Die neuralgische Amyotrophie: eine häufige Ursache uni- oder bilateraler Zwerchfellparesen

Zusammenfassung

Eine ein- oder beidseitige Zwerchfellparese kann verschiedene Ursachen haben, an erster Stelle stehen (intraoperative) Verletzungen des Nervus phrenicus. In bis zu 20% der Fälle lässt sich jedoch trotz umfangreicher Abklärung keine Erklärung finden. Die neuralgische Amyotrophie (NA, syn. Parsonage-Turner-Syndrom) ist eine häufige, im Alltag unterdiagnostizierte, multifokale autoimmun-inflammatorische Erkrankung, die überwiegend proximale Nervenabschnitte der oberen Extremitäten betrifft. Klassische Symptome sind akut einsetzende, starke Schmerzen im Bereich des Schultergürtels mit zeitverzögert auftretenden Paresen der Schulter- und Armmuskulatur. In mindestens 7% der Fälle ist der N. phrenicus (mit-)betroffen. Legt man die jährliche Inzidenz einer NA von 1:1000 zugrunde, ist die Entität als Ursache einer Zwerchfellfunktionsstörung wahrscheinlich nicht so ungewöhnlich, wie bislang angenommen. Die klinische Erfahrung zeigt jedoch, dass diese Diagnose oft nicht in Betracht gezogen und die Zwerchfellparese somit fälschlicherweise als idiopathisch klassifiziert wird. Fatal ist dies v.a. im Hinblick auf die Möglichkeit einer medikamentösen Therapie mittels Kortikosteroiden im Akutstadium einer NA sowie einer möglicherweise zu frühen operativen Zwerchfellraffung aufgrund des Potenzials der Erkrankung einer spontanen Heilung auch viele Monate nach Symptombeginn.

Ziel des vorliegenden Artikels ist es, das Bewusstsein für die Entität der NA als Ursache einer Zwerchfellparese zu schärfen und einen standardisierten Ansatz für die Diagnostik und Behandlung zu etablieren.

Abstract

There are several causes for unilateral or bilateral diaphragmatic paresis. The most common cause is an (intraoperative) injury to the phrenic nerve.

However, in up to 20% of cases, no explanation can be found despite extensive workup. Neuralgic amyotrophy (NA, also known as Parsonage-Turner syndrome) is a common underdiagnosed multifocal autoimmune-inflammatory disease that predominantly affects proximal nerve segments of the upper extremities. Classic symptoms include acute onset of severe pain in the shoulder girdle with delayed onset of paresis of the shoulder and arm muscles. In at least 7% of cases, the phrenic nerve is also affected. Based on the annual incidence of NA of 1:1000, the entity as a cause of diaphragmatic dysfunction is probably not as uncommon as previously thought. However, clinical experience shows that this diagnosis is often not considered, and diaphragmatic paresis gets wrongly classified as idiopathic.

This is particularly disastrous because in the early stage of NA, medical therapy with corticosteroids is mostly not considered and the possibility that surgical repair of the diaphragm may be performed prematurely, given that the condition may resolve spontaneously many months after symptom onset.

The aim of the present article is to raise awareness of the entity of NA as a cause of diaphragmatic paresis and to establish a standardized approach to diagnosis and treatment.

Schlüsselwörter

Zwerchfellparese - Atemmuskuläre Diagnostik - Seltene Erkrankungen - Parsonage Turner Syndrom - Neuralgische Amyotrophie

Keywords

Diaphragmatic paresis - Respiratory muscular diagnostics - Rare diseases - Parsonage-Turner syndrome - Neuralgic amyotrophy

