Höffding step and beyond: The impact of visual sensory impairment on cognitive performance in neuropsychological testing of survivors of acute methanol poisoning
Restricted accessResearch articleFirst published online August 4, 2023
Höffding step and beyond: The impact of visual sensory impairment on cognitive performance in neuropsychological testing of survivors of acute methanol poisoning
Sensory deficits can result in limitations regarding how well neuropsychological test findings can be interpreted. Only a few studies have investigated the influence of vision alteration on neuropsychological tests. In 2012 the Czech Republic experienced mass methanol poisoning. Methanol metabolites cause histotoxic hypoxia to the optic nerve.
OBJECTIVE:
In the current study, the effect of the toxic damage on the parts of the visual pathway on visual and non-visual neuropsychological measures was investigated using electrophysiological methods (visual evoked potential (VEP) and optical coherence tomography (OCT) with retinal nerve fibre layer (RNFL) thickness measurement.
METHODS:
53 individuals who experienced methanol poisoning participated in this research (76% men; ages 24 to 74 years, mean = 43.8±14.6 years; education 11.9±1.4 years). Each participant underwent comprehensive neurological, ophthalmological, and neuropsychological examinations.
RESULTS:
The results of mixed-effect models revealed significant small to a medium association between the Stroop test weak interference and Grooved Pegboard with the left eye global, nasal and temporal RNFL thickness. Also, medium associations between the Finger Tapping test and the Stroop test weak interference and left eye temporal RNFL, right eye temporal RNFL, and the latency P1 of VEP in the left eye were significant.
CONCLUSION:
The results of this study found a small to medium association (r = .15– .33; p = .010– .046) between RNFL thickness and cognitive visual test performance. Careful interpretation is suggested regarding results obtained from visual tests of the executive or motor functioning with participants with RNFL decrease or other types of early visual processing damage.
Alexander, D. M., Trengove, C., van Leeuwen, C. (2015) Donders is dead: Cortical traveling waves and the limits of mental chronometry in cognitive neuroscience. Cognitive Processing, 16(4), 365–375. https://doi.org/10.1007/s10339-015-0662-4
2.
Arora, V., Nijjar, I. B. S., Multani, A. S. (2007) CASE REPORT MRI findings in methanol intoxication: A report of two cases. The British Journal of Radiology, 80, 243–246. https://doi.org/10.1259/bjr/40137535
3.
Baltes, P. B., Lindenberger, U. (1997) Emergence of a powerful connection between sensory and cognitive functions across the adult life span: A new window to the study of cognitive aging?Psychology and Aging, 12(1), 12–21. https://doi.org/10.1037/0882-7974.12.1.12
4.
Bezdicek, O., Lukavsky, J., Stepankova, H., Nikolai, T., Axelrod, B. N., Michalec, J., Růžička, E., Kopecek, M. (2015) The Stroop Test: Normative standards in older Czech adults and discriminative validity for mild cognitive impairment in Parkinsons disease. Journal of Clinical and Experimental Neuropsychology, 37(8), 794–807. https://doi.org/10.1080/13803395.2015.1057106Prague.
5.
Bezdicek, O., Michalec, J., Vaneckova, M., Klempir, J., Liskova, I., Seidl, Z., Janikova, B., Miovsky, M., Hubacek, J., Diblik, P., Kuthan, P., Pilin, A., Kurcova, I., Fenclova, Z., Petrik, V., Navratil, T., Pelclova, D., Zakharov, S., Ruzicka, E. (2017) Cognitive sequelae of methanol poisoning involve executive dysfunction and memory impairment in cross-sectional and long-term perspective. Alcohol, 59, 27–35. https://doi.org/10.1016/j.alcohol.2016.12.003
6.
Bezdicek, O., Motak, L., Axelrod, B. N., Preiss, M., Nikolai, T., Vyhnalek, M., Poreh, A., Ruzicka, E. (2012) Czech version of the trail making test: Normative data and clinical utility. Archives of Clinical Neuropsychology, 27(8), 906–914. https://doi.org/10.1093/arclin/acs084
7.
