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Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 25  |  Issue : 6  |  Page : 1116-1121
 

Impact of COVID-19 on guillain-barre syndrome in India: A multicenter ambispective cohort study


1 Nizam's Institute of Medical Sciences, Hyderabad, Telangana, India
2 Post Graduate Institute of Medical Education and Research, Chandigarh, India
3 National Institute of Mental Health and Neuro Sciences, Bangalore, Karnataka, India
4 Krishna Institute of Medical Sciences Hospital, Secunderabad, Telangana, India
5 Dayanand Medical College, Ludhiana, Punjab, India
6 All India Institute of Medical Sciences, New Delhi, India
7 Lady Hardinge Medical College, New Delhi, India
8 Government Medical College Kozhikode, Kerala, India
9 Institute of Medical Sciences, Banaras Hindu University, Varanasi, India
10 Government Medical College, Thiruvananthapuram, Kerala, India
11 Apollo Hospitals, Sheshadripuram, Bangalore, India
12 PBM Hospital, Sardar Patel Medical College, Bikaner, India
13 Indira Gandhi Medical College and Hospital, Shimla, Himachal Pradesh, India
14 All India Institute of Medical Sciences, Jodhpur, Rajasthan, India
15 Shree Krishna Hospital and Pramukhswami Medical College, Bhaikaka University, Karamsad, Anand, Gujarat, India
16 Kalinga Hospital Limited, Bhubaneswar, Odisha, India
17 Apollo Gleneagles Hospitals, Kolkata, West Bengal, India
18 Lalitha Super Specialities Hospital Private Limited, Guntur, Andhra Pradesh, India
19 Goa Medical College, Goa, India
20 Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India
21 NH MMI Narayana Superspeciality Hospital, Raipur, Chattisgarh, India
22 All India Institute of Medical Sciences, Bhubaneswar, Odisha, India
23 Caritas Hospital, Kottayam, Kerala, India
24 Ramakrishna Care Medical Sciences Private Limited, Raipur, India
25 Pondicherry Institute of Medical Sciences, Pondicherry, India
26 Army Hospital, Guwahati, Assam, India

Date of Submission13-Jun-2022
Date of Decision01-Jul-2022
Date of Acceptance10-Jul-2022
Date of Web Publication3-Dec-2022

Correspondence Address:
Venugopalan Y Vishnu
Department of Neurology, MRC International Fellow in Neuromuscular Genomic Medicine, Room No. 704, CN Centre, Seventh Floor, All India Institute of Medical Sciences, New Delhi
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/aian.aian_523_22

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   Abstract 


Introduction/Aims: Studies conducted during the coronavirus disease 2019 (COVID-19) pandemic have reported varied data regarding the incidence of Guillain–Barre syndrome (GBS). The present study investigated demographic and clinical features, management, and outcomes of patients with GBS during a specified period of the COVID-19 pandemic, and compared these features to those of GBS in the previous year. Methods: A multicenter, ambispective cohort study including 26 centers across India was conducted. Data from a pre-COVID-19 period (March 1 to August 31, 2019) were collected retrospectively and collected ambispectively for a specified COVID-19 period (March 1 to August 31, 2020). The study was registered with the Clinical Trial Registry India (CTRI/2020/11/029143). Results: Data from 555 patients were included for analysis: pre-COVID-19 (n = 334) and COVID-19 (n = 221). Males were more commonly affected during both periods (male:female, 2:1). Gastroenteritis was the most frequent antecedent event in 2019 (17.4%), whereas fever was the most common event in 2020 (10.7%). Paraparesis (21.3% versus [vs.] 9.3%, P = 0.001) and sensory involvement (51.1% vs. 41.3%; P = 0.023) were more common during COVID-19 in 2020, whereas back pain (26.3% vs. 18.4%; P = 0.032) and bowel symptoms (20.7% vs. 13.7%; P = 0.024) were more frequent in the pre-COVID period. There was no difference in clinical outcomes between the two groups in terms of GBS disability score at discharge and 3 months after discharge. Independent predictors of disability in the pre-COVID period included areflexia/hyporeflexia, the requirementfor intubation, and time to bulbar weakness; in the COVID-19 period, independent predictors included time from onset to admission, intubation, and intubation requirement. The mortality rate was 2.3% during the entire study period (13/555 cases). Discussion: Results of this study revealed an overall reduction in the frequency of GBS during the pandemic. The lockdown likely reduced the risk for antecedent infections due to social distancing and improved hygiene, which may have resulted in the reduction of the frequency of GBS.


