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The association between ophthalmologic diseases and obstructive sleep apnea: a systematic review and meta-analysis

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Abstract

Purpose

The purpose of this study was to evaluate the association between obstructive sleep apnea (OSA) and ophthalmologic diseases, specifically glaucoma, nonarteritic anterior ischemic optic neuropathy (NAION), retinal vein occlusion (RVO), central serous chorioretinopathy (CSR), and floppy eyelid syndrome (FES), by performing a systematic review and meta-analysis of published studies.

Methods

PubMed, Embase, and Scopus databases were searched for observational studies on OSA and its association with select ophthalmologic diseases. Data was pooled for random-effects modeling. The association between OSA and ophthalmologic diseases was summarized using an estimated pooled odds ratio with a 95 % confidence interval.

Results

Relative to non-OSA subjects, OSA subjects have increased odds of diagnosis with glaucoma (pooled odds ratio (OR) = 1.242; P < 0.001) and floppy eyelids syndrome (pooled OR = 4.157; P < 0.001). In reverse, the overall pooled OR for OSA was 1.746 (P = 0.002) in the glaucoma group, 3.126 (P = 0.000) in the NAION group, and 2.019 (P = 0.028) in the CSR group. For RVO, one study with 5965 OSA patients and 29,669 controls demonstrated a 1.94-fold odds increase in OSA patients.

Conclusions

Our results suggest significant associations between OSA and glaucoma, NAION, CSR, and FES. Screening for OSA should be considered in patients with glaucoma, NAION, CSR, or FES.

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References

  1. Golbidi S, Badran M, Ayas N, Laher I (2012) Cardiovascular consequences of sleep apnea. Lung 190(2):113–132. doi:10.1007/s00408-011-9340-1

    Article  PubMed  Google Scholar 

  2. Kato M, Roberts-Thomson P, Phillips BG, Haynes WG, Winnicki M, Accurso V, Somers VK (2000) Impairment of endothelium-dependent vasodilation of resistance vessels in patients with obstructive sleep apnea. Circulation 102(21):2607–2610

    Article  CAS  PubMed  Google Scholar 

  3. Urbano F, Roux F, Schindler J, Mohsenin V (2008) Impaired cerebral autoregulation in obstructive sleep apnea. J Appl Physiol 105(6):1852–1857. doi:10.1152/japplphysiol.90900.2008

    Article  PubMed  Google Scholar 

  4. Nasr N, Traon AP, Czosnyka M, Tiberge M, Schmidt E, Larrue V (2009) Cerebral autoregulation in patients with obstructive sleep apnea syndrome during wakefulness. Eur J Neurol Off J Eur Fed Neurol Soc 16(3):386–391. doi:10.1111/j.1468-1331.2008.02505.x

    CAS  Google Scholar 

  5. Nieto FJ, Young TB, Lind BK, Shahar E, Samet JM, Redline S, D’Agostino RB, Newman AB, Lebowitz MD, Pickering TG (2000) Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study. Sleep Heart Health Study. JAMA 283(14):1829–1836

    Article  CAS  PubMed  Google Scholar 

  6. Peppard PE, Young T, Palta M, Skatrud J (2000) Prospective study of the association between sleep-disordered breathing and hypertension. N Engl J Med 342(19):1378–1384. doi:10.1056/NEJM200005113421901

    Article  CAS  PubMed  Google Scholar 

  7. Shahar E, Whitney CW, Redline S, Lee ET, Newman AB, Nieto FJ, O’Connor GT, Boland LL, Schwartz JE, Samet JM (2001) Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med 163(1):19–25. doi:10.1164/ajrccm.163.1.2001008

    Article  CAS  PubMed  Google Scholar 

  8. Arzt M, Young T, Finn L, Skatrud JB, Bradley TD (2005) Association of sleep-disordered breathing and the occurrence of stroke. Am J Respir Crit Care Med 172(11):1447–1451. doi:10.1164/rccm.200505-702OC

    Article  PubMed  PubMed Central  Google Scholar 

  9. Jimenez Caballero PE, Coloma Navarro R, Ayo Martin O, Segura Martin T (2013) Cerebral hemodynamic changes in obstructive sleep apnea syndrome after continuous positive airway pressure treatment. Sleep Breath = Schlaf & Atmung 17(3):1103–1108. doi:10.1007/s11325-013-0810-y

    Article  Google Scholar 

  10. Stein JD, Kim DS, Mundy KM, Talwar N, Nan B, Chervin RD, Musch DC (2011) The association between glaucomatous and other causes of optic neuropathy and sleep apnea. Am J Ophthalmol 152(6):989–998 . doi:10.1016/j.ajo.2011.04.030e983

