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Open Access 01-09-2020 | Optic Neuritis | Neuro

Optic chiasm measurements may be useful markers of anterior optic pathway degeneration in neuromyelitis optica spectrum disorders

Authors: Valentin Juenger, Graham Cooper, Claudia Chien, Meera Chikermane, Frederike Cosima Oertel, Hanna Zimmermann, Klemens Ruprecht, Sven Jarius, Nadja Siebert, Joseph Kuchling, Athina Papadopoulou, Susanna Asseyer, Judith Bellmann-Strobl, Friedemann Paul, Alexander U. Brandt, Michael Scheel

Published in: European Radiology | Issue 9/2020

Abstract

Objectives

We aimed to evaluate optic chiasm (OC) measures as potential imaging marker for anterior optic pathway damage assessment in the context of neuromyelitis optica spectrum disorders (NMOSD).

Materials and method

This cross-sectional study included 39 patients exclusively with aquaporin 4-IgG seropositive NMOSD of which 25 patients had a history of optic neuritis (NMOSD-ON) and 37 age- and sex-matched healthy controls (HC). OC heights, width, and area were measured using standard 3D T1-weighted MRI. Sensitivity of these measures to detect neurodegeneration in the anterior optic pathway was assessed in receiver operating characteristics analyses. Correlation coefficients were used to assess associations with structural measures of the anterior optic pathway (optic nerve dimensions, retinal ganglion cell loss) and clinical measures (visual function and disease duration).

Results

OC heights and area were significantly smaller in NMOSD-ON compared to HC (NMOSD-ON vs. HC p < 0.0001). An OC area smaller than 22.5 mm² yielded a sensitivity of 0.92 and a specificity of 0.92 in separating chiasms of NMOSD-ON from HC. OC area correlated well with structural and clinical measures in NMOSD-ON: optic nerve diameter (r = 0.4, p = 0.047), peripapillary retinal nerve fiber layer thickness (r = 0.59, p = 0.003), global visual acuity (r = − 0.57, p = 0.013), and diseases duration (r = − 0.5, p = 0.012).

Conclusion

Our results suggest that OC measures are promising and easily accessible imaging markers for the assessment of anterior optic pathway damage.

Key Points

• Optic chiasm dimensions were smaller in neuromyelitis optica spectrum disorder patients compared to healthy controls.

• Optic chiasm dimensions are associated with retinal measures and visual dysfunction.

• The optic chiasm might be used as an easily accessible imaging marker of neurodegeneration in the anterior optic pathway with potential functional relevance.

Jarius S, Wildemann B, Paul F (2014) Neuromyelitis optica: clinical features, immunopathogenesis and treatment. Clin Exp Immunol 176(2):149–164PubMedPubMedCentral

Waters P, Reindl M, Saiz A et al (2016) Multicentre comparison of a diagnostic assay: aquaporin-4 antibodies in neuromyelitis optica. J Neurol Neurosurg Psychiatry 87(9):1005–1015PubMedPubMedCentral

Hickman SJ, Brex PA, Brierley CM et al (2001) Detection of optic nerve atrophy following a single episode of unilateral optic neuritis by MRI using a fat-saturated short-echo fast FLAIR sequence. Neuroradiology 43:123–128PubMed

Hickman SJ, Toosy AT, Jones SJ et al (2004) A serial MRI study following optic nerve mean area in acute optic neuritis. Brain 127:2498–2505PubMed

Tian DC, Su L, Fan M et al (2018) Bidirectional degeneration in the visual pathway in neuromyelitis optica spectrum disorder (NMOSD). Mult Scler 24:1585–1593PubMed

Tur C, Goodkin O, Altmann DR et al (2016) Longitudinal evidence for anterograde trans-synaptic degeneration after optic neuritis. Brain 139:816–828PubMedPubMedCentral

Gabilondo I, Martinez-Lapiscina EH, Martinez-Heras E et al (2014) Trans-synaptic axonal degeneration in the visual pathway in multiple sclerosis. Ann Neurol 75:98–107PubMed

Sinnecker T, Oberwahrenbrock T, Metz I et al (2015) Optic radiation damage in multiple sclerosis is associated with visual dysfunction and retinal thinning~an ultrahigh-field MR pilot study. Eur Radiol 25:122–131PubMed

Kuchling J, Backner Y, Oertel FC et al (2018) Comparison of probabilistic tractography and tract-based spatial statistics for assessing optic radiation damage in patients with autoimmune inflammatory disorders of the central nervous system. Neuroimage Clin 19:538–550

10.

