Pathophysiological mechanisms Our understanding of CRPS has increased substantially in the past decades, which has led to the identification of three major pathophysiological pathways: aberrant inflammatory mechanisms, vasomotor dysfunction and maladaptive neuroplasticity. Aberrant inflammatory mechanisms Similarities between the classical symptoms of inflammation and the clinical features of CRPS (a red, hot, swollen painful limb with reduced function) have led several investigators to suggest that the disease is caused by an exaggerated inflammatory response. Multiple studies have supported this view (see [15] for review). Elevated 11
5 CHAPTER 1 levels of pro-inflammatory (TNF, IL-1,-8) and decreased levels of anti-inflammatory cytokines (IL-4,-10,TGF-β1) were found in serum and blister fluid of affected CRPS extremities [16-18], but these levels were not associated with disease duration or clinical features. An exception involved mechanical hyperalgesia which showed a significant relation with TNF-α [20]. Other post-traumatic inflammatory mediators of importance are the neuropeptides calcitonin-gene-related peptide (CGRP) and substance P, which were higher in CRPS patients serum than in the serum of healthy controls [21,22]. Elevated CGRP is probably responsible for the augmented flare response in CRPS patients [23,24] while substance P contributes to the increased protein extravasation in the affected CRPS limb [25] and stimulates keratinocytes to express cytokines [26,27]. These results indicate that neurogenic inflammation plays an important role in CRPS. However, the way in which the immune and nervous systems interact is still not fully understood and warrants further research. Vasomotor dysfunction Vascular disturbances in the distal part of the affected extremity are an important clinical feature of CRPS. Primarily small vessels are affected leading to microvascular disturbances, with an impact on microcirculation, skin temperature, and clinical appearance of the limb. In the acute stage the affected side is often warmer resulting from vasodilatation, induced by a profound central unilateral functional inhibition of sympathetic vasoconstrictor neurons [28-30], and the peripherally induced neurogenic inflammation via nociceptive C-fibers. During the chronic phase, vasoconstriction may be a dominant feature of the clinical phenotype and the affected limb becomes colder and bluish. This vasoconstriction is likely induced by changes in the microcirculation itself, such as endothelial dysfunction (decreased nitrous oxide and increased endothelin-1 release) [17,31,32] or vascular hyperreactivity (increased density of α-adrenergic receptors in the skin), while sympathetic vasoconstrictor activity returns [28,33]. However, not all CRPS cases pass through these different stages that are defined by skin temperature. About 20-30% of patients with CRPS have the cold type from the start [34,35]. Maladaptive neuroplasticity In patients with chronic pain, it is known that the central nervous system undergoes functional and structural changes that play a key role in the maintenance of pain, a phenomenon called central sensitization [36]. Central sensitization is associated with 12
6 GENERAL INTRODUCTION AND AIMS disinhibition of sensory circuits leading to spontaneous pain, allodynia, and hyperalgesia, and is an important feature in CRPS [37]. Disinhibition has been demonstrated on different levels of the nervous system in CRPS patients, ranging from the spinal cord [38] to the cerebral cortex [39,40], and is thought to be an important factor in the motor disturbances found in CRPS. It has been shown that lack of central inhibition plays a key role in the pathophysiology of dystonia [41], which is the most prevalent movement disorder in CRPS [42]. In addition, altered processing of noxious and tactile input has also been regarded important in the development of dystonia in CRPS [42]. Widespread