Skip to main content
Erschienen in:

11.06.2023 | Original Research Article

Age-associated changes in electroretinography measures in companion dogs

verfasst von: Michele M. Salzman, Natascha Merten, Wojciech K. Panek, Gilad Fefer, Alejandra Mondino, Hans D. Westermeyer, Margaret E. Gruen, Natasha J. Olby, Freya M. Mowat

Erschienen in: Documenta Ophthalmologica | Ausgabe 1/2023

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To determine the association between age and retinal full-field electroretinographic (ERG) measures in companion (pet) dogs, an important translational model species for human neurologic aging.

Methods

Healthy adult dogs with no significant ophthalmic abnormalities were included. Unilateral full-field light- and dark-adapted electroretinography was performed using a handheld device, with mydriasis and topical anaesthesia. Partial least squares effect screening analysis was performed to determine the effect of age, sex, body weight and use of anxiolytic medication on log-transformed ERG peak times and amplitudes; age and anxiolytic usage had significant effects on multiple ERG outcomes. Mixed model analysis was performed on data from dogs not receiving anxiolytic medications.

Results

In dogs not receiving anxiolytics, median age was 118 months (interquartile range 72–140 months, n = 77, 44 purebred, 33 mixed breed dogs). Age was significantly associated with prolonged peak times of a-waves (dark-adapted 3 and 10 cds/m2 flash p < 0.0001) and b-waves (cone flicker p = 0.03, dark-adapted 0.01 cds/m2 flash p = 0.001). Age was also significantly associated with reduced amplitudes of a-waves (dark-adapted 3 cds/m2 flash p < 0.0001, 10 cds/m2 flash p = 0.005) and b-waves (light-adapted 3 cds/m2 flash p < 0.0001, dark-adapted 0.01 cds/m2 flash p = 0.0004, 3 cds/m2 flash p < 0.0001, 10 cds/m2 flash p = 0.007) and flicker (light-adapted 30 Hz 3 cds/m2 p = 0.0004). Within the Golden Retriever breed, these trends were matched in a cross-sectional analysis of 6 individuals that received no anxiolytic medication.

Conclusions

Aged companion dogs have slower and reduced amplitude responses in both rod- and cone-mediated ERG. Consideration of anxiolytic medication use should be made when conducting ERG studies in dogs.
Anhänge
Nur mit Berechtigung zugänglich
Fußnoten
1
American Veterinary Medical Association Veterinary Economics Division, 2020.
 
