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Published in: Critical Care 5/2013

Open Access 01-10-2013 | Research

Muscle ultrasound for early assessment of critical illness neuromyopathy in severe sepsis

Authors: Alexander Grimm, Ulrike Teschner, Christine Porzelius, Katrin Ludewig, Jörg Zielske, Otto W Witte, Frank M Brunkhorst, Hubertus Axer

Published in: Critical Care | Issue 5/2013

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Abstract

Introduction

Muscle ultrasound is emerging as a promising tool in the diagnosis of neuromuscular diseases. The current observational study evaluates the usefulness of muscle ultrasound in patients with severe sepsis for assessment of critical illness polyneuropathy and myopathy (CINM) in the intensive care unit.

Methods

28 patients with either septic shock or severe sepsis underwent clinical neurological examinations, muscle ultrasound, and nerve conduction studies on days 4 and 14 after onset of sepsis. 26 healthy controls of comparable age underwent clinical neurological evaluation and muscle ultrasound only.

Results

26 of the 28 patients exhibited classic electrophysiological characteristics of CINM, and all showed typical clinical signs. Ultrasonic echogenicity of muscles was graded semiquantitatively and fasciculations were evaluated in muscles of proximal and distal arms and legs. 75% of patients showed a mean echotexture greater than 1.5, which was the maximal value found in the control group. A significant difference in mean muscle echotexture between patients and controls was found at day 4 and day 14 (both p < 0.001). In addition, from day 4 to day 14, the mean grades of muscle echotexture increased in the patient group, although the values did not reach significance levels (p = 0.085). Controls revealed the lowest number of fasciculations. In the patients group, fasciculations were detected in more muscular regions (lower and upper arm and leg) in comparison to controls (p = 0.08 at day 4 and p = 0.002 at day 14).

Conclusions

Muscle ultrasound represents an easily applicable, non-invasive diagnostic tool which adds to neurophysiological testing information regarding morphological changes of muscles early in the course of sepsis. Muscle ultrasound could be useful for screening purposes prior to subjecting patients to more invasive techniques such as electromyography and/or muscle biopsy.

