key: cord-0828888-84ykmc9g
authors: Goudarzi, Sogand; Esmaeeli, Shooka; Valencia, Juan D.; Lu, Maegan E.; Hales, Riley R.; Fehnel, Corey R.; Conley, Christopher M.; Quraishi, Sadeq A.; Nozari, Ala
title: Treatment Options for COVID-19–Related Guillain-Barré Syndrome: A Systematic Review of Literature
date: 2021-09-07
journal: Neurologist
DOI: 10.1097/nrl.0000000000000342
sha: b09d78b11cc9222de31a04002e65380477e52257
doc_id: 828888
cord_uid: 84ykmc9g

Central nervous system complications are reported in an increasing number of patients with Coronavirus Disease 2019 (COVID-19). COVID-19–related Guillain-Barré syndrome (GBS) is of particular importance given its association with higher mortality rates and prolonged respiratory failure. REVIEW SUMMARY: We conducted a systematic review of published cases for COVID-19–related GBS, and provide a summary of clinical management strategies for these cases. Sixty-three studies, including 86 patients, were included. Seventy-six cases with reported outcome data were eligible for the outcome analysis. Ninety-nine percent of patients were diagnosed with COVID-19 before diagnosis of GBS (median: 14 d prior, interquartile range: 7 to 20). Intravenous immunotherapy (intravenous immunoglobulin: 0.4 g/kg/d for 5 d) was the most frequently used treatment approach. The review indicated that the outcome was not favorable in 26% of cases (persistent neurological deficits). A mortality rate of 3.5% was observed in patients with COVID-19–related GBS. CONCLUSIONS: Although evidence to support specific treatments is lacking, clinicians should consider the benefits of immunotherapy and plasma exchange in addition to the standard antimicrobial and supportive therapies for patients who meet the diagnostic criteria for acute sensory and motor polyradiculoneuritis. Intravenous immunoglobulin treatment alone is not shown to result in improved outcomes or mortality. More extensive studies aimed at exploring the neurological manifestations and complications of COVID-19 and distinctive treatment options for COVID-19–related GBS are warranted.

A n increasing body of evidence has emerged to establish the link between Coronavirus Disease 2019 (COVID-19) infection and major neurological complications such as cerebrovascular accidents, acute transverse myelitis, encephalitis, and Guillain-Barré syndrome (GBS).

Angiotensin-converting enzyme 2 (ACE2) has been identified as an important severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) receptor, mediating its entry into the cell. 1 ACE2 receptors are widely expressed in the lungs, heart, and brain. 2 The expression of the ACE2 receptors on the endothelial cells of the blood-brain barrier facilitates the viral binding and entry into the central nervous system (CNS). 3-6 ACE2 receptors are highly expressed in the ventrolateral medulla and the nucleus of the solitary tract. 5 In addition to the direct viral binding and cell entry, activation of inflammatory mediators is thought to result in a proinflammatory state within the CNS. 7 In addition, COVID-19 is suggested to trigger a molecular mimicry phenomenon on the affected endothelial cells, where cross-reactions occur between antibodies and a large number of proteins present on the plasma membrane surface due to COVID-19 induced stress. 8, 9 As a result of the above mechanisms various pathways within the CNS can lead to direct injury to nerve tissue, in addition to a cytokine storm across the blood-brain barrier, hypoxia from COVID-19-related lung injury, and an uncontrolled immune response. 6, [10] [11] [12] [13] Figure 1 demonstrates different mechanisms through which SARS-CoV-2 may cause neuronal injuries.

Neurological manifestations are reported in up to 36% of patients with COVID-19. Among COVID-19-associated CNS conditions, GBS has emerged in an increasing number of case reports as an additional hazard with a significant risk of mortality or prolonged respiratory failure. 4, 11, 12, [14] [15] [16] [17] [18] [19] [20] We herein present an in-depth systematic review of COVID-19-related GBS cases with analysis. The purpose of this systematic review is to recapitulate the available treatments for COVID-19-related GBS and to provide a summary of clinical management strategies for this complication. We explore management obstacles in the intensive care unit (ICU) for COVID-19-related GBS patients during the pandemic.

