Clinical Profile,Follow-up,and Role of Neuroimaging in Pediatric Guillain-Barré Syndrome in the COVID Era: An Ambispective Study

Abstract

Background: To define the varied presentations of Guillain-Barré syndrome in children in the COVID era and 6 months’ follow-up outcome. Methods: Ambispective study of 15 months’ duration involving children with Guillain-Barré syndrome aged 1 month to 18 years at a tertiary care pediatric hospital. They were categorized into groups A and B based on COVID-19 serology testing. Hughes Disability Scale was used for disability assessment. Modified Rankin scale was used for improvement assessment in follow-up. Results: Of 19 children with Guillain-Barré syndrome, 9 (47%) were females and 10 (53%) were males. Groups A and B had children with negative (8) and positive serology (11), respectively. The most common presentation in both groups was motor weakness. Post-COVID pediatric Guillain-Barré syndrome presented with variants of Guillain-Barré syndrome rather than the classical form (P = .03). In group B, patients with elevated inflammatory markers had poor response to intravenous immunoglobulin, and 5 of 11 patients had good response to pulse steroids, probably depicting an inflammation-predominant pathology. Conclusion: Post-COVID Guillain-Barré syndrome in children presented with Guillain-Barré syndrome variants rather than the classic form. Neuroimaging is of great value in both confirming Guillain-Barré syndrome diagnosis and excluding differentials. Patients with elevated inflammatory markers and residual weakness may be given a pulse steroid trial.

Keywords

Guillain-Barré syndrome pediatrics post-COVID neuroimaging

Coronavirus disease–2019 (COVID-19) caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in children manifests commonly with respiratory and gastrointestinal symptoms.¹ Multisystem inflammatory disease–children (MIS-C) or Kawasaki disease-like presentation and neurologic manifestations are the other presentations.² Among the neurologic manifestations, encephalopathy/encephalitis, seizures, headache, and vomiting are common and intracranial hemorrhages, cranial nerve palsies, Guillain-Barré syndrome, and vision problems are the rare presentations.^2-5 The post-COVID neurologic manifestations are similar to those of other conditions resulting in either (1) direct injury due to neurotropism or (2) an immune-mediated phenomenon resulting in central and peripheral nervous system injuries.^2,6 The pathophysiology of Guillain-Barré syndrome is the postinfectious immune-mediated interdependent generation of antibodies by both cell-mediated and antibody-mediated immune responses (cellular and humoral), cross-reacting with gangliosides in peripheral nerve membranes resulting in their destruction.^7,8 The annual incidence of pediatric Guillain-Barré syndrome based on epidemiology studies is estimated at 0.34 to 1.34 per 100 000 person-years.^9,10 However, the incidence of pediatric Guillain-Barré syndrome due to COVID-19 is yet to be determined. Khalifa et al¹¹ reported probably the first case of post-COVID pediatric Guillain-Barré syndrome. Following this, more similar cases were reported.^12-34 Neuroimaging contributes a significant value in children with Guillain-Barré syndrome in confirming the diagnosis and excluding the differentials, especially in atypical presentations. Our study aimed to analyze the characteristics and outcomes of post-COVID Guillain-Barré syndrome in children and explored the utility of neuroimaging as an upfront diagnostic modality.

Methodology

This study was an ambispective study conducted for 15 months (May 2021 to July 2022) at a tertiary care pediatric hospital. The records were retrospectively reviewed from May 2021 to January 2022 (9 months). The cohort was prospectively followed up from February 2022 to July 2022 (6 months). Ethical approval from the institutional ethics committee was obtained (AIIMS/IEC/2022/5066). Inclusion criterion was children aged between 1 month and 18 years with a diagnosis of Guillain-Barré syndrome or its variants admitted to the inpatient ward and intensive care unit at the department of pediatrics. The National Institute of Neurological Disorders and Stroke (NINDS) Committee's diagnostic criteria modified by Asbury et al³⁵ were used to diagnose Guillain-Barré syndrome and its variants. Exclusion criterion was a diagnosis not consistent with Guillain-Barré syndrome. Informed assent or consent was obtained before enrollment. The basic demographic data, clinical manifestations, history of SARS-CoV-2 infection or exposure, investigations, treatment, and outcomes were recorded in a prestructured questionnaire. Inflammatory markers, including C-reactive protein, ferritin, and interleukin-6 levels, were done in all children.