Trial registration

German Clinical Trials Register, DRKS-ID:​DRKS00000642.
Appendix
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Literature
1.
go back to reference Latronico N, Bolton CF: Critical illness polyneuropathy and myopathy: a major cause of muscle weakness and paralysis. Lancet Neurol 2011, 10: 931-941. 10.1016/S1474-4422(11)70178-8CrossRefPubMed Latronico N, Bolton CF: Critical illness polyneuropathy and myopathy: a major cause of muscle weakness and paralysis. Lancet Neurol 2011, 10: 931-941. 10.1016/S1474-4422(11)70178-8CrossRefPubMed
2.
go back to reference Zink W, Kollmar R, Schwab S: Critical illness polyneuropathy and myopathy in the intensive care unit. Nat Rev Neurol 2009, 5: 372-379. 10.1038/nrneurol.2009.75CrossRefPubMed Zink W, Kollmar R, Schwab S: Critical illness polyneuropathy and myopathy in the intensive care unit. Nat Rev Neurol 2009, 5: 372-379. 10.1038/nrneurol.2009.75CrossRefPubMed
3.
go back to reference Bolton CF, Gilbert JJ, Hahn AF, Sibbald WJ: Polyneuropathy in critically ill patients. J Neurol Neurosurg Psychiatr 1984, 47: 1223-1231. 10.1136/jnnp.47.11.1223PubMedCentralCrossRefPubMed Bolton CF, Gilbert JJ, Hahn AF, Sibbald WJ: Polyneuropathy in critically ill patients. J Neurol Neurosurg Psychiatr 1984, 47: 1223-1231. 10.1136/jnnp.47.11.1223PubMedCentralCrossRefPubMed
4.
go back to reference Witt NJ, Zochodne DW, Bolton CF, Grand’Maison F, Wells G, Young GB, Sibbald WJ: Peripheral nerve function in sepsis and multiple organ failure. Chest 1991, 99: 176-184. 10.1378/chest.99.1.176CrossRefPubMed Witt NJ, Zochodne DW, Bolton CF, Grand’Maison F, Wells G, Young GB, Sibbald WJ: Peripheral nerve function in sepsis and multiple organ failure. Chest 1991, 99: 176-184. 10.1378/chest.99.1.176CrossRefPubMed
5.
go back to reference Visser LH: Critical illness polyneuropathy and myopathy: clinical features, risk factors and prognosis. Eur J Neurol 2006, 13: 1203-1212. 10.1111/j.1468-1331.2006.01498.xCrossRefPubMed Visser LH: Critical illness polyneuropathy and myopathy: clinical features, risk factors and prognosis. Eur J Neurol 2006, 13: 1203-1212. 10.1111/j.1468-1331.2006.01498.xCrossRefPubMed
6.
go back to reference Hermans G, De Jonghe B, Bruyninckx F, Van den Berghe G: Clinical review: critical illness polyneuropathy and myopathy. Crit Care 2008, 12: 238. 10.1186/cc7100PubMedCentralCrossRefPubMed Hermans G, De Jonghe B, Bruyninckx F, Van den Berghe G: Clinical review: critical illness polyneuropathy and myopathy. Crit Care 2008, 12: 238. 10.1186/cc7100PubMedCentralCrossRefPubMed
7.
go back to reference Garnacho-Montero J, Amaya-Villar R, García-Garmendía JL, Madrazo-Osuna J, Ortiz-Leyba C: Effect of critical illness polyneuropathy on the withdrawal from mechanical ventilation and the length of stay in septic patients. Crit Care Med 2005, 33: 349-354. 10.1097/01.CCM.0000153521.41848.7ECrossRefPubMed Garnacho-Montero J, Amaya-Villar R, García-Garmendía JL, Madrazo-Osuna J, Ortiz-Leyba C: Effect of critical illness polyneuropathy on the withdrawal from mechanical ventilation and the length of stay in septic patients. Crit Care Med 2005, 33: 349-354. 10.1097/01.CCM.0000153521.41848.7ECrossRefPubMed
8.