All articles in English and Spanish languages, including adult patients, and published in PubMed-indexed scientific journals were considered eligible. Randomized controlled trials, prospective and retrospective cohorts, case series, and case reports, as well as cross-sectional studies involving patients with COVID-19-related GBS were eligible for inclusion.

We performed a systematic search on databases PubMed, EMBASE, and Web of Science to identify studies with the

Descriptive statistics were tabulated for the analytic cohort. Continuous data were reported as median with interquartile ranges and compared using the Kruskal-Wallis test or Wilcoxon rank test. Categorical data were expressed as proportions and compared using the χ 2 test. The published outcome data for each case were classified into 2 categories. Clinical improvement, defined as neurological or autonomic, or respiratory symptoms improvement, weaning off the ventilator, or improvement of oxygen requirement and inflammatory markers. No improvement is defined as no sign of clinical improvement, worsening of the neurological examination, hemodynamic instability, and death. All analyses were conducted using R (The R Foundation for Statistical Computing, Vienna, Austria). 24 P-values <0.05 were considered to be significant.

To graphically summarize the studies' inclusion processes, we constructed a PRISMA diagram (Fig. 2) which demonstrates the selection mechanism of among the total of 99 discovered publications. 21 From a total of the final 63 publications (55 case reports and 8 case series), 86 cases were included in this study. Most of the cases were reported from Italy (30%), the United States (19%), and Spain (9%) (Fig. 3) . The reported in-hospital mortality rate among a total of 86 patients were 3.5%. Seventy-six cases reported the outcome of their management and were included in the final analysis; among them, 74% reported clinical improvement, while 26% reported no improvement. Demographic and clinical data stratified by patients' outcome are shown in Table 2 . Patients with no improvement were older (P = 0.003) and had a higher incidence of quadriplegia (P = 0.02), areflexia (P = 0.02) and respiratory failure (P = 0.004) ( Table 2) . Anti-ganglioside antibody was not found in patients with COVID-19-and Zika virusrelated GBS. The neuropathy in viral infections-related GBS could be due to other autoantibodies that are not detected as yet or the viruses produced nerve damage due to other neurotoxic effects Cappello 8 COVID-19 and molecular mimicry: the Columbus' Egg?

Does molecular mimicry explain both the acute pulmonary embolism and the multi-organ microvascular thrombosis that some patients experience?

It would be appropriate if this Journal would stimulate the scientific community on the fact that molecular mimicry phenomena can occur in SARS-CoV-2 It is also urgent to start the search for human epitopes that turn into autoantigens, and to remind this risk to all those who are currently working on vaccines Gigli et al 23 Guillain-Barré syndrome in the COVID-19 era: just an occasional cluster?

Compare the frequency of GBS cases during the March-April months of the last 3 y and to admissions for GBS during the same months of the current year in Friuli Venezia-Giulia, Italy

Compared with years 2017-2019, the increase of GBS cases in 2020 is 5.41-fold The suspicion that this striking difference could be due to the pandemic curve in our region is, therefore, legitimate Table 3 . Among a total of 86 cases, the most-reported comorbidity was hypertension (20%) and type 2 diabetes or prediabetes (9%). Cough (70%), fever (63%), dyspnea (24%), anosmia or ageusia (17%), diarrhea (16%), pharyngitis or upper respiratory infection (URI) symptoms (15%), and fatigue, myalgia, or arthralgia (12%) were the first COVID-19 infection symptoms reported among the patients, respectively. A majority of the cases (83%) were diagnosed using the reverse transcription-polymerase chain reaction technique; and 86% of the specimens were collected through nasopharyngeal (NP) swab. Forty-five percent of the cases reported cerebrospinal fluid polymerase chain reaction for COVID-19 results with no positive report. Seventy-eight percent of the cases reported their choice of treatment for COVID-19. These treatments included hydroxychloroquine (45%), antibiotics (34%), lopinavir/ritonavir (25%), darunavir and antiretroviral therapy (7%), umifenovir (3%), oseltamivir (3%), tocilizumab (1%), and corticosteroids (16%). There was no reported use of remdesivir among the cases we reviewed. Similarly, the use of Regeneron monoclonal antibodies against SARS-CoV-2 (casirivimab with imdevimab) has not been reported in any cases with COVID-19-related GBS; the only reported monoclonal antibody in this population was tocilizumab, a monoclonal antibody against the interleukin-6 receptor. One case reported at the Chest annual meeting reported the use of tocilizumab together with convalescent plasma, but the patient did not improve and remained dependent on ventilatory support. Among 92% of the cases that reported ventilator support status, 48% reported failure of weaning trials during the treatment period.