The SARS-CoV-2 serology test (IgM antibodies) was done in all patients at admission. The cohort was further divided into 2 subgroups based on the serology: group A consisted of children with negative SARS-CoV-2 serology, and group B included those with positive SARS-CoV-2 serology (post-COVID Guillain-Barré syndrome). The oropharyngeal swabs from all children were tested for COVID-19 by the reverse transcription polymerase chain reaction (RT-PCR). The electrophysiological study was done on 4 motor nerves and 2 sensory nerves in the upper limbs and lower limbs in all children, and the electrophysiological criteria by Hadden et al³⁶ were used for the classification of Guillain-Barré syndrome. The Guillain-Barré syndrome diagnosis was classified into subtypes, including acute motor axonal neuropathy, acute inflammatory demyelinating polyradiculoneuropathy, Miller-Fisher syndrome, polyneuritis cranialis variant, and descending variant of Guillain-Barré syndrome. The Hughes Disability Scale³⁷ was used for disability assessment. The modified Rankin Scale³⁸ was used for the assessment of improvement in follow-up at 1, 3, and 6 months after discharge from the hospital.

Hughes Disability Scale

The Hughes Guillain-Barré syndrome disability score was devised to assess the functional status of Guillain-Barré syndrome patients by Hughes et al in 1978.³⁷ The scoring of the scale ranges from 0 to 6, where 0 = healthy, 1 = minor symptoms and can run, 2 = can walk 10 meters or more without assistance but cannot run, 3 = can walk 10 meters only with assistance, 4 = bedridden, 5 = need for assisted ventilation, and 6 = dead.

Modified Rankin Scale

The Rankin Scale was devised to assess the degree of disability or the dependence for activities of daily living (ADL) of people with stroke or other causes of neurologic disabilities by Rankin et al³⁸ in 1957 and later modified in 2008. The scoring of the scale ranges from 0 to 6, where 0 = no symptoms; 1 = can carry out usual activities, despite symptoms; 2 = slight disability: able to look after own affairs without assistance, but cannot carry out all prior activities; 3 = moderate disability: needs help for previous activities, but can walk without assistance; 4 = moderately severe disability: cannot attend to own bodily needs or walk without assistance; 5 = severe disability: needs constant nursing, bedridden; and 6 = dead.

Results

Nineteen patients admitted during the study period with a diagnosis of Guillain-Barré syndrome or its variants in the department of pediatrics were enrolled.

Demographics and Clinical Presentation

Among the 19 children, 9 (47%) were female and 10 (53%) were male. The mean (SD) age in group A was 6 (±4.6) years and in group B was 8.4 (±4.7) years. Among them, 15 children had a history of COVID-like symptoms or in the family members at 1-4 weeks before the presentation. None of the children received COVID-19 vaccines. Only 1 patient previously had a history of Guillain-Barré syndrome–like illness 4 years back, which gradually recovered in 6 months. The rest had no preexisting neurologic disease or any other comorbidity. On serology testing, 11 tested positive, with very high titers of COVID-19 antibodies. On RT-PCR testing, all were negative at admission.

The most common presentation in both groups was motor weakness. In group A, all 8 children presented with weakness; in group B, 8 of 11 children presented with weakness. The other prominent manifestation in group B was the involvement of cranial nerves. The other symptoms included ataxia and paresthesias.

Guillain-Barré Syndrome and Its Variants

Seven of the 8 children in group A had classical Guillain-Barré syndrome, and 1 had a descending variant of Guillain-Barré syndrome. In group B, 4 children had classical Guillain-Barré syndrome, and 7 children presented with Guillain-Barré syndrome variants, including polyneuritis cranialis variant of Guillain-Barré syndrome in 4 children, descending variant of Guillain-Barré syndrome in 2 children, and Miller-Fisher syndrome variant of Guillain-Barré syndrome in 1 child. These descending variants were already reported in our previous study on post-COVID neurologic complications in children.⁵ Therefore, those with post-COVID Guillain-Barré syndrome presented with variants of Guillain-Barré syndrome rather than the classical symmetric ascending type of Guillain-Barré syndrome, and this association was found to be statistically significant (P = .03).

Hughes Disability Score

Hughes disability score in our cohort ranged from 2 to 5. There was no mortality in our cohort (score of 6). The demographic details and clinical characteristics are summarized in Table 1.

Table 1.

Demographics and Clinical Characteristics.

