Abstract
Guillain-Barrè syndrome (GBS) is an acute immune-mediated neuropathy, possibly triggered by a recent infection or vaccination, and driven by an immune attack targeting the peripheral nervous system. GBS typically leads to ascending limb weakness, often with sensory and cranial nerve involvement 1–2 weeks after immune stimulation, but emergency and neurology physicians should be aware of its important clinical heterogeneity. In rare cases, bilateral facial nerve palsy can be the main clinical manifestation, as the case of the variant formerly known as bilateral facial weakness with paresthesias. An increasing number of case reports of GBS in patients receiving COVID-19 vaccination have been reported both during the pre-clinical phase and after large-scale authorities’ approval. We report two cases of bifacial palsy with paresthesias, a rare variant of GBS, both occurring after the first dose of COVID-19 vaccine Vaxzevria™ (formerly COVID-19 vaccine AstraZeneca), showing a favorable outcome after high-dose immunoglobulin therapy, and discuss the literature of GBS post-COVID-19 vaccination.
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Introduction
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection has been associated with the development of autoimmune processes, such as anti-phospholipidic syndrome, immune thrombocytopenic purpura, and Guillain-Barrè syndrome (GBS) [1]. Molecular mimicry between the virus and human proteins has been suggested as a potential mechanism for these associations [2].
GBS can be triggered by respiratory or intestinal infections or by vaccination, being an episode of gastroenteritis caused by Campylobacter jejuni, influenza, and vaccination against influenza itself well-known causes of GBS. Clinical manifestations of the classic form of GBS include progressive, ascending, symmetrical flaccid limbs paralysis, along with areflexia or hyporeflexia with or without cranial nerve involvement, which can progress over days to weeks up to respiratory failure. Dysautonomic symptoms can be frequently reported [3]. Facial nerve palsy occurs in a significant number of cases of GBS, and can be observed in characteristic GBS variants, such as Miller-Fisher syndrome or pharyngeal-cervical-brachial weakness. In rare cases, bilateral facial nerve palsy can be the main clinical manifestation, as the case of the variant formerly known as bilateral facial weakness with paresthesias (BFP), whose incidence among all GBS manifestations is estimated to be about 1% [4].
A few small series or case reports of GBS occurring in patients with a recent history of COVID-19 have been published, but the link between COVID-19 and GBS remains to be investigated by case–control studies. As a general clinical aspect, GBS following COVID-19 is a sensori-motor variant whose manifestation can be independent from respiratory involvement. We can speculate that the molecular mimicry between SARS-CoV-2 spike protein and human proteins can trigger autoimmune diseases, including GBS [5,6,7,8,9].
The European Medicines Agency following the results of randomized, blinded, controlled trials approved four vaccines against COVID-19: two messenger RNA-based vaccines (Pfizer-BioNTech and Moderna); ChAdOx1 nCov-19 (AstraZeneca), a recombinant chimpanzee adenoviral vector encoding the spike glycoprotein of SARS-CoV-2; and Ad26.COV2.S (Johnson & Johnson/Janssen), a recombinant adenovirus type 26 vector encoding SARS-CoV-2 spike glycoprotein. DNA-based vaccines use adenoviruses whose replicative capacity has been eliminated and, additionally, have had the S protein’s DNA of the SARS-CoV-2 inserted.
An increasing number of case reports of GBS in patients receiving COVID-19 vaccination have been reported both during the pre-clinical phase and after large-scale authorities’ approval [9,10,11,12]. Here, we report two cases of GBS with facial bilateral palsy occurring after ChAdOx1-nCoV-19 vaccination and review the literature of GBS post-COVID-19 vaccination.
Case report
Patient 1
A caucasic 59-year-old woman, whose past medical history was remarkable only for acquired hypothyroidism due to Hashimoto thyroiditis, on Levothyroxine treatment, came to our observation because of acute onset of spontaneous burning pain of lower back, lower limb paresthesias, and bilateral facial weakness occurring 15 days after administration of the first dose of COVID-19 vaccine ChAdOx1 nCov-19. No fever, upper respiratory tract infection, or diarrhea was reported before or after vaccination.
Neurological examination demonstrated complete facial diplegia with Bell’s phenomenon and lagoftalm: she had bilateral loss of frontal forehead creases, could not raise her eyebrows, and could not whistle or smile. She had mild dysarthria due to facial diparesis with labial sounds. She had full strength in both upper and lower limbs; brisk upper limbs reflexes but lower limbs hyporeflexia. She had no objective sensory findings (VIDEO).
