• 1.

    Cassadou S, Boucau S, Petit-Sinturel M, Huc P, Leparc-Goffart I, Ledrans M, 2014. Emergence of chikungunya fever on the French side of Saint Martin island, October to December 2013. Euro Surveill 19: 13.

    • Search Google Scholar
    • Export Citation
  • 2.

    Thiberville S-D, Moyen N, Dupuis-Maguiraga L, Nougairede A, Gould EA, Roques P, de Lamballerie X, 2013. Chikungunya fever: epidemiology, clinical syndrome, pathogenesis and therapy. Antiviral Res 99: 345370.

    • Search Google Scholar
    • Export Citation
  • 3.

    van den Berg B, Walgaard C, Drenthen J, Fokke C, Jacobs BC, van Doorn PA, 2014. Guillain-Barre syndrome: pathogenesis, diagnosis, treatment and prognosis. Nat Rev Neurol 10: 469482.

    • Search Google Scholar
    • Export Citation
  • 4.

    van Doorn PA, Ruts L, Jacobs BC, 2008. Clinical features, pathogenesis, and treatment of Guillain-Barré syndrome. Lancet Neurol 7: 939950.

  • 5.

    Sahu R, Verma R, Jain A, Garg RK, Singh MK, Malhotra HS, Sharma PK, Parihar A, 2014. Neurologic complications in dengue virus infection: a prospective cohort study. Neurology 83: 16011609.

    • Search Google Scholar
    • Export Citation
  • 6.

    Davis LE, DeBiasi R, Goade DE, Haaland KY, Harrington JA, Harnar JB, Pergam SA, King MK, DeMasters BK, Tyler KL, 2006. West Nile virus neuroinvasive disease. Ann Neurol 60: 286300.

    • Search Google Scholar
    • Export Citation
  • 7.

    Lebrun G, Chadda K, Reboux A-H, Martinet O, Gaüzère B-A, 2009. Guillain-Barré syndrome after chikungunya infection. Emerg Infect Dis 15: 495.

  • 8.

    Oehler E, Fournier E, Leparc-Goffart I, Larre P, Cubizolle S, Sookhareea C, Lastère S, Ghawche F, 2015. Increase in cases of Guillain-Barré syndrome during a chikungunya outbreak, French Polynesia, 2014 to 2015. Euro Surveill 20: 30079.

    • Search Google Scholar
    • Export Citation
  • 9.

    Oehler E, Watrin L, Larre P, Leparc-Goffart I, Lastere S, Valour F, Baudouin L, Mallet H, Musso D, Ghawche F, 2014. Zika virus infection complicated by Guillain-Barre syndrome–case report, French Polynesia, December 2013. Euro Surveill 19: 20720.

    • Search Google Scholar
    • Export Citation
  • 10.

    Asbury AK, Cornblath DR, 1990. Assessment of current diagnostic criteria for Guillain-Barré syndrome. Ann Neurol 27: S21S24.

  • 11.

    Hughes RA, Swan AV, van Doorn PA, 2014 . Intravenous immunoglobulin for Guillain-Barré syndrome. Cochrane Database Syst Rev. Available at: http://onlinelibrary.wiley.com/doi/10.1002/14651858.CD002063.pub6/full. Accessed October 5, 2015.

    • Search Google Scholar
    • Export Citation
  • 12.

    Gérardin P, Couderc T, Bintner M, Tournebize P, Renouil M, Lémant J, Boisson V, Borgherini G, Staikowsky F, Schramm F, Lecuit M, Michault AEncephalchik Study Group, 2016. Chikungunya virus-associated encephalitis: a cohort study on La Réunion Island, 2005–2009. Neurology 86: 94102.

    • Search Google Scholar
    • Export Citation
  • 13.

    Torres JR, Córdova LG, Saravia V, Arvelaez J, Castro JS, 2015. Nasal skin necrosis: an unexpected new finding in severe chikungunya fever. Clin Infect Dis 62: 7881.

    • Search Google Scholar
    • Export Citation
  • 14.

    Rollé A, Schepers K, Cassadou S, Curlier E, Madeux B, Hermann-Storck C, Fabre I, Lamaury I, Tressières B, Thiery G, Hoen B, 2016. Severe sepsis and septic shock associated with chikungunya virus infection, Guadeloupe, 2014. Emerg Infect Dis 22: 891894.