Kuchling J, Brandt AU, Paul F, Scheel M (2017) Diffusion tensor imaging for multilevel assessment of the visual pathway: possibilities for personalized outcome prediction in autoimmune disorders of the central nervous system. EPMA J 8:279–294PubMedPubMedCentral

11.

Merle H, Olindo S, Bonnan M et al (2007) Natural history of the visual impairment of relapsing neuromyelitis optica. Ophthalmology 114:810–815PubMed

12.

Schmidt F, Zimmermann H, Mikolajczak J et al (2017) Severe structural and functional visual system damage leads to profound loss of vision-related quality of life in patients with neuromyelitis optica spectrum disorders. Mult Scler Relat Disord 11:45–50PubMed

13.

Stiebel-Kalish H, Hellmann MA, Mimouni M et al (2019) Does time equal vision in the acute treatment of a cohort of AQP4 and MOG optic neuritis? Neurol Neuroimmunol Neuroinflamm 6:e572PubMedPubMedCentral

14.

Beekman J, Keisler A, Pedraza O et al (2019) Neuromyelitis optica spectrum disorder: patient experience and quality of life. Neurol Neuroimmunol Neuroinflamm 6:e580PubMedPubMedCentral

15.

Hickman SJ, Brierley CM, Brex PA et al (2002) Continuing optic nerve atrophy following optic neuritis: a serial MRI study. Mult Scler 8:339–342PubMed

16.

Harrigan RL, Smith AK, Lyttle B et al (2017) Quantitative characterization of optic nerve atrophy in patients with multiple sclerosis. Mult Scler J Exp Transl Clin 3:2055217317730097PubMedPubMedCentral

17.

Trip SA, Schlottmann PG, Jones SJ et al (2006) Optic nerve atrophy and retinal nerve fibre layer thinning following optic neuritis: evidence that axonal loss is a substrate of MRI-detected atrophy. Neuroimage. 31:286–293PubMed

18.

Parravano JG, Toledo A, Kucharczyk W (1993) Dimensions of the optic nerves, chiasm, and tracts: MR quantitative comparison between patients with optic atrophy and normals. J Comput Assist Tomogr 17:688–690PubMed

19.

Manogaran P, Vavasour IM, Lange AP et al (2016) Quantifying visual pathway axonal and myelin loss in multiple sclerosis and neuromyelitis optica. Neuroimage Clin 11:743–750

20.

Manogaran P, Hanson JV, Olbert ED et al (2016) Optical coherence tomography and magnetic resonance imaging in multiple sclerosis and Neuromyelitis Optica Spectrum disorder. Int J Mol Sci 17:e1894PubMed

21.

Trip SA, Schlottmann PG, Jones SJ et al (2005) Retinal nerve fiber layer axonal loss and visual dysfunction in optic neuritis. Ann Neurol 58:383–391PubMed

22.

Oertel FC, Zimmermann HG, Brandt AU, Paul F (2018) Novel uses of retinal imaging with optical coherence tomography in multiple sclerosis. Expert Rev Neurother 19:31–43PubMed

23.

Oberwahrenbrock T, Traber GL, Lukas S et al (2018) Multicenter reliability of semiautomatic retinal layer segmentation using OCT. Neurol Neuroimmunol Neuroinflamm 5:e449PubMedPubMedCentral

24.

Dorr J, Wernecke KD, Bock M et al (2011) Association of retinal and macular damage with brain atrophy in multiple sclerosis. PLoS One 6:e18132PubMedPubMedCentral

25.

Ayadi N, Dörr J, Motamedi S (2018) Temporal visual resolution and disease severity in MS. Neurol Neuroimmunol Neuroinflamm 5(5):e49

26.

Oertel FC, Zimmermann H, Paul F, Brandt AU (2018) Optical coherence tomography in neuromyelitis optica spectrum disorders: potential advantages for individualized monitoring of progression and therapy. EPMA J 9:21–33PubMed

27.

Oertel FC, Kuchling J, Zimmermann H et al (2017) Microstructural visual system changes in AQP4-antibody-seropositive NMOSD. Neurol Neuroimmunol Neuroinflamm 4:e334PubMedPubMedCentral

28.

Bennett JL, de Seze J, Lana-Peixoto M et al (2015) Neuromyelitis optica and multiple sclerosis: seeing differences through optical coherence tomography. Mult Scler 21:678–688PubMedPubMedCentral

29.

Wingerchuk DM, Banwell B, Bennett JL et al (2015) International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 85:177–189PubMedPubMedCentral

30.

