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Severe acute myopathy following SARS-CoV-2 infection: a case report and review of recent literature

Severe acute myopathy following SARS-CoV-2 infection: a case report and review of recent literature Background: SARS-CoV2 virus could be potentially myopathic. Serum creatinine phosphokinase (CPK) is frequently found elevated in severe SARS-CoV2 infection, which indicates skeletal muscle damage precipitating limb weakness or even ventilatory failure. Case presentation: We addressed such a patient in his forties presented with features of severe SARS-CoV2 pneumonia and high serum CPK. He developed severe sepsis and acute respiratory distress syndrome (ARDS) and received intravenous high dose corticosteroid and tocilizumab to counter SARS-CoV2 associated cytokine surge. After 10 days of mechanical ventilation (MV), weaning was unsuccessful albeit apparently clear lung fields, having additionally severe and symmetric limb muscle weakness. Ancillary investigations in addition with serum CPK, including electromyogram, muscle biopsy, and muscle magnetic resonance imaging (MRI) suggested acute myopathy possibly due to skeletal myositis. Conclusion: We wish to stress that myopathogenic medication in SARS-CoV2 pneumonia should be used with caution. Additionally, serum CPK could be a potential marker to predict respiratory failure in SARS-CoV2 pneumonia as skeletal myopathy affecting chest muscles may contribute ventilatory failure on top of oxygenation failure due to SARS-CoV2 pneumonia. Keywords: Myopathy, Guillain-Barré syndrome, Nerve conduction, Electromyogram, SARS-CoV2 Background like skeletal muscle or sensory receptor organs. Neuro- Swarming spread of SARS-CoV2 pandemic revealed sub- tropism of this virus is apparent from the evidence of stantial and varied neuromuscular manifestations [1]. impairment of test and/or smell sensation early in the Recent data from Wuhan, China, suggest that neuro- course of illness, which specifies its affection toward gus- logical symptoms/signs are present in over 30% of pa- tatory or olfactory sensory nerve terminals. The virus is tients with severe SARS-CoV2 infection [1]. It spans also isolated from the cerebrospinal fluid suggesting po- from involvement of the central to the peripheral ner- tential neuroinvasive nature of SARS-CoV2. Involvement vous system manifesting as headache, dizziness, enceph- of the peripheral nerves was claimed to have association alopathy, epileptic seizures, and stroke or muscle with SARS-CoV2 infection resulting in Guillain-Barré weakness. This involvement indicates its affinity toward syndrome (GBS). On the other hand, skeletal muscle different levels of nervous system or the effector tissues damage due to SARS-CoV2 infection has been highlighted in several reports documenting nearly 23% * Correspondence: badrul.islam@icddrb.org of severe infection [1–3]. Importantly, weakness due to Laboratory Sciences and Services Division (LSSD), International Center for severe myopathy can adversely affect the outcome in Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh SARS-CoV2 pneumonia. Recently acute severe Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Islam et al. Skeletal Muscle (2021) 11:10 Page 2 of 7 myopathic weakness has been documented in six pa- immediately shifted to intensive care unit (ICU) address- tients in severe SARS-CoV2 pneumonia requiring mech- ing the severity of chest infection and need for respira- anical ventilation [3], however the mechanism of skeletal tory assistance. High flow oxygen was given through muscle damage remained elusive. Our patient may in nasal canula, intravenous fluid, and ceftriaxone 1g bd part address the pathogenesis of myopathy in SARS- were administered and necessary investigations were CoV2 infection. sent including deep nasopharyngeal swab for PCR for SARS-CoV2. Inspite of receiving high flow oxygen, due Case presentation to relentless desaturation of peripheral SpO2, he was A 42-year-hypertensive man having history of bronchial orotracheally intubated for assisted mechanical ventila- asthma presented with high-grade continuous fever, dry tion. His peripheral blood picture showed high total cough, and sore throat. He was brought to hospital for leukocyte count with neutrophilic leukocytosis, elevated difficulty in breathing, experienced on day 5 of his fe- serum C-reactive protein, procalcitonin, ferritin, and brile illness. On admission, he looked toxic, febrile (103 serum CPK (Table 1). Chest X-ray showed bilateral °F) and tachypnoeic (40 breaths/min) with low periph- bronchopneumonic patchy opacities but serum troponin, eral SpO2 (85%). He was hypotensive (90/40 mm Hg) serum pro-BNP, and echocardiogram was within normal having a rapid pulse (120/min). Wheeze and crackles range. He was PCR positive for SARS-CoV2 and re- were obvious on chest auscultation especially on mid ceived intravenous remdesivir (100 mg daily for 10 days), and lower zones of both lung fields along with woody tocilizumab (8 mg/kg; 2 doses), and dexamethasone (5 dull percussion note in the abovementioned areas. This mg q6h for 5 days and 5 mg bd for 7 days). Otherwise, suggested severe SARS-CoV2 pneumonia. He was in favor, he had intact orientation and his hemoglobin Table 1 Laboratory investigation findings of the presented case with acute myopathy following SARS-CoV2 infection Investigations (normal value and unit of measurement) Patient value on admission and range during hospital stay Hemoglobin (13.5-17.5 g/dl) 14.5 (14.5-9.2) Total leukocyte count (4500 to 11,000/μl) 21,100 (10,170-31,780) Polymorph (40-65%) 93% (62-94) Lymphocyte (30-50%) 4% (4-36) Total platelet count (150,000 to 400,000/μl) 295,000 (270,000 to 480,000/μl) C-reactive protein (< 5 mg/L) 300 (2.7-300) Serum procalcitonin (0.10-0.49 ng/mL) 5.69 (0.27-5.69) Serum ferritin (< 250 ng/mL) 811 (799-2185) Serum D-dimer (< 0.4 mcg/mL) 1.25 (1.25-5.55) Serum PT (11-13.5 s) 13 (13-15) Serum aPTT (25-35 s) 33 (30-33) Serum CPK (< 120 mcg/mL) 850 (637-1325) Serum electrolytes Na (135-145) mmol/L 138 (134-152) K (3.5-5.5) mmol/L 4.6 (3.5-5.1) Ca (8.5-10.5) mg/dl 8.6 (7.6-8.6) Mg (1.5-2.5) mmol/L 1.9 (1.9-3) Serum creatinine (60-110 μmol/L) 87 (71-155) Serum SGPT (7-56 U/L) 32 (32-45) Serum troponin-I (< 0.04 ng/ml) 0.02 (0.02-0.2) Serum Pro-BNP (< 125 pg/mL) 130 (109-130) Serum anti GM1 antibody (− ve) Cerebrospinal fluid (CSF) Total protein (up to 45 mg/dl) 10 Total WBC count (0-5/cmm) 05 PT prothrombin time, aPTT activated partial thromboplastin time, CPK creatinine phosphokinase, SGPT serum glutamic pyruvic transaminase, BNP brain natriuretic peptide, WBC white blood cells Islam et al. Skeletal Muscle (2021) 11:10 Page 3 of 7 level, coagulation profile (platelet count, PT, and APTT), pressure support ventilation (PSV) for the last 4 days serum electrolytes, serum anti-GM1 antibody titer and using continuous positive airway pressure (CPAP) mode blood sugar level were within normal limits and he had ventilation. preserved liver and renal functions (Table 1). However, He became SARS-CoV2 negative on repeat PCR on his serum D-dimer was elevated. Subsequently, high day 15 of his onset of weakness. Improvement of his resolution spiral CT scan of chest revealed bilateral dif- limb muscles showed fair progress (muscle power: dis- fuse ground glass densities and reticulation with features tal= 4/5 and proximal= 3/5) when he was discharged of consolidation and sub-segmental pulmonary embol- from hospital after 4 weeks of his hospital stay. His ism. Accordingly, he received subcutaneous low molecu- muscle power was normalized 1 month after his dis- lar weight heparin for 2 weeks from the second day of charge from hospital. At this time, his serum CPK, D- his ICU admission. In view of high CRP, increasing O dimer, and serum ferritin were within normal limit and requirement and inability to sustain a stable blood pres- a repeat MRI of his lower limb muscles appeared almost sure, tracheal aspirate, blood and urine samples were normal (Fig. 2f). sent for culture and sensitivity (CS) on the 3rd day of admission to exclude secondary bacterial infection. Cef- Discussion and conclusions triaxone was changed to intravenous teicoplanin (for 10 Severe acute myopathy can be a life-threatening compli- days) for a broader antibacterial coverage. Tracheal as- cation in SARS-CoV2 infection. Our patient presented pirate CS revealed growth of methicillin-resistant with SARS-CoV2 pneumonia complicated to acute re- Staphylococcus aureus (MRSA), which was fortunately spiratory distress syndrome (ARDS) and eventually de- sensitive to teicoplanin. He required sedation (intraven- veloped features of severe myopathy in quick succession. ous midazolam and fentanyl for 10 days) and muscle re- However, serum CPK was already elevated on admission laxation (IV vecuronium for 2 days) to maximize the suggesting the particular potential to damage the skeletal tolerability of mechanical ventilation. On the 10th day of muscle tissue from the beginning of illness. Throughout his mechanical ventilation, when sedation was gradually the illness, except severe pneumonia, sepsis, and skeletal withdrawn, weaning from ventilator was unsuccessful muscle damage, other major organ functions were stable. and marked symmetrical upper and lower limb weakness SARS CoV’s predilection for the skeletal muscle was was apparent. Both his upper and lower limbs were par- known from the pandemic that broke in March 2003 [4, alyzed (power 0/5), moderately wasted, flabby, and deep 5]. At that time, in addition to lung damage, muscle tendon reflexes could not be elicited with an intact sen- weakness and elevation of serum CPK level was docu- sation in all modalities. However, he was fully alert, and mented in more than 30% of the SARS-infected patients functions of all cranial nerves were preserved. At this [6]. Similar myopathogenic potential has also been docu- time, serum CPK was higher (1325 mcg/mL) than at ad- mented currently in around 20% severe SARS-CoV2 in- mission (850 mcg/mL). Electrophysiology done on day fection [1]. However, the pathogenesis of muscle damage 20 of admission revealed normal motor and sensory con- still remains unknown. duction but myopathic changes on needle electromyo- A series of six cases with acute myopathy has recently gram (EMG) examination, consisting of spontaneous been published from Italy [3]. All the cases in the Italian muscle fiber activity, small motor unit potentials, and a series showed marked prolongation of motor nerve distal full recruitment pattern (Fig. 1). Thigh and calf muscle Compound Muscle Action Potential (dCMAP) duration, MRI done on day 20, showed marked hyperintensity in which was absent in our case. Prolongation of dCMAP both the quadriceps muscles (Fig. 2e), mild hyperinten- indicates distal motor nerve myelin damage, frequently sity in the hamstrings, and patchy hyperintensity in the present in demyelinating GBS. Terminal motor axons leg muscles. Skeletal muscle histopathology done on day are vulnerable to immune-mediated attack because here 23 and muscle sections sampled from quadriceps the blood nerve barrier is deficient and axons become femoris showed variation in muscle fiber size