    Article  PubMed  PubMed Central  Google Scholar 

  11. Chou KT, Huang CC, Tsai DC, Chen YM, Perng DW, Shiao GM, Lee YC, Leu HB (2012) Sleep apnea and risk of retinal vein occlusion: a nationwide population-based study of Taiwanese. Am J Ophthalmol 154(1):200–205 . doi:10.1016/j.ajo.2012.01.011e201

    Article  PubMed  Google Scholar 

  12. Delaey C, Van De Voorde J (2000) Regulatory mechanisms in the retinal and choroidal circulation. Ophthalmic Res 32(6):249–256

    Article  CAS  PubMed  Google Scholar 

  13. Papst N, Demant E, Niemeyer G (1982) Changes in pO2 induce retinal autoregulation in vitro. Graefes Arch Clin Exp Ophthalmol 219(1):6–10

    Article  CAS  PubMed  Google Scholar 

  14. Stefansson E, Pedersen DB, Jensen PK, la Cour M, Kiilgaard JF, Bang K, Eysteinsson T (2005) Optic nerve oxygenation. Prog Retin Eye Res 24(3):307–332. doi:10.1016/j.preteyeres.2004.09.001

    Article  CAS  PubMed  Google Scholar 

  15. Orgul S, Gugleta K, Flammer J (1999) Physiology of perfusion as it relates to the optic nerve head. Surv Ophthalmol 43(Suppl 1):S17–S26

    Article  PubMed  Google Scholar 

  16. Hayreh SS (2001) The blood supply of the optic nerve head and the evaluation of it—myth and reality. Prog Retin Eye Res 20(5):563–593

    Article  CAS  PubMed  Google Scholar 

  17. Moghimi S, Ahmadraji A, Sotoodeh H, Sadeghniat K, Maghsoudipour M, Fakhraie G, Latifi G, Nassiri N, Giaconi JA (2013) Retinal nerve fiber thickness is reduced in sleep apnea syndrome. Sleep Med 14(1):53–57. doi:10.1016/j.sleep.2012.07.004

    Article  PubMed  Google Scholar 

  18. Xin C, Wang J, Zhang W, Wang L, Peng X (2014) Retinal and choroidal thickness evaluation by SD-OCT in adults with obstructive sleep apnea-hypopnea syndrome (OSAS). Eye (Lond) 28(4):415–421. doi:10.1038/eye.2013.307

    Article  CAS  Google Scholar 

  19. Casas P, Ascaso FJ, Vicente E, Tejero-Garces G, Adiego MI, Cristobal JA (2013) Retinal and optic nerve evaluation by optical coherence tomography in adults with obstructive sleep apnea-hypopnea syndrome (OSAHS). Graefes Arch Clin Exp Ophthalmol 251(6):1625–1634. doi:10.1007/s00417-013-2268-9

    Article  PubMed  Google Scholar 

  20. Zengin MO, Tuncer I, Karahan E (2014) Retinal nerve fiber layer thickness changes in obstructive sleep apnea syndrome: one year follow-up results. Int J Ophthalmol 7(4):704–708. doi:10.3980/j.issn.2222-3959.2014.04.22

    PubMed  PubMed Central  Google Scholar 

  21. Bayhan HA, Aslan Bayhan S, Intepe YS, Muhafiz E, Gurdal C (2015) Evaluation of the macular choroidal thickness using spectral optical coherence tomography in patients with obstructive sleep apnoea syndrome. Clin Exp Ophthalmol 43(2):139–144. doi:10.1111/ceo.12384

    Article  PubMed  Google Scholar 

  22. Shiba T, Takahashi M, Sato Y, Onoda Y, Hori Y, Sugiyama T, Bujo H, Maeno T (2014) Relationship between severity of obstructive sleep apnea syndrome and retinal nerve fiber layer thickness. Am J Ophthalmol 157(6):1202–1208. doi:10.1016/j.ajo.2014.01.028

    Article  PubMed  Google Scholar 

  23. Onen SH, Mouriaux F, Berramdane L, Dascotte JC, Kulik JF, Rouland JF (2000) High prevalence of sleep-disordered breathing in patients with primary open-angle glaucoma. Acta Ophthalmol Scand 78(6):638–641

    Article  CAS  PubMed  Google Scholar 

  24. Marcus DM, Costarides AP, Gokhale P, Papastergiou G, Miller JJ, Johnson MH, Chaudhary BA (2001) Sleep disorders: a risk factor for normal-tension glaucoma? J Glaucoma 10(3):177–183