Publication History

Received: 24 February 2023

Accepted after revision: 13 June 2023

Article published online:
30 August 2023

• Literatur

• 1 Windisch W, Criée C-P. Pathophysiologie und Grundlagen des respiratorischen Versagens. Pneumol 2010; 2: 74-80 DOI: 10.1007/s10405-009-0365-6.
• 2 Loring SH, Mead J. Action of the diaphragm on the rib cage inferred from a force-balance analysis. J Appl Physiol 1982; 53: 756-760 DOI: 10.1152/jappl.1982.53.3.756. (PMID: 6215388)
• 3 Ricoy J, Rodríguez-Núñez N, Álvarez-Dobaño JM. et al. Diaphragmatic dysfunction. Pulmonology 2019; 25: 223-235 DOI: 10.1016/j.pulmoe.2018.10.008. (PMID: 30509855)
• 4 Canbaz S, Turgut N, Halici U. et al. Electrophysiological evaluation of phrenic nerve injury during cardiac surgery – a prospective, controlled, clinical study. BMC Surg 2004; 4: 2 DOI: 10.1186/1471-2482-4-2.
• 5 Swallow EB, Dayer MJ, Oldfield WL. et al. Right hemi-diaphragm paralysis following cardiac radiofrequency ablation. Respir Med 2006; 100: 1657-1659 DOI: 10.1016/j.rmed.2005.12.012. (PMID: 16488125)
• 6 Carretero Gracia JA, Alvarez Alegret R, Peñalver Cuesta JC. Chronic sclerosing mediastinitis: infrequent cause of unilateral diaphragmatic paralysis. Arch Bronconeumol 2000; 36: 417-419 DOI: 10.1016/s0300-2896(15)30142-3. (PMID: 11000931)
• 7 Crausman RS, Summerhill EM, McCool FD. Idiopathic diaphragmatic paralysis: Bell’s palsy of the diaphragm?. Lung 2009; 187: 153-157 DOI: 10.1007/s00408-009-9140-z. (PMID: 19277778)
• 8 Wilcox PG, Pardy RL. Diaphragmatic weakness and paralysis. Lung 1989; 167: 323-341 DOI: 10.1007/BF02714961. (PMID: 2509822)
• 9 Laroche CM, Mier AK, Moxham J. et al. Diaphragm strength in patients with recent hemidiaphragm paralysis. Thorax 1988; 43: 170-174
• 10 Hart N, Nickol AH, Cramer D. et al. Effect of Severe Isolated Unilateral and Bilateral Diaphragm Weakness on Exercise Performance. Am J Respir Crit Care Med 2002; 165: 1265-1270 DOI: 10.1164/rccm.2110016. (PMID: 11991876)
• 11 Steier J, Jolley CJ, Seymour J. et al. Sleep-disordered breathing in unilateral diaphragm paralysis or severe weakness. Eur Respir J 2008; 32: 1479-1487 DOI: 10.1183/09031936.00018808. (PMID: 18684853)
• 12 McCool FD, Mead J. Dyspnea on immersion: mechanisms in patients with bilateral diaphragm paralysis. Am Rev Respir Dis 1989; 139: 275-276 DOI: 10.1164/ajrccm/139.1.275. (PMID: 2521439)
• 13 Kumar N, Folger WN, Bolton CF. Dyspnea as the predominant manifestation of bilateral phrenic neuropathy. Mayo Clin Proc 2004; 79: 1563-1565 DOI: 10.4065/79.12.1563. (PMID: 15595343)
• 14 Skatrud J, Iber C, McHugh W. et al. Determinants of hypoventilation during wakefulness and sleep in diaphragmatic paralysis. Am Rev Respir Dis 1980; 121: 587-593 DOI: 10.1164/arrd.1980.121.3.587.
• 15 Windisch W, Dreher M, Geiseler J. et al. S2k-Leitlinie: Nichtinvasive und invasive Beatmung als Therapie der chronischen respiratorischen Insuffizienz – Revision 2017. Pneumologie 2017; 71: 722-795 DOI: 10.1055/s-0043-118040.
