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GUILLAIN-BARRE SYNDROME; THE SEASONAL TRENDS IN A COHORT OF PAKISTANI POPULATION FROM SOUTHERN PUNJAB.

Byline: Nadeem Ahmad, Zaheer Ahmed Gill, Saeed Bin Ayaz, Noreen Akhtar, Aamir Waheed Butt and Waseem Iqbal

Keywords: Electrodiagnosis, Flaccid paralysis, Guillian-Barre Syndrome, Pakistan, Seasonal variation, Southern Punjab.

INTRODUCTION

GuillianBarre Syndrome(GBS) is a rapidly progressive acute inflammatory acquired peripheral polyneuropathy characterized by symmetrical weakness and areflexia. It is one of the most frequent causes of acute onset ascending flaccid weakness since eradication of polio with an incidence of 1-2 per 100,000/year in most populations1. Nearly two-third cases of GBS have a 4-6 weeks' preceding history of infection. Gastrointestinal and respiratory infections are the two most common identified antecedent infections either of bacterial or viral origin. Campylobacter jejuni, Cytomegalovirus, Epstein Bar Virus, Mycoplasma, Hepatitis E Virus, and recently, Zika virus are frequently identified responsible organisms2. GBS presents clinically as symmetrical ascending weakness with areflexia, oculomotor weakness, and ataxia3. However, other rare clinical presentations of GBS have been reported in the Pakistani literature4,5.

On the basis of neurophysiological properties, GBS is subdivided into four main subtypes including Acute Inflammatory Demyelinating Polyneuropathy(AIDP), Acute Motor Axonal Neuropathy(AMAN), Acute Motor and Sensory Axonal Neuropathy(AMSAN), and Miller Fisher Syndrome(MFS)6.

Contradictory evidence exists for seasonal variation of GBS with some studies suggesting a winter trend3, some reporting summer, spring or autumn peak7-9, and others finding no significant variation10. Seasonal variations in GBS are likely to be dependent on the seasonality of underlying illness considered to cause cross-reactivity with molecular epitope on the peripheral nerves. The subtypes of GBS are also thought to follow some seasonal tendencies independent of each other.

In our clinical practice in Southern Punjab, we observed a clustering of GBS occurrence in certain months and seasons of the year. So, we carried out this retrospective study to know the seasonal reporting and monthly variation of GBS. We then ascertained the seasonal preferences of GBS sub-types as determined on electrodiagnosis(EDX) i.e. nerve conduction studies(NCS) and electromyography(EMG). This, in turn, has an implication for seasonal demand for EDX procedures, neurology, neuro-intensive care, and neuro-rehabilitation services.

METHODOLOGY

It was a retrospective observational study carried out from January 2016 to October 2018 in the department of Physical Medicineand Rehabilitation(PMR) at Combined Military Hospital(CMH) Bahawalpur, which is one of the only two referral setups for EDX facilities in Southern Punjab. PMR specialty is relatively new in Pakistan. There are only two PMR physicians for 3.0 million population of southern Punjab. So, patients reporting here for EDX represent the bulk of GBS patients in this region.

A sample size of 135 was calculated using World Health Organization sample size calculator while using 95% confidence level, absolute precision of 7% and of anticipated population proportion of 21.9%11. We explored record of the department and retrospectively sampled the patients with an EDX diagnosis of GBS. Electrodiagnostic criteria of Hadden et al12 for GBS was followed for the diagnosis in our department. The criteria also classifies GBS into its subtypes that have a different pattern of clinical recovery. Patients with history of diabetes mellitus, porphyria, delayed milestones, cerebral palsies, and stroke were excluded. All EDX studies had been done with Nicolet Viasys EMG System using Viking Quest Master Software V. 9.00(Natus Medical Incorporated, WI, USA). The studies were carried out within four weeks of the onset of weakness.

The data were analyzed with Statistical Package for Social Sciences v 20.0(IBM Corp., Armonk, NY, USA). Demographic details including age, gender, residential area, month of referral, season, referring physician, and subtypes of GBS were documented in terms of frequencies and percentages. The seasons were divided as: Summer: May to August, autumn: September and October, winter: November to February, and spring: March and April. In order to compare the frequency of GBS in different seasons and months, we used the chi-square goodness-of-fit test. All tests for statistical significance had a level of significance set at a$?0.05.