    • Search Google Scholar
    • Export Citation
  • 15.

    Sivadon-Tardy V, Orlikowski D, Rozenberg F, Caudie C, Sharshar T, Lebon P, Annane D, Raphaël J-C, Porcher R, Gaillard J-L, 2006. Guillain-Barré syndrome, greater Paris area. Emerg Infect Dis 12: 990.

    • Search Google Scholar
    • Export Citation
  • 16.

    Webb AJ, Brain SA, Wood R, Rinaldi S, Turner MR, 2015. Seasonal variation in Guillain-Barré syndrome: a systematic review, meta-analysis and Oxfordshire cohort study. J Neurol Neurosurg Psychiatry 86: 11961201.

    • Search Google Scholar
    • Export Citation
  • 17.

    Soares CN, Cabral-Castro M, Oliveira C, Faria LC, Peralta JM, de Freitas MRG, Puccioni-Sohler M, 2008. Oligosymptomatic dengue infection: a potential cause of Guillain Barré syndrome. Arq Neuropsiquiatr 66: 234237.

    • Search Google Scholar
    • Export Citation
  • 18.

    Kanikannan MAK, Durga P, Venigalla NK, Kandadai RM, Jabeen SA, Borgohain R, 2014. Simple bedside predictors of mechanical ventilation in patients with Guillain-Barré syndrome. J Crit Care 29: 219223.

    • Search Google Scholar
    • Export Citation
  • 19.

    Rajabally YA, Uncini A, 2012. Outcome and its predictors in Guillain–Barré syndrome. J Neurol Neurosurg Psychiatry 83: 711718.

  • 20.

    Teo TH, Her Z, Tan JJ, Lum FM, Lee WW, Chan YH, Ong RY, Kam YW, Leparc-Goffart I, Gallian P, Rénia L, de Lamballerie X, Ng LF, 2015. Caribbean and La Réunion chikungunya virus isolates differ in their capacity to induce proinflammatory Th1 and NK cell responses and acute joint pathology. J Virol 89: 79557969.

    • Search Google Scholar
    • Export Citation
  • 21.

    Wei Chiam C, Fun Chan Y, Chai Ong K, Thong Wong K, Sam IC, 2015. Neurovirulence comparison of chikungunya virus isolates of the Asian and East/Central/South African genotypes from Malaysia. Gen Virol. 96: 32433254.

    • Search Google Scholar
    • Export Citation
  • 22.

    Willison HJ, Jacobs BC, van Doorn PA, 2016. Guillain-Barré syndrome. Lancet 388: 717727.

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Guillain–Barré Syndrome and Chikungunya: Description of All Cases Diagnosed during the 2014 Outbreak in the French West Indies

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  • 1 Service des Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Pointe-à-Pitre/Abymes, Pointe-à-Pitre, France;
  • | 2 Service des Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Martinique, Martinique, France
  • | 3 Faculté de Médecine Hyacinthe Bastaraud, Université des Antilles, Pointe-à-Pitre, France
  • | 4 INSERM CIC1424, Centre Hospitalier Universitaire de Pointe-à-Pitre/Abymes, Pointe-à-Pitre, France
  • | 5 Laboratoire de Virologie, Centre Hospitalier Universitaire de Pointe-à-Pitre/Abymes, Pointe-à-Pitre, France
  • | 6 Laboratoire de Virologie, Centre Hospitalier Universitaire de Martinique, Martinique, France
  • | 7 Service de Réanimation, Centre Hospitalier Universitaire de Pointe-à-Pitre/Abymes, Pointe-à-Pitre, France
  • | 8 Service de Neurologie, Centre Hospitalier Universitaire de Martinique, Martinique, France
  • | 9 Service de Réanimation, Centre Hospitalier Universitaire de Martinique, France
  • | 10 Service de Neurologie, Centre Hospitalier Universitaire de Pointe-à-Pitre/Abymes, Pointe-à-Pitre, France
  • | 11 Institut National de la Santé et de la Recherche Médicale, U 1127, CNRS, Unité Mixte de Recherche (UMR) 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, Paris, France
  • | 12 Service de Soins de Suite et Réadaptation, Centre Hospitalier Universitaire de Pointe-à-Pitre/Abymes, Pointe-à-Pitre, France
  • | 13 Cellule d'intervention en région (Cire), Santé Publique France, Saint-Maurice, France