go back to reference Garnacho-Montero J, Madrazo-Osuna J, García-Garmendia JL, Ortiz-Leyba C, Jiménez-Jiménez FJ, Barrero-Almodóvar A, Garnacho-Montero MC, Moyano-Del-Estad MR: Critical illness polyneuropathy: risk factors and clinical consequences. A cohort study in septic patients. Intensive Care Med 2001, 27: 1288-1296. 10.1007/s001340101009CrossRefPubMed Garnacho-Montero J, Madrazo-Osuna J, García-Garmendia JL, Ortiz-Leyba C, Jiménez-Jiménez FJ, Barrero-Almodóvar A, Garnacho-Montero MC, Moyano-Del-Estad MR: Critical illness polyneuropathy: risk factors and clinical consequences. A cohort study in septic patients. Intensive Care Med 2001, 27: 1288-1296. 10.1007/s001340101009CrossRefPubMed
9.
go back to reference Trojaborg W: Electrophysiologic techniques in critical illness-associated weakness. J Neurol Sci 2006, 242: 83-85. 10.1016/j.jns.2005.11.019CrossRefPubMed Trojaborg W: Electrophysiologic techniques in critical illness-associated weakness. J Neurol Sci 2006, 242: 83-85. 10.1016/j.jns.2005.11.019CrossRefPubMed
10.
go back to reference Bednarik J, Lukas Z, Vondracek P: Critical illness polyneuromyopathy: the electrophysiological components of a complex entity. Intensive Care Med 2003, 29: 1505-1514. 10.1007/s00134-003-1858-0CrossRefPubMed Bednarik J, Lukas Z, Vondracek P: Critical illness polyneuromyopathy: the electrophysiological components of a complex entity. Intensive Care Med 2003, 29: 1505-1514. 10.1007/s00134-003-1858-0CrossRefPubMed
11.
go back to reference Tennilä A, Salmi T, Pettilä V, Roine RO, Varpula T, Takkunen O: Early signs of critical illness polyneuropathy in ICU patients with systemic inflammatory response syndrome or sepsis. Intensive Care Med 2000, 26: 1360-1363. 10.1007/s001340000586CrossRefPubMed Tennilä A, Salmi T, Pettilä V, Roine RO, Varpula T, Takkunen O: Early signs of critical illness polyneuropathy in ICU patients with systemic inflammatory response syndrome or sepsis. Intensive Care Med 2000, 26: 1360-1363. 10.1007/s001340000586CrossRefPubMed
12.
go back to reference Khan J, Harrison TB, Rich MM, Moss M: Early development of critical illness myopathy and neuropathy in patients with severe sepsis. Neurology 2006, 67: 1421-1425. 10.1212/01.wnl.0000239826.63523.8eCrossRefPubMed Khan J, Harrison TB, Rich MM, Moss M: Early development of critical illness myopathy and neuropathy in patients with severe sepsis. Neurology 2006, 67: 1421-1425. 10.1212/01.wnl.0000239826.63523.8eCrossRefPubMed
13.
go back to reference Bird SJ: Diagnosis and management of critical illness polyneuropathy and critical illness myopathy. Curr Treat Options Neurol 2007, 9: 85-92. 10.1007/s11940-007-0034-1CrossRefPubMed Bird SJ: Diagnosis and management of critical illness polyneuropathy and critical illness myopathy. Curr Treat Options Neurol 2007, 9: 85-92. 10.1007/s11940-007-0034-1CrossRefPubMed
14.
go back to reference Koch S, Spuler S, Deja M, Bierbrauer J, Dimroth A, Behse F, Spies CD, Wernecke KD, Weber-Carstens S: Critical illness myopathy is frequent: accompanying neuropathy protracts ICU discharge. J Neurol Neurosurg Psychiatr 2011, 82: 287-293. 10.1136/jnnp.2009.192997CrossRefPubMed Koch S, Spuler S, Deja M, Bierbrauer J, Dimroth A, Behse F, Spies CD, Wernecke KD, Weber-Carstens S: Critical illness myopathy is frequent: accompanying neuropathy protracts ICU discharge. J Neurol Neurosurg Psychiatr 2011, 82: 287-293. 10.1136/jnnp.2009.192997CrossRefPubMed
15.
go back to reference Mayans D, Cartwright MS, Walker FO: Neuromuscular ultrasonography: quantifying muscle and nerve measurements. Phys Med Rehabil Clin N Am 2012, 23: 133-148. xii 10.1016/j.pmr.2011.11.009PubMedCentralCrossRefPubMed Mayans D, Cartwright MS, Walker FO: Neuromuscular ultrasonography: quantifying muscle and nerve measurements. Phys Med Rehabil Clin N Am 2012, 23: 133-148. xii 10.1016/j.pmr.2011.11.009PubMedCentralCrossRefPubMed
