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Autoimmune glial fibrillary acidic protein astrocytopathy masquerading as tuberculosis of the central nervous system: a case series

  • Amy ML Quek
    Correspondence
    Corresponding author: Dr. Amy May Lin Quek, Division of Neurology, National University Hospital, Singapore, NUHS Tower Block, 1E Kent Ridge Road, Level 10, Singapore 119228, Tel: +65-6779 5555
    Affiliations
    Division of Neurology, Department of Medicine, National University Hospital, Singapore, Singapore

    Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
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  • David Tang
    Affiliations
    Division of Neurology, Department of Medicine, National University Hospital, Singapore, Singapore
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  • Amanda Chin
    Affiliations
    Division of Neurology, Department of Medicine, National University Hospital, Singapore, Singapore
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  • Kay WP Ng
    Affiliations
    Division of Neurology, Department of Medicine, National University Hospital, Singapore, Singapore

    Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
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  • Hazel Lin
    Affiliations
    Department of Ophthalmology, National University Hospital, Singapore, Singapore
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  • Raymond CS Seet
    Affiliations
    Division of Neurology, Department of Medicine, National University Hospital, Singapore, Singapore

    Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore
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Open AccessPublished:September 23, 2022DOI:https://doi.org/10.1016/j.ijid.2022.09.029

      Highlights

      • Glial fibrillary acidic protein (GFAP) astrocytopathy may respond to steroids used in antituberculous treatment.
      • Brainstem, cerebellar, movement, and/or spinal cord features are typical.
      • Papillitis in the absence of raised intracranial pressure have been reported.
      • Cerebrospinal fluid GFAP-immunoglobulin G should be tested in patients with aseptic meningoencephalitis.
      • GFAP astrocytopathy responds favorably to immunotherapy.

      Abstract

      We describe the case history of three patients with meningoencephalitis who were initially treated for presumed tuberculous meningoencephalitis before being diagnosed with autoimmune glial fibrillary acidic protein (GFAP) astrocytopathy. We highlight the overlapping clinical features between autoimmune GFAP astrocytopathy and tuberculous meningoencephalitis and the challenges in early diagnosis, as both entities respond to an initial course of steroids accompanying antituberculous medications. Early evaluation of GFAP-immunoglobulin G in the cerebrospinal fluid of patients who present with aseptic meningoencephalitis could reveal autoimmune GFAP astrocytopathy, which responds favorably to immunotherapy.

      Keywords

      Introduction

      Tuberculosis (TB) is a devastating cause of meningoencephalitis (
      • Wilkinson RJ
      • Rohlwink U
      • Misra UK
      • van Crevel R
      • Mai NTH
      • Dooley KE
      • Caws M
      • Figaji A
      • Savic R
      • Solomons R
      • Thwaites GE
      Tuberculous Meningitis International Research Consortium. Tuberculous meningitis.
      ). Because early recognition and treatment are central to a favorable outcome, antituberculous medications are often initiated before mycobacterial culture results become available, especially in countries where TB is endemic (
      • Wilkinson RJ
      • Rohlwink U
      • Misra UK
      • van Crevel R
      • Mai NTH
      • Dooley KE
      • Caws M
      • Figaji A
      • Savic R
      • Solomons R
      • Thwaites GE
      Tuberculous Meningitis International Research Consortium. Tuberculous meningitis.
      ). We describe the case history of three patients with autoimmune glial fibrillary acidic protein (GFAP) astrocytopathy who were initially treated for tuberculous meningoencephalitis.