Ninety-nine percent of the patients were diagnosed with COVID-19 before GBS symptoms were recorded, with 1 patient who had GBS symptoms 7 days before the COVID-19 diagnosis. The median interval between COVID-19 diagnosis and the first recorded neurological symptoms was 14 (interquartile range = 7 to 20) days. Paresthesia (41%), quadriparesis (28%), areflexia (27%), paraparesis (26%), dysphagia (15%), facial paresis (14%), ataxia (12%), asthenia (12%), hypoesthesia (10%), respiratory failure (7%), facial diplegia (6%), paraplegia (3%), and quadriplegia (3%) were the GBS symptoms reported among the patients respectively. Forty-four percent of the cases reported performing biological tests for other viral infections. Among these patients, human immunodeficiency virus (68%), followed by influenza viruses (21%) were the most common tested viruses. Nineteen percent of the cases reported performing magnetic resonance imaging. Twelve percent of these cases did not detect any GBS-related findings. However, 31% reported enhancement of caudal nerve roots, and 12% reported abnormal enhancement of facial nerve. A motor nerve conduction study was performed in 76% of the cases. Among these cases, the most frequently examined nerves for velocity assessment were tibial nerve (54%), common peroneal nerve (37%), and the median nerve (37%). For those cases in which the tibial nerve was tested, 49% showed bilateral absent or decreased velocity, 26% showed unilateral decreased velocity, and 17% showed normal velocity at the tibial nerve. Among cases who reported common peroneal nerve testing, 71% had bilateral absent or decreased velocity, 21% had normal velocity, and 8% had unilateral decreased velocity at the common peroneal nerve. For cases with reported median nerve testing, 50% had bilateral absent or decreased velocity, 25% had normal velocity, and 25% had unilateral absent or decreased velocity at the median nerve. Sixty-five percent of the cases reported the type of GBS; among them, 54% were acute inflammatory demyelinating polyneuropathy (AIDP), 32% were acute motor-sensory axonal neuropathy (AMSAN), 11% were MFS and 4% had isolated facial diplegia. Almost all of the cases (98%) reported their choice of GBS management. Intravenous immunoglobulin (IVIG) (87%) was the most used treatment approach followed by plasma exchange (8%). Four percent of patients who received IVIG also underwent plasmapheresis; 2% received low molecular weight heparin (LMWH) or enoxaparin, and 1% Gabapentin. Two percent of patients were treated only with prednisone, and 5% received no specific GBS treatments. Detailed GBS clinical and management data are demonstrated in Table 4 and diagnostic data in Table 5 .

In this systematic review of reported COVID-19 cases, we did not identify a consensus on the diagnostic approach and treatment of patients with superimposed GBS. The most commonly reported treatment was IVIG, in addition to therapies aimed at the COVID-19 infection such as antibiotics and antiviral agents. Our findings confirm that quadriplegia, areflexia, and respiratory failure are associated with poor outcome among COVID-19-related GBS patients (P = 0.02, 0.02, and 0.004, respectively), but GBS subtypes and treatment strategies including IVIG and systemic steroids are not. Moreover, this review indicated a mortality rate of 3.5% in patients with COVID-19related GBS, which is more than twice the WHO reported mortality rate of 2.2% among general COVID-19 cases. 80 We also found a significantly higher rate of acute respiratory failure requiring mechanical ventilation in this population (47% vs. 16% in the general COVID-19 cases 81 ) and persistent neurological deficits (26% vs. 18.3% 82 ). Although available case reports do not provide evidence of causation, the poor outcome and high mortality rate in COVID-19-related GBS patients underscores the importance of early diagnosis and effective treatment of neurological complications in this population.

