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1 Supplementary appendix This appendix formed part of the original submission and has been peer reviewed. We post it as supplied by the authors. Supplement to: Schiller R, IJsselstijn H, Hoskote A, et al. Memory deficits following neonatal critical illness: a common neurodevelopmental pathway. Lancet Child Adolesc Health 2018; published online Jan 9. S (17)

2 Supplemental Table 1. Neuroimaging studies in relation to memory functioning in survivors of neonatal critical illness References Participants Age assessed Methods & materials Hippocampal findings Other neuroimaging findings Structurefunction associations A. Preterm birth Salvan et al.(2014) 28 Lawrence et al.(2010) 69 Aanes et al.(2015) 20 Nosarti et al.(2014) preterm children (GA <33 weeks) 10 fullterm controls. 22 very preterm children (GA <33 weeks). 22 fullterm controls. 42 very low birthweight children ( fullterm controls. 68 very preterm children (mean GA = 30 weeks) 43 fullterm controls. 20 years. Neuroimaging: Functional, structural and diffusion MRI 3 Memory tests: verbal paired associate learning task adapted from WMSR (in MRI). 20 years. Neuroimaging: Structural and functional MRI 1.5 Memory tests: verbal paired associates learning task (in MRI) years. Neuroimaging: Structural MRI 1.5 Memory tests: WMSIII (verbal and visual episodic memory immediate, delayed and recognition) years. Neuroimaging: Structural MRI 1.5 Memory tests: WMSRevised (visual memory immediate and delayed recall). Different activation in posterior area encompassing parts of the left hippocampus, parahippocampal gyrus and the thalamus during recall in Smaller bilateral posterior hippocampal volumes in No difference in hippocampal activation between groups. Smaller hippocampal volumes in patients, corrected for total intracranial Other: Patients showed a progressive increase in activation in an area encompassing right anterior corpus callosum, parts of the right caudate and superior fasciculus gyrus during encoding compared to decreased activation in healthy controls. Limbic system: Parahippocampal grey matter was larger in Limbic system: Reduced grey matter in the thalamus and left anterior cingulate gyrus in patients; reduced white matter volume in posterior corpus callosum extending to thalamus and hippocampal fornix in patients; larger white matter volume in the parahippocampal gyrus in Other: Smaller volumes in the temporal lobes, right insula, medial frontal gyrus and medial occipital lobe in Caudate nucleus was smaller in patients; larger grey matter in the medial/anterior frontal cortex in patients; smaller white matter volumes in temporal and frontal regions, right posterior brain regions and in the lingual gyrus and Patients scored similarly to healthy controls. Increased activity in the left parahippocampal gyrus in patients during encoding. Increased activation in the precentral gyri in patients during encoding and recall. Positive correlations were found between total, right and left hippocampal absolute volumes and all memory indices in Patients with the largest hippocampi had the highest memory scores. White matter in posterior corpus callosum/thalamus/hippo campal fornix was positively associated with executive functioning and total visual memory scores.