    Article  CAS  PubMed  Google Scholar 

  25. Girkin CA, McGwin G Jr, McNeal SF, Owsley C (2006) Is there an association between pre-existing sleep apnoea and the development of glaucoma? Br J Ophthalmol 90(6):679–681. doi:10.1136/bjo.2005.086082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Roberts TV, Hodge C, Graham SL, Burlutsky G, Mitchell P (2009) Prevalence of nocturnal oxygen desaturation and self-reported sleep-disordered breathing in glaucoma. J Glaucoma 18(2):114–118. doi:10.1097/IJG.0b013e318179f80c

    Article  PubMed  Google Scholar 

  27. Khandgave TP, Puthran N, Ingole AB, Nicholson AD (2013) The assessment of sleep apnoea as a risk factor in glaucoma. J Clin Diagn Res 7(7):1391–1393. doi:10.7860/JCDR/2013/5383.3147

    PubMed  PubMed Central  Google Scholar 

  28. Bilgin G (2014) Normal-tension glaucoma and obstructive sleep apnea syndrome: a prospective study. BMC Ophthalmol 14:27. doi:10.1186/1471-2415-14-27

    Article  PubMed  PubMed Central  Google Scholar 

  29. Johnson LN, Arnold AC (1994) Incidence of nonarteritic and arteritic anterior ischemic optic neuropathy. Population-based study in the state of Missouri and Los Angeles County, California. J Neuroophthalmol 14(1):38–44

    Article  CAS  PubMed  Google Scholar 

  30. Hattenhauer MG, Leavitt JA, Hodge DO, Grill R, Gray DT (1997) Incidence of nonarteritic anterior ischemic optic neuropathy. Am J Ophthalmol 123(1):103–107

    Article  CAS  PubMed  Google Scholar 

  31. Mojon DS, Hedges TR 3rd, Ehrenberg B, Karam EZ, Goldblum D, Abou-Chebl A, Gugger M, Mathis J (2002) Association between sleep apnea syndrome and nonarteritic anterior ischemic optic neuropathy. Arch Ophthalmol 120(5):601–605

    Article  PubMed  Google Scholar 

  32. Palombi K, Renard E, Levy P, Chiquet C, Deschaux C, Romanet JP, Pepin JL (2006) Non-arteritic anterior ischaemic optic neuropathy is nearly systematically associated with obstructive sleep apnoea. Br J Ophthalmol 90(7):879–882. doi:10.1136/bjo.2005.087452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Li J, McGwin G Jr, Vaphiades MS, Owsley C (2007) Non-arteritic anterior ischaemic optic neuropathy and presumed sleep apnoea syndrome screened by the Sleep Apnea scale of the Sleep Disorders Questionnaire (SA-SDQ). Br J Ophthalmol 91(11):1524–1527. doi:10.1136/bjo.2006.113803

    Article  PubMed  PubMed Central  Google Scholar 

  34. Bilgin G, Koban Y, Arnold AC (2013) Nonarteritic anterior ischemic optic neuropathy and obstructive sleep apnea. J Neuroophthalmol 33(3):232–234. doi:10.1097/WNO.0b013e31828eecbd

    Article  PubMed  Google Scholar 

  35. Arda H, Birer S, Aksu M, Ismailogullari S, Karakucuk S, Mirza E, Gumus K, Oner A (2013) Obstructive sleep apnoea prevalence in non-arteritic anterior ischaemic optic neuropathy. Br J Ophthalmol 97(2):206–209. doi:10.1136/bjophthalmol-2012-302598

    Article  PubMed  Google Scholar 

  36. Aptel F, Khayi H, Pepin JL, Tamisier R, Levy P, Romanet JP, Chiquet C (2015) Association of nonarteritic ischemic optic neuropathy with obstructive sleep apnea syndrome: consequences for obstructive sleep apnea screening and treatment. JAMA Ophthalmol 133(7):797–804. doi:10.1001/jamaophthalmol.2015.0893

    Article  PubMed  Google Scholar 

  37. Leveque TK, Yu L, Musch DC, Chervin RD, Zacks DN (2007) Central serous chorioretinopathy and risk for obstructive sleep apnea. Sleep Breath = Schlaf & Atmung 11(4):253–257. doi:10.1007/s11325-007-0112-3

    Article  Google Scholar 

  38. Jain AK, Kaines A, Schwartz S (2010) Bilateral central serous chorioretinopathy resolving rapidly with treatment for obstructive sleep apnea. Graefes Arch Clin Exp Ophthalmol 248(7):1037–1039. doi:10.1007/s00417-009-1257-5