The Guillain–Barré syndrome (GBS) has been reported as a possible complication of acute chikungunya infection. The chikungunya epidemics, which occurred in Martinique and Guadeloupe in 2014, affected 308,000 people in these two islands. GBS occurred during or immediately after acute chikungunya infection in 13 patients (10 men, three women; mean age: 61 years). Median time from acute chikungunya to GBS onset was 9 days. Twelve patients were treated with intravenous polyvalent immunoglobulins, nine of whom improved within 7 days. Five of 13 patients required mechanical ventilation. Two patients with severe GBS died. At 6 months of follow-up, 7/13 achieved a good functional recovery with no or minor residual symptoms. A 2-fold increase in incidence was observed during the year of chikungunya outbreak. This study supports prior reports suggesting that GBS may be a complication of chikungunya.

Introduction

Chikungunya infection (CHIK) is a viral disease caused by chikungunya virus (CHIKV), an arthropod-borne RNA alphavirus of the Togaviridae family, mostly transmitted by Aedes aegypti and Aedes albopictus mosquitoes.

In November 2013, the first autochthonous cases of CHIKV infection were identified in Saint-Martin, French West Indies (FWI).1 Since then, local transmission of the virus has been identified in virtually all Caribbean islands as well as in Central and South America. From December 2013 to January 2015, a major outbreak of CHIK occurred in Guadeloupe and Martinique, FWI, involving 308,000 suspected CHIK cases (39% of the 783,336 inhabitants of both islands).

CHIKV infection, after an incubation period of 2–6 days, results in an abrupt febrile illness and is characterized by severe polyarthralgia, maculopapular rash, headache, myalgia, and fatigue. While CHIKV infection is considered to be a relatively benign condition, many atypical clinical manifestations resulting in significant morbidity and mortality have been documented in the literature, including Guillain–Barré syndrome (GBS).2

GBS is an autoimmune polyneuropathy that presents with acute and rapidly progressive flaccid peripheral paralysis. GBS is a heterogeneous syndrome, each form has distinctive clinical, pathophysiological, and pathological features.3 The most common form of GBS in the United States and Europe is the acute inflammatory demyelinating polyradiculoneuropathy (AIDP). GBS is more common in men (ratio 3:2), and the annual incidence ranges between 0.89 and 1.89 cases per 100,000 population.3

GBS is a postinfectious illness that develops within 3 weeks after an acute infection, as a result of an aberrant immune response, which causes damage to the peripheral nerve.3,4 The most common GBS-causing infection is Campylobacter jejuni enteritis. Other agents associated with the development of GBS include cytomegalovirus, Epstein–Barr virus (EBV), Myxovirus influenzae, Mycoplasma pneumoniae, and Haemophilus influenzae.3 Different arboviral diseases have been reported to trigger the development of GBS including dengue fever,5 West Nile encephalitis,6 CHIK,2,7,8 and Zika.9

The objectives of this study were to describe all the cases of CHIKV-related GBS that were diagnosed during the recent outbreak of chikungunya in the FWI and to estimate the incidence of this complication.

Patients and Methods

Twenty-seven patients were admitted at the Martinique and Guadeloupe University Hospitals during the chikungunya outbreak (January 2014 to January 2015) with a diagnosis of GBS according to Asbury and Cornblath criteria, which include 1) typical signs and symptoms of acute polyradiculoneuropathy, 2) albuminocytologic dissociation on cerebrospinal fluid (CSF) analysis, 3) electromyography typical for GBS, and (4) absence of other possible causes of neuropathy.10 We reviewed the medical records of all cases of CHIKV-related GBS, defined by a laboratory confirmation of recent CHIKV infection (anti-CHIKV IgM antibodies in the serum and/or a positive CHIKV reverse transcription polymerase chain reaction in the plasma). Serologies for human immunodeficiency virus, hepatitis B virus, cytomegalovirus, and EBV were either negative or excluding recent infection in all CHIKV-related GBS cases. The medical records of patients with CHIKV-related GBS were abstracted using a standardized case report form (CRF). Once completed, CRFs were reviewed by a neurologist who assigned each one a category of the GBS classification proposed by van den Berg and others (Table 1).3 Severe GBS was defined by the presence of at least one of the following events: severe autonomic dysfunction, respiratory failure requiring mechanical ventilation (MV), or death. Patients' functional status at 6 months and 1 year was assessed using the GBS disability score.11