      Case 1

      A man aged 56 years presented with fever (38.5°C), confusion, headache, and hiccups. He had nuchal rigidity and intention tremors. Cerebrospinal fluid (CSF) examination revealed lymphocytic pleocytosis (151 × 109/µl white blood cells [WBC]), elevated protein (1.5 g/l; normal, 0.10-0.40 g/l), and reduced glucose (2.9 mmol/l, serum glucose 6.3 mmol/l), prompting the initiation of intravenous antibiotics and acyclovir. Brain magnetic resonance imaging (MRI) demonstrated diffuse leptomeningeal enhancement, especially in areas surrounding the brainstem and cerebellum (Figure 1a-c). He remained febrile despite treatment. A repeat lumbar puncture performed a week after hospitalization revealed an opening pressure of 18 cm H20, with worsening CSF indexes (WBC 234 × 109/µl, protein 1.17 g/l, and glucose 3 mmol/l). Results of his other investigations are summarized in Supplementary Table 1. Despite initial treatment, he developed further confusion and drowsiness, which prompted a switch in antimicrobial treatment to antituberculous medications and dexamethasone. Two weeks later, he made significant improvements in his consciousness and mentation. A repeat MRI brain showed significant reduction in leptomeningeal enhancement (Figure 1a-c), and a repeat lumbar puncture revealed improvement in CSF indexes (WBC 50 × 109/µl, protein 0.58 g/dl, and glucose 3.2 mmol/l). Eight weeks after initiation of anti-TB treatment, his headaches, tremors, and confusion recurred, coinciding with dexamethasone cessation. At this point, he complained of visual blurring and was found to have bilateral fundal disc swelling. MRI brain showed a linear and perivascular pattern of enhancement radiating from the periventricular region (Figure 1d, e). Subsequent CSF analysis revealed GFAP antibody positivity. He received intravenous methylprednisolone (1 g/day for 5 days), followed by oral prednisolone (1 mg/kg/day) and mycophenolate mofetil (2 g/day); oral prednisolone was gradually tapered over 3 months. He was continued on oral mycophenolate mofetil for 2 years and did not experience a disease relapse.
      Figure 1
      Figure 1MRI brain scans. MRI postcontrast axial fluid attenuated inversion recovery scans reveal leptomeningeal enhancement of the pons (a) and medulla (b), whereas sagittal T1-weighted scans reveal diffuse leptomeningeal uptake of gadolinium in the pons, medulla, and cerebellum (c), as highlighted by the bold arrows in images a (i), b (i), and c (i). A 2-week treatment with dexamethasone and antituberculous medications resulted in improvement and resolution in leptomeningeal enhancement as shown in images a (ii), b (ii), and c (ii). After steroid discontinuation, he developed further clinical deterioration. A repeat MRI of the brain revealed new findings of diffuse periventricular and deep white matter hyperintensities on axial fluid attenuated inversion recovery images (d), as well as linear, perivascular pattern of enhancement radiating from the periventricular region on gadolinium-enhanced sagittal T1-weighted images (e). Abbreviation: MRI, magnetic resonance imaging.

      Case 2

      A man aged 43 years from India presented with fever (40.2°C), confusion, hiccups, and neck stiffness. CSF opening pressure was 29 cm H20, with lymphocytic pleocytosis (287 WBC × 109/µl), elevated protein (2.37 g/dl), and low glucose (1.8 mmol/l, serum glucose 4.7 mmol/l) (Supplementary Table 1). MRI brain showed diffuse leptomeningeal enhancement. He developed generalized seizures and decreased consciousness and underwent endotracheal intubation for airway protection. Antituberculous medications and dexamethasone were initiated and he was successfully extubated a week later. Three weeks after commencement of antituberculous medications and dexamethasone, he developed persistent fever and weakness involving both lower limbs. MRI of the spine showed patchy and longitudinally extensive T2 hyperintensity changes involving the cervical and thoracic segments of the spinal cord. No tuberculomas were observed in his MRI brain scans. His clinical deterioration and neuroradiological findings were initially ascribed to tuberculous paradoxical reaction because he had previously responded to antituberculous medications, and increasing the dose of dexamethasone led to clinical improvement. GFAP antibodies were subsequently reported to be positive in CSF, whereas repeated mycobacterial cultures remained negative.

      Case 3

      A woman aged 59 years presented with fever (38.7°C), headache, confusion, and vomiting. She had dysmetria and myoclonus. MRI brain revealed diffuse leptomeningeal enhancement. CSF opening pressure was 21.2 cm H20, showing lymphocytic pleocytosis (WBC 505 × 109/µl), elevated protein (1.19 g/dl), and low glucose (2.2 mmol/l; serum glucose 5.4 mmol/l) (Supplementary Table 1). After the initiation of antituberculous medications and dexamethasone, her symptoms and CSF indexes improved. A repeat MRI of the brain 2 weeks into treatment revealed resolution of leptomeningeal enhancement. Autoimmune antibody test subsequently revealed GFAP positivity in the CSF. Oral dexamethasone was switched to prednisolone, and antituberculous medications were discontinued. She was continued on oral prednisolone for 3 months and remained disease-free for the subsequent 6 months.