with pre- unmyelinated just before they join the myoneural junc- dominantly spherical shape myosites and multifocal and tion. Therefore, immune mediated or direct viral inva- discrete myosite degeneration lacking infiltration of in- sion at the nerve terminals could be a possibility of flammatory cells (Fig. 2a-d). Other specific histopatho- paranodal disruption resulting features of distal demye- logic or histochemical analyses could not be done. lination. However, evidence goes in favor of indirect Eventually, he could be weaned from respirator and muscle injury, as viral particles could not be isolated maintain SpO2 with ambient air at day 18 from the day from damaged skeletal muscle tissues of the patients in- of intubation. He was mechanically ventilated with con- fected with SARS-CoV [4]. Additionally, prolongation of trol/assist control mode ventilation for the 1st 2 days dCMAP has also been documented in some cases of and then put onto synchronized intermittent mandatory critical care myopathy, postulated slowing of the muscle ventilation (SIMV) mode for 12 days and was on only Islam et al. Skeletal Muscle (2021) 11:10 Page 4 of 7 Fig. 1 Nerve conduction study, electromyogram, and disease trajectory. (a) Motor and sensory nerve conduction was normal despite severe muscle weakness. Compound muscle action potential (CMAP) amplitudes are measured in millivolts (mV); 2 mV per division for all motor study traces. DML, distal motor latency in ms. MCV1, motor conduction velocity in millisecond (ms). MCV2, motor conduction velocity in ms. Sensory nerve action potential (SNAP) amplitudes are measured in microvolts (μV); 20 μV per division for all sensory study traces. DSL, distal sensory latency. SCV, sensory conduction velocity. (b) Electromyogram (EMG) showing myopathic motor unit potentials, a full recruitment pattern and spontaneous muscle fiber activity in several sampled muscles. Motor unit potential (MUP) amplitudes are measured in microvolt (μV); 200 μV per division for all EMG traces fiber conduction velocity, and reduced sarcolemmal ex- SARS-CoV2 infection could be co-incidental as sufficient citability [7]. epidemiological evidence is lacking which was very obvi- Our patient presented with rapidly progressing sym- ous between GBS and Zika virus infection in recent past metrical quadriplagia and loss of deep tendon reflexes. [11]. Our clinical suspicion of GBS was also doubted, as We assumed the possibility of Guillain-Barré syndrome despite having marked muscle weakness, our patient did (GBS), which has been documented to be associated not have any cranial nerve deficits, elevated serum CPK, with SARS-CoV2 infection in recent literatures [8–10]. and cerebrospinal fluid assessment did not reveal albu- Based on our interpretation, this association of GBS and minocytological dissociation. Evaluation of serum anti- Islam et al. Skeletal Muscle (2021) 11:10 Page 5 of 7 Fig. 2 (See legend on next page.) Islam et al. Skeletal Muscle (2021) 11:10 Page 6 of 7 (See figure on previous page.) Fig. 2 Muscle histopathology and MRI of upper thigh axial sections. (a-d) Muscle histopathology sections sampled from quadriceps femoris muscle stained with hematoxylin and eosin, showed variation in muscle fiber size with predominantly spherical shape myosites and multifocal and discrete myosite degeneration lacking infiltration of inflammatory cells. (e) T2 weighted MRI section of the upper thigh done on day 20, showed marked hyperintensity in both the quadriceps muscles. (f) Repeat T2-weighted MRI of the same section of the thigh muscles done after 48 days of the 1st MRI shows both the quadriceps muscles appear normal GM1 antibody was within normal limit, which is a po- Although we were not able to determine whether our tential marker for pure motor AMAN variant of GBS, patient had CIM or SARS-CoV2 associated myopathy, prevalent in Bangladesh [12]. Eventually, electrophysi- the following arguments are in favor of CIM: (i) an epi- ology suggested myopathic involvement. We admit that sode of ARDS requiring prolonged mechanical ventila- ARDS, severe sepsis, and potentially myopathogenic tion, (ii) use of myopathogenic medication like muscle medications like corticosteroids and muscle relaxants relaxants and corticosteroids. On the other hand, SARS- that had been used in the ICU could possibly trigger CoV2-associated myopathy is favored by (i) presence of critical illness polyneuropathy/myopathy (CIP/CIM) [13] high serum CPK before the onset of mechanical ventila- and in part may contribute in the disease process. How- tion, (ii) the fact that high serum CPK is unusual in CIM ever, muscle relaxant was used for only 2 days and [19, 20], (iii) the remarkable synchronicity of myopathy serum CPK was already high at admission when none of and SARS-CoV2 infection, (iv) muscle MRI imaging these medications were used. Moreover, in critical care, compatible with myositis, (v) the similarity of our case myopathy raised serum CPK is not common. In light of with an Italian series of SARS-CoV2 cases [21], and (vi) recent evidence on CIP/CIM animal model, steroid may epidemiologic evidence of myopathogenicity in SARS- not be substantially contributing to CIM [14, 15]. MRI CoV2 infection [1–3]. of the pelvis and lower limb muscles clearly showed In conclusion, we want to stress the possible myotoxic hyperintensity in both quadriceps and leg muscles sug- effect of SARS-CoV2 that should be carefully assessed gestive of myositis. However, muscle histopathology particularly in severe SARS-CoV2 infection. In addition, showed multifocal and discrete myosite degeneration it