Table 1

Subtypes of Guillain–Barré syndrome

SubtypeLiteratureOur cases series
Demyelinating polyneuropathy
 AIDPSensorimotor GBS, often combined with cranial nerve deficits and frequent autonomic dysfunctionPredominant subtype (60–80% of patients) in North America and Europe54%
Axonal polyneuropathy
 AMANPure motor form but cranial nerves rarely affectedFrom 6–7% in Europe and North America to 30–65% in Asia, Central America, and South America0%
 AMSANClinically, AMSAN resembles the AMAN variant but has more sensory symptoms, and more severe than AMAN15%
Uncommon subtype of GBS
 MFSClinical triad of ophthalmoplegia, ataxia, and areflexia5% Europe and 20–25% in Asia15%
 Bickerstaff's brainstem encephalitisEncephalopathy and hyperreflexia with features of MFS such as ophthalmoplegia and ataxiaRare8%
 Pharyngeal–cervical–brachial variantWeakness of oropharyngeal, facial, neck, and shoulder muscles with swallowing dysfunction. Leg strength and leg reflexes are usually preservedRare8%

Adapted from Ref 3. AIDP = Acute inflammatory demyelinating polyradiculoneuropathy; AMAN = acute motor axonal neuropathy; AMSAN = acute motor and sensory axonal neuropathy; GBS = Guillain–Barré syndrome; MFS = Miller Fisher Syndrome.

We measured the annual incidence of GBS of each calendar year from 2011 to 2015, given that the span of the chikungunya outbreak coincided exactly with the year 2014. The number of cases was obtained by retrieving all those with GBS as a primary diagnosis from each hospital database. The annual incidence of GBS was calculated by dividing the number of confirmed GBS cases each year by the population size and expressed as a number of cases per 100,000 population. The incidence rates observed in 2011, 2012, and 2013 were compared with the 2014 incidence rate using a two-sample test of proportions (Stata 12®). In addition, we calculated the rate of CHIKV-related GBS in patients who had been infected by CHIKV by dividing the number of confirmed CHIKV-related GBS diagnosed in 2014 by the estimated number of CHIKV infection cases that occurred in 2014.

Results

Thirteen cases of CHIKV-related GBS (seven cases in Martinique, six in Guadeloupe) were identified in 10 men and three women. Table 2 shows the main characteristics of these patients. Their mean age was 61 years (range: 48–80). Eleven patients had presented with typical symptoms of CHIKV infection within 4 weeks before the onset of GBS, one patient only reported a headache and fatigue, and one could not be interviewed because of severe dysarthria. Median time from acute CHIKV infection to the first symptoms of GBS was 9 days (range: 1–22).

Table 2

Summary of clinical characteristics of the 13 CHIKV-related GBS cases

PatientsSexAge (year)Relevant medical historyClinical formsSevere autonomic dysfunctionPreceding event and diagnosis testsTime from preceding event to onset of neurological defects (days)MVTreatmentOutcome (days after IVIg treatment)Walk, 4 weeks unaided6-month outcome (GBS disability scale)1-year outcome
GBS1M53Type 2 diabetesAIDPNoCHIKFIgM+PCR S ND PCR CSF−21NoIVIgPartial recovery (1 day)Yes1/61/6
GBS2M48BPHAIDPNoCHIKFIgM+PCR S NDPCR CSF−8NoIVIgPartial recovery (1 day)Yes1/61/6
GBS3M59NoneMFSYesCHIKF