      Discussion

      Elucidating an autoimmune etiology in patients with meningoencephalitis can be challenging because autoimmune GFAP astrocytopathy may be clinically indistinguishable from the infectious causes of meningoencephalitis (
      • Flanagan EP
      • Hinson SR
      • Lennon VA
      • Fang B
      • Aksamit AJ
      • Morris PP
      • Basal E
      • Honorat JA
      • Alfugham NB
      • Linnoila JJ
      • Weinshenker BG
      • Pittock SJ
      • McKeon A.
      Glial fibrillary acidic protein immunoglobulin G as biomarker of autoimmune astrocytopathy: analysis of 102 patients.
      ;
      • Gravier-Dumonceau A
      • Ameli R
      • Rogemond V
      • Ruiz A
      • Joubert B
      • Muñiz-Castrillo S
      • Vogrig A
      • Picard G
      • Ambati A
      • Benaiteau M
      • Rulquin F
      • Ciron J
      • Deiva K
      • de Broucker T
      • Kremer L
      • Kerschen P
      • Sellal F
      • Bouldoires B
      • Genet R
      • Biberon J
      • Bigot A
      • Duval F
      • Issa N
      • Rusu EC
      • Goudot M
      • Dutray A
      • Devoize JL
      • Hopes L
      • Kaminsky AL
      • Philbert M
      • Chanson E
      • Leblanc A
      • Morvan E
      • Andriuta D
      • Diraison P
      • Mirebeau G
      • Derollez C
      • Bourg V
      • Bodard Q
      • Fort C
      • Grigorashvili-Coin I
      • Rieul G
      • Molinier-Tiganas D
      • Bonnan M
      • Tchoumi T
      • Honnorat J
      • Marignier R
      Glial fibrillary acidic protein autoimmunity: A French cohort study.
      ;
      • Héraud C
      • Capet N
      • Levraut M
      • Hattenberger R
      • Bourg V
      • Thomas P
      • Mondot L
      • Lebrun-Frenay C.
      Glial fibrillary acidic protein (GFAP) astrocytopathy presenting as mild encephalopathy with reversible splenium lesion.
      ;
      • Kimura A
      • Takekoshi A
      • Yoshikura N
      • Hayashi Y
      • Shimohata T.
      Clinical characteristics of autoimmune GFAP astrocytopathy.
      ;
      • Li J
      • Wang C
      • Cao Y
      • Shi J
      • Liu H
      • Zhou M
      • Liu C
      • Hu W.
      Autoimmune glial fibrillary acidic protein astrocytopathy mimicking acute disseminated encephalomyelitis: A case report.
      ;
      • Salvador GLO
      • Basso ACN
      • Barbieri PP
      • Leitao CA
      • Teixeira BCA
      • Neto AC.
      Central nervous system and spinal cord tuberculosis: revisiting an important disease.
      ;
      • Thwaites GE
      • van Toorn R
      • Schoeman J.
      Tuberculous meningitis: more questions, still too few answers.
      ;
      • Wang H
      • Chin JH
      • Fang BY
      • Chen X
      • Zhao AL
      • Ren HT
      • Guan HZ.
      Autoimmune glial fibrillary acidic protein astrocytopathy manifesting as subacute meningoencephalitis with descending myelitis: a case report.
      ;
      • Wilkinson RJ
      • Rohlwink U
      • Misra UK
      • van Crevel R
      • Mai NTH
      • Dooley KE
      • Caws M
      • Figaji A
      • Savic R
      • Solomons R
      • Thwaites GE
      Tuberculous Meningitis International Research Consortium. Tuberculous meningitis.
      ). Although the presence of CSF lymphocytic pleocytosis, increased protein, hypoglycorrhachia, and diffuse leptomeningeal enhancement on neuroimaging are suggestive of tuberculous meningoencephalitis, such findings could be similarly observed in patients with autoimmune GFAP astrocytopathy (
      • Iorio R
      • Damato V
      • Evoli A
      • Gessi M
      • Gaudino S
      • Di Lazzaro V
      • Spagni G
      • Sluijs JA
      • Hol EM.
      Clinical and immunological characteristics of the spectrum of GFAP autoimmunity: a case series of 22 patients.
      ;
      • Ip B
      • Lam C
      • Ip V
      • Chan A
