Cerebral malaria is associated with long-term mental health disorders: a cross sectional survey of a long-term cohort
© Idro et al. 2016
Received: 2 October 2015
Accepted: 15 March 2016
Published: 31 March 2016
Cerebral malaria (CM) and severe malarial anaemia (SMA) are associated with neuro-developmental impairment in African children, but long-term mental health disorders in these children are not well defined.
A cohort of children previously exposed to CM (n = 173) or SMA (n = 99) had neurologic assessments performed and screening for behaviour difficulties using the Strengths and Difficulties Questionnaire (SDQ) a median of 21 months after the disease episode. These findings were compared to concurrently recruited community children (CC, n = 108). Participants with SDQ total difficulties score ≥17 had a mental health interview with the child and adolescent version of the Mini-International Neuropsychiatric Interview (MINI-KID) and a sample had brain magnetic resonance imaging (MRI).
Fifty-five children had SDQ score ≥17. On the MINI-KID, these children were classified as having no difficulties (n = 18), behaviour difficulties only (n = 13) or a mental health disorder (n = 24). Behaviour difficulties were seen in similar frequencies in CM (3.5 %), SMA (4.0 %) and CC (2.8 %). In contrast, mental health disorders were most frequent in CM (10.4 %), followed by SMA (4.0 %) and CC (1.8 %). Externalizing disorders (conduct, oppositional defiance and attention deficit hyperactivity) were the most common mental health disorders. The median total coma duration was 72 (IQR 36.0–115.0) h in patients with mental health disorders compared to 48 (IQR 28.5–78.7) h in those without, p = 0.039. Independent risk factors for mental health disorder included neurologic deficit at discharge (OR 4.09 (95 % CI 1.60, 10.5) and seizure recurrences during hospitalization, (OR 2.80, 95 % CI 1.13, 6.97). Brain MRI findings consistent with small vessel ischaemic neural injury was seen in over half of these children.
Cerebral malaria may predispose children to mental health disorders, possibly as a consequence of ischaemic neural injury. There is urgent need for programmes of follow-up, diagnosis and interventions for these children.
Malaria is a leading cause of ill health, neuro-disability and death in tropical countries. In 2013, the World Health Organization estimated that there were 198 million clinical cases resulting in 584,000 deaths . The clinical manifestations range from asymptomatic parasitaemia to severe and fatal disease. The syndrome of severe malaria is defined by the presence of Plasmodium falciparum malaria parasites in peripheral blood and clinical or laboratory evidence of severe vital organ dysfunction . Among African children, severe malaria anaemia, malaria with respiratory distress/metabolic acidosis and malaria with impaired consciousness or coma encompass the majority of severe disease .
Over the past 15 years, it has become clearer that many survivors of cerebral malaria (severe malaria with coma) sustain brain injury, and 25 % have long-term neurologic and cognitive deficits [4, 5]. More recently, this research group documented a similar but narrower range of cognitive deficits after severe malaria anaemia . There have also been reports of behaviour difficulties and mental health disorders in cerebral malaria exposed children. These included inattentiveness, hyperactivity, impulsive, and aggressive behaviour, which disrupts normal childhood development [7, 8]. However, there is a paucity of cohort-based longitudinal studies of these problems; the burden of these disorders, the pathogenesis, and treatment needs are poorly understood. It is also unknown whether the difficulties follow other forms of severe malaria. The hypothesis was that, in addition to neurologic and cognitive deficits, cerebral malaria and the other forms of severe malaria predispose children to mental health disorders and that children younger than five years on exposure are at most risk.
The study examined a cohort of children with exposure to cerebral malaria or severe malaria anaemia to assess for mental health disorders and performed magnetic resonance imaging (MRI) on a subset of these children to assess associated structural changes in the brain. In addition, the study also assessed whether specific clinical features predicted mental health disorders.