• 16 Mier-Jedrzejowicz A, Brophy C, Moxham J. et al. Assessment of diaphragm weakness. Am Rev Respir Dis 1988; 137: 877-883 DOI: 10.1164/ajrccm/137.4.877. (PMID: 3354995)
• 17 Laroche CM, Carroll N, Moxham J. et al. Clinical significance of severe isolated diaphragm weakness. Am Rev Respir Dis 1988; 138: 862-866 DOI: 10.1164/ajrccm/138.4.862. (PMID: 3202460)
• 18 Parsonage MJ, Aldren Turner JW. Neuralgic amyotrophy; the shoulder-girdle syndrome. The Lancet 1948; 251: 973-978 DOI: 10.1016/S0140-6736(48)90611-4.
• 19 Beghi E, Kurland LT, Mulder DW. et al. Brachial plexus neuropathy in the population of Rochester, Minnesota, 1970–1981. Ann Neurol 1985; 18: 320-323 DOI: 10.1002/ana.410180308. (PMID: 2996415)
• 20 MacDonald BK, Cockerell OC, Sander JW. et al. The incidence and lifetime prevalence of neurological disorders in a prospective community-based study in the UK. Brain J Neurol 2000; 123: 665-676 DOI: 10.1093/brain/123.4.665. (PMID: 10733998)
• 21 van Alfen N, van Eijk JJJ, Ennik T. et al. Incidence of Neuralgic Amyotrophy (Parsonage Turner Syndrome) in a Primary Care Setting – A Prospective Cohort Study. Pt. 4. PLoS ONE 2015; 10: e0128361 DOI: 10.1371/journal.pone.0128361. (PMID: 26016482)
• 22 van Alfen N, van Engelen BGM. The clinical spectrum of neuralgic amyotrophy in 246 cases. Brain J Neurol 2006; 129: 438-450 DOI: 10.1093/brain/awh722. (PMID: 16371410)
• 23 Van Eijk JJJ, Groothuis JT, Van Alfen N. Neuralgic amyotrophy: An update on diagnosis, pathophysiology, and treatment. Muscle Nerve 2016; 53: 337-350 DOI: 10.1002/mus.25008. (PMID: 26662794)
• 24 van Alfen N. Clinical and pathophysiological concepts of neuralgic amyotrophy. Nat Rev Neurol 2011; 7: 315-322 DOI: 10.1038/nrneurol.2011.62. (PMID: 21556032)
• 25 Dartevel A, Colombe B, Bosseray A. et al. Hepatitis E and neuralgic amyotrophy: Five cases and review of literature. J Clin Virol 2015; 69: 156-164 DOI: 10.1016/j.jcv.2015.06.091. (PMID: 26209399)
• 26 van Eijk JJJ, Madden RG, van der Eijk AA. et al. Neuralgic amyotrophy and hepatitis E virus infection. Neurology 2014; 82: 498-503 DOI: 10.1212/WNL.0000000000000112. (PMID: 24401685)
• 27 Ismail II, Abdelnabi EA, Al-Hashel JY. et al. Neuralgic amyotrophy associated with COVID-19 infection: a case report and review of the literature. Neurol Sci 2021; 42: 2161-2165 DOI: 10.1007/s10072-021-05197-z.
• 28 Siepmann T, Kitzler HH, Lueck C. et al. Neuralgic amyotrophy following infection with SARS-CoV-2. Muscle Nerve 2020; 62: E68-E70 DOI: 10.1002/mus.27035.
• 29 Kuhlenbäumer G, Hannibal MC, Nelis E. et al. Mutations in SEPT9 cause hereditary neuralgic amyotrophy. Nat Genet 2005; 37: 1044-1046 DOI: 10.1038/ng1649. (PMID: 16186812)
• 30 Englert HM. Partial fascicular median-nerve atrophy of unknown origin. Handchirurgie 1976; 8: 61-62 (PMID: 184013)