	COVID-19 serology
	Negative:Group A, n (%)(n = 8)	Positive:Group B, n (%)(n = 11)
Gender
Male	5 (62.5)	5 (45.5)
Female	3 (37.5)	6 (54.5)
Symptoms
Weakness
Upper limb predominant	1 (12.5)	3 (27.3)
Lower limb predominant	2 (25)	2 (18.2)
Quadriparesis	5 (62.5)	3 (27.3)
Cranial nerve involvement
Facial palsy	3 (37.5)	4 (45.5)
Ocular palsy	–	3 (27.3)
Bulbar palsy	–	2 (18.2)
Paresthesia	1 (12.5)	4 (36.4)
Ataxia	–	1 (9.1)
Respiratory involvement	4 (50)	4 (36.4)
GBS variants
Classical GBS	7 (87.5)	4 (36.4)
Descending variant	1 (12.5)	2 (18.2)
MFS	–	1 (9.1)
Polyneuritis cranialis	–	4 (36.4)
Hughes GBS Disability Score
0-1	–	–
2	–	3 (27.3)
3	3 (37.5)	2 (18.2)
4	1 (12.5)	2 (18.2)
5	4 (50)	4 (36.4)
6	–	–

Abbreviations: GBS, Guillain-Barré syndrome; MFS, Miller-Fisher syndrome.

Investigations

The inflammatory markers were elevated in 6 children in group B and none in group A. Nerve conduction studies (NCS) were performed in all patients. Of them, 13 children had the demyelinating variants, 5 had the axonal variants, and 1 had no elicitable waveforms. Five children in group A and 8 in group B had the demyelinating variants. Among the children with the axonal variants, 3 were from group A and 2 were from group B. Lumbar puncture was done in all (19/19) patients and all had albumino-cytologic dissociation. Neuroimaging was done in all (19/19) patients. In children with classical and descending variants of Guillain-Barré syndrome, gadolinium enhancement of ventral nerve roots and cauda equina nerve roots were noted. In children with polyneuritis cranialis variant of Guillain-Barré syndrome, enhancement of multiple cranial nerves was noted (Figure 1A-F).

Clinical Complications

In our study, 8 of 19 children were admitted to the pediatric intensive care unit, and all 8 (4 each from groups A and B) required ventilatory support. Among the 19 children, 14 children had autonomic dysfunction (6 from group A and 8 from group B). One child from group B had syndrome of inappropriate antidiuretic hormone. The same child had posterior reversible encephalopathy syndrome and reversible cerebral vasoconstriction syndrome due to fluctuation in blood pressure. The investigations and clinical complications are summarized in Table 2.

Table 2.

Investigations and Clinical Complications.

		COVID-19 serology^a
		Negative:Group A (n = 8)	Positive:Group B (n = 11)
Investigations
Inflammatory markers
	CRP, mg/L, mean (range)	2.9 (4.2)	49.6 (331.3)
	Ferritin, ng/mL, mean (range)	165.9 (197)	261.1 (436)
	IL-6 levels, pg/mL, mean (range)	3.3 (2.4)	64.1 (347.8)
Nerve conduction studies
	Demyelinating	5 (62.5)	8 (72.7)
	Axonal	3 (37.5)	2 (18.2)
	Uncharacterizable	-	1 (9.1)
CSF examination
	Albumino-cytological dissociation	8 (100)	11 (100)
Neuroimaging: (suggestive of GBS)
	Nerve root enhancement	8 (100)	11 (100)
Complications
	Dysautonomias
	Hypertension	5 (62.5)	6 (54.5)
	Sweating	–	1 (9.1)
	Tachycardia	1 (12.5)	1 (9.1)
	SIADH	–	1 (9.1)
	RCVS	–	1 (9.1)
	PRES	–	1 (9.1)

Abbreviations: CRP, C-reactive protein; CSF, cerebrospinal fluid; GBS, Guillain-Barré syndrome; IL-6, interleukin-6; PRES, posterior reversible encephalopathy syndrome; RCVS, reversible cerebral vasoconstriction syndrome; SIADH, syndrome of inappropriate antidiuretic hormone.

Unless otherwise noted, values are n (%).

