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TOPIC OF THE ISSUE: ORIGINAL ARTICLE
Year : 2011  |  Volume : 59  |  Issue : 5  |  Page : 727-732

Clinical, electrophysiological subtypes and antiganglioside antibodies in childhood Guillain-Barré syndrome


1 Department of Neurology, Nizam's Institute of Medical Sciences, Hyderabad, India
2 Department of Biochemistry, Kamineni Hospitals, Hyderabad, India

Date of Submission30-Sep-2011
Date of Decision30-Sep-2011
Date of Acceptance30-Sep-2011
Date of Web Publication22-Oct-2011

Correspondence Address:
Meena A Kannan
Department of Neurology, Nizam's Institute of Medical Sciences, Hyderabad 500068
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.86549

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 » Abstract 

Background: Guillain-Barré syndrome (GBS) has been the most common cause of flaccid paralysis in children after the decline in the incidence of poliomyelitis. There are not any published data from the Indian subcontinent documenting electrophysiological patterns and antiganglioside antibodies in pediatric GBS. Materials and Methods: The study population included children with GBS referred for electrodiagnostic evaluation and also children with GBS admitted to our institute between August 2006 and July 2007. Nerve conduction studies were done to determine GBS subtypes and serum antiganglioside antibodies were measured using enzyme-linked immunosorbent assay (ELISA). Clinical and electrophysiological features were correlated with antiganglioside antibody results. Results: Of the 43 (male to female ratio = 2.1:1) children studied, 97.6% had motor weakness, 76.7% had cranial nerve palsies, 13.9% had autonomic disturbances and respiratory paralysis was found in 9.3% children. Antecedent illness was recorded in 69.8% children. The GBS subtype distribution was as follows: acute inflammatory demyelinating polyradiculoneuropathy (AIDP) in 21 (48.8%), acute motor axonal neuropathy (AMAN) in 19 (44.2%), and 3 (6.9%) children were unclassified. The severity of illness was similar in both AMAN and AIDP subtypes and the recovery in both the subtypes was complete without any significant difference in the duration of recovery. Preceding diarrheal illness was more common in AMAN subtype as compared to AIDP subtype (57.9% vs. 4.7%, P = 0.007). Sensory symptoms were more common in AIDP subtype than in AMAN subtype (66.6% vs. 21%, P = 0.03}. The commonest ganglioside antibody was IgM GM2. Anti GM3 antibodies were exclusively seen in children with AMAN and IgG GD1b was significantly associated with (36.7 vs. 4%; P = 0.007) AMAN subtype. IgG GT1b was identified in 50% of patients with AIDP as compared to 22.7% in patients with AMAN. Conclusion: In this study, AMAN subtype accounted for a significant proportion of pediatric GBS. AMAN was associated with diarrhea and specific antiganglioside antibodies. Recovery in children with GBS was complete, irrespective of the subtype.


Keywords: Acute axonal motor neuropathy, acute inflammatory demyelinating polyradiculoneuropathy, antiganglioside antibodies, Guillain-Barrι syndrome


How to cite this article:
Kannan MA, Ch RK, Jabeen S A, Mridula K R, Rao P, Borgohain R. Clinical, electrophysiological subtypes and antiganglioside antibodies in childhood Guillain-Barré syndrome. Neurol India 2011;59:727-32

How to cite this URL:
Kannan MA, Ch RK, Jabeen S A, Mridula K R, Rao P, Borgohain R. Clinical, electrophysiological subtypes and antiganglioside antibodies in childhood Guillain-Barré syndrome. Neurol India [serial online] 2011 [cited 2019 Oct 17];59:727-32. Available from: http://www.neurologyindia.com/text.asp?2011/59/5/727/86549