merits exploring, whether serum CPK is a potential without infiltration of inflammatory cells suggesting prognostic indicator for muscle weakness and prolonged noninflammatory pathology. However, role of neucleo- mechanical ventilation. tide analog antiviral drug remdicivir and anti-IL6 anti- body tocilizumab were unlikely to contribute in the Abbreviations process of weakness but they might influence the muscle CPK: Serum creatinine phosphokinase; EMG: Electromyogram; ARDS: Acute respiratory distress syndrome; MV: Mechanical ventilation; MRI: Magnetic biopsy findings specially extinguishing inflammatory evi- resonance imaging; GBS: Guillain-Barré syndrome; AMAN: Acute Motor dences where corticosteroids could also had a substantial Axonal Neuropathy; ICU: Intensive care unit; PT: Prothrombin time; role. These muscle histopathology features are nonspe- aPTT: Activated partial thromboplastin time; SGPT: Serum glutamic pyruvic transaminase; BNP: Brain natriuretic peptide; WBC: White blood cells; cific and similar to CIM or viral myositis found in influ- CS: Culture and sensitivity; MRSA: Methicillin-resistant Staphylococcus aureus; enza B. But infectious nature of myositis was established dCMAP: Distal Compound Muscle Action Potential; CIP: Critical illness as influenza B virus could be isolated from skeletal polyneuropathy; CIM: Critical illness myopathy muscle tissue [16]. Importantly, even in the past, neither muscle inflammation nor SARS-CoV could not be isolated Acknowledgements from cadavericskeletalmuscletissuefromconfirmed SARS- We acknowledge the contribution of icddr,b’s core donors including the governments of Bangladesh, Canada, Sweden, and the UK for their CoV infected patients with features of severe myopathy, sug- continuous support and commitment to icddr,b’s research efforts. gesting CIM, or indirect myotoxic effect of this virus [4]. This is acknowledged that Th1 cell-mediated cytokines can produce inflammatory response in muscle tissue [17]. Inter- Authors’ contributions BI has written the manuscript and performed the nerve electrophysiology, estingly, cytokine storm in SARS-CoV2 is also Th1 driven, MA has treated the patient in the ICU, ZI has performed the Anti GM1 that can induce muscle inflammation [18]. antibody test, SMB has performed the muscle histopathology. The authors We admit, due to limited laboratory facilities, we could read and approved the final manuscript. not explore further to identify the cause of this skeletal myopathy. Since thick filament myopathy is the com- Funding monest form of CIM, assessment of the content of my- This research activity was not funded. osin in relation to actin in the skeletal muscle tissue through electrophoretic separation could help a step for- Availability of data and materials ward to ascertain this type of myopathy with more All data generated or analyzed during this study are included in this precision. published article. Islam et al. Skeletal Muscle (2021) 11:10 Page 7 of 7 Declarations 14. Z’Graggen WJ, Schefold JC. Critical illness myopathy: glucocorticoids revisited? Acta physiologica (Oxford, England). 2019;225(2):e13205. Ethics approval and consent to participate 15. Akkad H, Cacciani N, Llano-Diez M, et al. Vamorolone treatment improves The study was approved by the ethics committees of the International skeletal muscle outcome in a critical illness myopathy rat model. Acta Center for Diarrhoeal Disease Research, Bangladesh and Bangladesh physiologica (Oxford, England). 2019;225(2):e13172. Specialized Hospital, Bangladesh. 16. Crum-Cianflone NF. Bacterial, fungal, parasitic, and viral myositis. Clinical microbiology reviews. 2008;21(3):473–94. https://doi.org/10.1128/CMR. 00001-08. Consent for publication 17. Moran EM, Mastaglia FL. Cytokines in immune-mediated inflammatory The patient’s wife gave written informed consent on behalf of the patient myopathies: cellular sources, multiple actions and therapeutic implications. (as the patient was unable to sign due to weakness). Clin Exp Immunol. 2014;178(3):405–15. https://doi.org/10.1111/cei.12445. 18. Coperchini F, Chiovato L, Croce L, Magri F, Rotondi M. The cytokine storm in COVID-19: an overview of the involvement of the chemokine/chemokine- Competing interests receptor system. Cytokine & growth factor reviews. 2020;53:25–32. https:// No authors have financial, professional, or personal conflict of interest that doi.org/10.1016/j.cytogfr.2020.05.003. may influence this manuscript to disclose. 19. Hund E. Neurological complications of sepsis: critical illness polyneuropathy and myopathy. Journal of neurology. 2001;248(11):929–34. https://doi.org/1 Author details 0.1007/s004150170043. Laboratory Sciences and Services Division (LSSD), International Center for 20. Shepherd S, Batra A, Lerner DP. Review of critical illness myopathy and Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh. neuropathy. The Neurohospitalist. 2017;7(1):41–8. https://doi.org/10.1177/1 Bangladesh Specialized Hospital, Dhaka, Bangladesh. 21. Madia F, Merico B, Primiano G, Cutuli SL, De Pascale G, Servidei S. Acute Received: 29 October 2020 Accepted: 4 April 2021 myopathic quadriplegia in COVID-19 patients in the intensive care unit. Neurology. 2020;95(11):492–4. https://doi.org/10.1212/WNL.00000000000102 References 1. Mao L, Jin H, Wang M, Hu Y, Chen S, He Q, et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. Publisher’sNote JAMA neurology. 2020;77(6):683–90. https://doi.org/10.1001/jamaneurol.202 Springer Nature remains neutral with regard to jurisdictional claims in 0.1127. published maps and institutional affiliations. 