Treatment

All children received intravenous immunoglobulin at 2 g/kg as per treatment protocol at admission. However, 3 children received a second dose of intravenous immunoglobulin at 2 g/kg in group B compared to 1 in group A, and 2 children (1 from each group) required plasma exchange as there was no significant improvement after 1 week of the first dose of intravenous immunoglobulin. In children with poor response to the first dose of intravenous immunoglobulin with elevated inflammatory markers, pulse steroids (5/11) were given, following which they showed brisk recovery. In children with poor clinical improvement in terms of persistent weakness, ventilator requirement, or autonomic dysfunctions after 2 weeks of second dose intravenous immunoglobulin or pulse steroids, third-line therapies including cyclophosphamide or rituximab were used. One child in group A required cyclophosphamide. In group B, 2 children received cyclophosphamide, and 1 required rituximab because of an unsatisfactory treatment response.

Outcome and Follow-up

Children were followed up at regular intervals and assessed with the mRS. The mean follow-up postdiagnosis was 12.4 ± 3.8 months. On follow-up at 3 months, in group A, the predominant mRS score was 1. In group B, the predominant mRS score was 0, and one child scored 4, because of complications of Guillain-Barré syndrome. On follow-up at 6 months, in group A, 8 of 8 children scored 0-1. In group B, 10 of 11 children scored 0-1. There was no mortality in our cohort (score of 6). The predominant residual symptom on follow-up was weakness. None were lost to follow-up. The treatment and outcomes are summarized in Table 3.

Table 3.

Treatment and Outcomes.

	COVID-19 serology
	Negative:Group A (n = 8)	Positive:Group B (n = 11)
Treatment
Intravenous immunoglobulin
Single dose	7 (87.5)	8 (72.7)
Two doses	1 (12.5)	3 (27.3)
Plasma exchange	1 (12.5)	1 (9.1)
Steroids	–	5 (45.5)
Cyclophosphamide/Rituximab	1 (12.5)	3 (27.3)
Ventilatory support	4 (50)	4 (36.4)
Outcomes
mRS score at 3-mo follow-up
0	2 (25)	5 (45.4)
1	3 (37.5)	2 (18.2)
2	2 (25)	2 (18.2)
3	1 (12.5)	1 (9.1)
4	–	1 (9.1)
5-6	–	–
mRS score at 6-mo follow-up
0	6 (75)	7 (63.6)
1	2 (25)	3 (27.3)
2	–	1 (9.1)
3-6	–	–

Abbreviation: mRS, Modified Rankin Scale.

Discussion

Guillain-Barré syndrome is a clinical diagnosis further supported by lumbar puncture and NCS. However, when a child presents with manifestations apart from classic symptoms of Guillain-Barré syndrome (symmetric ascending flaccid paralysis), neuroimaging may be of value both to confirm the diagnosis of Guillain-Barré syndrome and simultaneously exclude the other differentials, which commonly arise whenever we encounter an uncommon variant of Guillain-Barré syndrome. In our cohort, we found that the children with positive SARS-CoV-2 serology presenting with variants were more than classical Guillain-Barré syndrome. The Miller-Fisher syndrome variant, polyneuritis cranialis variant, and a descending variant of Guillain-Barré syndrome were diagnosed. A similar unexcitable Guillain-Barré syndrome variant was reported in an Indian child with post-COVID Guillain-Barré syndrome.¹⁸ In a systematic review by Abu-Rumeileh et al, including 73 patients aged 11-94 years with COVID-19–associated Guillain-Barré syndrome, they concluded that the most common presentation was a classic sensorimotor variant, even though few other variants were also reported.³⁹ A systematic review by Sansone et al reported that the demyelinating variety was more common in Western countries; however, a quarter of patients had the Miller-Fisher syndrome variant of Guillain-Barré syndrome.⁴⁰ In a systematic review by Jaberi et al,¹⁶ among the reported Guillain-Barré syndrome variants available, classic Guillain-Barré syndrome was the predominant type in 15 patients,^{11,17,20,22,23,27-29,31-34} Miller-Fisher syndrome variant in 4 patients,^21,25,26,30 and only 1 had polyneuritis cranialis variant.²⁴ In our cohort, 2 descending variants of post-COVID Guillain-Barré syndrome were diagnosed, and a similar variant was reported by Michael et al⁴¹ in a 4-year-old Indian child in 2021.

In a study by Garg et al on Indian children with pediatric Guillain-Barré syndrome, they reported that the COVID-19 pandemic led to a marked decline in the incidence of pediatric Guillain-Barré syndrome, and also, the electrophysiological profile was similar to that of the prepandemic era.¹⁴ In a study by La Rovere et al in 2021, among 365 children and adolescents with COVID-19–related neurologic involvement, only 4 (1.1%) patients had Guillain-Barré syndrome, of whom 2 were positive for COVID-19 antibodies and 2 were positive for COVID-19 RT-PCR and antibodies.⁵ In contrast to these studies, in the index study, there is an increased incidence of Guillain-Barré syndrome during the era of COVID-19, and also, post-COVID Guillain-Barré syndrome presented with variants of Guillain-Barré syndrome rather than classic forms of Guillain-Barré syndrome.

