Abstract
Purpose
To investigate the relationship between subjective cyclofusion ranges and objective ocular torsion in normal participants according to age.
Methods
This cross-sectional study included 120 participants aged ≥ 20 years with no ocular diseases. The subjective cyclofusion ranges were measured centrifugally and centripetally in the direction of excyclotorsion and incyclotorsion, respectively, concurrently with rotational diplopia production by rotation using synoptophore. Disc fovea angle (DFA) was defined as the angle formed by two lines: a line passing through the center of the optic nerve papilla and fovea and a horizontal line passing through the center of gravity of the optic papilla using fundus photographs.
Results
The participants were aged 49.1 ± 17.7 years. The total cyclofusion centrifugal (sum of extorsion and intorsion) and centripetal ranges were 10.9 ± 2.2° and 7.2 ± 1.8°, respectively, both of which decreased in participants in their 60 s and 70 s (p < 0.01). The DFA was − 7.0 ± 3.4° in the right eye (− : excyclo, + : incyclo) and − 8.0 ± 3.2° in the left, which was associated with age (p < 0.001). The correlation between the DFA and centrifugal (r = − 0.13, p = 0.16) and centripetal (r = − 0.002, p = 0.99) cyclofusion ranges of extorsion was not significantly different. The centrifugal (r = 0.37, p < 0.001) and centripetal (r = 0.40, p < 0.001) cyclofusion ranges of intorsion were positively correlated.
Conclusion
Subjective cyclofusion ranges decreased in both extorsion and intorsion in the elderly. Objective ocular torsion showed excyclotorsion with age. When strabismus surgery is performed in elderly patients with torsional strabismus, the decrease in subjective cyclofusion ranges should be considered.
Similar content being viewed by others
Data availability
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.
References
Guyton DL (2008) Ocular torsion reveals the mechanisms of cyclovertical strabismus The Weisenfeld Lecture. Invest Ophthalmol Vis Sci 49(3):847. https://doi.org/10.1167/iovs.07-0739
von Noorden GK, Murray E, Wong SY (1986) Superior oblique paralysis. Arch Ophthalmol 104(12):1771. https://doi.org/10.1001/archopht.1986.01050240045037
Kraft SP, O’Reilly C, Quigley PL, Allan K, Eustis HS (1993) Cyclotorsion in unilateral and bilateral superior oblique paresis. J Pediatr Ophthalmol Strabismus 30(6):361–367. https://doi.org/10.3928/0191-3913-19931101-05
Kushner BJ (1985) The role of ocular torsion on the etiology of A and V patterns. J Pediatr Ophthalmol Strabismus 22(5):171–179. https://doi.org/10.3928/0191-3913-19850901-04
Deng H, Irsch K, Gutmark R, Phamonvaechavan P, Foo FY, Anwar DS, Guyton D (2013) Fusion can mask the relationships between fundus torsion, oblique muscle overaction/underaction, and A- and V-pattern strabismus. J AAPOS 17(2):177–183. https://doi.org/10.1016/j.jaapos.2012.10.023
Shin KH, Lee HJ, Lim HT (2013) Ocular torsion among patients with intermittent exotropia: relationships with disease severity factors. Am J Ophthalmol 155(1):177–182. https://doi.org/10.1016/j.ajo.2012.07.011
Rutar T, Demer JL (2009) “Heavy Eye” syndrome in the absence of high myopia: a connective tissue degeneration in elderly strabismic patients. J AAPOS 13(1):36–44. https://doi.org/10.1016/j.jaapos.2008.07.008
Chaudhuri Z, Demer JL (2013) Sagging eye syndrome. JAMA Ophthalmol 131(5):619. https://doi.org/10.1001/jamaophthalmol.2013.783