changes in sensory and motor cortical areas and cerebral function have been demonstrated [40,43-59]. However, the exact role of these changes in the pathophysiology of CRPS has not been elucidated. Aims of this thesis The general objective of this thesis is to study peripheral and central factors that may contribute to the development of motor dysfunction in CRPS. Specifically, this thesis has the following four major aims: 1. To apply kinematic analysis in the evaluation of motor control in CRPS patients (Chapter 3) and study the role of pain on motor dysfunction in these patients (Chapter 4). 2. To evaluate the muscles responsiveness to botulinum toxin type A to gain insight in pathophysiological factors which may play a role in the motor dysfunction of chronic CRPS (Chapter 5). 3. To evaluate the circadian skin temperature profile to gain insight in pathophysiological factors which may play a role in the motor dysfunction of chronic CRPS (Chapter 6). 4. To investigate the origin and change in meaning over time of three terms (akinesia, bradykinesia, and hypokinesia) that are frequently used to describe motor dysfunction (Chapter 2). A general discussion of the results is provided in Chapter 7. 13
7 CHAPTER 1 References 1. Veldman PH, Reynen HM, Arntz IE, Goris RJ. Signs and symptoms of reflex sympathetic dystrophy: prospective study of 829 patients. Lancet 1993;342(8878): Marinus J, Moseley GL, Birklein F, Baron R, Maihöfner C, Kingery WS, Van Hilten JJ Clinical features and pathophysiology of complex regional pain syndrome. Lancet Neurol 2011;10(7): Sethna NF, Meier PM, Zurakowski D, Berde CB. Cutaneous sensory abnormalities in children and adolescents with complex regional pain syndromes. Pain 2007;131: Drummond PD. Sensory disturbances in complex regional pain syndrome: clinical observations, autonomic interactions, and possible mechanisms. Pain Med 2010;11: Maier C, Baron R, Tölle TR, Binder A, Birbaumer N, Birklein F, Gierthmühlen J, Flor H, Geber C, Huge V, Krumova EK, Landwehrmeyer GB, Magerl W, Maihöfner C, Richter H, Rolke R, Scherens A, Schwarz A, Sommer C, Tronnier V, Uçeyler N, Valet M, Wasner G, Treede R-D. Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): somatosensory abnormalities in 1236 patients with different neuropathic pain syndromes. Pain 2010;150: Birklein F, Riedl B, Sieweke N, Weber M, Neundorfer B. Neurological findings in complex regional pain syndromes analysis of 145 cases. Acta Neurol Scand 2000;101: Rommel O, Gehling M, Dertwinkel R, Witscher K, Zenz M, Malin JP, Jänig W. Hemisensory impairment in patients with complex regional pain syndrome. Pain 1999;80: Maleki J, LeBel AA, Bennett GJ, Schwartzman RJ. Patterns of spread in complex regional pain syndrome, type I (reflex sympathetic dystrophy). Pain 2000; 88: Van Rijn MA, Marinus J, Putter H, Bosselaar SR, Moseley GL, Van Hilten JJ. Spreading of complex regional pain syndrome: not a random process. J Neural Transm 2011 Sep;118(9): Merskey H, Bogduk N. Classification of chronic pain. Descriptions of chronic pain syndromes and definitions of pain terms, 2nd edn. Seattle: IASP Press, Harden R, Bruehl S, Perez R, Birklein F, Marinus J, Maihofner C, Lubenow T, Buvanendran A, Mackey S, Graciosa J, Mogilevski M, Ramsden C, Chont M, Vatine J-J. Validation of proposed diagnostic criteria (the Budapest Criteria ) for Complex Regional Pain Syndrome. Pain, 2010;150(2): De Mos M, de Bruijn AGJ, Huygen FJPM, Dieleman JP, Stricker BHCh, Sturkenboom MCJ. The incidence of complex regional pain syndrome: a population-based study. Pain 2007;129: Sandroni P, Benrud-Larson LM, McClelland RL, Low PA. Complex regional pain syndrome type I: incidence and prevalence in Olmsted county, a population-based study. Pain 2003;103: De Mos M, Huygen FJPM, van der Hoeven-Borgman M, Dieleman JP, Stricker BHC, Sturkenboom MCJ. Outcome of the complex regional pain syndrome. Clin J Pain 2009; 25: Parkitny L, McAuley JH, Di Pietro