• 31 Arányi Z, Csillik A, DéVay K. et al. Ultrasonography in neuralgic amyotrophy: Sensitivity, spectrum of findings, and clinical correlations. Muscle Nerve 2017; 56: 1054-1062 DOI: 10.1002/mus.25708. (PMID: 28556181)
• 32 Arányi Z, Csillik A, Dévay K. et al. Ultrasonographic identification of nerve pathology in neuralgic amyotrophy: Enlargement, constriction, fascicular entwinement, and torsion. Muscle Nerve 2015; 52: 503-511 DOI: 10.1002/mus.24615. (PMID: 25703205)
• 33 Sneag DB, Rancy SK, Wolfe SW. et al. Brachial plexitis or neuritis? MRI features of lesion distribution in Parsonage-Turner syndrome. Muscle Nerve 2018; 58: 359-366 DOI: 10.1002/mus.26108. (PMID: 29461642)
• 34 Nagano A. Spontaneous anterior interosseous nerve palsy. J Bone Joint Surg Br 2003; 85: 313-318 DOI: 10.1302/0301-620x.85b3.14147. (PMID: 12729100)
• 35 Tazaki K. Paralysis of anterior interosseous nerve and posterior interosseous nerve due to fascicular constriction. J-Jpn Soc Surg Hand 1996; 13: 142-142
• 36 van Alfen N, Hannibal MC, Chance PF. et al. Hereditary Neuralgic Amyotrophy – Retired chapter, for historical reference only. In: Adam MP, Everman DB, Mirzaa GM. GeneReviews. Seattle (WA): University of Washington; 1993
• 37 van Alfen N, Huisman WJ, Overeem S. et al. Sensory nerve conduction studies in neuralgic amyotrophy. Am J Phys Med Rehabil 2009; 88: 941-946 DOI: 10.1097/PHM.0b013e3181a5b980. (PMID: 19404188)
• 38 Ripellino P, Arányi Z, van Alfen N. et al. Imaging of neuralgic amyotrophy in the acute phase. Muscle Nerve 2022; 66: 709-714 DOI: 10.1002/mus.27732. (PMID: 36214185)
• 39 Wang T, Qi H, Wang Z. et al. The role of ultrasonography in diagnosis of neuralgic amyotrophy. Skeletal Radiol 2023; 52: 1305-1311 DOI: 10.1007/s00256-022-04253-9.
• 40 Cruz-Martínez A, Barrio M, Arpa J. Neuralgic amyotrophy: variable expression in 40 patients. J Peripher Nerv Syst JPNS 2002; 7: 198-204 DOI: 10.1046/j.1529-8027.2002.02025.x. (PMID: 12365568)
• 41 Tsairis P, Dyck PJ, Mulder DW. Natural history of brachial plexus neuropathy. Report on 99 patients. Arch Neurol 1972; 27: 109-117 DOI: 10.1001/archneur.1972.00490140013004. (PMID: 4339239)
• 42 van Alfen N, van der Werf SP, van Engelen BG. Long-term pain, fatigue, and impairment in neuralgic amyotrophy. Arch Phys Med Rehabil 2009; 90: 435-439 DOI: 10.1016/j.apmr.2008.08.216. (PMID: 19254608)
• 43 Lahrmann H, Grisold W, Authier FJ. et al. Neuralgic amyotrophy with phrenic nerve involvement. Muscle Nerve 1999; 22: 437-442 DOI: 10.1002/(sici)1097-4598(199904)22:4<437::aid-mus2>3.0.co;2-f.
• 44 McEnery T, Walsh R, Burke C. et al. Phrenic Nerve Palsy Secondary to Parsonage-Turner Syndrome: A Diagnosis Commonly Overlooked. Lung 2017; 195: 173-177 DOI: 10.1007/s00408-016-9972-2. (PMID: 28138789)
• 45 Mulvey DA, Aquilina RJ, Elliott MW. et al. Diaphragmatic dysfunction in neuralgic amyotrophy: an electrophysiologic evaluation of 16 patients presenting with dyspnea. Am Rev Respir Dis 1993; 147: 66-71 DOI: 10.1164/ajrccm/147.1.66.