IgM+PCR S+PCR CSF ND
1YesIVIg followed by PENo recoveryNo4/63/6
GBS4M58Chronic HCV infection since 1984AMSANYesCHIKFIgM+PCR S+PCR CSF+3YesIVIgPartial recovery (6 days)Yes1/62/6 CIDP
Prior history of dengue-related GBS in 2010
GBS5M49AlcoholismAIDPNoCHIKFIgM+PCR S−PCR CSF ND4NoIVIgPartial recovery (3 days)Yes1/6ND
GBS6F53Type 2 diabetesAIDPNoCHIKFIgM+PCR S−PCR CSF−15NoIVIgPartial recovery (7 days)Yes1/61/6
GBS7F62Depressive syndromeMFSNoCHIKFIgM+PCR S−PCR CSF−10YesIVIgPartial recovery (12 days)No2/61/6
GBS8M70HypertensionAIDPYesAnamnesis impossibleIgM+PCR S NDPCR CSF−NDYesIVIgDeathNo6/66/6
AIS with left hemiplegia and epilepsy sequelae8 days after IVIg
GBS9F66NoneBEYesCHIKFIgM+PCR S−PCR CSF ND8YesIVIg followed by PENo recoveryNo4/66/6 (death at 7 months)
GBS10M64HypertensionAIDPNoNo specificIgM+PCR ND19NoIVIgPartial recovery (9 days)Yes2/61/6
GBS11M80AIS without sequelAIDPYesCHIKFIgM+PCR S−PCR CSF+22NoNo treatmentNAYes1/61/6
GBS12M66AVB/PMPCB variantNoCHIKFIgM+PCR S+PCR CSF+4NoIVIgPartial recovery (15 days)No1/61/6
GBS13M62HypertensionAMSANNoCHIKFIgM+PCR S+PCR CSF ND13NoIVIgPartial recovery (9 days)No2/61/6
Total3,3/1Mean: 61 (range: 48–80)7 AIDP, 2 AMSAN, 2 MFS, and 2 variant forms5/1313/13 IgM+4/13 PCR S+3/13 PCR CSF+Median 95/1312 IVIg2 PE7/13

AIDP = acute inflammatory demyelinating polyneuropathy; AIS = acute ischemic stroke; AMSAN = acute motor sensory axonal neuropathy; AVB = atrioventricular block; BE = Bickerstaff's brainstem encephalitis; BPH = benign prostatic hyperplasia; CHIKF = chikungunya fever; CHIKV = chikungunya virus; CIDP = chronic inflammatory demyelinating polyneuropathy; F = female; GBS = Guillain–Barré syndrome; HCV = hepatitis C virus; IgM = immunoglobulin M; IVIg = intravenous immunoglobulin; M = male; MV = mechanical ventilation; ND = not done; PCB = pharyngeal–cervical–brachial; PCR CSF = CHIKV RNA in cerebrospinal fluid; PCR S = CHIKV RNA in serum; PE = plasma exchange; PM = pacemaker; + = positive; − = negative.

Cases were categorized in seven AIDP, two acute motor and sensory axonal neuropathy, two Miller Fisher syndrome, and two variant forms (one pharyngeal–cervical–brachial weakness and one Bickerstaff's brainstem encephalitis).

Twelve patients received intravenous immunoglobulins (IVIg). Nine of these patients showed a marked improvement neurologically within 7 days. Of the three patients who had no clinical response to IVIg, two received plasma exchange (PE). PE resulted in a slight improvement in one patient and no clinical response in the other. One patient received no specific treatment and completely recovered.

Six patients had severe GBS: four required MV and had severe autonomic dysfunction, one required MV but had no autonomic dysfunction, and one had severe autonomic dysfunction but did not require MV. Two of the 13 patients, both with severe GBS forms, died. One patient was 70 years old and bedbound, who received MV and died 8 days after IVIg initiation. The other patient had a Bickerstaff's brainstem encephalitis with severe autonomic dysfunction and required MV. They did not respond to specific GBS treatments (IVIg followed by PE) and died of complications of tetraplegia after 7 months. At 4 weeks of follow-up, seven patients were able to walk without aid. At 6 months, seven had achieved a good functional recovery with no or minor residual symptoms (GBS disability score ≤ 1), three had a GBS disability score of 2, and two had a score of 4. At 1 year of follow-up, one patient was lost to follow-up, and of the remaining 10 patients, eight had persisting non-disabling foot and/or hand paresthesia (GBS disability score ≤ 1), one had severe residual symptoms (GBS disability score of 3), and one developed a chronic inflammatory demyelinating polyneuropathy after initial cure of GBS symptoms. Finally, no relapse occurred in any patient.

The annual incidence rate of GBS in the FWI general population was 3.45/100,000 in 2014, compared with 1.77/100,000 over the 2011–2013 period (Table 3), which demonstrates a significant 2-fold increase during the year of the chikungunya outbreak (P = 0.006). The overall rate of CHIKV-related GBS among CHIKV-infected subjects in FWI was 13/308,000, that is, one case of GBS per 24,000.