    Article  PubMed  Google Scholar 

  39. Brodie FL, Charlson ES, Aleman TS, Salvo RT, Gewaily DY, Lau MK, Farren ND, Engelhard SB, Pistilli M, Brucker AJ (2015) Obstructive sleep apnea and central serous chorioretinopathy. Retina 35(2):238–243. doi:10.1097/IAE.0000000000000326

    Article  PubMed  PubMed Central  Google Scholar 

  40. Leroux les Jardins G, Glacet-Bernard A, Lasry S, Housset B, Coscas G, Soubrane G (2009) Retinal vein occlusion and obstructive sleep apnea syndrome. J Fr Ophtalmol 32(6):420–424. doi:10.1016/j.jfo.2009.04.012

    Article  CAS  PubMed  Google Scholar 

  41. Glacet-Bernard A, Leroux les Jardins G, Lasry S, Coscas G, Soubrane G, Souied E, Housset B (2010) Obstructive sleep apnea among patients with retinal vein occlusion. Arch Ophthalmol 128(12):1533–1538. doi:10.1001/archophthalmol.2010.272

    Article  PubMed  Google Scholar 

  42. Kanai H, Shiba T, Hori Y, Saishin Y, Maeno T, Takahashi M (2012) Prevalence of sleep-disordered breathing in patients with retinal vein occlusion. Nippon Ganka Gakkai Zasshi 116(2):81–85

    PubMed  Google Scholar 

  43. Culbertson WW, Ostler HB (1981) The floppy eyelid syndrome. Am J Ophthalmol 92(4):568–575

    Article  CAS  PubMed  Google Scholar 

  44. Muniesa M, Sanchez-de-la-Torre M, Huerva V, Lumbierres M, Barbe F (2014) Floppy eyelid syndrome as an indicator of the presence of glaucoma in patients with obstructive sleep apnea. J Glaucoma 23(1):e81–e85. doi:10.1097/IJG.0b013e31829da19f

    Article  PubMed  Google Scholar 

  45. Muniesa MJ, Huerva V, Sanchez-de-la-Torre M, Martinez M, Jurjo C, Barbe F (2013) The relationship between floppy eyelid syndrome and obstructive sleep apnoea. Br J Ophthalmol 97(11):1387–1390. doi:10.1136/bjophthalmol-2012-303051

    Article  PubMed  Google Scholar 

  46. Karger RA, White WA, Park WC, Rosales AG, McLaren JW, Olson EJ, Woog JJ (2006) Prevalence of floppy eyelid syndrome in obstructive sleep apnea-hypopnea syndrome. Ophthalmology 113(9):1669–1674. doi:10.1016/j.ophtha.2006.02.053

    Article  PubMed  Google Scholar 

  47. Ezra DG, Beaconsfield M, Collin R (2010) Floppy eyelid syndrome: stretching the limits. Surv Ophthalmol 55(1):35–46. doi:10.1016/j.survophthal.2009.02.025

    Article  PubMed  Google Scholar 

  48. Chambe J, Laib S, Hubbard J, Erhardt C, Ruppert E, Schroder C, Malan A, Bourcier T, Bourgin P (2012) Floppy eyelid syndrome is associated with obstructive sleep apnoea: a prospective study on 127 patients. J Sleep Res 21(3):308–315. doi:10.1111/j.1365-2869.2011.00968.x

    Article  PubMed  Google Scholar 

  49. Beis PG, Brozou CG, Gourgoulianis KI, Pastaka C, Chatzoulis DZ, Tsironi EE (2012) The floppy eyelid syndrome: evaluating lid laxity and its correlation to sleep apnea syndrome and body mass index. ISRN Ophthalmol 2012:650892. doi:10.5402/2012/650892

    Article  PubMed  PubMed Central  Google Scholar 

  50. McNab AA (2007) The eye and sleep apnea. Sleep Med Rev 11(4):269–276. doi:10.1016/j.smrv.2007.03.006

    Article  PubMed  Google Scholar 

  51. Kloos P, Laube I, Thoelen A (2008) Obstructive sleep apnea in patients with central serous chorioretinopathy. Graefes Arch Clin Exp Ophthalmol 246(9):1225–1228. doi:10.1007/s00417-008-0837-0

    Article  PubMed  Google Scholar 

  52. Yavas GF, Kusbeci T, Kasikci M, Gunay E, Dogan M, Unlu M, Inan UU (2014) Obstructive sleep apnea in patients with central serous chorioretinopathy. Curr Eye Res 39(1):88–92. doi:10.3109/02713683.2013.824986

    Article  CAS  PubMed  Google Scholar 

  53. Lin CC, Hu CC, Ho JD, Chiu HW, Lin HC (2013) Obstructive sleep apnea and increased risk of glaucoma: a population-based matched-cohort study. Ophthalmology 120(8):1559–1564. doi:10.1016/j.ophtha.2013.01.006