      • Mok V
      • Au E
      • Chan E
      • Lau A.
      Autoimmune glial fibillary acidic protein astrocytopathy associated meningoencephalomyelitis and bilateral sensorineuronal deafness.
      ;
      • Kimura A
      • Takekoshi A
      • Yoshikura N
      • Hayashi Y
      • Shimohata T.
      Clinical characteristics of autoimmune GFAP astrocytopathy.
      ;
      • Wang H
      • Chin JH
      • Fang BY
      • Chen X
      • Zhao AL
      • Ren HT
      • Guan HZ.
      Autoimmune glial fibrillary acidic protein astrocytopathy manifesting as subacute meningoencephalitis with descending myelitis: a case report.
      ). Because a delay in treatment carries a poor prognosis, antituberculous medications and steroids are often initiated before mycobacterial culture results become available, guided mostly by clinical suspicion (
      • Poplin V
      • Boulware DR
      • Bahr NC.
      Methods for rapid diagnosis of meningitis etiology in adults.
      ;
      • Thwaites GE
      • van Toorn R
      • Schoeman J.
      Tuberculous meningitis: more questions, still too few answers.
      ;
      • Wilkinson RJ
      • Rohlwink U
      • Misra UK
      • van Crevel R
      • Mai NTH
      • Dooley KE
      • Caws M
      • Figaji A
      • Savic R
      • Solomons R
      • Thwaites GE
      Tuberculous Meningitis International Research Consortium. Tuberculous meningitis.
      ).
      Patients with autoimmune GFAP astrocytopathy could respond to steroids that accompany antituberculous treatment and be erroneously diagnosed with tuberculous meningoencephalitis. Kimura and colleagues reported that nine of 14 patients with autoimmune GFAP astrocytopathy were initially treated with anti-TB medications (
      • Kimura A
      • Takekoshi A
      • Yoshikura N
      • Hayashi Y
      • Shimohata T.
      Clinical characteristics of autoimmune GFAP astrocytopathy.
      ), whereas only one of 22 patients from an Italian series of autoimmune GFAP astrocytopathy was initially treated for tuberculous meningitis (
      • Iorio R
      • Damato V
      • Evoli A
      • Gessi M
      • Gaudino S
      • Di Lazzaro V
      • Spagni G
      • Sluijs JA
      • Hol EM.
      Clinical and immunological characteristics of the spectrum of GFAP autoimmunity: a case series of 22 patients.
      ). Findings from these studies highlight differences in the treatment approach to meningoencephalitis, depending on the endemicity of TB (
      • Ip B
      • Lam C
      • Ip V
      • Chan A
      • Mok V
      • Au E
      • Chan E
      • Lau A.
      Autoimmune glial fibillary acidic protein astrocytopathy associated meningoencephalomyelitis and bilateral sensorineuronal deafness.
      ;
      • Wang H
      • Chin JH
      • Fang BY
      • Chen X
      • Zhao AL
      • Ren HT
      • Guan HZ.
      Autoimmune glial fibrillary acidic protein astrocytopathy manifesting as subacute meningoencephalitis with descending myelitis: a case report.
      ). Although information on the epidemiology of autoimmune GFAP astrocytopathy is sparsely available, existing data suggest that the disease is likely underrecognized given its recent discovery and poorer recognition among clinicians. A large cohort analysis in Indonesia highlighted that close to 60% of patients who were clinically diagnosed and treated for tuberculous meningitis lacked mycobacterial culture confirmation of TB (
      • Chaidir L
      • Annisa J
      • Dian S
      • Parwati I
      • Alisjahbana A
      • Purnama F
      • van der Zanden A
      • Ganiem AR
      • van Crevel R.
      Microbiological diagnosis of adult tuberculous meningitis in a ten-year cohort in Indonesia.