16.
go back to reference Pillen S, Arts IMP, Zwarts MJ: Muscle ultrasound in neuromuscular disorders. Muscle Nerve 2008, 37: 679-693. 10.1002/mus.21015CrossRefPubMed Pillen S, Arts IMP, Zwarts MJ: Muscle ultrasound in neuromuscular disorders. Muscle Nerve 2008, 37: 679-693. 10.1002/mus.21015CrossRefPubMed
17.
go back to reference Arts IM, van Rooij FG, Overeem S, Pillen S, Janssen HM, Schelhaas HJ, Zwarts MJ: Quantitative muscle ultrasonography in amyotrophic lateral sclerosis. Ultrasound Med Biol 2008, 34: 354-361. 10.1016/j.ultrasmedbio.2007.08.013CrossRefPubMed Arts IM, van Rooij FG, Overeem S, Pillen S, Janssen HM, Schelhaas HJ, Zwarts MJ: Quantitative muscle ultrasonography in amyotrophic lateral sclerosis. Ultrasound Med Biol 2008, 34: 354-361. 10.1016/j.ultrasmedbio.2007.08.013CrossRefPubMed
18.
go back to reference Pillen S, Verrips A, van Alfen N, Arts IM, Sie LT, Zwarts MJ: Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease. Neuromuscul Disord 2007, 17: 509-516. 10.1016/j.nmd.2007.03.008CrossRefPubMed Pillen S, Verrips A, van Alfen N, Arts IM, Sie LT, Zwarts MJ: Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease. Neuromuscul Disord 2007, 17: 509-516. 10.1016/j.nmd.2007.03.008CrossRefPubMed
19.
go back to reference Brunkhorst FM, Engel C, Bloos F, Meier-Hellmann A, Ragaller M, Weiler N, Moerer O, Gruendling M, Oppert M, Grond S, Olthoff D, Jaschinski U, John S, Rossaint R, Welte T, Schaefer M, Kern P, Kuhnt E, Kiehntopf M, Hartog C, Natanson C, Loeffler M, Reinhart K, German Competence Network Sepsis (SepNet): Intensive insulin therapy and pentastarch resuscitation in severe sepsis. N Engl J Med 2008, 358: 125-139. 10.1056/NEJMoa070716CrossRefPubMed Brunkhorst FM, Engel C, Bloos F, Meier-Hellmann A, Ragaller M, Weiler N, Moerer O, Gruendling M, Oppert M, Grond S, Olthoff D, Jaschinski U, John S, Rossaint R, Welte T, Schaefer M, Kern P, Kuhnt E, Kiehntopf M, Hartog C, Natanson C, Loeffler M, Reinhart K, German Competence Network Sepsis (SepNet): Intensive insulin therapy and pentastarch resuscitation in severe sepsis. N Engl J Med 2008, 358: 125-139. 10.1056/NEJMoa070716CrossRefPubMed
20.
go back to reference Brunkhorst FM, Oppert M, Marx G, Bloos F, Ludewig K, Putensen C, Nierhaus A, Jaschinski U, Meier-Hellmann A, Weyland A, Gründling M, Moerer O, Riessen R, Seibel A, Ragaller M, Büchler MW, John S, Bach F, Spies C, Reill L, Fritz H, Kiehntopf M, Kuhnt E, Bogatsch H, Engel C, Loeffler M, Kollef MH, Reinhart K, Welte T, German Study Group Competence Network Sepsis (SepNet): Effect of empirical treatment with moxifloxacin and meropenem vs meropenem on sepsis-related organ dysfunction in patients with severe sepsis: a randomized trial. JAMA 2012, 307: 2390-2399. 10.1001/jama.2012.5833CrossRefPubMed Brunkhorst FM, Oppert M, Marx G, Bloos F, Ludewig K, Putensen C, Nierhaus A, Jaschinski U, Meier-Hellmann A, Weyland A, Gründling M, Moerer O, Riessen R, Seibel A, Ragaller M, Büchler MW, John S, Bach F, Spies C, Reill L, Fritz H, Kiehntopf M, Kuhnt E, Bogatsch H, Engel C, Loeffler M, Kollef MH, Reinhart K, Welte T, German Study Group Competence Network Sepsis (SepNet): Effect of empirical treatment with moxifloxacin and meropenem vs meropenem on sepsis-related organ dysfunction in patients with severe sepsis: a randomized trial. JAMA 2012, 307: 2390-2399. 10.1001/jama.2012.5833CrossRefPubMed
21.