Goseki T (2021) Sagging eye syndrome. Jpn J Ophthalmol 65(4):448–453. https://doi.org/10.1007/s10384-021-00839-3
Kawai M, Goseki T, Ishikawa H, Hoshina M, Shoji N (2018) Causes, background, and characteristics of binocular diplopia in the elderly. Jpn J Ophthalmol 62(6):659–666. https://doi.org/10.1007/s10384-018-0617-2
Goseki T, Suh SY, Robbins L, Pineles SL, Velez FG, Demer JL (2020) Prevalence of sagging eye syndrome in adults with binocular diplopia. Am J Ophthalmol 209:55–61. https://doi.org/10.1016/j.ajo.2019.09.006
Harada M (1964) Surgical correction of cyclotropia. Jpn J Ophthalmol 8:88–96
Von Noorden GK (1969) Strabismus. Arch Ophthalmol (Chicago, Ill.: 1960) 82(3):393–414. https://doi.org/10.1001/archopht.1969.00990020395019
Helveston EM, Mora JS, Lipsky SN, Plager DA, Sprunger DT et al (1996) Surgical treatment of superior oblique palsy. Trans Am Ophthalmol Soc 123(3):436–437. https://doi.org/10.1016/s0002-9394(14)70166-7
von Noorden G, Jenkins RH, Chu MW (1996) horizontal transposition of the vertical rectus muscles for cyclotropia. Am J Ophthalmol 122(3):325–330. https://doi.org/10.1016/s0002-9394(14)72058-6
Flodin S, Pansell T, Rydberg A, Andersson Grönlund M (2019) Clinical measurements of normative subjective cyclotorsion and cyclofusion in a healthy adult population. Acta Ophthalmol 98(2):177–181. https://doi.org/10.1111/aos.14201
Arici C, Oguz V (2012) The effect of surgical treatment of superior oblique muscle palsy on ocular torsion. J AAPOS 16(1):21–25. https://doi.org/10.1016/j.jaapos.2011.09.015
Khanna RK, Pasco J, Santallier M, Pisella PJ, Arsene S (2018) Objective ocular torsion outcomes after unilateral horizontal rectus surgery in infantile esotropia. Graefes Arch Clin Exp Ophthalmol 256(9):1783–1788. https://doi.org/10.1007/s00417-018-4027-4
Bixenman WW, Von Noorden GK (1982) Apparent foveal displacement in normal subjects and in cyclotropia. Ophthalmology 89(1):58–62. https://doi.org/10.1016/s0161-6420(82)34862-9
Rohrschneider K (2004) Determination of the location of the fovea on the fundus. Invest Ophthalmol Vis Sci 45(9):3257. https://doi.org/10.1167/iovs.03-1157
Jonas RA, Wang YX, Yang H, Li JJ, Xu L, Panda-Jonas S, Jonas J (2015) Optic disc - fovea angle: the Beijing Eye Study 2011. PLoS ONE 10(11):e0141771. https://doi.org/10.1371/journal.pone.0141771
Miyata M, Yoshikawa M, Ohtsuki H, Muraoka Y, Hata M, Yokota S et al (2018) Age‐related change and sex difference over 60s in disc‐fovea angle in Japanese population: the Nagahama Study. Acta Ophthalmol 96(7). https://doi.org/10.1111/aos.13642
Sen DK, Singh B, Mathur GP (1980) Torsional fusional vergences and assessment of cyclodeviation by synoptophore method. Br J Ophthalmol 64(5):354–357. https://doi.org/10.1136/bjo.64.5.354
Sharma P, Prasad K, Khokhar S (1999) Cyclofusion in normal and superior oblique palsy subjects. J Pediatr Ophthalmol Strabismus 36(5):264–270. https://doi.org/10.3928/0191-3913-19990901-07
Palomo Álvarez C, Puell MC, Sánchez-Ramos C, Villena C (2005) Normal values of distance heterophoria and fusional vergence ranges and effects of age. Graefes Arch Clin Exp Ophthalmol 244(7):821–824. https://doi.org/10.1007/s00417-005-0166-5
McKelvie P, Friling R, Davey K, Kowal L (1999) Changes as the result of ageing in extraocular muscles: a post-mortem study. Aust N Z J Ophthalmol 27(6):420–425. https://doi.org/10.1046/j.1440-1606.1999.00244.x