Kim HJ, Paul F, Lana-Peixoto MA et al (2015) MRI characteristics of neuromyelitis optica spectrum disorder: an international update. Neurology 84:1165–1173PubMedPubMedCentral

31.

Wagner AL, Murtagh FR, Hazlett KS, Arrington JA (1997) Measurement of the normal optic chiasm on coronal MR images. AJNR Am J Neuroradiol 18:723–726PubMed

32.

Avery RA, Mansoor A, Idrees R et al (2016) Quantitative MRI criteria for optic pathway enlargement in neurofibromatosis type 1. Neurology 86:2264–2270PubMedPubMedCentral

33.

Kasmann-Kellner B, Schafer T, Krick CM, Ruprecht KW, Reith W, Schmitz BL (2003) Anatomical differences in optic nerve, chiasma and tractus opticus in human albinism as demonstrated by standardized clinical and MRI evaluation. Klin Monbl Augenheilkd 220:334–344PubMed

34.

Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis. Neurology. 33:1444–1452

35.

Cruz-Herranz A, Balk LJ, Oberwahrenbrock T et al (2016) The APOSTEL recommendations for reporting quantitative optical coherence tomography studies. Neurology 86:2303–2309PubMedPubMedCentral

36.

Tewarie P, Balk L, Costello F et al (2012) The OSCAR-IB consensus criteria for retinal OCT quality assessment. PLoS One 7:e34823PubMedPubMedCentral

37.

Schippling S, Balk L, Costello F et al (2015) Quality control for retinal OCT in multiple sclerosis: validation of the OSCAR-IB criteria. Mult Scler 21:163–170PubMed

38.

Hajian-Tilaki K (2013) Receiver operating characteristic (ROC) curve analysis for medical diagnostic test evaluation. Caspian J Intern Med 4:627–635PubMedPubMedCentral

39.

Smith SM, ThangY JM et al (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17:479–489PubMed

40.

Wickham H (2017) Tidyverse: easily Install and Load the “Tidyverse.”. Available via https://cranr-project.org/package. Accessed 10 Oct 2018

41.

Kassambara A (2017) ggpubr: “ggplot2” Based Publication Ready Plots. Available via https://cran.r-project.org/web/packages/ggpubr/index.html. Accessed 10 Oct 10 2018

42.

Robin X, Turck N, Hainard A et al (2011) pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12:77PubMedPubMedCentral

43.

Akaishi T, Kaneko K, Himori N et al (2017) Subclinical retinal atrophy in the unaffected fellow eyes of multiple sclerosis and neuromyelitis optica. J Neuroimmunol 313:10–15PubMed

44.

Oertel FC, Havla J, Roca-Fernandez A et al (2018) Retinal ganglion cell loss in neuromyelitis optica: a longitudinal study. J Neurol Neurosurg Psychiatry 89:1259–1265PubMed

45.

Noval S, Contreras I, Muñoz S, Oreja-Guevara C, Manzano B, Rebolleda G (2011) Optical coherence tomography in multiple sclerosis and neuromyelitis optica: an update. Mult Scler Int 2011:472790PubMedPubMedCentral

46.

Gold SM, Willing A, Leypoldt F, Paul F, Friese MA (2019) Sex differences in autoimmune disorders of the central nervous system. Semin Immunopathol 41:177–188PubMed

47.

Borisow N, Mori M, Kuwabara S, Scheel M, Paul F (2018) Diagnosis and treatment of NMO spectrum disorder and MOG-encephalomyelitis. Front Neurol 9:888PubMedPubMedCentral

Title: Optic chiasm measurements may be useful markers of anterior optic pathway degeneration in neuromyelitis optica spectrum disorders
Authors: Valentin Juenger
Graham Cooper
Claudia Chien
Meera Chikermane
Frederike Cosima Oertel
Hanna Zimmermann
Klemens Ruprecht
Sven Jarius
Nadja Siebert
Joseph Kuchling
Athina Papadopoulou
Susanna Asseyer
Judith Bellmann-Strobl
Friedemann Paul
Alexander U. Brandt
Michael Scheel
Publication date: 01-09-2020
Publisher: Springer Berlin Heidelberg
Keywords: Optic Neuritis
Neuromyelitis Optica Spectrum Disease
Published in: European Radiology / Issue 9/2020
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI: https://doi.org/10.1007/s00330-020-06859-w

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Optic chiasm measurements may be useful markers of anterior optic pathway degeneration in neuromyelitis optica spectrum disorders

Abstract

Objectives

Materials and method

Results

Conclusion

Key Points

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Materials and method

Results

Conclusion

Key Points

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