Keywords: Areflexia, COVID-19, GBS, Guillain–Barré


How to cite this article:
Sireesha Y, Shree R, Nagappa M, Patil A, Singla M, Padma Srivastava M V, Dhamija R K, Balaram N, Pathak A, Ramachandran D, Kumar S, Puri I, Sharma S, Panda S, Desai S, Samal P, Choudhary A, Vijaya P, Ferreira T, Nair S S, Sinha H P, Bhoi S K, Sebastian J, Sharma S, Basheer A, Bhartiya M, Mathukumalli N L, Jabeen SA, Lal V, Modi M, Sharma P P, Kaul S, Singh G, Agarwal A, Garg D, Jose J, Dev P, Iype T, Gopalakrishnan M, Upadhyay A, Bhatia R, Pandit AK, Singh RK, Salunkhe M, Yogeesh P M, Reyaz A, Nadda N, Jha M, Kumar B, Kushwaha P K, Chovatiya H, Madduluri B, Ramesh P, Goel A, Yadav R, Vishnu VY. Impact of COVID-19 on guillain-barre syndrome in India: A multicenter ambispective cohort study. Ann Indian Acad Neurol 2022;25:1116-21

How to cite this URL:
Sireesha Y, Shree R, Nagappa M, Patil A, Singla M, Padma Srivastava M V, Dhamija R K, Balaram N, Pathak A, Ramachandran D, Kumar S, Puri I, Sharma S, Panda S, Desai S, Samal P, Choudhary A, Vijaya P, Ferreira T, Nair S S, Sinha H P, Bhoi S K, Sebastian J, Sharma S, Basheer A, Bhartiya M, Mathukumalli N L, Jabeen SA, Lal V, Modi M, Sharma P P, Kaul S, Singh G, Agarwal A, Garg D, Jose J, Dev P, Iype T, Gopalakrishnan M, Upadhyay A, Bhatia R, Pandit AK, Singh RK, Salunkhe M, Yogeesh P M, Reyaz A, Nadda N, Jha M, Kumar B, Kushwaha P K, Chovatiya H, Madduluri B, Ramesh P, Goel A, Yadav R, Vishnu VY. Impact of COVID-19 on guillain-barre syndrome in India: A multicenter ambispective cohort study. Ann Indian Acad Neurol [serial online] 2022 [cited 2023 Feb 6];25:1116-21. Available from: https://www.annalsofian.org/text.asp?2022/25/6/1116/362579

on behalf of the GBS consortium - GBS consortium consisting of26 centers across India





   Introduction Top


Guillain–Barre syndrome (GBS) has been reported during the coronavirus disease 2019 (COVID-19) pandemic[1]; however, unlike the Zika virus pandemic,[2] epidemiological studies have not demonstrated a definite association between GBS and COVID-19.[3] Moreover, some regions have exhibited a reduction in the incidence of GBS during the COVID-19 pandemic.[3],[4] Some experts have argued that a small increase in GBS incidence due to COVID-19 may be disguised behind a larger decline from other causes.[3],[4]Because of COVID-19, the Government of India declared a nationwide lockdown from March 25, 2020, restricting a population of 1.38 billion to home, with access only to emergency hospital services.[5],[6] During the lockdown, hospital admissions secondary to all diseases, with the exception of COVID-19, declined throughout India.[7],[8]

The present study aimed to study the ramifications of the COVID-19 pandemic on the frequency of admissions for GBS compared with a similar pre-COVID period in 2019. We also aimed to characterize the clinical spectrum, outcomes, and predictors of GBS during the two study periods.