2. Guidon AC, Amato AA. COVID-19 and neuromuscular disorders. Neurology. 2020;94(22):959–69. https://doi.org/10.1212/WNL.0000000000009566. 3. Madia F, Merico B, Primiano G, Cutuli SL, De Pascale G, Servidei S. Acute myopathic quadriplegia in patients with COVID-19 in the intensive care unit. Neurology. 2020;95(11):492–4. https://doi.org/10.1212/WNL. 4. Leung TW, Wong KS, Hui AC, To KF, Lai ST, Ng WF, et al. Myopathic changes associated with severe acute respiratory syndrome: a postmortem case series. Archiv Neurol. 2005;62(7):1113–7. https://doi.org/10.1001/archneur.62. 7.1113. 5. Tsai LK, Hsieh ST, Chao CCm, Chen YC, Lin YH, Chang SC, Chang YC Neuromuscular disorders in severe acute respiratory syndrome. Archives of neurology 2004; 61(11): 1669-1673, DOI: https://doi.org/10.1001/archneur. 61.11.1669. 6. Lee N, Hui D, Wu A, Chan P, Cameron P, Joynt GM, et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med. 2003; 348(20):1986–94. https://doi.org/10.1056/NEJMoa030685. 7. Lacomis D. Electrophysiology of neuromuscular disorders in critical illness. Muscle & nerve. 2013;47(3):452–63. https://doi.org/10.1002/mus.23615. 8. Zhao H, Shen D, Zhou H, Liu J, Chen S. Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? The Lancet Neurology. 2020;19(5):383–4. https://doi.org/10.1016/S1474-4422(20)30109-5. 9. Toscano G, Palmerini F, Ravaglia S, Ruiz L, Invernizzi P, Cuzzoni MG, et al. Guillain-Barré syndrome associated with SARS-CoV-2. The New England journal of medicine. 2020;382(26):2574–6. https://doi.org/10.1056/NEJMc2 10. Scheidl E, Canseco DD, Hadji-Naumov A, Bereznai B. Guillain-Barré syndrome during SARS-CoV-2 pandemic: a case report and review of recent literature. Journal of the peripheral nervous system : JPNS. 2020;25(2):204–7. https:// doi.org/10.1111/jns.12382. 11. Cao-Lormeau VM, Blake A, Mons S, Lastère S, Roche C, Vanhomwegen J, et al. 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Severe acute myopathy following SARS-CoV-2 infection: a case report and review of recent literature

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Abstract

Background: SARS-CoV2 virus could be potentially myopathic. Serum creatinine phosphokinase (CPK) is frequently found elevated in severe SARS-CoV2 infection, which indicates skeletal muscle damage precipitating limb weakness or even ventilatory failure. Case presentation: We addressed such a patient in his forties presented with features of severe SARS-CoV2 pneumonia and high serum CPK. He developed severe sepsis and acute respiratory distress syndrome (ARDS) and received intravenous high dose corticosteroid and tocilizumab to counter SARS-CoV2 associated cytokine surge. After 10 days of mechanical ventilation (MV), weaning was unsuccessful albeit apparently clear lung fields, having additionally severe and symmetric limb muscle weakness. Ancillary investigations in addition with serum CPK, including electromyogram, muscle biopsy, and muscle magnetic resonance imaging (MRI) suggested acute myopathy possibly due to skeletal myositis. Conclusion: We wish to stress that myopathogenic medication in SARS-CoV2 pneumonia should be used with caution. Additionally, serum CPK could be a potential marker to predict respiratory failure in SARS-CoV2 pneumonia as skeletal myopathy affecting chest muscles may contribute ventilatory failure on top of oxygenation failure due to SARS-CoV2 pneumonia. Keywords: Myopathy, Guillain-Barré syndrome, Nerve conduction, Electromyogram, SARS-CoV2 Background like skeletal muscle or sensory receptor organs. Neuro- Swarming spread of SARS-CoV2 pandemic revealed sub- tropism of this virus is apparent from the evidence of stantial and varied neuromuscular manifestations [1]. impairment of test and/or smell sensation early in the Recent data from Wuhan, China, suggest that neuro- course of illness, which specifies its affection toward gus- logical symptoms/signs are present in over 30% of pa- tatory or olfactory sensory nerve terminals. The virus is tients with severe SARS-CoV2 infection [1]. It spans also isolated from the cerebrospinal fluid suggesting po- from involvement of the central to the peripheral ner- tential neuroinvasive nature of SARS-CoV2. Involvement vous system manifesting as headache, dizziness, enceph- of the peripheral nerves was claimed to have association alopathy, epileptic seizures, and stroke or muscle with SARS-CoV2 infection resulting in Guillain-Barré weakness. This involvement indicates its affinity toward syndrome (GBS). On the other hand, skeletal muscle different levels of nervous system or the effector tissues damage due to SARS-CoV2 infection has been highlighted in several reports documenting nearly 23% * Correspondence: badrul.islam@icddrb.org of severe infection [1–3]. Importantly, weakness due to Laboratory Sciences and Services Division (LSSD), International Center for severe myopathy can adversely affect the outcome in Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh SARS-CoV2 pneumonia. Recently acute severe Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Islam et al. Skeletal Muscle (2021) 11:10 Page 2 of 7 myopathic weakness has been documented in six pa- immediately shifted to intensive care unit (ICU) address- tients in severe SARS-CoV2 pneumonia requiring mech- ing the severity of chest infection and need for respira- anical ventilation [3], however the mechanism of skeletal tory assistance. High flow oxygen was given through muscle damage remained elusive. Our patient may in nasal canula, intravenous fluid, and ceftriaxone 1g bd part address the pathogenesis of myopathy in SARS- were administered and necessary investigations were CoV2 