In our study, magnetic resonance imaging (MRI) was done on all the patients to explore the utility of neuroimaging as an upfront diagnostic modality and also to rule out differential diagnosis. Those who had classical Guillain-Barré syndrome revealed post-gadolinium enhancement of ventral nerve roots. In patients with polyneuritis cranialis variant, enhancement of involved cranial nerves was also noted. The post-gadolinium enhancement of nerve roots may also be seen in inherited neuropathies.⁴² Intravenous immunoglobulin was used as the first line of management in all the children. Among the children with poor response to intravenous immunoglobulin, either a second dose of intravenous immunoglobulin or plasma exchange (PLEX) was tried.

The use of corticosteroids has been shown to be ineffective in the treatment of traditional forms of Guillain-Barré syndrome.⁴³ In our center, we do not routinely use and recommend using steroids in Guillain-Barré syndrome patients. But in the index study, pulse steroids were also used in addition to intravenous immunoglobulin and PLEX, as few patients affected with COVID-19 had underlying cytokine storms and intense inflammation, resulting in the severity of illness. These elevated cytokines contributed to dysregulation of the immune process, resulting in multisystem inflammatory syndrome in children (MIS-C) and other neurologic disorders, including Guillain-Barré syndrome. This possible altered pathophysiology of post-COVID Guillain-Barré syndrome compared to typical Guillain-Barré syndrome could be attributed to the good response to steroids and immunosuppressive agents, including cyclophosphamide and rituximab. In a systemic review by Jaberi et al,¹⁶ among 35 patients included from 26 case series/reports, serology reports were available for 13 patients, and of them, 2 patients who received steroids along with intravenous immunoglobulin had a good response.³² A good response was noted for steroids, intravenous immunoglobulin, and plasmapheresis in 3 pediatric Guillain-Barré syndrome patients who were positive for COVID-19 RT-PCR without COVID-19 serology reports.^17,21,34

In the index study, patients with post-COVID Guillain-Barré syndrome with elevated inflammatory markers had poor responses to intravenous immunoglobulin but responded better to steroids. Therefore, in patients with elevated inflammatory markers, steroids may be helpful by causing immunosuppression and varying responsiveness. Similarly, we noted that those with elevated inflammatory markers and residual weakness responded better to steroids. Although there could have been multiple exposures that could have resulted in Guillain-Barré syndrome, COVID-19 infection is known to trigger Guillain-Barré syndrome. We highlight the need for better-structured prospective multicentric studies with testing of antibody titers.

The limitations of this study include its design and the sample size being small to conclude the clinical features of post-COVID Guillain-Barré syndrome. The titers of serum auto-antibodies were not tested and clinically correlated. These children were not tested for all the possible viral infections that could have triggered the Guillain-Barré syndrome.

Conclusion

Post-COVID Guillain-Barré syndrome in children presented with variants of Guillain-Barré syndrome rather than the classical symmetric ascending type of Guillain-Barré syndrome. Neuroimaging is of great value in confirming Guillain-Barré syndrome diagnosis and excluding differentials and can be utilized in atypical presentations of Guillain-Barré syndrome. Post-COVID pediatric Guillain-Barré syndrome patients with elevated inflammatory markers and residual weakness may be given a pulse steroids trial after the first-line therapy (intravenous immunoglobulin). Early diagnosis, monitoring, and prevention of complications, including secondary infections, decubitus ulcers, and autonomic dysfunction, can improve the overall outcome in these children.

Footnotes

Authors Contributions

LS and ST contributed to the concept and study design; LS, DK, ST, PK, JPG, DK, BC, SD, and RG collected the clinical and MRI data; LS, DK, and PKG performed the analyses; LS, PK, JPG, DK, SP, and KS interpreted the data; LS, DK, PKG, and ST wrote the main manuscript text and figures. All authors reviewed and approved the manuscript.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Ethics Compliance Statements

Ethical approval was obtained from the institutional review board. Informed written consent/assent to participate/publish were obtained from the parents/guardians/patients.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Lokesh Saini

Pradeep Kumar Gunasekaran

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