RESULTS

Out of 152 cases, who were finally included after exploring the departmental record, 114(75%) were males and 38(25%) were females. Age at onset of the disease varied from one year to 86 years with a mean age of 39 +- 21 years. Majority 55(36.2%) belonged to Bahawalpur with Lodhran and Yazman to fall at second place 10(6.6%) each. AIDP was the most frequent sub-type of GBS 88(57.9%) followed by AMSAN 33(21.7%), AMAN 30(19.7%), and MFS 1(0.7%). Neurophysicians sent the maximal referrals for EDX 83(54.6%), followed by internal medicine specialists 48(31.6%), pediatricians 17(11.2%), neurosur-geons 3(2%), and orthopedic surgeons 1(0.7%). The highest reporting was in winter season 63(41.4%) followed by the summer season 53(34.9%)(p<0.001)(table-I). Although disease was found throughout the year, the month of May had the highest frequency 24(15.8%) followed by the month of Jan 20(13.2%)(p=0.002)(table-II).

Table-I: Variation of GuillianBarre Syndrome in reference to season.

Seasons###n(%)###I2###Df###p-

###value

Winter###63(41.4)

Spring###23(15.1)

###44.74###3###<0.001

Summer###53(34.9)

Autumn###13(18.6)

Table-II: Distribution of GuillianBarre Syndrome cases in different months(p=0.001).

Months###n(%)###I2###df###p-

###value

Jan###20(13.2)

Feb###12(7.9)

Mar###8(5.3)

Apr###15(9.9)

May###24(15.8)

Jun###5(3.3)

###29.9###11###0.002

Jul###16(10.5)

Aug###7(4.6)

Sep###8(5.3)

Oct###7(4.6)

Nov###16(10.5)

Dec###14(9.2)

AIDP and AMAN were significantly more frequent in winter season(p<0.001 and p=0.008 respectively) while AMSAN was significantly more common in summer season(p=0.01)(tableIII). Statistics for MFS were not computable. Regarding the association with a particular month, AIDP was significantly more common in May(p=0.025). AMAN and AMSAN could not find a particular predilection(p=0.178 and p=0.166 respectively)(table-IV). Statistics for MFS were not computable here as well.

Table-III: Distribution of different entities of GuillianBarre Syndrome based on the seasons.

###Winter###Spring###Summer###Autum###I2###p-value

Guillian- Barre Syndrome Entity###n(%)###n(%)###n(%)###n(%)

Acute Inflammatory

Demyelinating Polyneuropathy###36(40.9)###13(14.8)###32(36.4)###7(8)###27.36###<0.001

Acute Motor Axonal Neuropathy###15(50)###6(20)###7(23.3)###2(6.7)###11.87###0.008

Acute Motor and Sensory Axonal

Neuropathy###12(36.4)###4(12.1)###14(42.4)###3(9.1)###11.24###0.01

Miller Fisher Syndrome###-###-###-###1(100)###-

DISCUSSION

Seasonal variation in occurrence of GBS is not consistent and considered attributable to distinct geographical and racial distribution. With analysis of nearly three-year' data, we found seasonal and monthly clustering in GBS cases i.e. we came across maximum cases in winter season though new cases were observed throughout the year. In earlier Pakistani studies, Abbas et al3 observed winter as the trending season for GBS. Ali et al8 and Chand et al13 noted summer while Yaqoob et al14 documented increased reporting in the spring season. This difference is probably due to geographic and climatic variation in residing areas of the studied population. A logical explanation of GBS winter trend appears to be higher frequency of upper respiratory tract infection and flu-like symptoms in winter.

A definite seasonal trend has been reported in other parts of the world as well. Winter season was reported from Denmark, France, UK, and Australia15-18, autumn from Iran and Sweden9,19, summer from India and China7,20, and spring from Chile and Taiwan21,22. In contrast, no significant seasonal tendency was reported from Finland and Japan10,23. Hence the review of all these studies indicates that it is hard to define any specific trend of seasonal variations for GBS patients because the climate conditions are strikingly different even in the same country. So, the study with larger cohort size and maximum time span may only serve as reference study for that area of the world.

Our study reported maximum cases in May(n=24) and January(n=20). Occurrence of GBS from January to May accounted for more than 50% cases with January and May having a peak with over 20 cases per month. Ali et al8 reported maximum cases in June. Abbas et al and Sipila et al3,10 received bulk of the cases in January and February. Momen and colleagues noticed maximum number of cases in December9. Levison et al14 in a Danish study, observed maximum number of cases in December and January, while Wu et al19 in a Chinese study, described peak GBS incidence in July and August.