 » Introduction Top


Guillain-Barré syndrome (GBS) is an acute immune-mediated polyradiculoneuropathy with an incidence of 0.9-1.1 cases per 100,000 children below 15 years of age. [1],[2],[3] Since the marked decline in poliomyelitis, GBS has been the most frequent cause of acute flaccid paralysis (AFP) among children. [3] The disorder typically begins after recovery from an antecedent illness or vaccination. [4] Distal paresthesias evolve into symmetric progressive ascending areflexic motor weakness often in association with facial weakness and pain in limbs and back. Weakness may progress rapidly, necessitating the need for ventilatory support and may be associated with autonomic dysfunction. The clinical course of GBS in children can be somewhat milder, with a greater likelihood of recovery in comparison to adults. [5],[6] Diagnosis is based on certain characteristic clinical criteria and exclusion of other causes of polyneuropathy. [7]

Demyelination is considered to be the main pathological process underlying acute inflammatory demyelinating polyradiculoneuropathy (AIDP), the most common form of GBS . [1] In the early 1990s, the pure motor axonal form, acute motor axonal neuropathy (AMAN), was described from northern China. [8],[9] Other subtypes described include acute motor sensory axonal neuropathy (AMSAN), Miller-Fisher syndrome and other minor variants of GBS. [10] The incidence of different GBS subtypes has significant geographical variation. In the studies from Western world, AIDP accounts for 85-90% of GBS. [5] In contrast, in North China, studies indicate that AMAN accounts for 70% of GBS and less than a quarter is AIDP and other subtypes. [8]

The immunological basis of GBS involves an antibody attack on a variety of target glycolipid antigens on nerve terminals and axons and frequent elevation of antiganglioside antibodies in the acute phase has also been reported, [11] suggesting their role in the pathogenesis of GBS. Antiganglioside antibodies may be the factors determining the distribution of the damage by binding to the respective ganglioside antigens having a unique localization. This has been well studied in Miller-Fisher syndrome and AMAN variant. [12] Antiganglioside Gq 1b subtype has been associated with opthalmoplegia and Miller-Fisher syndrome. GM1, GQlb, and GDla subtypes have been seen in an axonal variant of GBS. The AIDP subtype is not commonly associated with any of these antibodies. [13] Presence of antibodies has not been found to be of much use in predicting the outcome, while it has been observed that the absence of antiganglioside antibodies is associated with poor recovery. [14] Prognosis in pediatric GBS has been found to be favorable as compared to adults. Most of the children recover completely without any residual deficits. [5] Even though the AMAN variant has been found to be more prevalent in children, there have been no data to support that it is associated with poor outcomes. [15]

There is a paucity of literature on pediatric GBS from India. The purpose of this study was to determine the frequency of different electrophysiological subtypes and their association with antiganglioside antibodies in pediatric GBS.


 » Materials and Methods Top


Patients

All pediatric patients between 1 and 18 years of age with GBS, fulfilling the clinical criteria [7] and referred for electrodiagnostic evaluation to the Electrodiagnostic Laboratory between August 2006 and July 2007, were included in the study. The demographic data recorded included age, sex, month of illness, duration of illness and preceding antecedent illness. Detailed clinical history and neurological examination were performed. Patient disability at the peak of the deficit was assessed using Hughes functional grading scale [16] (Grade 0: normal, Grade 1: able to run with minor signs and symptoms, Grade 2: able to walk 5 m independently, Grade 3: able to walk 5 m with aid, Grade 4: bed or chair bound, Grade 5: requires assisted ventilation, Grade 6: death). Outcome was assessed at 6 months of follow-up. All the children underwent a stool culture for polio virus under the AFP surveillance program.

Electrodiagnostic studies

Nerve conduction studies were performed within 4 weeks of onset of neurological symptoms and were repeated if the initial conduction studies were normal. Motor conduction studies were performed on median, ulnar, tibial and peroneal nerves using conventional techniques. Sensory nerve conduction studies were performed on median, ulnar and sural nerves using conventional techniques.