Lefèvre F, Leroy K, Delrieu B, Lassale D, Péchereau A (2007) Étude des rapports papille-fovéa par rétinophotographie chez le patient sain. J Fr Ophtalmol 30(6):598–606. https://doi.org/10.1016/s0181-5512(07)89664-1
Jethani J, Seethapathy G, Purohit J, Shah D (2010) Measuring normal ocular torsion and its variation by fundus photography in children between 5–15 years of age. Indian J Ophthalmol 58(5):417. https://doi.org/10.4103/0301-4738.67060
Pekel G, Acer S, Özbakis F, Yagci R, Sayin N (2014) Macular asymmetry analysis in sighting ocular dominance. Kaohsiung J Med Sci 30(10):531–536. https://doi.org/10.1016/j.kjms.2014.08.003
Demer JL, Kono R, Wright W (2003) Magnetic resonance imaging of human extraocular muscles in convergence. J Neurophysiol 89(4):2072–2085. https://doi.org/10.1152/jn.00636.2002
Kawai M, Goseki T, Ishikawa H, Tatsui S, Shoji N (2020) Standard coronal orbital magnetic resonance imaging is an effective technique for diagnosing sagging eye syndrome. Graefes Arch Clin Exp Ophthalmol 258(9):1983–1989. https://doi.org/10.1007/s00417-020-04718-4
Guyton DL (1988) Ocular torsion: sensorimotor principles. Graefes Arch Clin Exp Ophthalmol 226(3):241–245. https://doi.org/10.1007/BF02181189
Kertesz AE, Sullivan MJ (1978) The effect of stimulus size on human cyclofusional response. Vision Res 18(5):567–571. https://doi.org/10.1016/0042-6989(78)90204-3
Lança CC, Rowe FJ (2019) Measurement of fusional vergence: a systematic review. Strabismus 27(2):88–113. https://doi.org/10.1080/09273972.2019.1583675
Georgievski Z, Sleep M, Koklanis K (2007) Simulated torsional disparity disrupts horizontal fusion and stereopsis. J AAPOS 11(2):120–124. https://doi.org/10.1016/j.jaapos.2006.09.022
Miyata M, Hasebe S, Ohtsuki H, Sato M (2005) Assessment of cyclodisparity-induced slant perception with a synoptophore. Jpn J Ophthalmol 49(2):137–142. https://doi.org/10.1007/s10384-004-0158-8
Chaudhuri Z, Demer JL (2018) Long-term surgical outcomes in the sagging eye syndrome. Strabismus 26(1):6–10. https://doi.org/10.1080/09273972.2017.1421676
Van Rijn LJ, Van Der Steen J, Collewijn H (1994) Instability of ocular torsion during fixation: cyclovergence is more stable than cycloversion. Vision Res 34(8):1077–1087. https://doi.org/10.1016/0042-6989(94)90011-6
Taylor MJ, Roberts DC, Zee DS (2000) Effect of sustained cyclovergence on eye alignment: rapid torsional phoria adaptation. Invest Ophthalmol Vis Sci 41(5):1076–1083
Acknowledgements
We would like to thank Editage (www.editage.com) for English language editing.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Manami Kawai. The first draft of the manuscript was written by Manami Kawai, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
This research received approval from the ethics review board of Kitasato University School of Medical and Health Sciences (2021–010).
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Consent for publication
Patients signed informed consent regarding publishing their data.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kawai, M., Goseki, T., Okano, T. et al. Comparison of subjective cyclofusion ranges and objective ocular torsion in normal participants according to age. Graefes Arch Clin Exp Ophthalmol 260, 3675–3681 (2022). https://doi.org/10.1007/s00417-022-05734-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00417-022-05734-2