infection. sent including deep nasopharyngeal swab for PCR for SARS-CoV2. Inspite of receiving high flow oxygen, due Case presentation to relentless desaturation of peripheral SpO2, he was A 42-year-hypertensive man having history of bronchial orotracheally intubated for assisted mechanical ventila- asthma presented with high-grade continuous fever, dry tion. His peripheral blood picture showed high total cough, and sore throat. He was brought to hospital for leukocyte count with neutrophilic leukocytosis, elevated difficulty in breathing, experienced on day 5 of his fe- serum C-reactive protein, procalcitonin, ferritin, and brile illness. On admission, he looked toxic, febrile (103 serum CPK (Table 1). Chest X-ray showed bilateral °F) and tachypnoeic (40 breaths/min) with low periph- bronchopneumonic patchy opacities but serum troponin, eral SpO2 (85%). He was hypotensive (90/40 mm Hg) serum pro-BNP, and echocardiogram was within normal having a rapid pulse (120/min). Wheeze and crackles range. He was PCR positive for SARS-CoV2 and re- were obvious on chest auscultation especially on mid ceived intravenous remdesivir (100 mg daily for 10 days), and lower zones of both lung fields along with woody tocilizumab (8 mg/kg; 2 doses), and dexamethasone (5 dull percussion note in the abovementioned areas. This mg q6h for 5 days and 5 mg bd for 7 days). Otherwise, suggested severe SARS-CoV2 pneumonia. He was in favor, he had intact orientation and his hemoglobin Table 1 Laboratory investigation findings of the presented case with acute myopathy following SARS-CoV2 infection Investigations (normal value and unit of measurement) Patient value on admission and range during hospital stay Hemoglobin (13.5-17.5 g/dl) 14.5 (14.5-9.2) Total leukocyte count (4500 to 11,000/μl) 21,100 (10,170-31,780) Polymorph (40-65%) 93% (62-94) Lymphocyte (30-50%) 4% (4-36) Total platelet count (150,000 to 400,000/μl) 295,000 (270,000 to 480,000/μl) C-reactive protein (< 5 mg/L) 300 (2.7-300) Serum procalcitonin (0.10-0.49 ng/mL) 5.69 (0.27-5.69) Serum ferritin (< 250 ng/mL) 811 (799-2185) Serum D-dimer (< 0.4 mcg/mL) 1.25 (1.25-5.55) Serum PT (11-13.5 s) 13 (13-15) Serum aPTT (25-35 s) 33 (30-33) Serum CPK (< 120 mcg/mL) 850 (637-1325) Serum electrolytes Na (135-145) mmol/L 138 (134-152) K (3.5-5.5) mmol/L 4.6 (3.5-5.1) Ca (8.5-10.5) mg/dl 8.6 (7.6-8.6) Mg (1.5-2.5) mmol/L 1.9 (1.9-3) Serum creatinine (60-110 μmol/L) 87 (71-155) Serum SGPT (7-56 U/L) 32 (32-45) Serum troponin-I (< 0.04 ng/ml) 0.02 (0.02-0.2) Serum Pro-BNP (< 125 pg/mL) 130 (109-130) Serum anti GM1 antibody (− ve) Cerebrospinal fluid (CSF) Total protein (up to 45 mg/dl) 10 Total WBC count (0-5/cmm) 05 PT prothrombin time, aPTT activated partial thromboplastin time, CPK creatinine phosphokinase, SGPT serum glutamic pyruvic transaminase, BNP brain natriuretic peptide, WBC white blood cells Islam et al. Skeletal Muscle (2021) 11:10 Page 3 of 7 level, coagulation profile (platelet count, PT, and APTT), pressure support ventilation (PSV) for the last 4 days serum electrolytes, serum anti-GM1 antibody titer and using continuous positive airway pressure (CPAP) mode blood sugar level were within normal limits and he had ventilation. preserved liver and renal functions (Table 1). However, He became SARS-CoV2 negative on repeat PCR on his serum D-dimer was elevated. Subsequently, high day 15 of his onset of weakness. Improvement of his resolution spiral CT scan of chest revealed bilateral dif- limb muscles showed fair progress (muscle power: dis- fuse ground glass densities and reticulation with features tal= 4/5 and proximal= 3/5) when he was discharged of consolidation and sub-segmental pulmonary embol- from hospital after 4 weeks of his hospital stay. His ism. Accordingly, he received subcutaneous low molecu- muscle power was normalized 1 month after his dis- lar weight heparin for 2 weeks from the second day of charge from hospital. At this time, his serum CPK, D- his ICU admission. In view of high CRP, increasing O dimer, and serum ferritin were within normal limit and requirement and inability to sustain a stable blood pres- a repeat MRI of his lower limb muscles appeared almost sure, tracheal aspirate, blood and urine samples were normal (Fig. 2f). sent for culture and sensitivity (CS) on the 3rd day of admission to exclude secondary bacterial infection. Cef- Discussion and conclusions triaxone was changed to intravenous teicoplanin (for 10 Severe acute myopathy can be a life-threatening compli- days) for a broader antibacterial coverage. Tracheal as- cation in SARS-CoV2 infection. Our patient presented pirate CS revealed growth of methicillin-resistant with SARS-CoV2 pneumonia complicated to acute re- Staphylococcus aureus (MRSA), which was fortunately spiratory distress syndrome (ARDS) and eventually de- sensitive to teicoplanin. He required sedation (intraven- veloped features of severe myopathy in quick succession. ous midazolam and fentanyl for 10 days) and muscle re- However, serum CPK was already elevated on admission laxation (IV vecuronium for 2 days) to maximize the suggesting the particular potential to damage the skeletal tolerability of mechanical ventilation. On the 10th day of muscle tissue from the beginning of illness. Throughout his mechanical ventilation, when sedation was gradually the illness, except severe pneumonia, sepsis, and skeletal withdrawn, weaning from ventilator was unsuccessful muscle damage, other major organ functions were stable. and marked symmetrical upper and lower limb weakness SARS CoV’s predilection for the skeletal muscle was was apparent. Both his upper and lower limbs