For children 3 years or older, adult nerve conduction values were taken as normal because the nerve conduction parameters of children approach adult value by that age. [17],[18] For children of age 1-2 years, normal limits were set as 80% of the adult value for motor nerve conduction velocity (CV) and compound motor action potential (CMAP) amplitude and as 120% of the adult values for distal latencies because nerve conduction parameters approach 80-90% of the adult values by this age. [19] For children below the age of 1 year, normal limits were taken as half of the adult values for CV and CMAP, twice the values for distal latency because the mean values for nerve conduction velocities in children under the age of 1 year have been reported to be approximately 50% of the adult values. [18],[19]

Patients were classified as having AMAN or AIDP on the basis of the electrodiagnostic criteria proposed by Ho et al. [20] When patients had one of the following findings in two (or more) nerves during the first 2 weeks of illness, they were classified as having AIDP:

  • CV <90% of the lower limit of the normal if the amplitude is >50% of the lower limit of normal; <85% if the amplitude is <50% of the lower limit of normal.
  • Distal latency >110% of the upper limit of normal if the amplitude is normal; >120% of the upper limit of normal if the amplitude is less than the lower limit of normal.
  • Evidence of unequivocal temporal dispersion.
  • F response latency >120% of the normal.
When patients had no evidence of demyelination as defined and had a decrease in CMAP amplitude to <80% of the lower limit of normal in two (or more) nerves, they were classified as having AMAN. None of the features of AIDP, dCMAP<80% LLN in at least 2 nerves and SNAP <50% LLN in at least 2 nerves was classified as AMSAN. Unclassified patients had milder conduction abnormalities, which did not meet the criteria of AIDP or AMAN or AMSAN.

Antiganglioside antibodies

The serum antiganglioside antibodies (IgG and IgM) were assayed using Euroimmune (Germany) kits. GM 1 , GM 2 , GM 3 , GD la , GD lb , GT lb and GQ 1b subtypes were tested. This test is a qualitative enzyme-linked immunosorbent assay (ELISA)-based in vitro assay for human antibodies in serum. The test kit contains test strips coated with parallel lines of purified antigens. Blot strips are incubated with diluted (1:10) patient's serum. In the case of positive samples, specific antibodies of the class IgG or IgM will bind to the antigens. To detect the bound antibodies, a second incubation is carried out using an enzyme-labeled anti-human IgG/IgM enzyme conjugate, which is capable of promoting a color.

Statistical analysis

Descriptive statistics were done for the demographic data. Differences in proportions were examined by the Fisher's exact test or chi-square test, using the graph pad statistical software in Windows 2001.


 » Results Top


During the study period, 247 patients were diagnosed to have GBS and confirmed at Nizam's Institute of Medical Sciences and Niloufer Pediatric Hospital, Hyderabad. Forty-three (17.4%) cases in the pediatric age group were analyzed. The basic characteristics of the children are given in [Table 1], [Figure 1]. There were 29 (67.4%) male and 14 (32.5%) female patients (M:F = 2.1:1). The mean age was 8 years (range 11 months to 18 years). Seventeen (39.5%) children were less than 5 years of age, 11 (25.6%) were between 5 and 10 years of age, and 16 (37.2%) were >10 years of age. The mean duration of the illness was 6.8 days. Thirty (69.8%) children had antecedent illness: fever in 21 (48.8%), acute respiratory infection in 11 (25.6%), and gastroenteritis in 13 (30.2%). One child developed GBS after an anti-rabies vaccination. The peak incidence was seen between August and September [Figure 2]. Weakness was seen in 42 (97.6%) patients, sensory symptoms in 18 (41.9%), cranial nerve dysfunction in 33 (76.7%), autonomic dysfunction in 6 (13.9%) (labile blood pressure in 4, hypotension in 1 and sinus tachycardia in 1), and respiratory weakness in 4 (9.3%) children. Twenty-three (53.5%) children were in Hughes Grade 4. Immunotherapy, intravenous immunoglobulin, was given to 36 (83.7%) children [Figure 2].
Figure 1: Male predominance in childhood GBS