      ). It is unclear what proportion of patients who were culture-negative could harbor GFAP antibody positivity, which would support a diagnosis of autoimmune GFAP astrocytopathy. Whether GFAP antibodies could be also present in culture-confirmed tuberculous meningoencephalitis remains uncertain. Although oligoclonal bands are not routinely tested in these clinical settings, future studies should examine their value of measuring oligoclonal bands to identify patients who may require a more detailed analysis of neural autoimmune antibodies. The optimal duration of immunotherapy in patients with autoimmune GFAP astrocytopathy who present with meningoencephalitis should also be examined in future studies.
      Despite overlapping features, several clinical clues may differentiate between autoimmune GFAP astrocytopathy and tuberculous meningoencephalitis. Optic disc edema is observed in 30% of GFAP astrocytopathy from papillitis arising from inflammatory vasculopathy (
      • Chen JJ
      • Aksamit AJ
      • McKeon A
      • Pittock SJ
      • Weinshenker BG
      • Leavitt JA
      • Morris PP
      • Flanagan EP.
      Optic disc edema in glial fibrillary acidic protein autoantibody-positive meningoencephalitis.
      ;
      • Flanagan EP
      • Hinson SR
      • Lennon VA
      • Fang B
      • Aksamit AJ
      • Morris PP
      • Basal E
      • Honorat JA
      • Alfugham NB
      • Linnoila JJ
      • Weinshenker BG
      • Pittock SJ
      • McKeon A.
      Glial fibrillary acidic protein immunoglobulin G as biomarker of autoimmune astrocytopathy: analysis of 102 patients.
      ). Unlike papilledema from raised intracranial pressure, CSF opening pressure in papillitis from autoimmune GFAP astrocytopathy is typically normal or minimally elevated (
      • Chen JJ
      • Aksamit AJ
      • McKeon A
      • Pittock SJ
      • Weinshenker BG
      • Leavitt JA
      • Morris PP
      • Flanagan EP.
      Optic disc edema in glial fibrillary acidic protein autoantibody-positive meningoencephalitis.
      ). Brainstem or movement disorders are reported in up to two-thirds of autoimmune GFAP astrocytopathy cases. Our patients had intention tremors, hiccups, and myoclonus, which could also prompt early GFAP-immunoglobulin G evaluation (
      • Gravier-Dumonceau A
      • Ameli R
      • Rogemond V
      • Ruiz A
      • Joubert B
      • Muñiz-Castrillo S
      • Vogrig A
      • Picard G
      • Ambati A
      • Benaiteau M
      • Rulquin F
      • Ciron J
      • Deiva K
      • de Broucker T
      • Kremer L
      • Kerschen P
      • Sellal F
      • Bouldoires B
      • Genet R
      • Biberon J
      • Bigot A
      • Duval F
      • Issa N
      • Rusu EC
      • Goudot M
      • Dutray A
      • Devoize JL
      • Hopes L
      • Kaminsky AL
      • Philbert M
      • Chanson E
      • Leblanc A
      • Morvan E
      • Andriuta D
      • Diraison P
      • Mirebeau G
      • Derollez C
      • Bourg V
      • Bodard Q
      • Fort C
      • Grigorashvili-Coin I
      • Rieul G
      • Molinier-Tiganas D
      • Bonnan M
      • Tchoumi T
      • Honnorat J
      • Marignier R
      Glial fibrillary acidic protein autoimmunity: A French cohort study.
      ). Diffuse MRI leptomeningeal enhancement is common in both clinical entities. However, basal enhancement is more pronounced in TB (
      • Salvador GLO
      • Basso ACN
      • Barbieri PP
      • Leitao CA
      • Teixeira BCA
      • Neto AC.
      Central nervous system and spinal cord tuberculosis: revisiting an important disease.
      ), whereas perivascular enhancement radiating from periventricular regions is encountered in 30-50% of autoimmune GFAP astrocytopathy (
      • Flanagan EP
      • Hinson SR
      • Lennon VA
      • Fang B
      • Aksamit AJ
      • Morris PP
      • Basal E
      • Honorat JA
      • Alfugham NB
      • Linnoila JJ
      • Weinshenker BG