    Article  PubMed  Google Scholar 

  54. Sergi M, Salerno DE, Rizzi M, Blini M, Andreoli A, Messenio D, Pecis M, Bertoni G (2007) Prevalence of normal tension glaucoma in obstructive sleep apnea syndrome patients. J Glaucoma 16(1):42–46. doi:10.1097/01.ijg.0000243472.51461.24

    Article  PubMed  Google Scholar 

  55. Boonyaleephan S (2008) Bilateral acute onset myopia and angle closure glaucoma after oral topiramate: a case report. J Med Assoc Thail 91(12):1904–1907

    Google Scholar 

  56. Karakucuk S, Goktas S, Aksu M, Erdogan N, Demirci S, Oner A, Arda H, Gumus K (2008) Ocular blood flow in patients with obstructive sleep apnea syndrome (OSAS). Graefes Arch Clin Exp Ophthalmol 246(1):129–134. doi:10.1007/s00417-007-0656-8

    Article  PubMed  Google Scholar 

  57. Kadyan A, Asghar J, Dowson L, Sandramouli S (2010) Ocular findings in sleep apnoea patients using continuous positive airway pressure. Eye (Lond) 24(5):843–850. doi:10.1038/eye.2009.212

    Article  CAS  Google Scholar 

  58. Lin PW, Friedman M, Lin HC, Chang HW, Wilson M, Lin MC (2011) Normal tension glaucoma in patients with obstructive sleep apnea/hypopnea syndrome. J Glaucoma 20(9):553–559. doi:10.1097/IJG.0b013e3181f3eb81

    Article  PubMed  Google Scholar 

  59. Boyle-Walker M, Semes LP, Clay OJ, Liu L, Fuhr P (2011) Sleep apnea syndrome represents a risk for glaucoma in a veterans’ affairs population. ISRN Ophthalmol 2011:920767. doi:10.5402/2011/920767

    Article  PubMed  PubMed Central  Google Scholar 

  60. Aptel F, Chiquet C, Tamisier R, Sapene M, Martin F, Stach B, Grillet Y, Levy P, JL P, Sleep Registry of the French Federation of Pneumology Paris F (2014) Association between glaucoma and sleep apnea in a large French multicenter prospective cohort. Sleep Med 15(5):576–581. doi:10.1016/j.sleep.2013.11.790

    Article  PubMed  Google Scholar 

  61. Nowak MS, Jurowski P, Gos R, Prost ME, Smigielski J (2011) Pulsatile ocular blood flow in subjects with sleep apnoea syndrome. Arch Med Sci 7(2):332–336. doi:10.5114/aoms.2011.22087

    Article  PubMed  PubMed Central  Google Scholar 

  62. Mojon DS, Goldblum D, Fleischhauer J, Chiou AG, Frueh BE, Hess CW, Gugger M, Bassetti C, Boehnke M, Mathis J (1999) Eyelid, conjunctival, and corneal findings in sleep apnea syndrome. Ophthalmology 106(6):1182–1185. doi:10.1016/S0161-6420(99)90256-7

    Article  CAS  PubMed  Google Scholar 

  63. Acar M, Firat H, Acar U, Ardic S (2013) Ocular surface assessment in patients with obstructive sleep apnea-hypopnea syndrome. Sleep Breath = Schlaf & Atmung 17(2):583–588. doi:10.1007/s11325-012-0724-0

    Article  Google Scholar 

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Acknowledgments

This study was led by Dr. Leh-Kiong Huon while she was a visiting scholar in Sleep Surgery and Sleep Medicine at Stanford University School of Medicine. No funding was received for this research. All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speaker’s bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements,) or non-financial interest (personal or professional relationships, affiliations, and knowledge or beliefs) in the subject matter or materials discussed in this manuscript. As this is a bibliographic research, it was considered “exempt” from IRB approval.

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Correspondence to Christian Guilleminault.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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This meta-analysis emphasize the association of sleep disordered breathing and ophthalmologic disorders caused or propagated by variable pathologic mechanism; therefore, clinicians should consider this evidence a reason to pay more attention in their clinical practices of ophthalmology and consider screening patients for sleep disorders or referring patients to sleep disorders evaluation when clinically appropriate.

Rashid Nadeem

Illinois, USA

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Huon, LK., Liu, S.YC., Camacho, M. et al. The association between ophthalmologic diseases and obstructive sleep apnea: a systematic review and meta-analysis. Sleep Breath 20, 1145–1154 (2016). https://doi.org/10.1007/s11325-016-1358-4

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