The study was performed at Mulago Hospital, Kampala, Uganda, as a sub-study within a larger study of neuro-cognitive impairment in children with severe malaria from April 2012 to December 2014. In this study, children with cerebral malaria, severe malaria anaemia, or community children were enrolled if they were between 18 months and 12 years of age. Cerebral malaria was defined as: (1) coma (Blantyre Coma Score [(BCS) ≤ 2]; (2) Plasmodium falciparum on blood smear; and (3) no other known cause of coma (e.g., meningitis, a prolonged postictal state or hypoglycaemia-associated coma reversed by glucose infusion). Severe malarial anaemia was defined as presence of P. falciparum on blood smear in children with a haemoglobin level ≤5 g/dL. Children with cerebral malaria or severe malaria anaemia were managed according to the Ugandan Ministry of Health treatment guidelines at the time of the study. These included intravenous quinine treatment followed by artemisinin combination therapy if the child could take orally. All underwent a medical history and physical examination. Children with cerebral malaria were assessed for malaria retinopathy  by indirect ophthalmoscopy. Clinical laboratory testing was performed as previously described . Patients with a haemoglobin <5 g/dL received a blood transfusion.
Community children were recruited from the nuclear family, extended family, or household compound area of children with cerebral malaria or severe malaria anaemia. Eligible controls were ages 18 months to 12 years and currently healthy. Exclusion criteria for all children included: (1) known chronic illness requiring medical care; (2) known developmental delay; or (3) prior history of coma, head trauma, hospitalization for malnutrition, or cerebral palsy. Additional exclusion criteria for children with severe malaria anaemia included: (1) impaired consciousness on physical exam; (2) other clinical evidence of central nervous system disease; or (3) more than one seizure prior to hospitalization. Additional exclusion criteria for community children included: (1) illness requiring medical care within the previous 4 weeks; or (2) major medical or neurological abnormalities on screening physical exam.
Children in the main study were asked to participate in the present study of behaviour difficulties and mental health disorders. An earlier preliminary study, documented that behaviour difficulties after cerebral malaria developed within 6 months of exposure . Thus, only children from the main study who had completed at least 6 months follow up, were considered for this study. All eligible children with cerebral were invited, along with a random sample of 115 children with severe malaria anaemia and 115 community children. A sample size of 175 children with cerebral malaria, 88 with severe malaria anaemia and 88 community children was estimated to have >80 % power to demonstrate a two-fold increase in the risk of behaviour or mental health disorders in children with cerebral malaria as compared to severe malaria anaemia or community children. Ethical approval was granted by the Institutional Review Boards for human studies at Makerere University School of Medicine and the University of Minnesota and written consent was obtained from parents or guardians of study participants.
Screening for behaviour difficulties and mental health disorders
Each child underwent screening for behaviour difficulties using the Strengths and Difficulties Questionnaire (SDQ) . The SDQ is a 25 item behaviour screening tool that comprises five subscales (emotional, conduct, hyperactivity or peer problems, and a pro-social scale) each with five items. Scores from these items are used to generate the total difficulties score (range 0 to 40), which is the sum of scores from all the subscales except the pro-social scale. A total difficulties score of ≥17 is interpreted as abnormal behaviour. Similar cut off levels are used to define abnormalities in each subscale. The SDQ was previously validated in neighbouring Democratic Republic of Congo which has similar socio-cultural settings with Uganda . The parent’s version of the questionnaire was used. The English language version of the questionnaire was translated into Luganda, the most widely used language in central Uganda, and parents could choose to use either version.
Diagnosis of behaviour difficulty or mental health disorder
Children with SDQ total difficulties score ≥17 were invited for a detailed mental health interview using the Mini-International Neuro-Psychiatric Interview for Children and Adolescents (MINI KID) [12, 13]. The MINI KID was chosen because of its diagnostic relevance based on DSM-IV and ICD 10 criteria. It has also been used previously in child mental health surveys in Uganda [14, 15]. Depending on reported symptoms and observations, the appropriate diagnosis e.g. attention deficit and hyperactivity disorder (ADHD), depression or conduct disorder was made. Children with an observed difficulty that did not fulfil a specific mental health disorder criterion were described as having behaviour difficulties only. In both cases referral was made to local services for care.
Brain magnetic resonance imaging
Brain MRI were performed on selected cerebral malaria exposed children with mental health sequelae and two randomly selected children without sequelae (behaviour difficulty, mental health disorder or neurologic deficits). Images were acquired using a Phillips Achieva 1·5 Tesla 16 channel A series machine under sedation using chloral hydrate. MRI sequences included T1 (3D multi plannar isotropic scans; FOV 240 mm, slice thickness 1 mm, TE 4.6, TR = 25, slice gap 0.4 mm and flip angle = 30) and T2 weighted scans (2D scans; TE110, shortest TR, slice thickness 4 mm, slice gap 1 mm, and flip angle = 90), Fluid Attenuated Inversion Recovery (FLAIR) and diffusion weighted imaging (DWI). Qualitative analyses of the images were performed by a radiologist who was not aware of the child’s diagnosis for global and focal changes and lesions.