Table 3

Annual incidence rate of GBS in FWI in the general population from 2011 to 2015

2011
2012
2013
2014
2015
MartiniqueGuadeloupeMartiniqueGuadeloupeMartiniqueGuadeloupeMartiniqueGuadeloupeMartiniqueGuadeloupe
Adults GBS9512367171069
Total GBS cases1415132715
Total FWI population796,926791,678787,670783,336778,375
GBS incidence (n/100,000 population)1.761.891.653.451.93

FWI = French West Indies; GBS = Guillain–Barré syndrome.

Discussion

Chikungunya is usually a benign illness. However, atypical, complicated, and/or severe forms have been described, including neurological, cardiac, renal, dermatological, and ocular manifestations.1214

In this case series of CHIKV-related GBS, several features differed from those of other case series already published. Patients were older, with a mean age of 61 years compared with 50 years.15,16 The time from infection to GBS was shorter, except in the case of GBS secondary to Zika where this time was similar.4,9 Interestingly, five patients still had detectable CHIKV viremia at GBS diagnosis, which has not been reported in other post-arbovirus GBS,17 including in the recently reported post-Zika GBS outbreak in French Polynesia.9 However, these five patients were indistinguishable from the other eight patients in terms of clinical or temporal patterns. Compared with previously published data, we observed a higher rate of MV and cardiovascular autonomic dysfunction.18 Despite an initially severe presentation, most patients had a rapid improvement as 54% of them were able to walk unaided at 4 weeks. However, 6-month3 and 1-year recovery rates19 were similar to those already described.

Our study strongly suggests a link between chikungunya and GBS, based on the clinical and virological evidence of recent CHIKV infection. The comparison of annual incidence rates before and after the epidemic provides an epidemiological argument for causality. We thus confirm prior reports suggesting that GBS may be a complication of chikungunya.2,7,8,14 Our data add to those recently acquired from Polynesia and La Réunion island on the mounting evidence regarding the links between CHKV and severe neurological disease.8,12 To our knowledge, this is the largest series of GBS temporally associated with a chikungunya outbreak. Our data show that although the rate of CHIKV-related GBS was relatively low (one case of GBS per 24,000), CHIKV infection contributed to a 2-fold increase of the overall incidence of GBS in the Caribbean. CHIKV may belong to three main genotypes, the West Africa, East/Central/South African (ECSA), and Asian. The latter two genotypes have been associated with neurological disease in La Réunion12 and the Caribbean, respectively.14 Recent clinical and experimental data indicate differences in the pathogenicity between the Asian and ECSA lineages.20,21 However, GBS is an acute autoimmune neuropathy resulting most likely from an epigenetic modification or environmental trigger in a genetically susceptible host.22

Whether some arboviruses have a greater ability than others to induce GBS remains unclear. Indeed, a large number of Zika-related GBS has been described during the Zika outbreak in French Polynesia (42 cases/268,270 inhabitants, a 20-fold increased incidence),9 which contrasts with the rarity of other arboviral-related GBS.57,17 A previous exposure to dengue virus may have predisposed to GBS, and this hypothesis deserves further investigation.

In conclusion, our data strongly suggests the existence of a relationship between CHIKV and GBS. CHIKV may therefore be added to the list of viruses associated with GBS, especially in the context of an epidemic.

REFERENCES

  • 1.

    Cassadou S, Boucau S, Petit-Sinturel M, Huc P, Leparc-Goffart I, Ledrans M, 2014. Emergence of chikungunya fever on the French side of Saint Martin island, October to December 2013. Euro Surveill 19: 13.

    • Search Google Scholar
    • Export Citation
  • 2.

    Thiberville S-D, Moyen N, Dupuis-Maguiraga L, Nougairede A, Gould EA, Roques P, de Lamballerie X, 2013. Chikungunya fever: epidemiology, clinical syndrome, pathogenesis and therapy. Antiviral Res 99: 345370.

    • Search Google Scholar
    • Export Citation
  • 3.

    van den Berg B, Walgaard C, Drenthen J, Fokke C, Jacobs BC, van Doorn PA, 2014. Guillain-Barre syndrome: pathogenesis, diagnosis, treatment and prognosis. Nat Rev Neurol 10: 469482.

    • Search Google Scholar
    • Export Citation
  • 4.

    van Doorn PA, Ruts L, Jacobs BC, 2008. Clinical features, pathogenesis, and treatment of Guillain-Barré syndrome. Lancet Neurol 7: 939950.