3 cerebellum in Cheong et al.(2013) 70 Gimenez et al.(2005) 71 Gimenez et al.(2004) 29 Nosarti et al.(2002) 72 Isaacs et al.(2000) 30 Brumbaugh et al.(2016) extremely preterm children (GA <28 weeks). 132 fullterm controls. 14 preterm children (GA 34 weeks) 14 fullterm controls. 22 preterm children (GA mean = 29 weeks). 22 fullterm controls. 72 preterm children (GA <33 weeks). 48 fullterm controls. 11 preterm children (GA 30 weeks). 8 fullterm controls. 52 late preterm children (GA 3436 weeks). 74 fullterm controls. 18 years. Neuroimaging: Structural MRI 3T years. Neuroimaging: Structural and functional MRI 1.5 Memory tests: RAVLT, RCFT (verbal and visuospatial memory immediate and delayed recall) and a declarative memory task (in MRI) years. Neuroimaging: Structural MRI 1.5 Memory tests: RAVLT, RCFT (verbal and visuospatial memory immediate and delayed recall) years. Neuroimaging: Structural MRI years. Neuroimaging: structural MRI and MRS on 1.5 Memory tests: RBMT, WMSForm I, CAVLT2, Design Learning subtest of AMIPB, and RCFT (everyday memory, logical memory immediate and delayed recall, pairedassociate learning, verbal and visuospatial memory immediate and delayed). 613 years. Neuroimaging: Structural MRI 3 Memory tests: WISCIII spatial span, colour span test, CMS Dot Smaller hippocampal volume in patients, adjusted for total brain volumes in Significant increase in right hippocampus activation in patients during memory. Increased activation in the right hippocampus was associated with larger right hippocampal Adjusted for total brain volume, only the left hippocampal volume remained smaller in 12.1% decrease in left and 15.6% decrease in right hippocampal volumes in patients, adjusted for whole brain Smaller hippocampal volumes in patients, adjusted for total brain Similar hippocampal volumes in patients and controls. Limbic system: Smaller thalamus and amygdala in patients, adjusted for total brain Other: Total brain volume, cortical grey and white matter volumes, basal ganglia and cerebellum volumes were smaller in Limbic system: Smaller bilateral thalami volumes in Other: 6% decrease in whole brain volume, 11.8% decrease in cortical grey matter volume and 42% increase in size of the lateral ventricles in patients, after controlling for whole brain Limbic system: Smaller thalamus in Other: Similar intracranial volume, but significant decreases in total tissue Total brain tissue volume explained between 2040% of the IQ and educational outcome differences between preterm and control adolescents. Amygdala volume and IQ were positively associated as well. Right hippocampal activation was positively associated with facename recognition. A positive significant association was found between verbal shortterm memory and left hippocampal volume in the premature group. The greater the volume loss, the lower level of longterm verbal retention. predicted everyday memory.

4 Fraello et al.(2011) 31 Brunnemann et al.(2013) 24 Peterson et al.(2000) 27 Omizzolo et al.(2013) 25 Thompson et al.(2014) 26 Thompson et al.(2013) preterm children (mean GA = 28 weeks) 20 fullterm controls. 21 preterm children (GA <34 weeks and < 1900). 19 fullterm controls. 25 preterm children (600 to fullterm controls. 145 preterm children (GA <30 weeks or < fullterm children. 125 very preterm children (<1250 grams or GA <30 weeks). 25 fullterm controls. 184 very preterm children (GA <30 weeks or < fullterm controls. Locations and Word Lists. 12 years. Neuroimaging: Structural MRI 1.5Tesla (Siemens or GE system; accounted for in analyses). Memory tests: digit span WISCIII, nonword repetition subtest CTPP, and CELFIII (verbal memory immediate recall and workingmemory). 711 years. Neuroimaging: Structural MRI 1.5 Memory tests: VLMT, RAVLT, RCFT (verbal and visuospatial memory immediate and delayed recall). In addition, two episodic memory retrieval subprocesses, familiarity and recollection, were measured with an experiment. 8 years. Neuroimaging: Structural MRI years. Neuroimaging: Structural MRI 3T. Memory tests: WMTBC, CVLTC and CMS (verbal and visuospatial workingmemory, verbal memory and visuospatial memory immediate and delayed recall). Termequivalent age and 7 years. Termequivalent age and 7 years. Neuroimaging: T2/proton density weighted MRI 1.5 Tesla (termequivalent age) and structural MRI 3 Tesla (at 7 years). Memory tests (7 years): WASI forward and backward digit recall, block recall, CVLT and CMS (verbal and visuospatial memory immediate and delayed recall, verbal working memory). *Scores were not standardized but raw scores were used. Neuroimaging (termequivalent age): Structural 1.5T MRI. Memory tests (7 years): CVLT Children and Dot locations (verbal and visual memory). Similar hippocampal volume between patients and controls. Smaller hippocampal volumes in patients, adjusted for total cerebral Reduced bilateral hippocampal volumes in Difference reduced when gender, intracranial volume and neonatal brain abnormality were added. At 7 years of age, hippocampi of patients differed significantly in shape from controls. No differences between groups in morphological change from infancy to 7 years. change was smaller in patients, adjusted for neonatal brain abnormality score. Patients hippocampi were less infolded. Straighter hippocampi were associated with white matter injury. Other: Patients had significantly larger volumes of bilateral frontal grey and right frontal white matter than controls. Patients had smaller regional volumes in right parietal and bilateral temporal white matter. Other: Smaller cerebral volume in patients than controls. Limbic system: Smaller bilateral amygdala Other: Smaller grey matter volumes, smaller basal ganglia, larger ventricles and smaller white matter volume in the posterior corpus callosum in No associations between the brain measures and cognitive outcomes in was not associated with memory. was not associated with learning or memory. No association between hippocampal shape and memory. No significant associations between infant hippocampal shape and memory at 7 years. Larger infant