Table-IV: Distribution of different entities of GuillianBarre Syndrome based on the months.

Miller###Acute Motor###Acute###Acute###Guillian-

Fisher###and Sensory###Motor###Inflammatory###Barre

Syndrome###Axonal###Axonal###Demyelinating###Syndrome

###Neuropathy###Neuropathy###Polyneuropathy###Entity

-###1(3)###8(26.7)###11(12.5)###Jan

###n(%)

-###3(9.1)###2(6.7)###7(8)###Feb

###n(%)

-###2(6.1)###1(3.3)###5(5.7)###Mar

###n(%)

-###2(6.1)###5(16.7)###8(9.1)###Apr

###n(%)

-###5(15.2)###3(10)###16(18.2)###May

###n(%)

-###1(3)###2(6.7)###2(2.3)###Jun

###n(%)

-###5(15.2)###2(6.7)###9(10.2)###Jul

###n(%)

-###3(9.1)###-###4(4.5)###Aug

###n(%)

-###2(6.1)###2(6.7)###4(4.5)###Sep

###n(%)

1(100)###1(3)###-###5(5.7)###Oct

###n(%)

-###7(21.2)###2(6.7)###7(8)###Nov

###n(%)

-###1(3)###3(10)###10(11.4)###Dec

###n(%)

###15.36###12.67###21.91###I2

-###0.166###0.178###0.025###p-value

AIDP was the most frequent sub-type of GBS in our study. Other Pakistani studies have also observed AIDP as the most common variant8,13. Most other studies from India, China, UK, and Australia have reported AIDP as the most frequent form of GBS7,17,18,21. On the contrary, one recent study from Pakistan, one from Ethiopia, and one from Bangladesh showed opposite results with AMAN to be the most common variety11,24,25. The difference could be partly accounted for variations in the environmental factors, pathogenic mechanisms, genetic susceptibility, and other triggering factors such as different infections operating in different populations25. Here, it may be noted that the EDX features evolve over time and may be misleading in early stages of the disease25. Serial recordings are, therefore, may be recommended.

In this study, we found that AIDP and AMAN were significantly more frequent in winter season, while AMSAN was in summer season. Regarding monthly distribution, AIDP found a significant association with the month of May. This association of AIDP appears to be different from the seasonal findings. This probably resulted from statistical mis-interpretation as the total cases in other months of summer and winter seasons were less for AIDP. Thus a reliable conclusion regarding a particular month could not be drawn. MFS did not find any association with a particular season or month. While reviewing the literature, Webb et al17 reported all types of GBS to be more frequent in winter season. Shrivastava et al7 found AIDP more common in spring and AMAN more common in summer seasons. The higher frequency of admissions in the winter season was associated with a higher incidence of patients reporting a respiratory prodromal illness17.

Seasonal variation in GBS is particularly important for our understanding of the likely pathogenesis of the disease. This may have public health implications in the future for identifying prodromal infections that could be prevented to reduce the incidence of GBS in specic regions. It also has some potential implications for provision of tertiary neurological and rehabilitation services, particularly in regions with a high incidence of summer GBS due to AMAN, which can result in longer admissions and greater bed occupancy, particularly in neuro intensive care.

There are few limitations to this study. First, it was a retrospective study based on notes review. This may contribute to as certainment or under-reporting error. Second, in our study, Close tridum jejuni serology and anti-ganglio side antibodies were not systematically performed, and therefore these were not addressed in our study. Finally, we had only one case for MFS, thus conclusion based on this small number of patients could not be drawn.

ACKNOWLEDGMENT

We greatly value and acknowledge the patronage and guiding help of Prof Dr Brig(R) P.H.K Niazi, the pioneer of the specialty of Physical Medicineand Rehabilitation(PMandR) in Pakistan. It was his intellectual and moral support that helped us learn and perform the NCS/EMG studies with confidence.

CONCLUSION

The clustering of GBS cases were found in winter season and in the month of May in our cohort. AIDP and AMAN were significantly more frequent in winter season, while AMSAN was significantly more frequent in summer season.

CONFLICT OF INTEREST

This study has no conflict of interest to be declared by any author.

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Author:Nadeem Ahmad, Zaheer Ahmed Gill, Saeed Bin Ayaz, Noreen Akhtar, Aamir Waheed Butt and Waseem Iqbal
Publication:Pakistan Armed Forces Medical Journal
Geographic Code:9INDI
Date:Aug 31, 2020
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