   Methods Top


Study design

The present investigation was a multicenter, national, ambispective, observational cohort study. The Department of Neurology, All India Institute of Medical Sciences (AIIMS), New Delhi, created a GBS consortium consisting of 26 centers across India. Retrospective data were collected from a pre-COVID period (March 1 to August 31, 2019) and ambispective data were collected from a COVID-19 pandemic period (March 1 to August 31, 2020). Ethics clearance was obtained from the Institutional Ethics Committees of each participating center. The study was registered prospectively with the Clinical Trial Registry India (CTRI/2020/11/029143).

Study participants

All GBS patients >12 years of age fulfilling the diagnostic criteria for GBS or one of its variants (as per the National Institute of Neurological Disorders and Stroke [NINDS] criteria) were recruited[9] and admitted within 4 weeks of symptom onset. Informed written consent was obtained from all participants in the prospective period. Patients with suspected subacute inflammatory demyelinating polyneuropathy,[10]toxic neuropathies, and vasculitic neuropathies were excluded.

Data collection

Data were collected using a pre-designed, standardized method, and included demographic information; antecedent events; neurological symptoms; and signs of GBS at study entry, at discharge, and 3 months after discharge; treatment received; and associated morbidity and mortality. Disability was scored using the modified Rankin Scale (mRS)[11] and GBS disability score (Hughes score).[12] Autonomic function testing was performed, gauged by history, examination, nerve conduction study, autonomic function tests (all participating centers used one or more of these), and the presence of autonomic dysfunction was noted.[3] Nerve conduction studies and cerebrospinal fluid (CSF) findings were recorded, along with other investigations. In accordance with a study by Hadden et al.[13] the site investigators categorized electrophysiological subtypes as follows: demyelinating, axonal, inexcitable, equivocal, and normal. Anonymized data from all centers were pooled for analysis.

Statistical analysis

Continuous variables are expressed as mean (±standard deviation), median (interquartile range[IQR]), and frequency (%). The Mann–Whitney U-test, Wilcoxon Rank Sum test, and Kruskal–Wallis test were used to compare continuous and non-parametric data, and the χ2 test or Fisher's exact test was used to compare proportions. Shapiro–Wilk test was used to test the normality of the data. Univariate and stepwise multi variable logistic regression analyses were performed to observe the independent effect of factors on mRS at discharge and GBS disability score at discharge and 3 months after discharge. Variables were selected for the regression model if they statistically correlated with the outcome on univariate analysis or were clinically known to be associated with the outcome. Stepwise logistic regression was performed with a probability of removal at 0.1 and a probability of inclusion at 0.05.Differences with a two-tailed P ≤ 0.05 were considered to be statistically significant. Bonferroni correction was performed, wherever applicable. Stata version 14 (StataCorp, College Station, TX, USA) was used for all analyses.


   Results Top


A total of 555 patients with GBS were identified: n = 334 in 2019 (i.e., pre-COVID period) and n = 221 in 2020 (i.e., COVID-19 pandemic period).

Demographic and clinical characteristics

The median age was 38 years (interquartile range [IQR] 24–52 years) and 36 years (25–54 years) in 2019 and 2020, respectively. Males were more commonly affected (male: female, 2.1:1 (2019) and 2:1 (2020)). Detailed demographic and clinical characteristics of the two groups are summarized in [Table 1]. Only five patients acquired COVID-19 preceding GBS. Clinical characteristics were similar in both groups although there were minor differences. Paraparesis and sensory involvement were noted to be more frequent in 2020 than in 2019. Reported back pain and bowel symptoms were less frequent during the COVID-19 period. No other significant differences were noted between the two groups, including symptom onset to admission, bulbar involvement, or intubation. The median duration of baseline features viz. symptom onset to presentation, bulbar weakness, intubation, and treatment did not vary between the two groups [Supplementary Table 1]. There was no difference in electrophysiology pattern [Supplementary Table 2], GBS antibody status, or CSF parameters, except for significantly higher CSF protein values in 2019.
Table 1: Clinical characteristics of patients