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Figure 2: Seasonal distribution of GB patients

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Table 1: Demographic and clinical features of children with GBS

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Different subtypes of GBS based on electrophysiological abnormalities included AIDP in 21 (48.8%), AMAN in 19 (44.2%) and unclassified in 3 (6.9%) children [Figure 3]. Both AMAN (68.4%) and AIDP (71.4%) have a male predominance. Sensory symptoms were significantly less in the AMAN subtype (21.0% vs. 66.67%, P = 0.03). Gastroenteritis was significantly associated with the AMAN (57.9%) subtype when compared to AIDP (4.7%) (P = 0.007). There was no significant difference between mean Hughes grade of illness in both the subtypes (3.7 ± 0.8 vs. 3.6 ± 0.7) [Table 2]. All the children, except three, were in Hughes Grade 1 at 6 months. Three children were in Hughes Grade 2 at 6 months of follow-up and all of them belonged to the AMAN subtype.
Figure 3: Different patterns of GBS

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Table 2: Clinical features in different patterns of GBS

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A total of 42 patients were tested for IgG and 40 patients were tested for IgM antibodies. IgG antibodies were positive in 22 (51.2%) children and IgM antibodies tested positive in 27 (67.5%) children. The presence of antibodies correlated with several clinical features and patterns of GBS [Table 3]. Different subtypes of IgG antibodies were correlated with different subtypes of GBS [Figure 4]. The commonest IgG antibodies seen in our series were GT1b in 16 (38.1%) patients, followed by GQ1b in 11 (26.2%) patients. The GD1b antibody was more commonly seen in AMAN subtype, when compared to the AIDP (36.7% vs. 4%, P < 0.007) children.
Figure 4: IgG antibodies in different subtypes of GBS

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Table 3: Antiganglioside antibodies in different patterns of GBS

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 » Discussion Top


GBS affects all ages, but is more frequent in adults over 40 years of age. In children, it mostly occurs after 3 years of age. Median age of the children in our study was 8 years, similar to the previous studies. [21] In our study, there was male gender predominance. Nachamkin et al. [22] reported a slight male predominance (M:F = 1.3:1) in the Mexican population. Similar gender differences were noted in Turkish children. [23] In our study, the clinical features did not differ from adult patients. Cranial nerve dysfunction was seen in 72.9% patients, with the facial nerve being most commonly affected. These findings are consistent with previous published literature. [24] Bulbar involvement was seen in 37% of our study population. Similar bulbar involvement was reported in Taiwanese children. [25] Sensory symptoms were seen in only 45% of children, which is on an average less than the reported findings in literature. This could be due to the younger children's inability to explain sensory symptoms. Respiratory weakness and requirement for mechanical ventilation was less common in childhood GBS. Respiratory weakness was seen in 13% of Japanese children with GBS. [26] In our study, only 11% of patients required mechanical ventilation. Antecedent illness was reported in two-thirds of patients with GBS. [4] Majority of our population showed antecedent events. Seasonal clustering of cases was seen in our study, similar to the observations in other studies. [22]

In this study of pediatric GBS, AMAN accounted for 44.2% of GBS cases. The reported frequency of AMAN in children in Japan [26] was about 48% and it was 38% in Mexican children. [22] The reported frequency of AMAN in Chinese children ranged between 65% and 86%. [8],[20] In contrast, AIDP was the predominant reported subtype in children from North America. [5] The reported incidence of AMAN in adults was less when compared with these studies. [27] This difference in the incidence of AMAN between children and adults could be due to the different antecedent infections in children. The incidence of AMAN in our study was less when compared to the Chinese childhood population. It could be partly due to the milder cases not being referred for both electrodiagnostic evaluation and also for admission to territory care centers. The other factor could be that in our institute there is no pediatric service.