Bezdicek, O., Stepankova, H., Moták, L., Axelrod, B. N., Woodard, J. L., Preiss, M., Nikolai, T., Růžička, E., Poreh, A. (2014) Czech version of Rey Auditory Verbal Learning test: Normative data. Aging, Neuropsychology, and Cognition, 21(6), 693–721. https://doi.org/10.1080/13825585.2013.865699
8.
Bezdíček, O., Klempíř, J., Lišková, I., Michalec, J., Vaněčková, M., Seidl, Z., Janíková, B., Miovský, M., Hubáček, J. A., Diblík, P., Kuthan, P., Pilin, A., Kurcová, I., Fenclová, Z., Petrik, V., Navrátil, T., Pelclová, D., Růžička, E., Zakharov, S. (2014) Sequelae of methanol poisoning for cognition | Účinky intoxikace metanolem na kognitivní funkce. Ceska a Slovenska Neurologie a Neurochirurgie, 77(3), 320–325.
9.
Bruce, J. M., Bruce, A. S., Arnett, P. A. (2007) Mild visual acuity disturbances are associated with performance on tests of complex visual attention in MS. Journal of the International Neuropsychological Society, 13(3), 544–548. https://doi.org/10.1017/S1355617707070658
10.
Bukacova, K., Mana, J., Klempíř, J., Lišková, I., Brozová, H., Poláková, K., Žák, I., Pelclová, D., Zakharov, S., Růžička, E., Bezdicek, O. (2021) Cognitive changes after methanol exposure: Longitudinal perspective. Toxicology Letters, 349, 101–108. https://doi.org/10.1016/j.toxlet.2021.06.008
11.
Bylsma, F. W., Doninger, N. (2004) Neuropsychological assessment in individuals with severe visual impairment. Topics in Geriatric Rehabilitation, 20(3), 196–203. https://doi.org/10.1097/00013614-200407000-00007
12.
Cursiefen, C., Bergue, A. (2002) Acute bilateral blindness caused by accidental methanol intoxication during fire "eating. British Journal of Ophthalmology, 86(9), 1064–1065.
13.
Davis, A. S., Hertza, J., Williams, R. N., Gupta, A. S., Ohly, J. G. (2009) The influence of corrected visual acuity on visual attention and incidental learning in patients with multiple sclerosis. Applied Neuropsychology, 16(3), 165–168.
Esmael, A., Elsherif, M., Abdelsalam, M., Sabry, D., Mamdouh, M., Belal, T. (2020) Retinal thickness as a potential biomarker of neurodegeneration and a predictor of early cognitive impairment in patients with multiple sclerosis. Neurological Research, 42(7), 564–574. https://doi.org/10.1080/01616412.2020.1761174
17.
Feaster, H. T., Bruce, J. M. (2011) Visual acuity is associated with performance on visual and non-visual neuropsychological tests in multiple sclerosis. Clinical Neuropsychologist, 25(4), 640–651. https://doi.org/10.1080/13854046.2011.565075
18.
Folstein, M. F., Folstein, S. E., McHugh, P. R., Fanjiang, G. (2001) Mini -Mental State Examination User’s Guide. Psychological Assessment Resources.
19.
Friston, K. J., Price, C. J., Fletcher, P., Moore, C., Frackowiak, R. S. J., Dolan, R. J. (1996) The trouble with cognitive subtraction. NeuroImage, 4(2), 97–104. https://doi.org/10.1006/nimg.1996.0033
20.
Frydrychová, Z., Kopeĉek, M., Bezdíček, O., Štěpánková Georgi, H. (2018) České normy pro revidovaný reyův auditorně-verbální test učení (ravlt) pro populaci starších osob.eskvenská Psychologie. Československá Psychologie, 62(4), 330–349.
21.
Guerrier, L., Cransac, C., Pages, B., Saint-Aubert, L., Payoux, P., Páran, P., Pariente, J. (2019) Posterior Cortical Atrophy: Does Complaint Match the Impairment? A Neuropsychological and FDG-PET Study. Frontiers in Neurology, 10(September), 1–12. https://doi.org/10.3389/fneur.2019.01010
22.
Haegerstorm-Portnoy, G., Schneck, M. E., Brabyn, J. A. (1999) Seeing into Old Age: Vision Function Beyond Acuity. Optometry and Vision Science, 76(3), 141–158.
23.