Clinical diagnosis of GBS can be particularly challenging in patients with severe COVID-19 symptoms. 2,20 A considerable variety of early neurological symptoms have been reported after the onset of COVID-19 symptoms. The interval between the first reported signs of viral infection and the onset of neurological symptoms ranged from 0 to 60 days, with 1 case reporting GBS symptoms 7 days before COVID-19 symptoms occurred. 27 

The geographical distribution of reported COVID-19-related GBS resembles the worldwide distribution 80 of COVID-19 infections at the time of this report (Fig. 3) . The most commonly diagnosed type of GBS in this population is reported to be AIDP, as is typical in dengue or Zika virus-related GBS. However, one study reported that COVID-19-related GBS patients were mainly diagnosed with acute motor axonal neuropathy (AMAN) and AMSAN. The authors further stated that patients with AIDP had better outcomes than those diagnosed with AMAN or AMSAN. 22 We could not corroborate these findings, nevertheless, and failed to validate an association between GBS types and patient outcomes in this review. Gupta and colleagues also speculated that COVID-19-related GBS may have a different pathogenetic mechanism compared with other types of GBS. However, the findings reported in this review indicate a common clinical and pathogenetic characteristics between COVID-19-related GBS and other types of GBS. 22

Management of the COVID-19 infection is overshadowed by many epidemiological, clinical and social factors and a lack of effective therapies and accepted treatment protocols. While several experimental strategies have been used to treat patients with significant symptoms, current management of COVID-19 primarily focuses on providing supportive therapies including mechanical ventilation. 83 Recent experimental therapies have shown some promise, including antiviral agents such as the adenosine analogue remdesivir and the protease inhibitors lopinavir and ritonavir. [84] [85] [86] [87] [88] Chloroquine and hydroxychloroquine have been shown to inhibit COVID-19 in vitro and were widely used in patients with COVID-19 until newer studies proved their lack of clinical efficiency. 84, 89 While hydroxychloroquine has largely fallen out of favor as a primary therapeutic option for COVID-19, 90 a significant percentage of existing case studies in our review have documented its use in treatment. In the COVID-19-GBS cases included in this review, 25% were treated with lopinavir or ritonavir, and 43% were treated with hydroxychloroquine. 14, 15, [17] [18] [19] [20] 25, 27, 29 Further, antibiotics such as azithromycin and amoxicillin were also used in 33% of the cases we analyzed. 14, 19, 20, 26, 28, 29 The body of evidence is increasing in support of the use of monoclonal antibodies (tocilizumab, casirivimab, and imdevimab) in general COVID-19 patients, 91,92 but given the limited data available in patients with COVID-19related GBS, it is impossible to determine their clinical importance and outcome effects in this population.

Steroids were administered to 12% of the cases that were included in our analysis. 20, 29, 83 Recent guidelines on the management of critically ill adults with COVID-19 recommends against routine use of steroids in mechanically ventilated adults without acute respiratory distress syndrome; however, they can be used in the presence of acute respiratory distress syndrome and in patients experiencing a refractory shock. 93 Studies suggest that corticosteroids may lead to prolonged viral shedding, hence the need to limit their routine use. 12, 94 Available literature argues, nevertheless, that steroids could mitigate the fatal immune system activation seen in COVID-19, 83 based on their positive effects during the Ebola epidemic and as the first-line therapy for the postviral autoimmune response to herpes virus encephalitis. 83, [95] [96] [97] A recent study showed that intravenous dexamethasone therapy for 10 days was associated with decreased 28-day mortality in COVID-19 patients receiving respiratory support but no benefit in those who did not require respiratory support. These findings suggest that the benefits of diminished immunopathologic activation may outweigh possible prolonged viral shedding in the subset of COVID-19 patients requiring ventilatory support. 98 The effects of steroid use during the management of typical GBS patients has also been widely studied. 99 Consistent with earlier reports from GBS in general population, 99 our review indicates that systemic steroids does not affect the outcome, defined as mortality or ICU admission, in patients with COVID-19-related GBS.