5 Beauchamp et al.(2008) 23 Ball et al.(2012) 33 Thompson et al.(2008) 22 B. Congenital Heart Disease MunozLopez et al.(2017) 36 Latal et al.(2016) preterm children (GA < 30 weeks or <1250 No controls. 71 preterm children (GA <36 weeks). No controls. 184 preterm children (GA < 30 weeks or < fullterm controls. 40 children treated with arterial switch operation to correct for transposition of the great arteries and had sustained significant neonatal cyanosis. 64 healthy controls. 48 children with cardiopulmonary bypass Termequivalent age and two years. Termequivalent age. Termequivalent age. Neuroimaging (termequivalent age): Structural MRI at 1.5 Memory tests (2 years): delayed alternation task (workingmemory). Neuroimaging: Structural MRI and DTI 3 Neuroimaging: Structural MRI at years. Neuroimaging: Structural MRI 1.5 Memory tests: CMS, RBMTII or RBMTC (verbal and visuospatial memory immediate and delayed recall and recognition, event and spatial memory) years. Neuroimaging: Structural MRI. Memory tests: Increasing prematurity was related to volume reductions in the hippocampus. Smaller hippocampal volume in patients, but disappeared after correcting for total brain White matter injury, exposure to postnatal steroids and indomethacin were found to negatively influence hippocampal volumes in 40% of subjects had hippocampal volume reduction of 10%. Patients had 10% lower total hippocampal volumes. Limbic system: Increasing prematurity was related to volume reductions in the thalamus and posterior cingulate cortex. Other: Increasing prematurity was related to volume reductions in the orbitofrontal cortex and centrum semiovale. Other: Total brain volume was significantly smaller in Other: Total grey and white matter and basal ganglia volumes did not differ between groups. Patients had a small but significant increase in cerebrospinal fluid. 35% of patients had neuroradiological abnormalities. hippocampal volumes were associated with better verbal memory at 7 years, adjusted for white matter injury. Infants who perseverated on the working memory task had significantly smaller hippocampal volumes than preterm infants who exhibited intact working memory, even after adjusting for relevant perinatal, sociodemographic and developmental factors. Across the cohort, memory was positively associated with hippocampal In patients with hippocampal reductions, these were associated with poorer memory, whereas these associations were not found in patients with normal hippocampal volumes. correlated with working