Iseri, P. K., Altinaş, Ö., Tokay, T., Yüksel, N. (2006) Relationship between Cognitive Impairment and Retinal Morphological and Visual Functional Abnormalities in Alzheimer Disease. Journal of Neuro-Ophthalmology, 26(1), 18–24. https://doi.org/10.1097/01.wno.0000204645.56873.26
24.
Kempen, J. H., Mark, K., Feldman, S. T. (1994) Effect of VisualImpairment on Neuropsychological Test Performance.. Journal ofClinical and Experimental Neuropsychology, 16(2), 223–231. https://doi.org/10.1080/01688639408402633
25.
Kergoat, H., Kergoat, M.-J., Justino, L., Chertkow, H., Robillard, A., Bergman, H. (2002) Visual Retinocortical Function in Dementia of the Alzheimer Type. Gerontology, 48(4), 197–203. https://doi.org/10.1159/000058350
26.
Kløve, H. (1963) Clinical neuropsychology. In. The medical clinics of North America–Saunders.
27.
Kotikova, K., Zogala, D., Ptacnik, V., Trnka, J., Kupka, K., Vaneckova, M., Seidl, Z., Diblik, P., Heissigerova,J, Navratil, T., Komarc, M., Zak, I., Polakova, K., Brozova, H., Zakharov, S. (2021) Efficiency of 123I-ioflupane SPECT as the marker of basal ganglia damage in acute methanol poisoning: 6-year prospective study. Clinical Toxicology, 59(3), 235–245. https://doi.org/10.1080/15563650.2020.1802033
28.
Kromer, R., Serbecic, N., Hausner, L., Froelich, L., Beutelspacher, S. C. (2013) Comparison of Visual Evoked Potentials and Retinal Nerve Fiber Layer Thickness in Alzheimer’s Disease. Frontiers in Neurology, 4. https://doi.org/10.3389/fneur.2013.00203
29.
La Fleur, C. G., Salthouse, T. A. (2014) Out of sight, out of mind? Relations between visual acuity and cognition. Psychonomic Bulletin & Review, 21(5), 1202–1208. https://doi.org/10.3758/s13423-014-0594-5
30.
Lezak, M. D. (Ed.). (2012), Neuropsychological assessment–5th edOxford University Press.
31.
Lindenberger, U., Baltes, P. B. (1994) Sensory functioning and intelligence in old age: A strong connection. Psychology and Aging, 9(3), 339–355. https://doi.org/10.1037/0882-7974.9.3.339
32.
Lindenberger, U., Ghisletta, P. (2009) Cognitive and sensory declines in old age: Gauging the evidence for a common cause. Psychology and Aging, 24(1), 1–16. https://doi.org/10.1037/a0014986
33.
Mana, J., Vaneckova, M., Klempíř, J., Lišková, I., Brožová, H., Poláková, K., Seidl, Z., Miovský, M., Pelclová, D., Bukačová, K., Maréchal, B., Kober, T., Zakharov, S., Růžička, E., Bezdicek, O. (2019) Methanol Poisoning as an Acute Toxicological Basal Ganglia Lesion Model: Evidence from Brain Volumetry and Cognition. Alcoholism: Clinical and Experimental Research, 43(7), 1486–1497. https://doi.org/10.1111/acer.14077
34.
Nurieva, O., Diblik, P., Kuthan, P., Sklenka, P., Meliska, M., Bydzovsky, J., Heissigerova, J., Urban, P., Kotikova, K., Navratil, T., Komarc, M., Seidl, Z., Vaneckova, M., Pelclova, D., Zakharov, S. (2018) Progressive Chronic Retinal al Loss Following Acute Methanol-induced Optic Neuropathy: Four-Year Prospective Cohort Study. American Journal of Ophthalmology, 191, 100–115. https://doi.org/10.1016/j.ajo.2018.04.015Axon.
35.
Nurieva, O., Hubacek, J. A., Urban, P., Hlusicka, J., Diblik, P., Kuthan, P., Sklenka, P., Meliska, M., Bydzovsky, J., Heissigerova, J., Kotikova, K., Navratil, T., Komarc, M., Seidl, Z., Vaneckova, M., Vojtova, L., Zakharov, S. (2019) Clinical and genetic determinants of chronic visual pathway changes after methanol– induced optic neuropathy: Four-year follow-up study. Clinical Toxicology, 57(6), 387–397. https://doi.org/10.1080/15563650.2018.1532083
36.