Literatur
1.
Zurück zum Zitat Klein R, Klein BEK, Linton KLP (2020) Prevalence of age-related maculopathy: the beaver dam eye study. Ophthalmology 127(4s):S122-s132PubMedCrossRef Klein R, Klein BEK, Linton KLP (2020) Prevalence of age-related maculopathy: the beaver dam eye study. Ophthalmology 127(4s):S122-s132PubMedCrossRef
2.
Zurück zum Zitat Owsley C et al (2022) How vision is impaired from aging to early and intermediate age-related macular degeneration: insights from ALSTAR2 baseline. Transl Vis Sci Technol 11(7):17PubMedPubMedCentralCrossRef Owsley C et al (2022) How vision is impaired from aging to early and intermediate age-related macular degeneration: insights from ALSTAR2 baseline. Transl Vis Sci Technol 11(7):17PubMedPubMedCentralCrossRef
4.
Zurück zum Zitat Brown RL, Barrett AE (2011) Visual impairment and quality of life among older adults: an examination of explanations for the relationship. J Gerontol B Psychol Sci Soc Sci 66(3):364–373PubMedCrossRef Brown RL, Barrett AE (2011) Visual impairment and quality of life among older adults: an examination of explanations for the relationship. J Gerontol B Psychol Sci Soc Sci 66(3):364–373PubMedCrossRef
5.
6.
Zurück zum Zitat Lee CS et al (2019) Associations between recent and established ophthalmic conditions and risk of Alzheimer’s disease. Alzheimers Dement 15(1):34–41PubMedCrossRef Lee CS et al (2019) Associations between recent and established ophthalmic conditions and risk of Alzheimer’s disease. Alzheimers Dement 15(1):34–41PubMedCrossRef
7.
Zurück zum Zitat Baker ML et al (2009) Early age-related macular degeneration, cognitive function, and dementia: the cardiovascular health study. Arch Ophthalmol 127(5):667–673PubMedPubMedCentralCrossRef Baker ML et al (2009) Early age-related macular degeneration, cognitive function, and dementia: the cardiovascular health study. Arch Ophthalmol 127(5):667–673PubMedPubMedCentralCrossRef
8.
9.
Zurück zum Zitat Christinaki E et al (2022) Retinal imaging biomarkers of neurodegenerative diseases. Clin Exp Optom 105(2):194–204PubMedCrossRef Christinaki E et al (2022) Retinal imaging biomarkers of neurodegenerative diseases. Clin Exp Optom 105(2):194–204PubMedCrossRef
10.
Zurück zum Zitat Moons L, De Groef L (2022) Multimodal retinal imaging to detect and understand Alzheimer’s and Parkinson’s disease. Curr Opin Neurobiol 72:1–7PubMedCrossRef Moons L, De Groef L (2022) Multimodal retinal imaging to detect and understand Alzheimer’s and Parkinson’s disease. Curr Opin Neurobiol 72:1–7PubMedCrossRef
11.
Zurück zum Zitat Chalkias IN et al (2021) Ocular biomarkers and their role in the early diagnosis of neurocognitive disorders. Eur J Ophthalmol 31(6):2808–2817PubMedCrossRef Chalkias IN et al (2021) Ocular biomarkers and their role in the early diagnosis of neurocognitive disorders. Eur J Ophthalmol 31(6):2808–2817PubMedCrossRef
12.
Zurück zum Zitat Merten N et al (2020) Macular ganglion cell-inner plexiform layer as a marker of cognitive and sensory function in midlife. J Gerontol A Biol Sci Med Sci 75(9):e42–e48PubMedPubMedCentralCrossRef Merten N et al (2020) Macular ganglion cell-inner plexiform layer as a marker of cognitive and sensory function in midlife. J Gerontol A Biol Sci Med Sci 75(9):e42–e48PubMedPubMedCentralCrossRef
15.
Zurück zum Zitat Gotoh Y, Machida S, Tazawa Y (2004) Selective loss of the photopic negative response in patients with optic nerve atrophy. Arch Ophthalmol 122(3):341–346PubMedCrossRef Gotoh Y, Machida S, Tazawa Y (2004) Selective loss of the photopic negative response in patients with optic nerve atrophy. Arch Ophthalmol 122(3):341–346PubMedCrossRef
16.
Zurück zum Zitat Machida S et al (2008) Correlation between photopic negative response and retinal nerve fiber layer thickness and optic disc topography in glaucomatous eyes. Invest Ophthalmol Vis Sci 49(5):2201–2207PubMedCrossRef Machida S et al (2008) Correlation between photopic negative response and retinal nerve fiber layer thickness and optic disc topography in glaucomatous eyes. Invest Ophthalmol Vis Sci 49(5):2201–2207PubMedCrossRef
17.
Zurück zum Zitat Birch DG et al (2002) Quantitative electroretinogram measures of phototransduction in cone and rod photoreceptors: normal aging, progression with disease, and test-retest variability. Arch Ophthalmol 120(8):1045–1051PubMedCrossRef Birch DG et al (2002) Quantitative electroretinogram measures of phototransduction in cone and rod photoreceptors: normal aging, progression with disease, and test-retest variability. Arch Ophthalmol 120(8):1045–1051PubMedCrossRef
18.
Zurück zum Zitat Birch DG, Anderson JL (1992) Standardized full-field electroretinography. Normal values and their variation with age. Arch Ophthalmol 110(11):1571–1576PubMedCrossRef Birch DG, Anderson JL (1992) Standardized full-field electroretinography. Normal values and their variation with age. Arch Ophthalmol 110(11):1571–1576PubMedCrossRef
19.
Zurück zum Zitat Joshi NR, Ly E, Viswanathan S (2017) Intensity response function of the photopic negative response (PhNR): effect of age and test-retest reliability. Doc Ophthalmol 135(1):1–16PubMedPubMedCentralCrossRef Joshi NR, Ly E, Viswanathan S (2017) Intensity response function of the photopic negative response (PhNR): effect of age and test-retest reliability. Doc Ophthalmol 135(1):1–16PubMedPubMedCentralCrossRef
20.
Zurück zum Zitat Neveu MM et al (2011) Electroretinogram measures in a septuagenarian population. Doc Ophthalmol 123(2):75–81PubMedCrossRef Neveu MM et al (2011) Electroretinogram measures in a septuagenarian population. Doc Ophthalmol 123(2):75–81PubMedCrossRef