Data analysis was performed using STATA version 12 (STATA Corp, Tx). Proportions of patients with specific behaviour difficulties and mental health disorders between groups were compared using Chi square analysis, with a Bonferroni correction for multiple comparisons. Multivariate logistic regression was used to assess clinical and demographic risk factors for mental health disorders.
Parents of 392/430 (91.1 %) invited children accepted participation. Ten children were excluded; two with developmental issues that may have preceded the study, but were previously unreported, one who had developed severe HIV/AIDS, and seven who did not complete the assessments. Parents of two other children (one cerebral malaria-exposed and one community child) withdrew consent. Of the remaining 380 participants, 173 were had cerebral malaria, 99 had severe malaria anaemia and 108 were community children. One hundred and three children (59.5 %) with cerebral malaria, 62 (62.6 %) with severe malaria anaemia, 62.6 % and 42 (38.9 %) community children were male. The mean (SD) ages of the three groups were: cerebral malaria 4.1(2.0) years; severe malaria anaemia 3.4(1.5) years and community controls 4.3(1.9) years while the median time from exposure to assessment was 21 (IQR 12–24) months.
Behaviour difficulties on screening with the SDQ
Spread of total difficulties scores of the SDQ in children exposed to cerebral malaria compared to children exposed to severe malaria anaemia only and to community controls
Range of total difficulties scores
Cerebral malaria, n = 173 (%)
Severe malaria anaemia, n = 99 (%)
Community controls, n = 108 (%)
Total for the range of scores, n = 380 (%)
Normal scores, 0–13
Borderline scores, 14–16
Abnormal scores, 17 or higher
Abnormal SDQ scores in children exposed to severe malaria compared to community children
Abnormal SDQ scores by difficulty groups
Cerebral malaria (CM), n = 173 (%)
Severe malaria anaemia (SMA), n = 99 (%)
Community children CC), n = 108 (%)
P a value (CM vs CC)
P a value (SMA vs CC)
P a value (CM vs SMA)
Abnormal total difficulties score (scores 17–40)
32 (18.5 %)
15 (15.2 %)
8 (7.4 %)
Abnormal emotional score (scores 5–10)
37 (21.4 %)
18 (18.2 %)
13 (12.0 %)
Abnormal conduct score (scores 4–10)
37 (21.4 %)
22 (22.2 %)
11 (10.2 %)
An abnormal hyperactivity score (scores 7–10)
27 (15.6 %)
11 (11.1 %)
4 (3.7 %)
Abnormal peer relations score (scores 4–10)
38 (22.0 %)
16 (16.2 %)
14 (13.0 %)
Abnormal pro-social score (scores 0–4)
14 (8.1 %)
6 (6.1 %)
5 (4.6 %)
With the SDQ subscales, children with cerebral malaria had abnormal scores more frequently detected in conduct and hyperactivity scores than community children (Table 2). Children with severe malaria anaemia also had more frequent abnormal conduct scores than community children, and differences in hyperactivity scores between children with severe malaria anaemia and community children approached significance (Table 2).
