Abstract
Paediatric cerebral malaria is the most serious complication of Plasmodium falciparum infection. While the majority recover, long-term cognitive impairment has been highlighted as a significant and neglected problem. Persistent or serious deficits in processes such as attention or behavioural inhibition should be manifest in changes to performance on oculomotor tasks. Therefore we investigated the impact of cerebral malaria on the development of reflexive pro-saccades and antisaccades. In a longitudinal study, 47 children previously admitted with retinopathy-confirmed cerebral malaria (mean age at admission 54 months), were compared with 37 local healthy controls (mean ages at first study visit 117 and 110 months respectively). In each of three or four test sessions, over a period of up to 32 months, participants completed 100 prosaccade tasks and 100 antisaccade tasks. Eye movements were recorded using infrared reflectance oculography; prosaccade, correct antisaccade and error prosaccade latency, and antisaccade directional error rate were calculated. Hierarchical linear modelling was used to investigate the effect of age and the influence of cerebral malaria on these parameters. Data were also collected from an independent, older group (mean age 183 months) of 37 local healthy participants in a separate cross-sectional study. Longitudinal data exhibited the expected decrease in latency with age for all saccade types, and a decrease in the antisaccade directional error rate. Hierarchical linear modelling confirmed that age had a statistically significant effect on all parameters (p< = 0.001). However, there were no statistically significant differences between the cerebral malaria and control groups. Combining groups, comparison with the literature demonstrated that antisaccade directional error rate for the Malawi sample was significantly higher than expected, while latencies for all saccade types were indistinguishable from published. The high directional error rate was also confirmed in the older, healthy Malawian participants from the cross sectional study. Our observation of similar oculomotor performance in cerebral malaria and control groups at long follow-up periods suggests that cerebral malaria survivors are not at a generally increased risk of persistent cognitive deficits. Our data raise questions about the prevailing hypothesis that cerebral malaria has gross impacts on the development of processes such as attention and behavioural inhibition. More importantly, our novel finding of a clear difference in antisaccade performance between all of the Malawi participants and published data suggests that the Malawian paediatric population as a whole faces serious challenges to cognitive development beyond cerebral malaria.
Highlights
Malaria presents a substantial global health challenge, with an estimated annual incidence of approximately two million cases and over 600 000 deaths per year[1]
We examined a second group of participants who were originally recruited for the Brain Imaging in Normal Kids (BRINK) study [41]
Data were available from 47 retinopathy-confirmed cerebral malaria survivors and 37 control participants (Table 1), all with normal visual acuity
Summary
Malaria presents a substantial global health challenge, with an estimated annual incidence of approximately two million cases and over 600 000 deaths per year[1]. It has been reported that impairments in aspects of executive function such as attention and working memory are both relatively common and long term [8,9,10]. There are well established links between specific oculomotor parameters and cognitive processes [26], including attention [27,28], working memory [29,30] and inhibitory control [31,32], all key aspects of executive function. If cerebral malaria survivors are at risk of long-term impairments in cognition, related to executive function, we would expect to see performance deficits in saccade tasks compared to a non-cerebral malaria local control group. We conducted a longitudinal case control study of retinopathy-confirmed cerebral malaria using both prosaccade and antisaccade tasks. As many of our participants were relatively young even at the end of the longitudinal study, a smaller cross-sectional study was conducted in a group of normally developing, older participants to confirm the developmental course of the parameters of interest in the population we were examining
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