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Outcomes

There were significant differences in the percentage of patients receiving treatment for GBS in 2020 versus 2019. However, there was no difference in clinical outcomes between the two groups in terms of GBS disability score at discharge and at 3 months after discharge, and mRS at discharge, including ventilator dependence and complications [Table 2]. Independent predictors of disability, analyzed using multivariate logistic regression, included areflexia/hyporeflexia, the requirement for intubation, time to bulbar weakness in the pre-COVID period, and time from onset to admission, intubation, and requirement for intubation in the COVID-19 period [Supplementary Table 3] and [Supplementary Table 4].
Table 2: Management data for 2019 and 2020

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COVID-19-positive patients in 2020

There were only five (2.3%) patients (male to female ratio, 4:1) with the proven antecedent (real-time polymerase chain reaction positive for severe acute respiratory syndrome coronavirus 2 [SARS-CoV-2] within 4 weeks of GBS onset, n = 4) or concurrent (SARS-CoV-2 positive at the time of GBS onset, n = 1) COVID-19. All patients presented with quadriparesis with areflexia, three exhibited autonomic dysfunction, intubation was required in two patients, and the duration of ventilator support was <1 week. Electrophysiology results were suggestive of axonal and demyelinating patterns in two patients, respectively, whereas it was not performed in one patient. Hyponatremia was noted in only 1 (20%) patient, which was attributed to the syndrome of inappropriate antidiuretic hormone secretion. Intravenous immunoglobulin (IVIG) was administered to four patients, whereas one patient received steroids. One patient died during the hospital stay; the remaining patients had an mRS score ranging from 3 to 5 at discharge.


   Discussion Top


We found a substantial reduction in the number of GBS cases during the government-imposed lockdown for COVID-19. Similarly, an epidemiological study from the United Kingdom (UK) reported a reduction in the incidence of GBS when March–May 2020 was compared with the same months in 2016–2019.[3] Increased hygiene, social distancing, and confinement to home were presumed to have decreased fecal and air-borne transmission of communicable diseases, thereby leading to a lower incidence of GBS. Based on these results, we cannot deny the possible association between COVID-19 and GBS.

Studies have reported a decrease in the incidence of infectious diseases during lockdowns.[14],[15] The total number of cases of influenza in Japan was significantly decreased when compared between September 30, 2019, and March 15, 2020, with the time frames from 2014–2019.[14] Similar results were noted when the impact of quarantine on the occurrence of other acute respiratory diseases (influenza A, influenza B, human metapneumovirus) was studied in Brazil during the COVID-19 pandemic.[15] Even the number of cases of tuberculosis has reportedly declined, probably due to a decrease in droplet aerosol transmission.[16],[17] These studies suggest that containment measures did, in fact, decrease the spread of other infectious diseases; as such, these results can be used to minimize the spread of other infections in the future. When community hygiene was adopted during the outbreak of severe respiratory distress syndrome in 2003 in Hong Kong, there was also a marked reduction in other respiratory infections.[18]

There are studies, however, that contradict our observations. In Italy, Filosto et al.[19] reported a significant increase in the number of GBS cases from March to April 2020 compared to the same months in 2019. The relative incidence in 2020, compared to 2019, was 2.6.[19] Italy witnessed a large number of COVID-19 cases, and a substantial proportion of the population was infected during the study period and was positive for COVID-19 (88%), providing a plausible explanation.[19] However, there is a possibility that specific unknown epidemiological or genetic factors have led to an increased incidence of GBS selective to their region.

Differences in clinical features during the COVID-19 period compared to the pre-pandemic period could be explained by the heterogeneity of the disease. However, the severity and outcomes did not differ despite differences in clinical characteristics. The explanation is likely to be multifactorial, including the COVID-19 pandemic, patient factors, such as reluctance to undergo invasive procedures such as plasmapheresis, and hospital factors such as the concentration of workforce toward COVID-19 management. We did not find any significant difference between the two groups in terms of treatment modality. Outcomes (i.e., mRS and GBS disability scores at discharge and 3 months after discharge) did not differ between the two groups. Our results were similar to those reported in Western countries for all these parameters.[3],[20] A cohort study from the UK reported no significant difference in the clinical presentation of GBS during the COVID-19 pandemic, except for the increased need for intubation attributed to the greater pulmonary involvement of COVID-19.[3]