21.
Zurück zum Zitat Kaeberlein M, Creevy KE, Promislow DE (2016) The dog aging project: translational geroscience in companion animals. Mamm Genome 27(7–8):279–288PubMedPubMedCentralCrossRef Kaeberlein M, Creevy KE, Promislow DE (2016) The dog aging project: translational geroscience in companion animals. Mamm Genome 27(7–8):279–288PubMedPubMedCentralCrossRef
22.
Zurück zum Zitat Mowat FM et al (2008) Topographical characterization of cone photoreceptors and the area centralis of the canine retina. Mol Vis 14:2518–2527PubMedPubMedCentral Mowat FM et al (2008) Topographical characterization of cone photoreceptors and the area centralis of the canine retina. Mol Vis 14:2518–2527PubMedPubMedCentral
23.
Zurück zum Zitat Beltran WA et al (2014) Canine retina has a primate fovea-like bouquet of cone photoreceptors which is affected by inherited macular degenerations. PLoS ONE 9(3):e90390PubMedPubMedCentralCrossRef Beltran WA et al (2014) Canine retina has a primate fovea-like bouquet of cone photoreceptors which is affected by inherited macular degenerations. PLoS ONE 9(3):e90390PubMedPubMedCentralCrossRef
24.
Zurück zum Zitat Urfer SR, Greer K, Wolf NS (2011) Age-related cataract in dogs: a biomarker for life span and its relation to body size. Age 33(3):451–460PubMedCrossRef Urfer SR, Greer K, Wolf NS (2011) Age-related cataract in dogs: a biomarker for life span and its relation to body size. Age 33(3):451–460PubMedCrossRef
25.
Zurück zum Zitat Donzel E, Arti L, Chahory S (2017) Epidemiology and clinical presentation of canine cataracts in France: a retrospective study of 404 cases. Vet Ophthalmol 20(2):131–139PubMedCrossRef Donzel E, Arti L, Chahory S (2017) Epidemiology and clinical presentation of canine cataracts in France: a retrospective study of 404 cases. Vet Ophthalmol 20(2):131–139PubMedCrossRef
27.
Zurück zum Zitat Heywood R, Hepworth PL, Van Abbe NJ (1976) Age changes in the eyes of the beagle dog. J Small Anim Pract 17(3):171–177PubMedCrossRef Heywood R, Hepworth PL, Van Abbe NJ (1976) Age changes in the eyes of the beagle dog. J Small Anim Pract 17(3):171–177PubMedCrossRef
28.
Zurück zum Zitat Panek WK et al (2020) Plasma neurofilament light chain as a translational biomarker of aging and neurodegeneration in dogs. Mol Neurobiol 57(7):3143–3149PubMedPubMedCentralCrossRef Panek WK et al (2020) Plasma neurofilament light chain as a translational biomarker of aging and neurodegeneration in dogs. Mol Neurobiol 57(7):3143–3149PubMedPubMedCentralCrossRef
29.
Zurück zum Zitat Panek WK et al (2021) Plasma amyloid beta concentrations in aged and cognitively impaired pet dogs. Mol Neurobiol 58(2):483–489PubMedCrossRef Panek WK et al (2021) Plasma amyloid beta concentrations in aged and cognitively impaired pet dogs. Mol Neurobiol 58(2):483–489PubMedCrossRef
30.
Zurück zum Zitat Lewczuk P et al (2017) Cerebrospinal fluid Abeta42/40 corresponds better than Abeta42 to amyloid PET in Alzheimer’s disease. J Alzheimers Dis 55(2):813–822PubMedCrossRef Lewczuk P et al (2017) Cerebrospinal fluid Abeta42/40 corresponds better than Abeta42 to amyloid PET in Alzheimer’s disease. J Alzheimers Dis 55(2):813–822PubMedCrossRef
33.
34.
Zurück zum Zitat Snigdha S et al (2012) Age and distraction are determinants of performance on a novel visual search task in aged beagle dogs. Age 34(1):67–73PubMedCrossRef Snigdha S et al (2012) Age and distraction are determinants of performance on a novel visual search task in aged beagle dogs. Age 34(1):67–73PubMedCrossRef
35.
Zurück zum Zitat Studzinski CM et al (2006) Visuospatial function in the beagle dog: an early marker of cognitive decline in a model of human aging and dementia. Neurobiol Learn Mem 86(2):197–204PubMedCrossRef Studzinski CM et al (2006) Visuospatial function in the beagle dog: an early marker of cognitive decline in a model of human aging and dementia. Neurobiol Learn Mem 86(2):197–204PubMedCrossRef
36.
Zurück zum Zitat du PercieSert N et al (2020) The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol 18(7):e3000410CrossRef du PercieSert N et al (2020) The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol 18(7):e3000410CrossRef
37.
Zurück zum Zitat Creevy KE et al (2019) 2019 AAHA canine life stage guidelines. J Am Anim Hosp Assoc 55(6):267–290PubMedCrossRef Creevy KE et al (2019) 2019 AAHA canine life stage guidelines. J Am Anim Hosp Assoc 55(6):267–290PubMedCrossRef
38.
Zurück zum Zitat Ekesten B et al (2013) Guidelines for clinical electroretinography in the dog: 2012 update. Doc Ophthalmol 127(2):79–87PubMedCrossRef Ekesten B et al (2013) Guidelines for clinical electroretinography in the dog: 2012 update. Doc Ophthalmol 127(2):79–87PubMedCrossRef
39.
Zurück zum Zitat Freeman KS et al (2013) Effects of chemical restraint on electroretinograms recorded sequentially in awake, sedated, and anesthetized dogs. Am J Vet Res 74(7):1036–1042PubMedCrossRef Freeman KS et al (2013) Effects of chemical restraint on electroretinograms recorded sequentially in awake, sedated, and anesthetized dogs. Am J Vet Res 74(7):1036–1042PubMedCrossRef
41.
Zurück zum Zitat Birch DG (1989) Clinical electroretinography. In: Fuller DG, Birch DG (eds) Ophthalmology clinics of North America. Assessment of visual function for the clinicians. WB Saunders Co, New York, pp 469–498 Birch DG (1989) Clinical electroretinography. In: Fuller DG, Birch DG (eds) Ophthalmology clinics of North America. Assessment of visual function for the clinicians. WB Saunders Co, New York, pp 469–498
