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Nodding Syndrome: the Unresolved Mystery of a Pediatric Disease in Sub-Saharan Africa

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Nodding Syndrome: the Unresolved Mystery of a Pediatric Disease in Sub-Saharan Africa HOT TOPICS FROM THE OXFORD INFECTION AND IMMUNITY IN CHILDREN COURSE Nodding Syndrome: The Unresolved Mystery of a Pediatric Disease in Sub-Saharan Africa Gasim Abd-Elfarag, MD and Michaël Boele van Hensbroek, MD, PhD are generally poor and often had a history of displacement as a Nodding syndrome is a mysterious neurologic illness of unknown result of civil conflict.1 etiology, presenting with distinctive clinical features often at early age. Currently, it affects children in restricted geographical areas in South Sudan, Northern Uganda and Southern Tanzania and is associated with CLINICAL PRESENTATION high mortality and morbidity, especially in the children with severe dis- The early stage of NS is often characterized by the occur- ease. In this paper, we will give an outline of what is known about nodding rence of a repetitive head nodding, with a frequency of 5–20 nods syndrome with respect to epidemiology, clinical presentation, etiology per minute, which is the result of a brief loss of neck muscle tone and treatment. In addition, a possible approach to resolving the mystery is due to generalized seizure activity recorded by electroencephalo- presented. gram.8,10,17,18 Nodding episodes may be provoked by food and cold weather8,10,17,18,20 and in 20% are preceded by prodromal symptoms, (Pediatr Infect Dis J 2019;38:S67–S71) including dizziness, inattention, excessive sleepiness or expres- sionless staring when food is offered.17 EPIDEMIOLOGY When the disease progresses, which occur in over 80% of Nodding syndrome (NS) poses a major public health con- cases, other types of seizures, including partial complex, generalized cern in parts of Tanzania, Uganda and South Sudan, with thousands tonic-clonic and atypical absence seizures may develop.10,12,15,17–19 of children affected.1–4 However, it is not a new disease. The first In addition, 30% of children become mentally retarded, which may reports describing possible NS cases came from southern Tanzania present in the early stages with dull affect, slow reaction time and in the 1960s.5,6 In the 1990s, cases were also reported from southern school dropout.10,12,15,17–19,21,22 Wasting and growth retardation occur Sudan (now South Sudan)4,6,7 and in the first decade of this century, in 73% and 41% of NS children, respectively.8,15,17,20,22 Psychiatric from western and northern Uganda.6,8 In addition, in 1983, a seizure manifestations are common and may include, wandering (9%), illness resembling head nodding was described among the Bassa aggressiveness (27%), sleep disturbances (23%), mood changes and Kpelle population in Liberia.9 The first symptoms of NS nearly (36%) and catatonia.17,19,22 On the other hand, focal neurologic always occur when children are between 5 and 15 years of age, abnormalities, visual impairment and cranial nerve palsies are XXX although there have been reports of symptoms starting as early as 2 uncommon.8,10,17,21 years and in adults up to 32 years of age.6,8,10–12 It is unknown, what proportion of NS cases progress to The reported NS prevalence varies by region and over time. severe disease, which is characterized by altered level of con- Western Equatoria State in South Sudan is considered to have the sciousness, impairment or loss of speech, inability to stand, urinary highest prevalence of NS among children 5–18 years of age (4.6% incontinence, drooling of saliva and delayed sexual maturity.8,10,17–20 in 2002 and 8.4% in 2013).6,13,14 However, the 2013 prevalence Mortality is high at this stage; often as a result of continuing sei- was obtained from a household survey, which used definitions zures, severe burns or drowning. There have been no reports of any that included children with both NS and epilepsy without nodding child with NS recovering from the illness. episodes. In Uganda, the overall prevalence of NS is estimated at 0.7% of children between 5–18 years of age, while in the Ugan- dan district of Kitgum the prevalence was found to be much higher DIAGNOSIS (4.6%).11,15 The current burden of NS in Tanzania is not known.6 There are no laboratory markers or findings as to imaging Presently, NS is found in the Ulanga district (southern that can be used to diagnose NS. The diagnosis, therefore, can only Tanzania), the Equatoria and Lakes states (South Sudan), and in be made using clinical criteria, resulting in considerable confusion Kitgum, Pader and Lamwo districts (northern Uganda).6,16 Most and debate on the right case definition that should be used. For reports of new NS, defined as children in whom nodding episodes example, some clinicians have included children with generalized are present for less than 12 