Abstract
Purpose
To describe the pattern of quantitative parasympathetic cardiovascular autonomic function among patients with normal-tension glaucoma (NTG) and high-tension primary open-angle glaucoma (HTG) patients.
Methodology
This was cross-sectional study of ninety-two subjects enrolled into three groups: HTG (31 patients), NTG (31 patients) and Control (30 patients). All the participants had anthropometric assessment, ophthalmic examination, baseline cardiovascular examination and the three parasympathetic components of Ewing’s battery of autonomic cardiovascular function tests namely heart rate (HR) response to deep breathing, HR response to Valsalva manoeuvre and HR response to standing.
Result
The baseline PR intervals were significantly prolonged in HTG (0.18 ± 0.03 s) and NTG (0.18 ± 0.04 s) groups compared with control (0.15 ± 0.03 s) (p = 0.008). The HTG group had a significantly longer mean RR interval (1.09 ± 0.17 s) than the NTG group (1.03 ± 0.20 s) and control (0.97 ± 0.17 s) during the expiratory phase of the HR response to deep breathing test (p = 0.037). The HTG group also had significantly longer mean RR intervals around the 15th beat (p = 0.033) and 30th beats (p = 0.202) post-standing during the HR response to standing test. The HR response to Valsalva manoeuvre test showed a significantly higher mean Valsalva ratio in the NTG group (1.65 ± 0.48) compared to the HTG group (1.45 ± 0.31) and control (1.43 ± 0.25) (p = 0.034).
Conclusion
This study demonstrated that normal-tension and high-tension primary open-angle glaucoma have higher parasympathetic cardiovascular activity than normal individuals.
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Data availability
This has been deposited in a data repository. https://data.mendeley.com/datasets/hv23rs8xg6/draft?a=f288d643-b893-4c26-bc5c-7bdccb045b90.
References
Tham YC, Li X, Wong TY et al (2014) Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology 121:2081–2090. https://doi.org/10.1016/j.ophtha.2014.05.013
Anderson DR (2011) Normal-tension glaucoma (Low-tension glaucoma). Indian J Ophthalmol 59(Suppl 1):S97–S101. https://doi.org/10.4103/0301-4738.73695
Chan TCW, Bala C, Siu A et al (2017) Risk factors for rapid glaucoma disease progression. Am J Ophthalmol. https://doi.org/10.1016/j.ajo.2017.06.003
Gibbons CH, Cheshire WP, Fife TD (2014) Model coverage policy: autonomic testing. American Academy of Neurology
McDougal DH, Gamlin PD (2015) Autonomic control of the eye. Compr Physiol 5:439–473. https://doi.org/10.1002/cphy.c140014.Autonomic
Riva CE, Titze P, Hero M et al (1997) Choroidal blood flow during isometric exercises. Investig Ophthalmol Vis Sci 38:2338–2343
Choi J, Jeong J, Cho HS, Kook MS (2006) Effect of nocturnal blood pressure reduction on circadian fluctuation of mean ocular perfusion pressure: a risk factor for normal tension glaucoma. Investig Ophthalmol Vis Sci 47:831–836. https://doi.org/10.1167/iovs.05-1053
Quill B, Henry E, Simon E, Brien CJO (2015) Evaluation of the effect of hypercapnia on vascular function in normal tension glaucoma. Biomed Res Int 2015:1–11
Gherghel D, Orgül S, Dubler B et al (1999) Is vascular regulation in the central retinal artery altered in persons with vasospasm? Arch Ophthalmol 117:1359–1362
Emre M, Orgül S, Gugleta K, Flammer J (2004) Ocular blood flow alteration in glaucoma is related to systemic vascular dysregulation. Br J Ophthalmol 88:662–666. https://doi.org/10.1136/bjo.2003.032110
Banerjee A, Khurana I (2017) Altered autonomic balance in normal tension glaucoma. Asian J Pharm Clin Res 10:6–8
Kurysheva NI, Shlapak VN, Ryabova TY (2018) Heart rate variability in normal tension glaucoma. Medicine (Baltimore) 97:e9744. https://doi.org/10.1097/MD.0000000000009744