• 46 Podnar S. Idiopathic phrenic neuropathies: A case series and review of the literature. Muscle Nerve 2015; 52: 986-992 DOI: 10.1002/mus.24673. (PMID: 25846409)
• 47 Tsao BE, Ostrovskiy DA, Wilbourn AJ. et al. Phrenic neuropathy due to neuralgic amyotrophy. Neurology 2006; 66: 1582-1584 DOI: 10.1212/01.wnl.0000216140.25497.40. (PMID: 16717226)
• 48 Dai Y, Patel A, Bierner SM. Phrenic nerve palsy in patients with neuralgic amyotrophy: case series study. Eur J Phys Rehabil Med 2019; 55: 519-521 DOI: 10.23736/S1973-9087.19.05294-8. (PMID: 31058474)
• 49 van Alfen N, Doorduin J, van Rosmalen MHJ. et al. Phrenic neuropathy and diaphragm dysfunction in neuralgic amyotrophy. Neurology 2018; 91: e843-e849 DOI: 10.1212/WNL.0000000000006076. (PMID: 30054437)
• 50 van Eijk JJJ, Dalton HR, Ripellino P. et al. Clinical phenotype and outcome of hepatitis E virus-associated neuralgic amyotrophy. Neurology 2017; 89: 909-917 DOI: 10.1212/WNL.0000000000004297. (PMID: 28768846)
• 51 Spiesshoefer J, Herkenrath S, Henke C. et al. Evaluation of Respiratory Muscle Strength and Diaphragm Ultrasound: Normative Values, Theoretical Considerations, and Practical Recommendations. Respiration 2020; 99: 369-381 DOI: 10.1159/000506016. (PMID: 32396905)
• 52 Nason LK, Walker CM, McNeeley MF. et al. Imaging of the Diaphragm: Anatomy and Function. RadioGraphics 2012; 32: E51-E70 DOI: 10.1148/rg.322115127. (PMID: 22411950)
• 53 Kabitz H-J, Walterspacher S, Mellies U. et al. Empfehlungen der Deutschen Atemwegsliga zur Messung der Atemmuskelfunktion. Pneumologie 2014; 68: 307-314 DOI: 10.1055/s-0034-1365283.
• 54 Laveneziana P, Albuquerque A, Aliverti A. et al. ERS statement on respiratory muscle testing at rest and during exercise. Eur Respir J 2019; 53: 1801214 DOI: 10.1183/13993003.01214-2018. (PMID: 30956204)
• 55 Steier J, Kaul S, Seymour J. et al. The value of multiple tests of respiratory muscle strength. Thorax 2007; 62: 975-980 DOI: 10.1136/thx.2006.072884. (PMID: 17557772)
• 56 van Alfen N, van Engelen BG, Hughes RA. Treatment for idiopathic and hereditary neuralgic amyotrophy (brachial neuritis). Cochrane Database Syst Rev 2009; 2009: CD006976 DOI: 10.1002/14651858.CD006976.pub2. (PMID: 19588414)
• 57 van Eijk JJJ, van Alfen N, Berrevoets M. et al. Evaluation of prednisolone treatment in the acute phase of neuralgic amyotrophy: an observational study. J Neurol Neurosurg Psychiatry 2009; 80: 1120-1124 DOI: 10.1136/jnnp.2008.163386. (PMID: 19321467)
• 58 Chuk R, Sheppard M, Wallace G. et al. Pediatric Hereditary Neuralgic Amyotrophy: Successful Treatment With Intravenous Immunoglobulin and Insights Into SEPT9 Pathogenesis. Child Neurol Open 2016; 3: 2329048X16668970 DOI: 10.1177/2329048X16668970.
• 59 Eijk JJ van, Cuppen I, Alfen N van. et al. Treatment for neonatal neuralgic amyotrophy. Eur J Paediatr Neurol 2009; 13: 283-285 DOI: 10.1016/j.ejpn.2008.04.007. (PMID: 18571949)