months, are from South Sudan and from seizures, living in NS-endemic areas, in their NS study population 4 new Ugandan districts (Gulu, Lira, Amuru and Oyam districts), even when head nodding was not present. Their argument was that which have not reported cases in the past.6 In villages, NS tends NS may be part of a spectrum of a neurologic illness with epilepsy to cluster in families, with many families having more than one as the hallmark. To overcome this confusion, a consensus was child with NS or epilepsy without nodding episodes.5,6,11,12,14,17–19 reached in 2012 at the International Scientific Meeting on Nodding Furthermore, it was observed that the NS-affected communities Syndrome in Kampala, Uganda, on a case definition that should be used in all future NS studies (Table 1).23 With respect to laboratory findings, around 20% of children Accepted for publication March 1, 2019. with NS are anemic, 45% have a raised eosinophil count and 80% Global Child Health Group, Department of Paediatrics and Department of a raised erythrocyte sedimentation rate. But white blood cell and Global Health, Academic Medical Center, University of Amsterdam, The platelet counts, renal and hepatic function tests and cerebrospinal Netherlands. Address for correspondence: Michaël Boele van Hensbroek, MD, PhD, Depart- fluid (CSF) basic investigations (cells, protein and glucose) are ment of Global Health, Emma Children’s Hospital, Academic Medical generally normal.10,17,24 Centre, University of Amsterdam, Amsterdam, The Netherlands. E-mail: Electroencephalographic (EEG) recordings are generally [email protected]. abnormal in patients with NS, showing evidence of general- Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved. ISSN: 0891-3668/19/3806-0S67 ized and focal epilepsies in 90% and 9% of NS cases, respec- DOI: 10.1097/INF.0000000000002327 tively.17 In children who developed nodding episodes during EEG The Pediatric Infectious Disease Journal • Volume 38, Number 6S, June 2019 www.pidj.com | S67 Abd-Elfarag et al The Pediatric Infectious Disease Journal • Volume 38, Number 6S, June 2019 recordings, evidence of atonic seizure was shown by the presence (120 cases and 119 controls in total) conducted in South Sudan and of electrodecrement and paraspinal electromyographic dropout.10 using skin snip to diagnose OV infection found it in around 86% of This high percentage of EEG abnormalities are used by clini- NS cases compared with 48% of controls.13,21 These findings were cians who believe that NS is a form of epilepsy to make their in line with findings from Uganda (Table 2). Despite the association case. Others argue that using history and clinical examination, between OV and NS, it remains unclear how an OV infection could NS cases can easily be distinguished from (pure) epilepsy with- lead to NS. OV is not known to be neuroinvasive but causes river out nodding episodes. blindness by eliciting a secondary inflammatory response to some Magnetic resonance imaging (MRI) studies of the brain of of its antigens.26–29 Furthermore, there were no reports of NS before NS cases show evidence of gliotic changes and cortical and cer- 1960, while OV has been around for thousands of years, has no age ebellar atrophy.17,25 The cortical atrophy is more prominent in the restrictions and exists in many other parts of Africa where NS has occipital lobe and the parieto-occipital areas of the brain, when never been reported.30 On the other hand, there have been argu- compared with the anterior lobe. In addition, evidence of cerebel- ments brought forward in favor of a link between OV and NS: (1) lar atrophy was shown in most of the NS cases, but with varying The OV strain found in NS endemic areas may have become more degrees.17 The MRI was unable to detect any focal changes in the virulent (neuroinvasive) over time, (2) it may not be OV, but another cerebral cortex or the hippocampus.17 as yet unidentified pathogens (eg, a neurotropic virus) transmitted by the same vector (black fly) that is responsible as OV and (3) presence of other cross-reacting filarial species, which may only be ETIOLOGY AND PATHOGENESIS found in NS-endemic areas, may cause NS but not in other oncho- The etiology of NS remains unknown, and the pathogenesis cerciasis endemic areas. has not been clarified. Previous studies have looked into possible Mansonella perstans (MP), also a vector-borne human filar- infectious causes, nutritional deficiencies, exposure to toxins and ial nematode, was also found to be associated with NS in a case– the possibility of underlying genetic or autoimmune disorders. control study conducted in South Sudan (69 cases and 65 controls) with an OR 3.2 (P value 0.005; Table 2).16 However, the possible Infections causal link between NS and MP infection has also been disputed With respect to infectious etiologies, Onchocerca volvulus with similar arguments.
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