Specific behaviour difficulties and mental health disorders
Behaviour difficulties and mental health disorders after severe malaria
Behaviour difficulty or mental health disorder
Cerebral malaria, n = 173, (%)
Severe malaria anaemia, n = 99, (%)
Community controls, n = 108, (%)
p a value (CM vs CC)
p a value (SMA vs CC)
p a value (CM vs SMA)
Behaviour difficulty only
Mental health disorder
Long-term mental health disorders and brain MRI findings in children with cerebral malaria
Age on exposure, years
Specific mental health disorder on DSM-IV criteria
Brain MRI findings
Episodic aggressive behaviour, wets his bed, restless and inattentive
ADHD (inattentive type) also has anxiety and depressive symptoms
Brain MRI not done
Extremely quiet; plays alone and destroys property; bed wetting
Major depression (current)
Normal brain MRI
Running away from home, often leaves the classroom and moves around
Brain MRI not done
Aggressive behaviour, inattentive, excessive talking, conduct problems
ADHD (inattentive type) conduct disorder
Bilateral punctuate (but few) white matter, high T2 signal foci measuring 1.5–2.0 mm in the parietal regions regions of the cerebral hemispheres close to the vertex. No restriction of water diffusion (on DWI)
Shy, low self esteem
Social phobia (social anxiety disorder)
Normal brain MRI
Fighting, aggressive behaviour, anger, lies, poor concentration at school and spending nights outside home
Conduct disorder ADHD (inattentive type)
Brain MRI not done
Fears being alone; cries often, aggressive to peers and easily confused
Separation anxiety disorder
Generalised widening of sulcal spaces and sylvian fissures and numerous bilateral hyperintensities in the grey mater and subcortical regions of the frontal, occipital and temporal lobes
Irritable, aggressive towards siblings, sucking thumb
Adjustment disorder (current)
Bilateral hyper-intensities around the frontal horns of the lateral ventricles—largest measuring 5-7 mm and also the temporal and occipital horns. No oedema or restricted diffusion on DWI
Feeding problems, weight loss, fearful, quiet and plays alone, nightmares. Separated from parents
Major depression (current)
Normal brain MRI
Defiant and indifferent—not caring attitude, labile mood, disorganised, misplaces objects
Oppositional defiant disorder
Brain MRI not done
Loss of interest; poor concentration and irritability
Major depression (current)
Oppositional defiant disorder
Irritable, aggressive, self injurious behaviour, head banging, excessive crying, temper tantrums, regression in speech
Oppositional defiant disorder Also has epilepsy, bilateral hyperreflexia and upgoing babinksi reflexes and learning disability
High signal white mater intensities on T2 weighted imaging and FLAIR (iso-intense on T1 WI)
Violent and aggressive behaviour stealing
ADHD Conduct disorder Has severe sequelae with visual, hearing, speech impairment, epilepsy and learning difficulties
Marked global brain atrophy involving the cerebral hemispheres, midbrain, brainstem and cerebellum and reduced grey-white mater differentiation. Focal encephalomalacia in both occipital lobes and demyelination with extensive T2 W and T2FLAIR white mater peri-ventricular hyperintensities and in the right external capsule, cerebellae penducle and cerebellar hemispheres
Fearfulness, very slow, irritable, quiet, frequent headaches
Major depression (current) also has some anxiety symptoms and learning difficulties
Worsening episodes of aggressive behaviour; fighting, resists change, forgetful, cries often, throws stones; enuresis
ADHD inattentive type; conduct disorder
Bilateral hyper-intensities around the parietal and occipital areas—largest measuring 2–3.7 mm and also the temporal and occipital horns. No oedema or restricted diffusion on DWI
Wets himself during day; Isolates himself and hides, quiet most of the time
Separation anxiety disorder. Major depression (current)
Bilateral punctuate white mater high T2 signal foci (hypo-intense on T1 WSE) measuring 1.5-2.0 mm in the parietal regions. No restriction of water diffusion on DWI
Forgetfulness, fearful and reduced concentration; declining academic performance and often punished
On discharge from hospital, neurologic deficits were documented in 41/173(23.1 %) children with cerebral malaria. These included motor difficulties (weakness, hyperreflexia and global hypotonia) in 35 (20.2 %) children, visual (9/173, 5.2 %), hearing (1/173, 0.6 %) and speech and language (17/173, 9.8 %) impairments. In addition, gait problems and ataxia probably a result of an incomplete recovery from a severe illness were observed in 25/173 (14.4 %). At the time of follow-up assessment, these deficits had resolved except in five children (2.9 %) who initially had severe motor deficits.