42.
Zurück zum Zitat Mentzer AE et al (2005) Influence of recording electrode type and reference electrode position on the canine electroretinogram. Doc Ophthalmol 111(2):95–106PubMedCrossRef Mentzer AE et al (2005) Influence of recording electrode type and reference electrode position on the canine electroretinogram. Doc Ophthalmol 111(2):95–106PubMedCrossRef
44.
Zurück zum Zitat Passareli J et al (2021) Comparison among TonoVet, TonoVet Plus, Tono-Pen Avia Vet, and Kowa HA-2 portable tonometers for measuring intraocular pressure in dogs. Vet World 14(9):2444–2451PubMedPubMedCentralCrossRef Passareli J et al (2021) Comparison among TonoVet, TonoVet Plus, Tono-Pen Avia Vet, and Kowa HA-2 portable tonometers for measuring intraocular pressure in dogs. Vet World 14(9):2444–2451PubMedPubMedCentralCrossRef
45.
Zurück zum Zitat Weleber RG (1981) The effect of age on human cone and rod ganzfeld electroretinograms. Invest Ophthalmol Vis Sci 20(3):392–399PubMed Weleber RG (1981) The effect of age on human cone and rod ganzfeld electroretinograms. Invest Ophthalmol Vis Sci 20(3):392–399PubMed
47.
Zurück zum Zitat Jorge L et al (2019) Is the retina a mirror of the aging brain? Aging of neural retina layers and primary visual cortex across the lifespan. Front Aging Neurosci 11:360PubMedCrossRef Jorge L et al (2019) Is the retina a mirror of the aging brain? Aging of neural retina layers and primary visual cortex across the lifespan. Front Aging Neurosci 11:360PubMedCrossRef
49.
Zurück zum Zitat Silva MF et al (2021) Simultaneous changes in visual acuity, cortical population receptive field size, visual field map size, and retinal thickness in healthy human aging. Brain Struct Funct 226(9):2839–2853PubMedPubMedCentralCrossRef Silva MF et al (2021) Simultaneous changes in visual acuity, cortical population receptive field size, visual field map size, and retinal thickness in healthy human aging. Brain Struct Funct 226(9):2839–2853PubMedPubMedCentralCrossRef
50.
Zurück zum Zitat Tillman MA, Panorgias A, Werner JS (2016) Age-related change in fast adaptation mechanisms measured with the scotopic full-field ERG. Doc Ophthalmol 132(3):201–212PubMedPubMedCentralCrossRef Tillman MA, Panorgias A, Werner JS (2016) Age-related change in fast adaptation mechanisms measured with the scotopic full-field ERG. Doc Ophthalmol 132(3):201–212PubMedPubMedCentralCrossRef
51.
Zurück zum Zitat Jackson GR et al (2006) Impact of aging and age-related maculopathy on inactivation of the a-wave of the rod-mediated electroretinogram. Vis Res 46(8–9):1422–1431PubMedCrossRef Jackson GR et al (2006) Impact of aging and age-related maculopathy on inactivation of the a-wave of the rod-mediated electroretinogram. Vis Res 46(8–9):1422–1431PubMedCrossRef
52.
Zurück zum Zitat Panorgias A et al (2017) Senescent changes and topography of the dark-adapted multifocal electroretinogram. Invest Ophthalmol Vis Sci 58(2):1323–1329PubMedPubMedCentralCrossRef Panorgias A et al (2017) Senescent changes and topography of the dark-adapted multifocal electroretinogram. Invest Ophthalmol Vis Sci 58(2):1323–1329PubMedPubMedCentralCrossRef
53.
Zurück zum Zitat Paulsen AJ et al (2021) Generational differences in the 10-year incidence of impaired contrast sensitivity. Ophthalmic Epidemiol 28(2):175–182PubMedCrossRef Paulsen AJ et al (2021) Generational differences in the 10-year incidence of impaired contrast sensitivity. Ophthalmic Epidemiol 28(2):175–182PubMedCrossRef
54.
Zurück zum Zitat Varadaraj V et al (2021) Association of vision impairment with cognitive decline across multiple domains in older adults. JAMA Netw Open 4(7):e2117416PubMedPubMedCentralCrossRef Varadaraj V et al (2021) Association of vision impairment with cognitive decline across multiple domains in older adults. JAMA Netw Open 4(7):e2117416PubMedPubMedCentralCrossRef
56.
Zurück zum Zitat Jay AR et al (2013) Pharmacokinetics, bioavailability, and hemodynamic effects of trazodone after intravenous and oral administration of a single dose to dogs. Am J Vet Res 74(11):1450–1456PubMedCrossRef Jay AR et al (2013) Pharmacokinetics, bioavailability, and hemodynamic effects of trazodone after intravenous and oral administration of a single dose to dogs. Am J Vet Res 74(11):1450–1456PubMedCrossRef
57.
Zurück zum Zitat Bossini L et al (2012) Off-label uses of trazodone: a review. Expert Opin Pharmacother 13(12):1707–1717PubMedCrossRef Bossini L et al (2012) Off-label uses of trazodone: a review. Expert Opin Pharmacother 13(12):1707–1717PubMedCrossRef
58.
Zurück zum Zitat Dupanloup A, Osinchuk S (2021) Relationship between the ratio of optic nerve sheath diameter to eyeball transverse diameter and morphological characteristics of dogs. Am J Vet Res 82(8):667–675PubMedCrossRef Dupanloup A, Osinchuk S (2021) Relationship between the ratio of optic nerve sheath diameter to eyeball transverse diameter and morphological characteristics of dogs. Am J Vet Res 82(8):667–675PubMedCrossRef
Metadaten
Titel
Age-associated changes in electroretinography measures in companion dogs
verfasst von
Michele M. Salzman
Natascha Merten
Wojciech K. Panek
Gilad Fefer
Alejandra Mondino
Hans D. Westermeyer
Margaret E. Gruen
Natasha J. Olby
Freya M. Mowat
Publikationsdatum
11.06.2023
Verlag
Springer Berlin Heidelberg
Erschienen in
Documenta Ophthalmologica / Ausgabe 1/2023
Print ISSN: 0012-4486
Elektronische ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-023-09938-7