Gasser P, Flammer J (1991) Blood-cell velocity in the nailfold capillaries of patients with normal-tension and high-tension glaucoma. Am J Ophthalmol 111:585–588. https://doi.org/10.1016/S0002-9394(14)73703-1
Ewing D, Campbell I, Clarke B (1980) Assessment of cardiovascular effects in diabetic autonomic neuropathy and prognostic implications. Ann Intern Med 92:308–311
Mafwiri M, Bowman RJC, Wood M, Kabiru J (2005) Primary open-angle glaucoma presentation at a tertiary unit in Africa: intraocular pressure levels and visual status. Ophthalmic Epidemiol 12:299–302. https://doi.org/10.1080/09286580500180572
Abdull MM, Gilbert CC, Evans J (2015) Primary open angle glaucoma in northern Nigeria: stage at presentation and acceptance of treatment. BMC Ophthalmol 15:111. https://doi.org/10.1186/s12886-015-0097-9
Olajide O, Onabolu O, Jagun O et al (2017) Spectrum of glaucoma presentation in a suburban teaching hospital in South Western Nigeria. Heal Sci J 10:1–4. https://doi.org/10.21767/1791-809X.1000466
Olawoye O, Tarella S (2018) Spectrum of glaucoma presentation in a Nigerian Tertiary Hospital. Niger J Ophthalmol 22:1–15. https://doi.org/10.4103/0189-9171.142747
Ajite KO, Fadamiro CO, Ajayi IA et al (2016) Demographic characteristics of normal tension glaucoma seen in a suburban tertiary hospital. Int J Ophthalmol Eye Sci 4:215–219. https://doi.org/10.19070/2332-290X-1600044
Majeed F, Tauheed S, Aamir IS et al (2007) Frequency of normal-tension glaucoma in suspected cases of primary open angle glaucoma. Pak J Ophthalmol 23:192–197
Riccadonna M, Covi G, Pancera P et al (2003) Autonomic system activity and 24-hour blood pressure variations in subjects with normal- and high-tension glaucoma. J Glaucoma 12:156–163. https://doi.org/10.1097/00061198-200304000-00011
Nieminen T, Lehtimäki T, Mäenpää J et al (2007) Ophthalmic timolol: plasma concentration and systemic cardiopulmonary effects. Scand J Clin Lab Invest 67:237–245. https://doi.org/10.1080/00365510601034736
Farkouh A, Frigo P, Czejka M (2016) Systemic side effects of eye drops: a pharmacokinetic perspective. Clin Ophthalmol 10:2433–2441. https://doi.org/10.2147/OPTH.S118409
Stewart WC, Stewart JA, Jackson AL (2002) Cardiovascular effects of timolol maleate, brimonidine or brimonidine/timolol maleate in concomitant therapy. Acta Ophthalmol Scand 80:277–281. https://doi.org/10.1034/j.1600-0420.2002.800309.x
Mancia G, Grassi G (2014) The autonomic nervous system and hypertension. Circ Res 114:1804–1814. https://doi.org/10.1161/CIRCRESAHA.114.302524
Gherghel D, Hosking SL, Armstrong R, Cunliffe IA (2007) Autonomic dysfunction in unselected and untreated primary open angle glaucoma patients: a pilot study. Ophthalmic Physiol Opt 27:336–341. https://doi.org/10.1111/j.1475-1313.2007.00485.x
Wierzbowska J, Wierzbowski R, Wierzbowska J et al (2012) Cardiac autonomic dysfunction in patients with normal tension glaucoma: 24-h heart rate and blood pressure variability analysis. Br J Ophthalmol 96:624–628. https://doi.org/10.1136/bjophthalmol-2011-300945
Mroczkowska S, Benavente-Perez A, Negi A et al (2013) Primary open-angle glaucoma vs normal-tension glaucoma: the vascular perspective. JAMA Ophthalmol 131:36–43. https://doi.org/10.1001/2013.jamaophthalmol.1
Grassi G (2016) Sympathomodulatory effects of antihypertensive drug treatment. Am J Hypertens 29:665–675. https://doi.org/10.1093/ajh/hpw012
Grassi G (2000) Sympathoexcitatory responses to the acute blood pressure fall induced by central or peripheral antihypertensive drugs. Am J Hypertens 13:29–34. https://doi.org/10.1016/S0895-7061(99)00150-8
Mapstone R, Clark CV (1985) The prevalence of autonomic neuropathy in glaucoma. Trans Ophthalmol Soc U K 104:265–269
Bojić L, Čagalj S, Račić G, Karaman-Kraljević K (1993) Cardiovascular reflex testing and pupil cycle time in open-angle glaucoma. Ophthalmologica 206:158–161. https://doi.org/10.1159/000310383