were par- known from the pandemic that broke in March 2003 [4, alyzed (power 0/5), moderately wasted, flabby, and deep 5]. At that time, in addition to lung damage, muscle tendon reflexes could not be elicited with an intact sen- weakness and elevation of serum CPK level was docu- sation in all modalities. However, he was fully alert, and mented in more than 30% of the SARS-infected patients functions of all cranial nerves were preserved. At this [6]. Similar myopathogenic potential has also been docu- time, serum CPK was higher (1325 mcg/mL) than at ad- mented currently in around 20% severe SARS-CoV2 in- mission (850 mcg/mL). Electrophysiology done on day fection [1]. However, the pathogenesis of muscle damage 20 of admission revealed normal motor and sensory con- still remains unknown. duction but myopathic changes on needle electromyo- A series of six cases with acute myopathy has recently gram (EMG) examination, consisting of spontaneous been published from Italy [3]. All the cases in the Italian muscle fiber activity, small motor unit potentials, and a series showed marked prolongation of motor nerve distal full recruitment pattern (Fig. 1). Thigh and calf muscle Compound Muscle Action Potential (dCMAP) duration, MRI done on day 20, showed marked hyperintensity in which was absent in our case. Prolongation of dCMAP both the quadriceps muscles (Fig. 2e), mild hyperinten- indicates distal motor nerve myelin damage, frequently sity in the hamstrings, and patchy hyperintensity in the present in demyelinating GBS. Terminal motor axons leg muscles. Skeletal muscle histopathology done on day are vulnerable to immune-mediated attack because here 23 and muscle sections sampled from quadriceps the blood nerve barrier is deficient and axons become femoris showed variation in muscle fiber size with pre- unmyelinated just before they join the myoneural junc- dominantly spherical shape myosites and multifocal and tion. Therefore, immune mediated or direct viral inva- discrete myosite degeneration lacking infiltration of in- sion at the nerve terminals could be a possibility of flammatory cells (Fig. 2a-d). Other specific histopatho- paranodal disruption resulting features of distal demye- logic or histochemical analyses could not be done. lination. However, evidence goes in favor of indirect Eventually, he could be weaned from respirator and muscle injury, as viral particles could not be isolated maintain SpO2 with ambient air at day 18 from the day from damaged skeletal muscle tissues of the patients in- of intubation. He was mechanically ventilated with con- fected with SARS-CoV [4]. Additionally, prolongation of trol/assist control mode ventilation for the 1st 2 days dCMAP has also been documented in some cases of and then put onto synchronized intermittent mandatory critical care myopathy, postulated slowing of the muscle ventilation (SIMV) mode for 12 days and was on only Islam et al. Skeletal Muscle (2021) 11:10 Page 4 of 7 Fig. 1 Nerve conduction study, electromyogram, and disease trajectory. (a) Motor and sensory nerve conduction was normal despite severe muscle weakness. Compound muscle action potential (CMAP) amplitudes are measured in millivolts (mV); 2 mV per division for all motor study traces. DML, distal motor latency in ms. MCV1, motor conduction velocity in millisecond (ms). MCV2, motor conduction velocity in ms. Sensory nerve action potential (SNAP) amplitudes are measured in microvolts (μV); 20 μV per division for all sensory study traces. DSL, distal sensory latency. SCV, sensory conduction velocity. (b) Electromyogram (EMG) showing myopathic motor unit potentials, a full recruitment pattern and spontaneous muscle fiber activity in several sampled muscles. Motor unit potential (MUP) amplitudes are measured in microvolt (μV); 200 μV per division for all EMG traces fiber conduction velocity, and reduced sarcolemmal ex- SARS-CoV2 infection could be co-incidental as sufficient citability [7]. epidemiological evidence is lacking which was very obvi- Our patient presented with rapidly progressing sym- ous between GBS and Zika virus infection in recent past metrical quadriplagia and loss of deep tendon reflexes. [11]. Our clinical suspicion of GBS was also doubted, as We assumed the possibility of Guillain-Barré syndrome despite having marked muscle weakness, our patient did (GBS), which has been documented to be associated not have any cranial nerve deficits, elevated serum CPK, with SARS-CoV2 infection in recent literatures [8–10]. and cerebrospinal fluid assessment did not reveal albu- Based on our interpretation, this association of GBS and minocytological dissociation. Evaluation of serum anti- Islam et al. Skeletal Muscle (2021) 11:10 Page 5 of 7 Fig. 2 (See legend on next page.) Islam et al. Skeletal Muscle (2021) 11:10 Page 6 of 7 (See figure on previous page.) Fig. 2 Muscle histopathology and MRI of upper thigh axial sections. (a-d) Muscle histopathology sections sampled from quadriceps femoris muscle stained with hematoxylin and eosin, showed variation in muscle fiber size with predominantly spherical shape myosites and multifocal and discrete myosite degeneration lacking infiltration of inflammatory cells. (e) T2 weighted MRI section of the upper thigh done on day 20, showed marked hyperintensity in both the quadriceps muscles. (f) Repeat T2-weighted MRI of the same section of the thigh muscles done after 48 days of the 1st MRI shows both the quadriceps muscles appear normal GM1 antibody was within normal limit, which is a po- Although we were not able to determine whether our tential marker for pure motor AMAN variant of