go back to reference Arts IMP, Pillen S, Schelhaas HJ, Overeem S, Zwarts MJ: Normal values for quantitative muscle ultrasonography in adults. Muscle Nerve 2010, 41: 32-41. 10.1002/mus.21458CrossRefPubMed Arts IMP, Pillen S, Schelhaas HJ, Overeem S, Zwarts MJ: Normal values for quantitative muscle ultrasonography in adults. Muscle Nerve 2010, 41: 32-41. 10.1002/mus.21458CrossRefPubMed
22.
go back to reference Scholten RR, Pillen S, Verrips A, Zwarts MJ: Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nerve 2003, 27: 693-698. 10.1002/mus.10384CrossRefPubMed Scholten RR, Pillen S, Verrips A, Zwarts MJ: Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nerve 2003, 27: 693-698. 10.1002/mus.10384CrossRefPubMed
23.
go back to reference Heckmatt JZ, Leeman S, Dubowitz V: Ultrasound imaging in the diagnosis of muscle disease. J Pediatr 1982, 101: 656-660. 10.1016/S0022-3476(82)80286-2CrossRefPubMed Heckmatt JZ, Leeman S, Dubowitz V: Ultrasound imaging in the diagnosis of muscle disease. J Pediatr 1982, 101: 656-660. 10.1016/S0022-3476(82)80286-2CrossRefPubMed
24.
go back to reference Reimers CD, Ziemann U, Scheel A, Rieckmann P, Kunkel M, Kurth C: Fasciculations: clinical, electromyographic, and ultrasonographic assessment. J Neurol 1996, 243: 579-584. 10.1007/BF00900945CrossRefPubMed Reimers CD, Ziemann U, Scheel A, Rieckmann P, Kunkel M, Kurth C: Fasciculations: clinical, electromyographic, and ultrasonographic assessment. J Neurol 1996, 243: 579-584. 10.1007/BF00900945CrossRefPubMed
25.
go back to reference Scheel AK, Reimers CD: [Detection of fasciculations and other types of muscular hyperkinesias with ultrasound]. Ultraschall Med 2004, 25: 337-341. 10.1055/s-2004-813488CrossRefPubMed Scheel AK, Reimers CD: [Detection of fasciculations and other types of muscular hyperkinesias with ultrasound]. Ultraschall Med 2004, 25: 337-341. 10.1055/s-2004-813488CrossRefPubMed
26.
go back to reference Arts IMP, Overeem S, Pillen S, Schelhaas HJ, Zwarts MJ: Muscle changes in amyotrophic lateral sclerosis: a longitudinal ultrasonography study. Clin Neurophysiol 2011, 122: 623-628. 10.1016/j.clinph.2010.07.023CrossRefPubMed Arts IMP, Overeem S, Pillen S, Schelhaas HJ, Zwarts MJ: Muscle changes in amyotrophic lateral sclerosis: a longitudinal ultrasonography study. Clin Neurophysiol 2011, 122: 623-628. 10.1016/j.clinph.2010.07.023CrossRefPubMed
27.
go back to reference Bolton CF: Neuromuscular manifestations of critical illness. Muscle Nerve 2005, 32: 140-163. 10.1002/mus.20304CrossRefPubMed Bolton CF: Neuromuscular manifestations of critical illness. Muscle Nerve 2005, 32: 140-163. 10.1002/mus.20304CrossRefPubMed
28.
go back to reference Pillen S, Tak RO, Zwarts MJ, Lammens MM, Verrijp KN, Arts IM, van der Laak JA, Hoogerbrugge PM, van Engelen BG, Verrips A: Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol 2009, 35: 443-446. 10.1016/j.ultrasmedbio.2008.09.016CrossRefPubMed Pillen S, Tak RO, Zwarts MJ, Lammens MM, Verrijp KN, Arts IM, van der Laak JA, Hoogerbrugge PM, van Engelen BG, Verrips A: Skeletal muscle ultrasound: correlation between fibrous tissue and echo intensity. Ultrasound Med Biol 2009, 35: 443-446. 10.1016/j.ultrasmedbio.2008.09.016CrossRefPubMed
29.
go back to reference Jacobson JA: Musculoskeletal ultrasound: focused impact on MRI. AJR Am J Roentgenol 2009, 193: 619-627. 10.2214/AJR.09.2841CrossRefPubMed Jacobson JA: Musculoskeletal ultrasound: focused impact on MRI. AJR Am J Roentgenol 2009, 193: 619-627. 10.2214/AJR.09.2841CrossRefPubMed
30.