Khan MM, Ghosh S, Bera C (2015) Study of autonomic activities in primary open angle glaucoma. J Evol Med Dent Sci 4:16865–16870. https://doi.org/10.14260/jemds/2015/2536
Ewing DJ, Burt AA, Campbell IW, Clarke BF (1973) Vascular reflexes in diabetic autonomic neuropathy. Lancet 302:1354–1356. https://doi.org/10.1016/S0140-6736(73)93323-0
Ogunlade O, Ayoka AO, Akintomide A et al (2015) Non-invasive assessment of cardiac autonomic functions in healthy young adults in Ile-Ife, South-Western Nigeria. Int J Clin Cardiol 2:036
Khan JC (2002) Pulsatile ocular blood flow: the effect of the Valsalva manoeuvre in open angle and normal tension glaucoma: a case report and prospective study. Br J Ophthalmol 86:1089–1092. https://doi.org/10.1136/bjo.86.10.1089
Begum S, Razak A (2015) Valsalva ratio: a measure of stress in first year medical students. Int J Res Med Sci 3:1599–1604
Schuman JS, Massicotte EC, Connolly S et al (2000) Increased intraocular pressure and visual field defects in high resistance wind instrument players. Ophthalmology 107:127–133
Bussel II, Aref AA (2014) Dietary factors and the risk of glaucoma: a review. Ther Adv Chronic Dis 5:188–194. https://doi.org/10.1177/2040622314530181
Krist D, Cursiefen C, Jünemann A (2001) Transient intrathoracic and abdominal pressure elevation in the history of 64 patients with normal-tension glaucoma. Klin Monbl Augenheilkd 218:209–213. https://doi.org/10.1055/s-2001-14915
Wong-Riley M (2010) Energy metabolism of the visual system. Eye Brain 2:99–116
Morgan JE (2004) Circulation and axonal transport in the optic nerve. Eye 18:1089–1095. https://doi.org/10.1038/sj.eye.6701574
Palamar M, Dag MY, Yagci A (2015) The effects of valsalva manoeuvre on ocular response analyzer measurements. Clin Exp Optom 98:447–450. https://doi.org/10.1111/cxo.12303
van Meurs JC, van den Bosch WA (1993) Suprachoroidal hemorrhage following a valsalva maneuver. Arch Ophthalmol 111:1025–1026
Vieira GM, Oliveira HB, De Andrade DT et al (2006) Intraocular pressure variation during weight lifting. Arch Ophthalmol 124:1251–1254. https://doi.org/10.1001/archopht.124.9.1251
Macey PM, Kumar R, Woo MA et al (2013) Heart rate responses to autonomic challenges in obstructive sleep apnea. PLoS ONE 8:e76631. https://doi.org/10.1371/journal.pone.0076631
Flammer J, Mozaffarieh M (2008) Autoregulation, a balancing act between supply and demand. Can J Ophthalmol 43:317–321. https://doi.org/10.3129/i08-056
Collignon N, Dewe W, Guillaume S, Collignon-Brach J (1998) Ambulatory blood pressure monitoring in glaucoma patients. The nocturnal systolic dip and its relationship with disease progression. Int Ophthalmol 22:19–25. https://doi.org/10.1023/A:1006113109864
Leffler CT, Saul JP, Cohen RJ (1994) Rate-related and autonomic effects on atrioventricular conduction assessed through beat-to-beat PR interval and cycle length variahility. J Cardivascular Electrophysiol 5:2–15
Sheridan E, Heneghan C, O’Malley MO, et al (2001) Characterization of autonomic nervous influences on PR and RR intervals in the electrocardiogram. In: 23rd Annual international conference of the IEEE engineering in medicine and biology society, pp 540–543
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Approval was obtained from the Ethics and Research Committee of Obafemi Awolowo University Teaching Hospital, Ile-Ife, Nigeria (OAUTHC/ERC/2017/12/01), and the study was therefore performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All participants gave their informed consent prior to their inclusion in the study.
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Awe, O.O., Ogundare, O. & Adegbehingbe, B.O. Assessment of parasympathetic cardiovascular activity in primary open-angle glaucoma. Int Ophthalmol 42, 1111–1119 (2022). https://doi.org/10.1007/s10792-021-02097-1
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DOI: https://doi.org/10.1007/s10792-021-02097-1