GBS, patient had CIM or SARS-CoV2 associated myopathy, prevalent in Bangladesh [12]. Eventually, electrophysi- the following arguments are in favor of CIM: (i) an epi- ology suggested myopathic involvement. We admit that sode of ARDS requiring prolonged mechanical ventila- ARDS, severe sepsis, and potentially myopathogenic tion, (ii) use of myopathogenic medication like muscle medications like corticosteroids and muscle relaxants relaxants and corticosteroids. On the other hand, SARS- that had been used in the ICU could possibly trigger CoV2-associated myopathy is favored by (i) presence of critical illness polyneuropathy/myopathy (CIP/CIM) [13] high serum CPK before the onset of mechanical ventila- and in part may contribute in the disease process. How- tion, (ii) the fact that high serum CPK is unusual in CIM ever, muscle relaxant was used for only 2 days and [19, 20], (iii) the remarkable synchronicity of myopathy serum CPK was already high at admission when none of and SARS-CoV2 infection, (iv) muscle MRI imaging these medications were used. Moreover, in critical care, compatible with myositis, (v) the similarity of our case myopathy raised serum CPK is not common. In light of with an Italian series of SARS-CoV2 cases [21], and (vi) recent evidence on CIP/CIM animal model, steroid may epidemiologic evidence of myopathogenicity in SARS- not be substantially contributing to CIM [14, 15]. MRI CoV2 infection [1–3]. of the pelvis and lower limb muscles clearly showed In conclusion, we want to stress the possible myotoxic hyperintensity in both quadriceps and leg muscles sug- effect of SARS-CoV2 that should be carefully assessed gestive of myositis. However, muscle histopathology particularly in severe SARS-CoV2 infection. In addition, showed multifocal and discrete myosite degeneration it merits exploring, whether serum CPK is a potential without infiltration of inflammatory cells suggesting prognostic indicator for muscle weakness and prolonged noninflammatory pathology. However, role of neucleo- mechanical ventilation. tide analog antiviral drug remdicivir and anti-IL6 anti- body tocilizumab were unlikely to contribute in the Abbreviations process of weakness but they might influence the muscle CPK: Serum creatinine phosphokinase; EMG: Electromyogram; ARDS: Acute respiratory distress syndrome; MV: Mechanical ventilation; MRI: Magnetic biopsy findings specially extinguishing inflammatory evi- resonance imaging; GBS: Guillain-Barré syndrome; AMAN: Acute Motor dences where corticosteroids could also had a substantial Axonal Neuropathy; ICU: Intensive care unit; PT: Prothrombin time; role. These muscle histopathology features are nonspe- aPTT: Activated partial thromboplastin time; SGPT: Serum glutamic pyruvic transaminase; BNP: Brain natriuretic peptide; WBC: White blood cells; cific and similar to CIM or viral myositis found in influ- CS: Culture and sensitivity; MRSA: Methicillin-resistant Staphylococcus aureus; enza B. But infectious nature of myositis was established dCMAP: Distal Compound Muscle Action Potential; CIP: Critical illness as influenza B virus could be isolated from skeletal polyneuropathy; CIM: Critical illness myopathy muscle tissue [16]. Importantly, even in the past, neither muscle inflammation nor SARS-CoV could not be isolated Acknowledgements from cadavericskeletalmuscletissuefromconfirmed SARS- We acknowledge the contribution of icddr,b’s core donors including the governments of Bangladesh, Canada, Sweden, and the UK for their CoV infected patients with features of severe myopathy, sug- continuous support and commitment to icddr,b’s research efforts. gesting CIM, or indirect myotoxic effect of this virus [4]. This is acknowledged that Th1 cell-mediated cytokines can produce inflammatory response in muscle tissue [17]. Inter- Authors’ contributions BI has written the manuscript and performed the nerve electrophysiology, estingly, cytokine storm in SARS-CoV2 is also Th1 driven, MA has treated the patient in the ICU, ZI has performed the Anti GM1 that can induce muscle inflammation [18]. antibody test, SMB has performed the muscle histopathology. The authors We admit, due to limited laboratory facilities, we could read and approved the final manuscript. not explore further to identify the cause of this skeletal myopathy. Since thick filament myopathy is the com- Funding monest form of CIM, assessment of the content of my- This research activity was not funded. osin in relation to actin in the skeletal muscle tissue through electrophoretic separation could help a step for- Availability of data and materials ward to ascertain this type of myopathy with more All data generated or analyzed during this study are included in this precision. published article. Islam et al. Skeletal Muscle (2021) 11:10 Page 7 of 7 Declarations 14. Z’Graggen WJ, Schefold JC. Critical illness myopathy: glucocorticoids revisited? Acta physiologica (Oxford, England). 2019;225(2):e13205. Ethics approval and consent to participate 15. Akkad H, Cacciani N, Llano-Diez M, et al. Vamorolone treatment improves The study was approved by the ethics committees of the International skeletal muscle outcome in a critical illness myopathy rat model. Acta Center for Diarrhoeal Disease Research, Bangladesh and Bangladesh physiologica (Oxford, England). 2019;225(2):e13172. Specialized Hospital, Bangladesh. 16. Crum-Cianflone NF. Bacterial, fungal, parasitic, and viral myositis. Clinical microbiology reviews. 2008;21(3):473–94. https://doi.org/10.1128/CMR. 00001-08. Consent for publication 17. Moran EM, Mastaglia FL. 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