• 60 Johnson NE, Petraglia AL, Huang JH. et al. Rapid resolution of severe neuralgic amyotrophy after treatment with corticosteroids and intravenous immunoglobulin. Muscle Nerve 2011; 44: 304-305 DOI: 10.1002/mus.22100.
• 61 Moriguchi K, Miyamoto K, Takada K. et al. Four cases of anti-ganglioside antibody-positive neuralgic amyotrophy with good response to intravenous immunoglobulin infusion therapy. J Neuroimmunol 2011; 238: 107-109 DOI: 10.1016/j.jneuroim.2011.08.005.
• 62 Morishima R, Nagaoka U, Nagao M. et al. Chronic Brachial Plexus Neuritis That Developed into Typical Neuralgic Amyotrophy and Positively Responded to Immunotherapy. Intern Med 2018; 57: 1021-1026 DOI: 10.2169/internalmedicine.9482-17.
• 63 Naito K, Fukushima K, Suzuki S. et al. Intravenous Immunoglobulin (IVIg) with Methylprednisolone Pulse Therapy for Motor Impairment of Neuralgic Amyotrophy: Clinical Observations in 10 Cases. Intern Med 2012; 51: 1493-1500 DOI: 10.2169/internalmedicine.51.7049.
• 64 Wu P, Yang JY, Chen L. et al. Surgical and conservative treatments of complete spontaneous posterior interosseous nerve palsy with hourglass-like fascicular constrictions: a retrospective study of 41 cases. Neurosurgery 2014; 75: 250-257 DOI: 10.1227/NEU.0000000000000424.
• 65 Gstoettner C, Mayer JA, Rassam S. et al. Neuralgic amyotrophy: a paradigm shift in diagnosis and treatment. J Neurol Neurosurg Psychiatry 2020; 91: 879-888 DOI: 10.1136/jnnp-2020-323164. (PMID: 32487526)
• 66 Caleffi Pereira M, Dacha S, Testelmans D. et al. Assessing the effects of inspiratory muscle training in a patient with unilateral diaphragm dysfunction. Breathe 2019; 15: e90-e96 DOI: 10.1183/20734735.0129-2019.
• 67 Petrovic M, Lahrmann H, Pohl W. et al. Idiopathic diaphragmatic paralysis—Satisfactory improvement of inspiratory muscle function by inspiratory muscle training. Respir Physiol Neurobiol 2009; 165: 266-267 DOI: 10.1016/j.resp.2008.11.010. (PMID: 19111633)
• 68 Chan JS, Mann LM, Doherty CJ. et al. The effect of inspiratory muscle training and detraining on the respiratory metaboreflex. Exp Physiol 2023; 108: 636-649 DOI: 10.1113/EP090779.
• 69 Haidl P, Jany B, Geiseler J. et al. Leitlinie zur Langzeit-Sauerstofftherapie. Pneumologie 2020; 74: 813-841 DOI: 10.1055/a-1252-1492.
• 70 Onders RP, Elmo M, Kaplan C. et al. Extended use of diaphragm pacing in patients with unilateral or bilateral diaphragm dysfunction: A new therapeutic option. Surgery 2014; 156: 776-786 DOI: 10.1016/j.surg.2014.07.021. (PMID: 25239317)
• 71 Podgaetz E, Garza-Castillon R, Andrade RS. Best Approach and Benefit of Plication for Paralyzed Diaphragm. Thorac Surg Clin 2016; 26: 333-346 DOI: 10.1016/j.thorsurg.2016.04.009. (PMID: 27427528)
• 72 Wiesemann S, Haager B, Passlick B. Surgical Therapy of Acquired Unilateral Diaphragmatic Paralysis: Indication and Results. Zentralbl Chir 2016; 141 (Suppl. 01) S43-49 DOI: 10.1055/s-0042-113192. (PMID: 27607888)