Computed tomography obtained when she was admitted to the emergency department was unremarkable. Cerebrospinal fluid examination (CSF) revealed clear fluid, normal opening pressure, glucose 59 mg/dl (normal range: 50–70 mg/dl), proteins 259 mg/dl (normal range: 15–45 mg/dl), and WBCs 1/mm^3, consistent with CSF albuminocytologic dissociation. The Meningitis/Encephalitis Panel (FILMARRAY™ multiplex PCR system bioMèrieux) on CSF was negative as well as the cerebrospinal fluid culture. RT-PCR testing for SARS-CoV-2 on CSF was negative. Diagnostic work-up for facial diplegia was completed by testing for antibodies against Borrelia burgdoferI on CSF and serum, paraneoplastic panel, Ab Anti-acethylcoline receptor, serological testing for autoimmune diseases, and serological tests for HIV, syphilis, cytomegalovirus, hepatitis B, hepatitis C, and herpes simplex virus. All these examinations did not report positive findings. Chest X-Ray was unremarkable.
Electrophysiological study revealed multifocal demyelinating sensorimotor (Table 1) polyradiculoneuropathy consistent with the diagnosis of GBS, AIDP variant, according to the electrodiagnostic criteria for classification of GBS [8]. Following Wakerley et al. [9] suggestions, the case was diagnosed as a variant of GBS with bifacial weakness with paresthesias (BFP), since the patient met all the proposed clinical diagnostic criteria for this variant. Intravenous immunoglobulins (IVIG) (0.4 g/kg per day) were administered along a 5-day period. Symptoms improved starting from the second day of IVIG treatment. The patient was discharged from hospital 2 days after the IVIG course was completed. She had slight movements of her facial muscles, and the distal paresthesias of his lower extremities were reduced.
Patient 2
A Caucasian 43‐year‐old male previously healthy patient with an uneventful medical history was admitted to our department with a subacute onset of facial pain and numbness with weakness of eye closure, observed 7 days after administration of COVID-19 vaccine first dose ChAdOx1. During the subsequent 7 days, he started suffering from lower limbs and hands paresthesias. Neurologic examination at the time of our observation revealed facial diplegia with left-side prevalence; symmetrical weakness with Medical Research Council (MRC) grade 4 + out of 5 in distal muscle groups of both upper and lower limbs; normal upper limbs tendon reflexes but lower limbs hyporeflexia; no sensory deficit was observed.
Cerebrospinal fluid examination (CSF) revealed clear fluid, normal opening pressure, glucose 71 mg/dl (normal range: 50–70 mg/dl), proteins 200 mg/dl (normal range: 15–45 gm/dl), and WBCs 6/mm^3, consistent with CSF albuminocytologic dissociation examination. Screening for other infectious, autoimmune, metabolic, or systemic diseases, as performed for patient N. 1, was unremarkable. Unfortunately RT-PCR for SARS-CoV-2 virus on CSF was not performed in this case. Diagnostic criteria for bifacial weakness with paresthesias variant of GBS were fulfilled and the patient started on the second day from admission intravenous immunoglobulin at the dosage of 0.4 g/kg per day for 5 days. After 8 days, he showed significant improvement of facial strength and reduction of paresthesias. During hospitalization, he had a single episode of atrial fibrillation, solved with pharmacological cardioversion with flecainide, interpreted as a disautonomyc manifestation of GBS.
Electrophysiological study revealed multifocal demyelinating sensorimotor polyradiculoneuropathy (Table 1), with prevalent involvement of lower limbs compatible with the diagnosis of Guillain-Barré syndrome (GBS), AIDP variant, according to electrodiagnostic criteria for classification of GBS (8), with a mid CMAP reduction in lower limbs.
Discussion
Our study reports 2 cases of BFP occurring within 2 weeks after the first dose of ChAdOx1 nCov-19 vaccine was administered. The link between such COVID-19 vaccine and BFP is suggested by the temporal association between vaccine administration and clinical manifestations of BFP and by the lack of other known factors able to trigger GBS.
About two-third of patients affected by GBS report symptoms suggesting a recent or ongoing infection, such as fever or gastrointestinal and upper respiratory tract manifestations. A definitive infection can be identified in half of the cases suffering GBS and COVID-19 itself has been shown to be able to trigger GBS based on epidemiological investigations [13]. Filosto et al. [12] reported an increase in GBS incidence during the COVID-19 outbreak in Northern Italy, supporting a pathogenic link (rate of 47.9 cases of GBS per 100 000 COVID-19 infections). Such link between SARS-CoV-2 infection and GBS was confirmed by a systematic review and meta-analysis of observational cohorts and case series, which highlighted the association between COVID-19 and GBS, reporting a high percentage of demyelinating GBS variant and estimating GBS prevalence as 15 cases per 100,000 SARS-CoV-2 infections [14, 15]. We also found 5 case reports in literature of facial diplegia in COVID-19 infection context [16,17,18,19].