In our study, antecedent illness was seen equally in both subtypes of GBS. Gastroenteritis was significantly associated with AMAN when compared with AIDP (57.9% vs. 4.7%, P = 0.007) and upper respiratory tract infection was significantly associated with AIDP (7.6% vs. 47.6%, P = 0.0001). Similar associations had been reported in Japanese children. [26] We did not evaluate campylobacter antibodies in the present study to correlate with antecedent gastroenteritis.

The present study did not show any difference in the clinical features between the two subtypes of GBS, similar to previous published reports. [21],[26] The sensory symptoms in the present study were significantly less in the AMAN subtype. There was no significant difference in the mean grade of illness at the peak of the disease in both the subtypes. There were no deaths in the present study. All the children in both the groups, except three children, showed complete recovery. There children, who were in functional Grade 2 at 6 months belonged to AMAN subtype. Though the rate of recovery was slow in the AMAN subtype, as compared to AIDP, both AMAN and AIDP children had a good recovery. Slow and complete recovery of AMAN subtype had been reported in the earlier studies. [21],[22],[26] Patients with AMAN subtype continued to improve even after 6 months. The rate of recovery of pediatric GBS was faster in the present study as compared to adults. [28]

The reported frequency of serum antiganglioside antibodies varies in different geographical areas. In the present study, IgG antibodies were positive in 52.3% of patients. There was no significant difference between AIDP and AMAN subtypes. Our study did not find any correlation between clinical features and the type of antibodies. IgG GD1b antibodies had been significantly associated with the AMAN subtype in the present study. In a study in adult patients with GBS from South India, [29] Of the 10 patients of AMAN, 8 patients had GD1b antibody in the serum (unpublished data). The significance of the GD1b antibody in GBS has been studied earlier. [14],[30] Nachamkin et al. [22] reported a higher proportion of children with AMAN having GD1b antibody from Mexico. IgG GM1 antibody had been shown to be significantly associated with the AMAN subtype, [26] but the same was not found in the present study. This may be due to the regional variation and different antecedent infections in the population. In the present study, IgG GT1b was found in a higher proportion of patients with AIDP. This is in contradiction to previous published reports. [28] In the present study, IgG GM3 is associated with AMAN, a finding which has not been described earlier. An earlier unpublished study from our institute showed the presence of GM3 antiganglioside antibodies in adult patients. [29] The presence of antiganglioside antibodies in serum was not found to be of much use in predicting the outcome. [31] However, the absence of antibodies has been shown to be associated with poor outcomes. [14] In the present study, no correlation between the presence and absence of antibodies with the outcome was found.

To conclude, childhood GBS shares common clinical features with adult GBS and has a favorable outcome, with lower rates of residual deficits than adults. The rate of recovery is faster in children, when compared to adults. Although AIDP is a slightly common subtype in children, AMAN constituted a significant proportion of pediatric GBS as compared with adults. The clinical features did not differ in the different subtypes of GBS. GD1b antibody was the commonest antiganglioside antibody associated with the AMAN variant. [31]


 » Acknowledgments Top


We thank Dr Ananth Reddy, Professor of Pediatrics, and our colleagues at Niloufer Pediatric Hospital, Hyderabad, for their cooperation and help in this study.

 
 » References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]

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Ahmed S. El-Beleidy,Asser A. Khattab,Seham A. El-Sherbini,Tarek Z. El-Adely,Hala M. Sleem,Rabab E.S. EL-Haware
Pediatria Polska. 2013; 88(3): 224
[Pubmed] | [DOI]
11 Anti-GM2 ganglioside antibodies are a biomarker for acute canine polyradiculoneuritis
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Journal of the Peripheral Nervous System. 2013; 18(1): 75
[Pubmed] | [DOI]
12 Guillain-Barré syndrome
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Seminars in Neurology. 2012; 32(3): 179-186
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Online since 20th March '04
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