  • 5.

    Sahu R, Verma R, Jain A, Garg RK, Singh MK, Malhotra HS, Sharma PK, Parihar A, 2014. Neurologic complications in dengue virus infection: a prospective cohort study. Neurology 83: 16011609.

    • Search Google Scholar
    • Export Citation
  • 6.

    Davis LE, DeBiasi R, Goade DE, Haaland KY, Harrington JA, Harnar JB, Pergam SA, King MK, DeMasters BK, Tyler KL, 2006. West Nile virus neuroinvasive disease. Ann Neurol 60: 286300.

    • Search Google Scholar
    • Export Citation
  • 7.

    Lebrun G, Chadda K, Reboux A-H, Martinet O, Gaüzère B-A, 2009. Guillain-Barré syndrome after chikungunya infection. Emerg Infect Dis 15: 495.

  • 8.

    Oehler E, Fournier E, Leparc-Goffart I, Larre P, Cubizolle S, Sookhareea C, Lastère S, Ghawche F, 2015. Increase in cases of Guillain-Barré syndrome during a chikungunya outbreak, French Polynesia, 2014 to 2015. Euro Surveill 20: 30079.

    • Search Google Scholar
    • Export Citation
  • 9.

    Oehler E, Watrin L, Larre P, Leparc-Goffart I, Lastere S, Valour F, Baudouin L, Mallet H, Musso D, Ghawche F, 2014. Zika virus infection complicated by Guillain-Barre syndrome–case report, French Polynesia, December 2013. Euro Surveill 19: 20720.

    • Search Google Scholar
    • Export Citation
  • 10.

    Asbury AK, Cornblath DR, 1990. Assessment of current diagnostic criteria for Guillain-Barré syndrome. Ann Neurol 27: S21S24.

  • 11.

    Hughes RA, Swan AV, van Doorn PA, 2014 . Intravenous immunoglobulin for Guillain-Barré syndrome. Cochrane Database Syst Rev. Available at: http://onlinelibrary.wiley.com/doi/10.1002/14651858.CD002063.pub6/full. Accessed October 5, 2015.

    • Search Google Scholar
    • Export Citation
  • 12.

    Gérardin P, Couderc T, Bintner M, Tournebize P, Renouil M, Lémant J, Boisson V, Borgherini G, Staikowsky F, Schramm F, Lecuit M, Michault AEncephalchik Study Group, 2016. Chikungunya virus-associated encephalitis: a cohort study on La Réunion Island, 2005–2009. Neurology 86: 94102.

    • Search Google Scholar
    • Export Citation
  • 13.

    Torres JR, Córdova LG, Saravia V, Arvelaez J, Castro JS, 2015. Nasal skin necrosis: an unexpected new finding in severe chikungunya fever. Clin Infect Dis 62: 7881.

    • Search Google Scholar
    • Export Citation
  • 14.

    Rollé A, Schepers K, Cassadou S, Curlier E, Madeux B, Hermann-Storck C, Fabre I, Lamaury I, Tressières B, Thiery G, Hoen B, 2016. Severe sepsis and septic shock associated with chikungunya virus infection, Guadeloupe, 2014. Emerg Infect Dis 22: 891894.

    • Search Google Scholar
    • Export Citation
  • 15.

    Sivadon-Tardy V, Orlikowski D, Rozenberg F, Caudie C, Sharshar T, Lebon P, Annane D, Raphaël J-C, Porcher R, Gaillard J-L, 2006. Guillain-Barré syndrome, greater Paris area. Emerg Infect Dis 12: 990.

    • Search Google Scholar
    • Export Citation
  • 16.

    Webb AJ, Brain SA, Wood R, Rinaldi S, Turner MR, 2015. Seasonal variation in Guillain-Barré syndrome: a systematic review, meta-analysis and Oxfordshire cohort study. J Neurol Neurosurg Psychiatry 86: 11961201.

    • Search Google Scholar
    • Export Citation
  • 17.

    Soares CN, Cabral-Castro M, Oliveira C, Faria LC, Peralta JM, de Freitas MRG, Puccioni-Sohler M, 2008. Oligosymptomatic dengue infection: a potential cause of Guillain Barré syndrome. Arq Neuropsiquiatr 66: 234237.

    • Search Google Scholar
    • Export Citation
  • 18.