Based on biological plausibility and temporal association, vaccines have been suggested to increase GBS risk. Vaccine-associated GBS is defined by a characteristic clinical syndrome suggesting an acute immunomediated polyneuropathy within the 6-week period after vaccine administration [20]. Most of the data about the link between vaccination and GBS regards patients receiving influenza vaccine. In 1976, a sevenfold increase of GBS cases was noticed in the USA during the national H1N1 swine flu vaccination program. Moreover, a study investigating GBS incidence during the 1992–1993 and 1993–1994 vaccination programs reported that influenza vaccine was associated with a 1.7-fold increase of GBS risk, as compared to unvaccinated population [21, 22]. In any case, an extensive review of the literature found a post-influenza vaccination risk expressed as a hazard ratio (HR) of 1.11 (95% CI: 0.51–2.43), which was lower than observed after influenza infection (HR = 4.89, 95% CI: 1.17–20.36). Evidence regarding other vaccines is extremely limited although a number of case report highlights a strict time relationship between vaccination and GBS [20, 23, 24].
Looking at COVID-19 vaccination campaign, the Food and Drug Administration (FDA) has announced that 100 cases of GBS have been reported after the administration of approximately 13 million doses of Johnson & Johnson’s COVID vaccine, deciding to include GBS among the potential side effects (https://www.fda.gov/media/150723/downlad). The European medicine agency (EMA) did the same for the AstraZeneca vaccine (https://www.ema.europa.eu/en/documents/covid-19-vaccine-safety-update/covid-19-vaccine-safety-update-vaxzevria-previously-covid-19-vaccine-astrazeneca-8-september-2021_en.pdf).
A systematic literature review performed by searching the Pubmed and Scopus databases with the search string “Guillain-Barrè Syndrome and COVID vaccination” retrieved 78 articles: 67 did not report data on patients with GBS following COVID-19 vaccination and 11 were found to report data on GBS cases following COVID-19 vaccination. Table 2 reports the main clinical characteristics of the 2 patients observed and of the 19 patients retrieved by the literature search. Bilateral facial palsy was reported in 15 patients, and all patients reported albuminocytological dissociation. Two studies reported small clusters “of an unusual variant of Guillain–Barre syndrome” following the vaccination. First study reported 4 cases of BFP GBS variant occurring 11 to 22 days after administration of the first dose of AZV were reported [25]; the second report described seven cases of BFP GBS variant syndrome occurring within 2 weeks of the first COVID-19 vaccine [26].
We also searched Pubmed and Scopus databases with the search string “facial diplegia covid vaccination,” founding other two case reports in which clinical, electrophysiological, and laboratoristic data were compatible with Guillain-Barrè syndrome diagnosis [34, 35].
Facial diplegia or bilateral facial nerve palsy (B-FNP) is rare with an incidence of just 1 per 500,000 population and only 20% cases are idiopathic [27].
Interestingly a viral vector vaccine (both Johnson & Johnson and Astrazeneca) was administered to 14/15 patients observed, including both our cases and those reported by literature. Notably, as reported worldwide, the highest risk of GBS after vaccination is attributed to flu virus-based vaccination, either a live attenuated or inactivated influenza vaccine. There is evidence that adenovirus-vector might induce higher levels of specific T cells, whereas mRNA vaccines might induce higher antibody titers [39]. We also know that cell-mediated autoimmune mechanisms may be relevant in the pathogenesis of Bell’s palsy, as demonstrated by the elevated concentrations of the cytokines interleukin-1 (IL-1), IL-6, and tumor necrosis factor-alpha (TNF-alpha) in patients with Bell’s palsy, compared with control populations, suggesting an activation of cell-mediated effectors [40]. Anyway, the pathophysiology of the BFP and the link between this clinical and vaccination against COVID-19 still remain unclear and require further research.
Conclusion
This study warrants early recognition and treatment through active surveillance for GBS after COVID-19 vaccination, with specific focus on the rare bilateral facial palsy as a main symptom of GBS. Future research should aim to determine the predisposing host factors and biological mechanisms underlying this association and the high frequency of facial nerve involvement. Perhaps the SARS-CoV-2 antigen or chimpanzee adenovirus adjuvant contained in the vaccination may induce immune mechanisms leading to neuropathy for cross-reaction between antibodies against the spike protein and peripheral nerve constituents.
Change history
18 July 2022
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Andreozzi, V., D’arco, B., Pagliano, P. et al. Bilateral facial palsy after COVID-19 vaccination. Neurol Sci 43, 4069–4079 (2022). https://doi.org/10.1007/s10072-022-05982-4
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DOI: https://doi.org/10.1007/s10072-022-05982-4