go back to reference Boon AJ, Smith J, Harper CM: Ultrasound applications in electrodiagnosis. PM R 2012, 4: 37-49. 10.1016/j.pmrj.2011.07.004CrossRefPubMed Boon AJ, Smith J, Harper CM: Ultrasound applications in electrodiagnosis. PM R 2012, 4: 37-49. 10.1016/j.pmrj.2011.07.004CrossRefPubMed
31.
go back to reference Walker FO, Donofrio PD, Harpold GJ, Ferrell WG: Sonographic imaging of muscle contraction and fasciculations: a correlation with electromyography. Muscle Nerve 1990, 13: 33-39. 10.1002/mus.880130108CrossRefPubMed Walker FO, Donofrio PD, Harpold GJ, Ferrell WG: Sonographic imaging of muscle contraction and fasciculations: a correlation with electromyography. Muscle Nerve 1990, 13: 33-39. 10.1002/mus.880130108CrossRefPubMed
32.
go back to reference Cartwright MS, Demar S, Griffin LP, Balakrishnan N, Harris JM, Walker FO: Validity and reliability of nerve and muscle ultrasound. Muscle Nerve 2013, 47: 515-521. 10.1002/mus.23621CrossRefPubMed Cartwright MS, Demar S, Griffin LP, Balakrishnan N, Harris JM, Walker FO: Validity and reliability of nerve and muscle ultrasound. Muscle Nerve 2013, 47: 515-521. 10.1002/mus.23621CrossRefPubMed
33.
go back to reference Hebert JJ, Koppenhaver SL, Parent EC, Fritz JM: A systematic review of the reliability of rehabilitative ultrasound imaging for the quantitative assessment of the abdominal and lumbar trunk muscles. Spine 2009, 34: E848-E856. 10.1097/BRS.0b013e3181ae625cCrossRefPubMed Hebert JJ, Koppenhaver SL, Parent EC, Fritz JM: A systematic review of the reliability of rehabilitative ultrasound imaging for the quantitative assessment of the abdominal and lumbar trunk muscles. Spine 2009, 34: E848-E856. 10.1097/BRS.0b013e3181ae625cCrossRefPubMed
34.
go back to reference Cartwright MS, Kwayisi G, Griffin LP, Sarwal A, Walker FO, Harris JM, Berry MJ, Chahal PS, Morris PE: Quantitative neuromuscular ultrasound in the intensive care unit. Muscle Nerve 2013, 47: 255-259. 10.1002/mus.23525CrossRefPubMed Cartwright MS, Kwayisi G, Griffin LP, Sarwal A, Walker FO, Harris JM, Berry MJ, Chahal PS, Morris PE: Quantitative neuromuscular ultrasound in the intensive care unit. Muscle Nerve 2013, 47: 255-259. 10.1002/mus.23525CrossRefPubMed
35.
go back to reference Boyd JH, Forbes J, Nakada T, Walley KR, Russell JA: Fluid resuscitation in septic shock: a positive fluid balance and elevated central venous pressure are associated with increased mortality. Crit Care Med 2011, 39: 259-265. 10.1097/CCM.0b013e3181feeb15CrossRefPubMed Boyd JH, Forbes J, Nakada T, Walley KR, Russell JA: Fluid resuscitation in septic shock: a positive fluid balance and elevated central venous pressure are associated with increased mortality. Crit Care Med 2011, 39: 259-265. 10.1097/CCM.0b013e3181feeb15CrossRefPubMed
36.
go back to reference Grimm A, Witte OW, Axer H: Muscle ultrasound in neurology – an overview. Neurophys Lab 2013, 35: 47-60. 10.1016/j.neulab.2013.02.001CrossRef Grimm A, Witte OW, Axer H: Muscle ultrasound in neurology – an overview. Neurophys Lab 2013, 35: 47-60. 10.1016/j.neulab.2013.02.001CrossRef
37.
go back to reference Llano-Diez M, Renaud G, Andersson M, Marrero HG, Cacciani N, Engquist H, Corpeño R, Artemenko K, Bergquist J, Larsson L: Mechanisms underlying ICU muscle wasting and effects of passive mechanical loading. Crit Care 2012, 16: R209. 10.1186/cc11841PubMedCentralCrossRefPubMed Llano-Diez M, Renaud G, Andersson M, Marrero HG, Cacciani N, Engquist H, Corpeño R, Artemenko K, Bergquist J, Larsson L: Mechanisms underlying ICU muscle wasting and effects of passive mechanical loading. Crit Care 2012, 16: R209. 10.1186/cc11841PubMedCentralCrossRefPubMed