F, Stanton TR, O Connell NE, Marinus J, Van Hilten JJ, Moseley GL. Inflammation in complex regional pain syndrome: a systematic review and meta-analysis. Neurology, 2013;80(1): Huygen FJPM, de Bruijn AGJ, de Bruin MT, Groeneweg JG, Klein J, Zijlstra FJ. Evidence for local inflammation in complex regional pain syndrome type 1. Mediators Inflamm 2002;11: Groeneweg JG, Huygen FJ, Heijmans-Antonissen C, Niehof S, Zijlstra FJ. Increased endothelin-1 and diminished nitric oxide levels in blister fluids of patients with intermediate cold type complex regional pain syndrome type 1. BMC Musculoskelet Disord 2006;7:91. 14
8 GENERAL INTRODUCTION AND AIMS 18. Wesseldijk F, Huygen FJ, Heijmans-Antonissen C, Niehof SP, Zijlstra FJ. Tumor necrosis factor-alpha and interleukin-6 are not correlated with the characteristics of complex regional pain syndrome type 1 in 66 patients. Eur J Pain 2008;12: Wesseldijk F, Huygen FJ, Heijmans-Antonissen C, Niehof SP, Zijlstra FJ. Six years follow-up of the levels of TNF-alpha and IL-6 in patients with complex regional pain syndrome type 1. Mediators Inflamm 2008;2008: Maihöfner C, Handwerker HO, Neundörfer B, Birklein F. Mechanical hyperalgesia in complex regional pain syndrome: a role for TNF-alpha? Neurology, 2005;65(2): Birklein F, Schmelz M, Schifter S, Weber M. The important role of neuropeptides in complex regional pain syndrome. Neurology 2001; 57: Schinkel C, Gaertner A, Zaspel J, Zedler S, Faist WE, Schuermann M. Inflammatory mediators are altered in the acute phase of posttraumatic complex regional pain syndrome. Clin J Pain 2006;22: Leis S, Weber M, Isselmann A, Schmelz M, Birklein F. Substance-P-induced protein extravasation is bilaterally increased in complex regional pain syndrome. Exp Neurol 2003; 183: Leis S, Weber M, Schmelz M, Birklein F. Facilitated neurogenic inflammation in unaffected limbs of patients with complex regional pain syndrome. Neurosci Lett 2004;359: Weber M, Birklein F, Neundorfer B, Schmelz M. Facilitated neurogenic inflammation in complex regional pain syndrome. Pain 2001;91: Dallos A, Kiss M, Polyanka H, Dobozy A, Kemény L, Husz S. Effects of the neuropeptides substance P, calcitonin-gene-related peptide, vasoactive intestinal polypeptide and galanin on the production of nerve growth factor and inflammatory cytokines in cultured human keratinocytes. Neuropeptides 2006;40: Kingery WS. Role of neuropeptide, cytokine, and growth factor signalling in complex regional pain syndrome. Pain Med 2010;11: Wasner G, Heckmann K, Maier C, Baron R. Vascular abnormalities in acute reflex sympathetic dystrophy (CRPS I): Complete inhibition of sympathetic nerve activity with recovery. Arch Neurol 1999;56(5): Wasner G, Schattschneider J, Heckmann K, Maier C, Baron R. Vascular abnormalities in reflex sympathetic dystrophy (CRPS I): Mechanisms and diagnostic value. Brain 2001;124(pt 3): Haensch CA, Jörg J, Lerch H. I-123-metaiodobenzylguanidine uptake of the forearm shows dysfunction in peripheral sympathetic mediated neurovascular transmission in complex regional pain syndrome type I (CRPS I). J Neurol 2002;249(12): Schattschneider J, Hartung K, Stengel M, Ludwig J, Binder A, Wasner G, Baron R. Endothelial dysfunction in cold type complex regional pain syndrome. Neurology 2006;67(4): Groeneweg JG, Antonissen CH, Huygen FJ, Zijlstra FJ. Expression of endothelial nitric oxide synthase and endothelin-1 in skin tissue from amputated limbs of patients with complex regional pain syndrome. Mediators Inflamm 2008;2008: Wasner G. Vasomotor disturbances in complex regional pain syndrome--a review. Pain medicine 2010;11(8): Bruehl S, Harden RN, Galer BS, Saltz S, Backonja M, Stanton-Hicks M. Complex regional pain syndrome: are there distinct subtypes and sequential stages of the syndrome? Pain 2002;95(1-2): Eberle T, Doganci B, Krämer HH, Geber C, Fechir M, Magerl W, Birklein F. Mechanical but not painful electrical stimuli trigger TNF alpha release in human skin. Exp Neurol 2010;221:
9 CHAPTER Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nature Neurosci 2007;10(11): Del Valle L, Schwartzman RJ, Alexander G. Spinal cord histopathological alterations in a patient with longstanding complex regional pain syndrome. Brain Behav Immun 2008; 23: Van de Beek, WJT, Vein A, Hilgevoord AAJ, Van Dijk JG, Van Hilten JJ. Neurophysiologic aspects of patients with generalized or multifocal tonic dystonia of reflex sympathetic dystrophy. J Clin Neurophysiol 2002:19(1): Schwenkreis P, Janssen F, Rommel O, Pleger B, Volker B, Hosbach I, Dertwinkel R, Maier C. Tegenthoff, M. Bilateral motor cortex disinhibition in complex regional pain syndrome (CRPS) type I of the hand. Neurology 2003;61: Maihòfner C, Baron R, DeCol R, Binder A, Birklein F, Deuschl G, Handwerker HO, Schattschneider J. The motor system shows adaptive changes in complex regional pain syndrome. Brain 2007;130: Hallett M. Neurophysiology of dystonia: The role of inhibition. Neurobiol Dis 2011;42(2): Van Hilten JJ, Blumberg H, Schwartzman RJ. Movement disorders and dystrophy pathophysiology and measurement. In: Wilson P, Stanton-Hicks M, Harden N, editors. CRPS: current diagnosis and therapy. Seattle: IASP Press; p Ribbers GM, Mulder T, Geurts AC, den Otter RA. Reflex sympathetic dystrophy of the left hand and motor impairments of the unaffected right hand: impaired central motor processing? Arch Phys Med Rehabil 2002;83: Juottonen K, Gockel M, Silén T, Hurri H, Hari R, Forss N. Altered central sensorimotor processing in patients with complex regional pain syndrome. Pain 2002;98: McCabe CS, Haigh RC, Halligan PW, Blake DR. Referred sensations in patients with complex regional pain syndrome type 1. Rheumatology 2003;42: Maihòfner C, Handwerker HO, Neundorfer B, Birklein F. Patterns of cortical reorganization in complex regional pain syndrome. Neurology 2003;61: Maihöfner C, Handwerker HO, Neundorfer B, Birklein F. Cortical reorganization during recovery from complex regional pain syndrome. Neurology 2004;63: Forderreuther S, Sailer U, Straube A. Impaired self-perception of the hand in complex regional pain syndrome (CRPS). Pain 2004;110: Moseley GL. Why do people with complex regional pain syndrome take longer to recognize their affected hand? Neurology 2004;62: Moseley GL. Distorted body image in complex regional pain syndrome. Neurology 2005;65: Pleger B, Tegenthoff M, Ragert P, Förster AF, Dinse HR, Schwenkreis P, Nicolas V, Maier C. Sensorimotor returning in complex regional pain syndrome parallels pain reduction. Ann Neurol 2005;57: Frettloh J, Huppe M, Maier C. Severity and specificity of neglect-like symptoms in patients with complex regional pain syndrome (CRPS) compared to chronic limb pain of other origins. Pain 2006;124: Lewis JS, Kersten P, McCabe CS, McPherson KM, Blake DR. Body perception disturbance: a contribution to pain in complex regional pain syndrome (CRPS). Pain 2007;133: Moseley GL, Zalucki NM, Wiech K. Tactile discrimination, but not tactile stimulation alone, reduces chronic limb pain. Pain 2008;137: Moseley GL, Parsons TJ, Spence C. Visual distortion of a limb modulates the pain and swelling evoked by movement. Curr Biol 2008;18:R
10 GENERAL INTRODUCTION AND AIMS 56. Moseley GL, Gallace A, Spence C. Space-based, but not arm-based, shift in tactile processing in complex regional pain syndrome and its relationship to cooling of the affected limb. Brain 2009;132: Seifert F, Kiefer G, DeCol R, Schmelz M, Maihofner C. Differential endogenous pain modulation in complexregional pain syndrome. Brain 2009;132: Moseley GL, Gallace A, Spence C. Bodily illusions in health and disease: physiological and clinical perspectives and the concept of a cortical body matrix. Neurosci Biobehav Rev 2012 Jan;36(1): Mancini F, Longo MR, Kammers MP, Haggard P. Visual distortion of body size modulates pain perception. Psychol Sci 2011;22:
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