6 Von Rhein et al.(2014) 38 C. Neonatal ECMO treatment Cooper et al.(2011) 74 Schiller et al.(2017) 42 Cooper et al.(2015) 34 Van den Bosch et al.(2015) 75 Schiller et al.(2017) 41 surgery. 32 healthy controls. 39 children with cardiopulmonary bypass surgery. 32 healthy controls. 21 children with neonatal hypoxia/ischaemia due to cardiorespiratory disease 12 healthy controls. 23 children treated with neonatal ECMO. 54 healthy controls. 40 children treated for acute hypoxic respiratory failure: 27 treated with ECMO and 13 with conventional management. 64 healthy controls. 23 children treated with neonatal ECMO. 43 healthy controls. 38 children with CDH and/or treated with neonatal ECMO. No controls years. Neuroimaging: Structural MRI years. Neuroimaging: Structural MRI 1.5 Memory tests: CMS (every day memory, workingmemory). 815 years. Neuroimaging: Structural MRI and DTI 3 Memory tests: NEPSY IIINL (verbal memory). 815 years. Neuroimaging: Structural MRI 1.5 Memory tests: CMS (verbal and visuospatial memory immediate and delayed recall). 815 years. Neuroimaging: Structural MRI 3 Memory tests: NEPSYIIINL (verbal memory). 812 years. Neuroimaging: Structural MRI and DTI 3 Memory tests: RAVLT, RCFT (verbal and visuospatial memory Similar hippocampal volumes between groups when adjusted for total brain Patients with cyanotic heart disease showed more hippocampal volume loss than those with acyanotic heart disease. volumes in patients, a 21% reduction. Smaller left, right and bilateral hippocampal No difference in hippocampal volume between patients treated with ECMO and conventional treatment. Limbic system: Grey matter reductions were most pronounced in limbic cortex. Patients with cyanotic heart disease showed more thalamic volume loss than those with acyanotic heart disease. Other: Lower total brain volume, white matter and cortical grey matter No regionspecific differences when adjusted for total brain volume; cyanotic patients had more white matter and corpus callosum volume loss than acyanotic heart disease Other: Whole brain volume was similar between groups. Limbic system: Lower fractional anisotropy (FA) in the left cingulum bundle and higher MD in the left PHC in Other: Lower global FA in patients, but similar global MD. Other: Lower white matter volume but higher cerebrospinal fluid volume in patients; increase in cerebrospinal fluid in ECMO relative to conventional management group. Limbic system: Left thalamus was significantly smaller in No differences were found in the amygdala or anterior cingulate cortex volumes between groups. Other: Global brain volume, white matter volume, grey matter volume, cerebellum and insula volumes were similar in both groups. memory in patients, adjusted for total brain Autobiographical event recall was positively associated with hippocampal Verbal memory was positively associated with hippocampal Positive correlations were found between hippocampal volumes and memory and learning. No associations were found between thalamus and neuropsychological outcome. Mean diffusivity (MD) in the left parahippocampal region of the cingulum (PHC)

7 immediate and delayed recall and recognition). was negatively associated with visuospatial memory. MD in the left and right PHC were negatively associated with verbal memory. Bilateral hippocampal volume was positively associated with verbal memory. Abbreviations: ECMO, extracorporeal membrane oxygenation; CDH, congenital diaphragmatic hernia; GA, gestational age; MRI, Magnetic Resonance Imaging; DTI, Diffusion Tensor Imaging; MRS, Magnetic Resonance Spectroscopy; WISC, Wechsler Intelligence Scale; CMS, Children s Memory Scale; WMS, Wechsler Memory Scale; WASI, Wechsler Abbreviated Scale of Intelligence; CVLT, California Verbal Learning Test; WMTBC, Working Memory Test Battery for Children; VLMT, Verbal Learning and Memory Test; RAVLT, Rey Auditory Verbal Learning Test; RCFT, Rey Complex Figure Test; CTPP, Comprehensive Test of Phonological Processing; CELF, Clinical Evaluation of Language Fundamentals; RBMT, Rivermead Behavioural Memory Test; CAVLT, Children s Auditory Verbal Learning Test; AMIPB, Adult Memory and Information Processing Battery; NEPSYIINL, Dutch Version of the Developmental Neuropsychological Assessment.

Supplementary Online Content

Supplementary Online Content Devenney E, Bartley L, Hoon C, et al. Progression in behavioral variant frontotemporal dementia: a longitudinal study. JAMA Neurol. Published online October 26, 2015. doi:10.1001/jamaneurol.2015.2061.