IVIG was used in 87% of the GBS cases included in our review. When treating the parainfectious form of GBS that cooccurs with COVID-19, IVIG, or plasma exchange may not only mitigate the neuroinflammatory response but may also prove beneficial in controlling the associated systemic inflammation and sepsis. 12, 100, 101 In this setting, however, a clinical concern is related to the association between IVIG and the risk of thromboembolism. 102 COVID-19 is commonly associated with a prothrombotic state, as evident from an increase in the D-dimer levels 103 and reported cases of venous thromboembolism and embolic strokes. 104 Current guidelines support the use of thromboprophylaxis with low molecular weight heparin, in COVID-19 patients without contraindications. Those with clinical evidence of a venous thromboembolism should be treated with therapeutic doses of anticoagulation. 105 The most common dose for IVIG was 0.4 g/kg/d for 5 days. 4, 11, [14] [15] [16] [17] [18] 20 Overall, outcomes with these medications were greatly variable and unpredictable. In patients treated with IVIG and some combination of hydroxychloroquine, antivirals, and antibiotics, outcomes ranged from complete recovery 4 to persistent lower extremity weakness 20 to death from progressive respiratory failure. 17 Despite uncertainty regarding COVID-19 and GBS management, one report recommended antiviral agents and IVIG as a reasonable therapeutic strategy at this point. 14 

Only 7 reported cases of COVID-19-associated GBS have been treated with plasmapheresis alone or in addition to IVIG. 28, 47 A randomized controlled trial in 2014 suggested that IVIG and plasmapheresis are equally effective in treating GBS. 106 Some experts, however, believe that plasmapheresis may be a better therapeutic approach and should be considered before IVIG in GBS. Historically, IVIG has been more widely used because of its availability and simplicity; it requires no specialized equipment and has a relatively low risk of adverse events. 106 There is also no evidence at this time that a combination therapy with IVIG and plasmapheresis is associated with better long-term or short-term outcomes compared with standard therapy in GBS patients. [106] [107] [108] [109] Although the Surviving Sepsis Campaign panel of experts recommend against routine use of IVIG in COVID-19 patients, it may be reasonable to consider these treatment options in the subgroup of COVID-19 patients with a suspected or confirmed GBS.