Nurieva, O., Kotikova, K., Urban, P., Pelclova, D., Petrik, V., Navratil, T., Zakharov, S. (2016) Prevalence, dynamics, and biochemical predictors of optic nerve remyelination after methanol-induced acute optic neuropathy: A 2-year prospective study in 54 patients. Monatshefte Für Chemie - Chemical Monthly, 147(1), 239–249. https://doi.org/10.1007/s00706-015-1580-y
37.
Paasma, R., Hovda, K. E., Jacobsen, D. (2009) Methanol poisoning and long term sequelae—A six years follow-up after a large methanol outbreak. BMC Clinical Pharmacology, 9, 1–5. https://doi.org/10.1186/1472-6904-9-5
38.
Parikh, R. S., Parikh, S. R., Sekhar, G. C., Prabakaran, S., Babu, J. G., Thomas, R. (2007) Normal Age-Related Decay of Retinal Nerve Fiber Layer Thickness. Ophthalmology, 114(5), 921–926. https://doi.org/10.1016/j.ophtha.2007.01.023
39.
Reitan, R. M. (1992) Reitan Neuropsychology Laboratory. Trail Making Test. Manual for administration and scoring.
40.
Reitan, R. M., Wolfson, D. (1993) Neuropsychology Press. The Halstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation,–2nd ed.
41.
Ricker, K. L. (2006) Setting Cut-Scores: A Critical Review of the Angoff and Modified Angoff Methods. Alberta Journal of Educational Research, 52(1), 2006 Spring 2006. https://doi.org/10.11575/AJER.V52I1.55111
42.
Rosenbloom, M. J., Sullivan, E. V., Sassoon, S. A., O’Reilly, A., Fama, R., Kemper, C. A., Deresinski, S., Pfefferbaum, A. (2007) Alcoholism, HIV infection, and their comorbidity: Factors affecting self-rated health-related quality of life. Journal of Studies on Alcohol and Drugs, 68(1), 115–125. https://doi.org/10.15288/jsad.2007.68.115
43.
Sharpe, J. A., Hostovsky, M., Bilbao, J. M., Rewcastle, N. B. (1982) Methanol optic neuropathy: A histopathological study. Neurology, 32(10), 1093–1100. https://doi.org/10.1212/wnl.32.10.1093
44.
Sternäng, O., Jonsson, B., Wahlin, Å., Nyberg, L., Nilsson, L.-G. (2010) Examination of the Common Cause Account in a Population-Based Longitudinal Study with Narrow Age Cohort Design. Gerontology, 56(6), 553–563. https://doi.org/10.1159/000279754
45.
Štěpánková, H., Nikolai, T., Lukavský, J., Bezdíček, O., Vrajová, M., Kopeček, M. (2015) Mini – Mental State Examination – česká normativní studie Mini – Mental State Examination – Czech Normative Study. Ceska a Slovenska Neurologie a Neurochirurgie, 78/111(1), 57–63. https://doi.org/10.14735/amcsnn201557
46.
Urban, P., Zakharov, S., Diblík, P., Pelclová, D., Ridzoň, P. (2016) Visual evoked potentials in patients after methanol poisoning. International Journal of Occupational Medicine and Environmental Health, 29(3), 471–478. https://doi.org/10.13075/ijomeh.1896.00452
47.
Vaneckova, M., Zakharov, S., Klempir, J., Ruzicka, E., Bezdicek, O., Brozova, H., Diblik, P., Miovsky, M., Hubacek, J. A., Urban, P., Ridzon, P., Pelclova, D., Burgetova, A., Masek, M., Kotikova, K., Peterova, K., Liskova, I., Hamplova, L., Seidl, Z. (2015) Imaging findings after methanol intoxication (cohort of 46 patients). Neuroendocrinology letters, 36(8), 101–108.
48.
Vaněčková, M., Zakharov, S., Klempíř, J., Růžička, E., Bezdíček, O., Lišková, I., Diblík, P., Miovský, M., Hubáček, J. A., Urban, P., Ridzoň, P., Pelclová, D., Burgetová, A., Mašek, M., Seidl, Z. (2014) Methanol intoxication on magnetic resonance imaging— Case reports | Intoxikace metanolem v obraze magnetické rezonance— Kazuistiky. Ceska a Slovenska Neurologie a Neurochirurgie, 77(2), 235–239.