Brain MRI findings
Risk factors for mental health disorders after severe malaria
Factors associated with behaviour difficulties and mental health disorders following severe malaria
Demographic and clinical features
Cerebral malaria exposed children, N = 173
Severe malaria anaemia exposed children, N = 99
With mental health disorder, n = 18
No mental health disorder, n = 155
p a value
With mental health disorder, n = 4
No mental health disorder, n = 95
p a value
Gender, male (%)
Age on exposure, mean (SD) yr
Duration of fever prior to hospitalization, median (IQR) days
Profound coma (BCS ≤ 1 or GCS ≤ 6) on admission
Seizure recurrences during hospitalization, (%)
Admission Hb, mean (SD) in g/dl
Admission lactate, mean (SD)
Hypoglycaemia (blood glucose <2.2 mmol/L) on admission
Presence of malaria retinopathy, %
Total duration of coma, median (IQR) hoursb
72.0 (36.0, 115)
48.0 (28.5, 78.7)
Neurologic sequelae on discharge, %
This study set out to describe behaviour difficulties and mental health disorders following cerebral malaria and the structural brain imaging changes associated with these sequelae, determine the early predictive features and examine if children exposed to other complications of severe malaria and in particular, severe malaria anaemia, have similar increased risk. The study found that cerebral malaria but not severe malaria anaemia was associated with an increased risk of mental health disorders. Externalizing problems (conduct, oppositional defiance and attention deficit hyperactivity disorders) were the most common problems. In affected children, brain imaging suggested that small vessel ischaemic injury is linked to these difficulties.
This is the first study to systematically document the mental health sequelae of more than one form of severe malaria in children and to have combined clinical assessments with diagnostic imaging. The data suggests that (1) over 10 % of cerebral malaria exposed children may have long-term mental health sequelae; (2) the sequelae, especially the externalizing behaviours of ADHD, conduct and oppositional defiant disorders, may be a consequence micro-vascular ischaemic neural injury and develop within 12 months of exposure to cerebral malaria. There was no relationship between gender, age on exposure, peripheral blood parasite density on hospitalization, haemoglobin and lactic acid levels and these sequelae. However, features of a more severe disease—seizure recurrences during hospitalization and discharge with neurologic sequelae, were independently associated. The slower recovery from coma may also be a consequence of the suggested ischaemic brain injury in affected individuals. The imaging data here is similar to that reported in Malawi except for the clearer evidence of small vessel ischaemia . Three patterns are recognizable; normal brain MRI, small vessel ischaemic brain injury and severe brain injury with extensive cortical atrophy. No detailed volumetric analysis was however performed and the effect cerebral cortical volume loss on function was not determined. However, although the study appears to suggest the mental health sequelae as a direct consequence of the brain injury, it could also be that some is a consequence of stress associated with suffering a serious disease. Additional data and analysis would be helpful to delineate te different contributions.
Between the years 1994 and 2004, it was estimated that annually, there were a minimum 2.8 million hospitalizations with severe malaria in Africa . About 10 % of this hospitalization is due to cerebral malaria . Although the burden of malaria has declined since then, with mental health disorders being described in about 10 % of child survivors of cerebral malaria , our study suggests that since 1994, cerebral malaria may be responsible for severe mental health problems in at least 30,000 children annually in the malaria endemic regions of Africa. The need to work towards malaria eradication in the continent cannot be overstated.
Currently, there are no interventions for children who develop these problems and no programmes for follow-up to identify affected individuals. With up to 25 % of cerebral malaria survivors developing long-term neuro-cognitive deficits  and 10 % showing evidence of mental health disorders, it is more urgent than ever to put in place programmes of post hospitalization follow-up care for exposed children. However, with the limited trained mental health specialists and tools to identify these deficits, there is also need to develop or adapt simple and appropriate screening tools to identify patients at risk.
This study has some limitations; first, the study did not systematically examine effects of the home environment (e.g. parenting and child rearing) on the outcomes which could have contributed to the difficulties. Secondly, the psychometric properties, such as internal consistency, of the instruments used are not reported although all have previously been used in East Africa. Third, the pre-morbid state of the participants is unknown. This study, therefore, cannot be absolute in its attribution of causation.
In addition to high mortality and long-term neuro-disability, cerebral malaria predisposes children to mental health disorders, probably as a result of ischaemic neural injury. There is urgent need to put in place programmes for follow-up, identification and interventions for these children.
RI, AKM, PB, KS, BA, RO, CCJ and JN designed the study. RI wrote the first draft, SLK obtained and interpreted the brain images and all participated in the interpretation of the data and critically reviewed the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
This study was supported by a Child Development grant from The Waterloo Foundation (Grant Number 1025/1398). The original cohort was supported by the National Institute of Neurological Disorders and Stroke and the Fogarty International Center (Grant Number R01NS055349). Dr. Idro was also partially supported by a Wellcome Trust Directors Discretionary Research Fund to Prof Kevin Marsh.
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