Out of the cases we reviewed, none reported the use of convalescent plasma therapy in the treatment of COVID-19-related GBS. However, the use of convalescent serum therapy for COVID-19 is a rapidly emerging but controversial area of research. Plasma is collected from previously infected individuals to passively transfer antibodies to an infected patient, with the goal to improve clinical symptoms and mortality. 110 Plasma exchange with convalescent serum could be an innovative approach to the management of COVID-19-associated GBS. While current randomized controlled trials have not shown a significantly beneficial or detrimental effect of convalescent plasma on mortality in COVID-19 patients, lower mortality rates have been associated with those who receive plasma containing higher concentrations of neutralizing antibodies. Some studies suggest convalescent exchange may have the greatest benefit 112 In regard to possible adverse effects, the largest safety study to date has noted transfusion reactions occurring in <1% of patients and causing death in 0.3%. Possible reactions include transfusion-associated circulatory overload, transfusion-related acute lung injury, and severe allergic reaction. 113 While the use of convalescent plasma has not demonstrated significant effects on mortality in general COVID-19 patients, further research is needed to assess its impact on COVID-19related GBS. 114 One case report has documented the use of convalescent plasma in a patient COVID-19-related GBS; however, its efficacy is unclear as the patient developed worsening respiratory failure and was unable to be weaned from ventilatory support at time of publication. 115 In addition, addressing the use of convalescent plasma in COVID-19-related GBS presents unique challenges apart from its use in general COVID-19 patients. One study reported deferring the use of convalescent plasma out of concern for potential parainfectious antibody-mediated peripheral nerve damage from donor plasma. 68 Due to the ambiguity of current evidence in this subset of COVID-19 patients, further research is needed to assess its efficacy in this population. It should be noted, however, that the most recent guidelines suggest using convalescent plasma in the management of COVID-19 patients only in the setting of a clinical trial. 113 Critical Care in COVID-19 Patients With GBS In our study, patients with poor outcomes or who showed no clinical improvement were associated with longer ICU stays (P = 0.02, Table 2 ). The ICU management of COVID-19-related GBS presents a unique set of challenges and obstacles. Poorer outcomes and longer ICU admissions highlight the increased mortality risk in this population and the potential burden on hospital resources. As mentioned above and presented in Table 1 , there is a highly variable temporal relationship between the development of neurological and respiratory symptoms of GBS and COVID-19. In particular, evidence from several case reports suggests that possible symptom overlap portends more considerable obstacles in its management. 17, 28 As both diagnoses may be complicated by severe respiratory failure and the need for early respiratory support, ICU admission is often indicated but may not be feasible in some centers given the scarcity of resources during a pandemic. 17 It is unclear if the development of ventilator-dependent respiratory failure in reported patients is caused by the sequelae of GBS-related neuromuscular dysfunction or COVID-19 respiratory symptoms. Out of the cases we analyzed, 47% required mechanical ventilation and ICU admission, highlighting the need for critical care resources in these patients. [15] [16] [17] [18] 20, 26, 28, 31 A retrospective study in Wuhan, China reported that 71% of 52 COVID-19 patients with unspecified GBS status admitted to the ICU required mechanical ventilation. 116 Similarly, a retrospective study of 76 GBS patients admitted to the ICU showed that 78% required mechanical ventilation. 117 Although the precise pathophysiology of respiratory failure in COVID-19 patients with GBS remains unclear, the increased prevalence of ventilator dependency among cases we reviewed suggests a possible synergistic response associated with a worst outcome (P = 0.004), which warrants further investigation. Indeed, recent literature does support this hypothesis and suggest that the presence of significant respiratory symptoms in the acute phase of COVID-19 may be associated with more severe forms of GBS. 4 As such, respiratory complications in COVID-19 patients with GBS, including prolonged ventilator dependence and bacterial superinfection, pose a significant obstacle to patient recovery, particularly in areas with limited ICU resources. Current guidelines advise managing mechanically ventilated adults with COVID-19 similar to patients with other causes of acute respiratory failure. These ventilation strategies include low tidal volume ventilation at 4 to 8 mL/kg of predicted body weight, titrated positive end-expiratory pressure and reduction of barotrauma by restricting the peak and plateau inspiratory pressures. 94 However, the efficacy of other mechanical ventilation strategies in COVID-19 patients, as well as COVID-19-related GBS patients, has not yet been extensively investigated. The documented association between mechanical ventilation and no clinical improvement in this review (P = 0.007) underscores the need for carefully designed studies of ventilation strategies among this group of patients.

The main limitation of the current systematic review of the literature is the low number of available cases worldwide and an even lower number of cases with the reported outcome. To facilitate further studies, we suggest that while reporting cases, authors report the outcome of the case as well. Despite the limitations, this systematic review and analysis is the first systematic study that rigorously assesses the effect of treatment outcomes and discusses the ICU challenges and management of COVID-19-related GBS patients during the COVID-19 pandemic.

To conclude, GBS should be considered as a potential highrisk complication in critically ill COVID-19 patients with early-onset weakness and pulmonary findings that are inconsistent with the severity of their respiratory status. Although evidence to support specific treatments are lacking, clinicians should consider the benefits of immunotherapy and plasma exchange, in addition to standard antimicrobial and supportive therapies, if the diagnostic criteria for an acute sensory and motor polyradiculoneuritis are met. This review indicated that IVIG treatment alone did not result in improved outcomes or mortality. Hence, the effects of more aggressive treatment options including plasmapheresis and convalescent plasma exchange should be examined further for this group of high-risk patients. More extensive studies aimed at exploring neurological manifestations and complications of COVID-19, together with distinctive treatment options for COVID-19-related GBS are warranted.

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