49.
Vleugels, L., Lafosse, C., VanNunen, A., Charlier, M., Ketelaer, P., Vandenbussche, E. (2001) Visuoperceptual impairment in MS patients: Nature and possible neural origins. Multiple Sclerosis, 7(6), 389–401. https://doi.org/10.1191/135245801701567113
50.
Wechsler, D. (2010) ní škála pro dospělé. WAIS-III. Hogrefe Testcentrum. Wechslerova inteligenční škála pro dospělé., WAIS-III. Hogrefe Testcentrum.
51.
Wieder, L., Gäde, G., Pech, L. M., Zimmermann, H., Wernecke, K. D., Dörr, J. M., Bellmann-Strobl, J., Paul, F., Brandt, A. U. (2013) Low contrast visual acuity testing is associated with cognitive performance in multiple sclerosis: A cross-sectional pilot study. BMC Neurology, 13. https://doi.org/10.1186/1471-2377-13-167
52.
Yamasaki, T., Horie, S., Ohyagi, Y., Tanaka, E., Nakamura, N., Goto, Y., Kanba, S., Kira, J., Tobimatsu, S. (2016) A Potential VEP Biomarker for Mild Cognitive Impairment: Evidence fromSelective Visual Deficit of Higher-Level Dorsal Pathway. Journal of Alzheimer’s Disease, 53(2), 661–676. https://doi.org/10.3233/JAD-150939
53.
Yang, C. S., Tsai, W. J., Lirng, J. F. (2005) Ocular manifestations and MRI findings in a case of methanol poisoning. Eye (Basingstoke), 19(7), 806–809. https://doi.org/10.1038/sj.eye.6701639
54.
Zakharov, S. (2012) Odborné doporučení pro intoxikaci metanolem. Urgentní medicína, 15(3), 33–37.
55.
Zakharov, S., Nurieva, O., Navratil, T., Diblik, P., Kuthan, P., & Pelclova, D. (2014a). Acute methanol poisonings: Folates administration and visual sequelae. Journal of Applied Biomedicine, 12(4), 309–316. https://doi.org/10.1016/j.jab.2014.04.001
56.
Zakharov, S., Nurieva, O., Navratil, T., Diblik, P., Kuthan, P., & Pelclova, D. (2014b). Acute methanol poisonings: Folates administration and visual sequelae. Journal of Applied Biomedicine, 12(4), 309–316. https://doi.org/10.1016/j.jab.2014.04.001
57.
Zakharov, S., Pelclova, D., Diblik, P., Urban, P., Kuthan, P., Nurieva, O., Kotikova, K., Navratil, T., Komarc, M., Belacek, J., Seidl, Z., Vaneckova, M., Hubacek, J. A., Bezdicek, O., Klempir, J., Yurchenko, M., Ruzicka, E., Miovsky, M., Janikova, B., Hovda, K. E. (2015) Long-term visual damage after acute methanol poisonings: Longitudinal cross-sectional study in 50 patients. Clinical Toxicology, 53(9), 884–892. https://doi.org/10.3109/15563650.2015.1086488
58.
Zakharov, S., Pelclova, D., Urban, P., Navratil, T., Diblik, P., Kuthan, P., Hubacek, J. A., Miovsky, M., Klempir, J., Vaneckova, M., Seidl, Z., Pilin, A., Fenclova, Z., Petrik, V., Kotikova, K., Nurieva, O., Ridzon, P., Rulisek, J., Komarc, M., Hovda, K. E. (2014) Czech mass methanol outbreak 2012: Epidemiology, challenges and clinical features. Clinical Toxicology, 52(10), 1013–1024. https://doi.org/10.3109/15563650.2014.974106
59.
Zhao, A., Fang, F., Li, B., Chen, Y., Qiu, Y., Wu, Y., Xu, W., Deng, Y. (2021) Visual Abnormalities Associate With Hippocampus in Mild Cognitive Impairment and Early Alzheimer’s Disease. Frontiers in Aging Neuroscience, 12, 597491. https://doi.org/10.3389/fnagi.2020.597491