We found significantly higher CSF protein values in 2019, which may be due to differences in the timing of lumbar puncture. The axonal pattern on electrophysiology was most common in both groups. Only five patients were positive for COVID-19, and they exhibited axonal (n = 2) and demyelinating (n = 2) patterns on electrophysiology. A systematic review by Uncini et al.[21] reported a demyelinating variant in 80.5% of all GBS cases associated with COVID-19. However, individual case reports have described nearly equal distributions of axonal or demyelinating patterns.[22]

Plasmapheresis was associated with higher GBS disability scores at discharge and 3 months after discharge. The poorer outcomes may reflect its use in more advanced diseases. Several other factors could have confounded this result because decisions regarding plasmapheresis or IVIG depend on individual centers or neurologist preferences, the presence of dysautonomia, sepsis or cardiac issues and, most importantly, financial constraints (i.e., plasma exchange is less expensive than IVIG in our settings). Moreover, the confidence interval (CI) was wide affecting the precision of this finding.

Some patients received corticosteroids alone or in combination with IVIG or plasmapheresis. Although there is no definite evidence supporting their efficacy in GBS, they have been used in clinical practice, especially when patients cannot afford IVIG or plasmapheresis. A Cochrane review addressing corticosteroids in GBS concluded that there was no significant difference in disability after 4 weeks of use. However, two large trials (467 patients) reported a slight improvement in disability after 4 weeks with the use of intravenous corticosteroids.[23]

In our study, the mortality rate was only 2.3% (13/555), which is lower than the overall mortality rate in the International GBS Outcome Study (IGOS) (44/659 [7%])[24] and that reported by Hughes et al.[25] (approximately 5%). Both lower mortality and less ventilatory assistance may be due to the greater treatment response in our population.

Our study had several limitations. First, data extraction for the 2019 period and a significant proportion of 2020 (as per approval of the Institute Ethics Committee) was performed retrospectively from the medical record sections of hospitals. As such, we may have missed some cases or some parameter data. Moreover, we did not collect data regarding total hospital admissions. Second, the data represent only a small proportion of the Indian population and do not include data from primary and/or secondary health care systems. Third, the lockdown restricted access to travel, which may have contributed to the decreased number of patients. Finally, we did not test COVID-19 antibodies in patients presenting to us with GBS in 2020 and, therefore, may have missed milder cases of COVID-19-triggered GBS.

In conclusion, India witnessed an overall decrease in the frequency of GBS, with no phenotypic variations, during the COVID-19 pandemic. The lockdown measures likely decreased the risk for antecedent infections and probably reflected a beneficial decrease in GBS frequency during the pandemic period.

Ethics approval

Institutional ethics approval was taken from the All India Institute of Medical Sciences (IEC-808/07.08.2020, RP-21/2020) and all participating centers as well.

Abbreviations

AF, atrial fibrillation; COVID-19, coronavirus disease 2019; CSF, cerebrospinal fluid; CTRI, Clinical Trial Registry India; DM, diabetes mellitus; DVT, deep vein thrombosis; GBS, Guillain–Barre syndrome; HTN, hypertension; IGOS, International GBS Outcome Study; IQR, interquartile range; IVIG, intravenous immunoglobulin; MFS, Miller–Fischer syndrome; MRI, magnetic resonance imaging; mRS, modified Rankin Scale; NINDS, National Institute of Neurological Disorders and Stroke; PLEX, plasmapheresis; SARS-CoV-2, severe acute respiratory syndrome Coronavirus 2; UK, United Kingdom; UL, upper limb; URI, upper respiratory tract infection; UTI, urinary tract infection; VAP, ventilator-associated pneumonia

Acknowledgement

V.Y.V. is supported by a Medical Research Council (UK) strategic award to establish an International Centre for Genomic Medicine in Neuromuscular Diseases (MR/S005021/1).

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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