Neu im Fachgebiet Augenheilkunde

Kompetente Gesprächsführung

Mit schwierigen Gesprächen und der Übermittlung schlechter Nachrichten ist der Augenarzt/die Augenärztin im Krankenhaus und in der Praxis immer wieder konfrontiert. Eine gute Arzt-Patienten-Kommunikation basiert auf Respekt und Empathie und …

Sekundäre chorioidale Neovaskularisation – Wirklich so häufig?

Das Auftreten einer sekundären chorioidalen Neovaskularisation ist eine Komplikation im Rahmen einer chronischen Chorioretinopathia centralis serosa. Die Diagnose wird mittels multimodaler Bildgebung gestellt. Die Therapie erfolgt in der Regel mit …

Therapie der Chorioretinopathia centralis serosa im Vergleich – Mikrosekundenpulslaser versus photodynamische Therapie

Zum gegenwärtigen Zeitpunkt steht für die Behandlung der Chorioretinopathia centralis serosa (CCS) keine zugelassene Therapie zur Verfügung. Obwohl die CCS eine hohe Selbstresorptionsrate aufweist, können häufige Rezidive oder eine Chronifizierung …

Diagnostik und Klassifikation der Chorioretinopathia centralis serosa – Was brauche ich wirklich?

Die multimodale Bildgebung spielt bei der Diagnostik und Klassifikation der Chorioretinopathia centralis serosa (CCS) eine bedeutende Rolle. In diesem Beitrag sollen die wichtigsten Bildgebungsmodalitäten bei der CCS wie optische …

Update Augenheilkunde

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.