    Kanikannan MAK, Durga P, Venigalla NK, Kandadai RM, Jabeen SA, Borgohain R, 2014. Simple bedside predictors of mechanical ventilation in patients with Guillain-Barré syndrome. J Crit Care 29: 219223.

    • Search Google Scholar
    • Export Citation
  • 19.

    Rajabally YA, Uncini A, 2012. Outcome and its predictors in Guillain–Barré syndrome. J Neurol Neurosurg Psychiatry 83: 711718.

  • 20.

    Teo TH, Her Z, Tan JJ, Lum FM, Lee WW, Chan YH, Ong RY, Kam YW, Leparc-Goffart I, Gallian P, Rénia L, de Lamballerie X, Ng LF, 2015. Caribbean and La Réunion chikungunya virus isolates differ in their capacity to induce proinflammatory Th1 and NK cell responses and acute joint pathology. J Virol 89: 79557969.

    • Search Google Scholar
    • Export Citation
  • 21.

    Wei Chiam C, Fun Chan Y, Chai Ong K, Thong Wong K, Sam IC, 2015. Neurovirulence comparison of chikungunya virus isolates of the Asian and East/Central/South African genotypes from Malaysia. Gen Virol. 96: 32433254.

    • Search Google Scholar
    • Export Citation
  • 22.

    Willison HJ, Jacobs BC, van Doorn PA, 2016. Guillain-Barré syndrome. Lancet 388: 717727.

Author Notes

Address correspondence to Kinda Schepers, Department of Infectious Diseases, Dermatology, and Internal Medicine, University Medical Center of Guadeloupe, BP 465, 97159 Pointe-à-Pitre Cedex, France. E-mail: kinda.schepers@chu-guadeloupe.fr

Authors' addresses: Stephanie Balavoine and Kinda Schepers, Service des Maladies Infectieuses et Tropicales, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, E-mails: stephanie.balavoine@chu-guadeloupe.fr and kinda.schepers@chu-guadeloupe.fr. Mathilde Pircher, Service des Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Martinique, Martinique, France, E-mail: mathilde.pircher@chu-fortdefrance.fr. Bruno Hoen, Service des Maladies Infectieuses et Tropicales, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, Faculté de Médecine Hyacinthe Bastaraud, Université des Antilles, Pointe-à-Pitre, France, and INSERM, CIC1424, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, E-mail: bruno.hoen@chu-guadeloupe.fr. Cecile Herrmann-Storck, Laboratoire de Virologie, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, E-mail: cecile.herrmann@chu-guadeloupe.fr. Fatiha Najioullah, Laboratoire de Virologie, Centre Hospitalier Universitaire de Martinique, Martinique, France, E-mail: fatiha.najioullah@chu-fortdefrance.frm. Benjamin Madeux, Intensive Care Unit, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, E-mail: benjamin.madeux@chu-guadeloupe.fr. Aissatou Signate, Service de Neurologie, Centre Hospitalier Universitaire de Martinique, Martinique, France, E-mail: aissatou.signate@chu-fortdefrance.fr. Ruddy Valentino, Intensive Care Unit, Centre Hospitalier Universitaire de Martinique, Martinique, France, E-mail: ruddy.valentino@chu-fortdefrance.fr. Annie Lannuzel, Service de Neurologie, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, Faculté de Médecine Hyacinthe Bastaraud, Université des Antilles, Pointe-à-Pitre, France, and Institut National de la Santé et de la Recherche Médicale, U 1127, CNRS, Unité Mixte de Recherche (UMR) 7225, Sorbonne Universités, UPMC Univ Paris 06, UMR S 1127, Institut du Cerveau et de la Moelle épinière, ICM, Paris, France, E-mail: annie.lannuzel@chu-guadeloupe.fr. Magali Saint Louis, Service de Soins de Suite et Readaptation, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, E-mail: magali.saint-louis@chu-guadeloupe.fr. Sylvie Cassadou, Cellule d'intervention en région (Cire), Santé publique France, Saint Maurice, France, E-mail: sylvie.cassadou@ars.sante.fr. André Cabié, Service des Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Martinique, Martinique, France, INSERM, CIC1424, CHU Pointe-à-Pitre, Pointe-à-Pitre, France, and Faculté de Médecine Hyacinthe Bastaraud, Université des Antilles, Pointe à Pitre, France, E-mail: andre.cabie@chu-fortdefrance.fr.

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