      • Pittock SJ
      • McKeon A.
      Glial fibrillary acidic protein immunoglobulin G as biomarker of autoimmune astrocytopathy: analysis of 102 patients.
      ;
      • Gravier-Dumonceau A
      • Ameli R
      • Rogemond V
      • Ruiz A
      • Joubert B
      • Muñiz-Castrillo S
      • Vogrig A
      • Picard G
      • Ambati A
      • Benaiteau M
      • Rulquin F
      • Ciron J
      • Deiva K
      • de Broucker T
      • Kremer L
      • Kerschen P
      • Sellal F
      • Bouldoires B
      • Genet R
      • Biberon J
      • Bigot A
      • Duval F
      • Issa N
      • Rusu EC
      • Goudot M
      • Dutray A
      • Devoize JL
      • Hopes L
      • Kaminsky AL
      • Philbert M
      • Chanson E
      • Leblanc A
      • Morvan E
      • Andriuta D
      • Diraison P
      • Mirebeau G
      • Derollez C
      • Bourg V
      • Bodard Q
      • Fort C
      • Grigorashvili-Coin I
      • Rieul G
      • Molinier-Tiganas D
      • Bonnan M
      • Tchoumi T
      • Honnorat J
      • Marignier R
      Glial fibrillary acidic protein autoimmunity: A French cohort study.
      ). Spinal cord involvement may occur in autoimmune GFAP astrocytopathy, manifesting as longitudinally extensive myelitis on MRI (
      • Flanagan EP
      • Hinson SR
      • Lennon VA
      • Fang B
      • Aksamit AJ
      • Morris PP
      • Basal E
      • Honorat JA
      • Alfugham NB
      • Linnoila JJ
      • Weinshenker BG
      • Pittock SJ
      • McKeon A.
      Glial fibrillary acidic protein immunoglobulin G as biomarker of autoimmune astrocytopathy: analysis of 102 patients.
      ;
      • Gravier-Dumonceau A
      • Ameli R
      • Rogemond V
      • Ruiz A
      • Joubert B
      • Muñiz-Castrillo S
      • Vogrig A
      • Picard G
      • Ambati A
      • Benaiteau M
      • Rulquin F
      • Ciron J
      • Deiva K
      • de Broucker T
      • Kremer L
      • Kerschen P
      • Sellal F
      • Bouldoires B
      • Genet R
      • Biberon J
      • Bigot A
      • Duval F
      • Issa N
      • Rusu EC
      • Goudot M
      • Dutray A
      • Devoize JL
      • Hopes L
      • Kaminsky AL
      • Philbert M
      • Chanson E
      • Leblanc A
      • Morvan E
      • Andriuta D
      • Diraison P
      • Mirebeau G
      • Derollez C
      • Bourg V
      • Bodard Q
      • Fort C
      • Grigorashvili-Coin I
      • Rieul G
      • Molinier-Tiganas D
      • Bonnan M
      • Tchoumi T
      • Honnorat J
      • Marignier R
      Glial fibrillary acidic protein autoimmunity: A French cohort study.
      ). Finally, after an initial antituberculous treatment response, disease recrudescence with steroid taper, which could be construed as tuberculous paradoxical reaction, should also prompt consideration of autoimmune GFAP astrocytopathy. Because autoimmune GFAP astrocytopathy responds favorably to immunosuppressants, early evaluation with CSF GFAP-immunoglobulin G should be considered in patients with suspected tuberculous meningoencephalitis with atypical features.

      Funding

      This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

      Ethical approval

      Written informed consent was obtained from all patients.

      CRediT authorship contribution statement

      Amy ML Quek: Writing – original draft, Writing – review & editing. David Tang: Writing – original draft, Writing – review & editing. Amanda Chin: Writing – original draft, Writing – review & editing. Kay WP Ng: Writing – review & editing. Hazel Lin: Writing – review & editing. Raymond CS Seet: Writing – original draft, Writing – review & editing.

      Declaration of competing interest

      The authors have no competing interests to declare.

      Appendix. Supplementary materials

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