38.
go back to reference Grimm A, Günther A, Witte OW, Axer H: Critical illness polyneuropathy and critical illness myopathy. Med Klin Intensivmed Notfmed 2012, 107: 649-660. 10.1007/s00063-012-0186-yCrossRefPubMed Grimm A, Günther A, Witte OW, Axer H: Critical illness polyneuropathy and critical illness myopathy. Med Klin Intensivmed Notfmed 2012, 107: 649-660. 10.1007/s00063-012-0186-yCrossRefPubMed
39.
go back to reference Kerbaul F, Brousse M, Collart F, Pellissier JF, Planche D, Fernandez C, Gouin F, Guidon C: Combination of histopathological and electromyographic patterns can help to evaluate functional outcome of critical ill patients with neuromuscular weakness syndromes. Crit Care 2004, 8: R358-R366. 10.1186/cc2925PubMedCentralCrossRefPubMed Kerbaul F, Brousse M, Collart F, Pellissier JF, Planche D, Fernandez C, Gouin F, Guidon C: Combination of histopathological and electromyographic patterns can help to evaluate functional outcome of critical ill patients with neuromuscular weakness syndromes. Crit Care 2004, 8: R358-R366. 10.1186/cc2925PubMedCentralCrossRefPubMed
40.
go back to reference Rich MM, Bird SJ, Raps EC, McCluskey LF, Teener JW: Direct muscle stimulation in acute quadriplegic myopathy. Muscle Nerve 1997, 20: 665-673. 10.1002/(SICI)1097-4598(199706)20:6<665::AID-MUS2>3.0.CO;2-6CrossRefPubMed Rich MM, Bird SJ, Raps EC, McCluskey LF, Teener JW: Direct muscle stimulation in acute quadriplegic myopathy. Muscle Nerve 1997, 20: 665-673. 10.1002/(SICI)1097-4598(199706)20:6<665::AID-MUS2>3.0.CO;2-6CrossRefPubMed
41.
go back to reference Lefaucheur J-P, Nordine T, Rodriguez P, Brochard L: Origin of ICU acquired paresis determined by direct muscle stimulation. J Neurol Neurosurg Psychiatr 2006, 77: 500-506. 10.1136/jnnp.2005.070813PubMedCentralCrossRefPubMed Lefaucheur J-P, Nordine T, Rodriguez P, Brochard L: Origin of ICU acquired paresis determined by direct muscle stimulation. J Neurol Neurosurg Psychiatr 2006, 77: 500-506. 10.1136/jnnp.2005.070813PubMedCentralCrossRefPubMed
42.
go back to reference Misawa S, Noto Y, Shibuya K, Isose S, Sekiguchi Y, Nasu S, Kuwabara S: Ultrasonographic detection of fasciculations markedly increases diagnostic sensitivity of ALS. Neurology 2011, 77: 1532-1537. 10.1212/WNL.0b013e318233b36aCrossRefPubMed Misawa S, Noto Y, Shibuya K, Isose S, Sekiguchi Y, Nasu S, Kuwabara S: Ultrasonographic detection of fasciculations markedly increases diagnostic sensitivity of ALS. Neurology 2011, 77: 1532-1537. 10.1212/WNL.0b013e318233b36aCrossRefPubMed
43.
go back to reference Hund E, Genzwürker H, Böhrer H, Jakob H, Thiele R, Hacke W: Predominant involvement of motor fibres in patients with critical illness polyneuropathy. Br J Anaesth 1997, 78: 274-278. 10.1093/bja/78.3.274CrossRefPubMed Hund E, Genzwürker H, Böhrer H, Jakob H, Thiele R, Hacke W: Predominant involvement of motor fibres in patients with critical illness polyneuropathy. Br J Anaesth 1997, 78: 274-278. 10.1093/bja/78.3.274CrossRefPubMed
Metadata
Title
Muscle ultrasound for early assessment of critical illness neuromyopathy in severe sepsis
Authors
Alexander Grimm
Ulrike Teschner
Christine Porzelius
Katrin Ludewig
Jörg Zielske
Otto W Witte
Frank M Brunkhorst
Hubertus Axer
Publication date
01-10-2013
Publisher
BioMed Central
Published in
Critical Care / Issue 5/2013
Electronic ISSN: 1364-8535
DOI
https://doi.org/10.1186/cc13050

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