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Exposure to Secondhand Smoke in Children is Associated with a Thinner Retinal Nerve Fiber Layer: The Hong Kong Children Eye Study

  • Author Footnotes
    1 Drs Li and Yuan served jointly as first authors.
    Jian Li
    Footnotes
    1 Drs Li and Yuan served jointly as first authors.
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Department of Ophthalmology, Affiliated Hangzhou First People's Hospital, Zhejiang University School of Medicine, Hangzhou, China
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  • Author Footnotes
    1 Drs Li and Yuan served jointly as first authors.
    Nan Yuan
    Footnotes
    1 Drs Li and Yuan served jointly as first authors.
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China
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  • Wai Kit Chu
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China
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  • Carol Y. Cheung
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China
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  • Shumin Tang
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Department of Ophthalmology, The First Affiliated Hospital of Fujian Medical University, Fuzhou, China
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  • Fen Fen Li
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China
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  • Li Jia Chen
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Department of Ophthalmology and Visual Sciences, Prince of Wales Hospital, Hong Kong
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  • Ka Wai Kam
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Department of Ophthalmology and Visual Sciences, Prince of Wales Hospital, Hong Kong
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  • Alvin L. Young
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Department of Ophthalmology and Visual Sciences, Prince of Wales Hospital, Hong Kong
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  • Patrick Ip
    Affiliations
    Department of Paediatrics and Adolescent Medicine, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China
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  • Clement C. Tham
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Department of Ophthalmology and Visual Sciences, Prince of Wales Hospital, Hong Kong

    Hong Kong Eye Hospital, Hong Kong SAR, China
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  • Chi Pui Pang
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China
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  • Jason C. Yam
    Correspondence
    Inquiries to Jason C. Yam, Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong Eye Hospital, 147K Argyle St, Kowloon, Hong Kong, China
    Affiliations
    Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China

    Department of Ophthalmology and Visual Sciences, Prince of Wales Hospital, Hong Kong

    Hong Kong Eye Hospital, Hong Kong SAR, China

    Department of Ophthalmology, Hong Kong Children's Hospital SAR, China
    Search for articles by this author
  • Author Footnotes
    1 Drs Li and Yuan served jointly as first authors.
Published:October 28, 2020DOI:https://doi.org/10.1016/j.ajo.2020.10.016

      Highlights

      • Children exposed to secondhand smoke had a thinner peripapillary retinal nerve fiber layer.
      • As the optic nerve, quantified by retinal nerve fiber layer thickness, is part of the central nervous system, exposure tosecond hand smoke could lead to neurodevelopmental deficits.
      • It is recommended that children avoid exposure to cigarette smoke in living environments.

      Purpose

      We sought to assess the effects of exposure to secondhand smoke (SHS) on peripapillary retinal nerve fiber layer (p-RNFL) thickness in children.

      Design

      Cross-sectional study.

      Methods

      Children 6-8 years of age were consecutively recruited from the population-based Hong Kong Children Eye Study. All participants received comprehensive ophthalmic examinations and p-RNFL thickness was measured by spectral-domain optical coherence tomography. SHS data were derived from a validated questionnaire. Associations between p-RNFL thickness and SHS exposure status, number of smokers in the family, and quantity of smoking in the family were determined by multivariate linear regression after adjusting for potential confounders.

      Results

      Among the Hong Kong Children Eye Study cohort (n = 3,103), approximately one-third of children were exposed to SHS (35.4%, n = 1,097). Compared to those without exposure to SHS, children exposed to SHS had similar age (P = .83), gender (P = .17), body mass index (P = .44), birth weight (P = .23), and axial length (P = .34), but had lower family income (P < .001) and lower parental education level (P < .001). After adjusting for all the above factors, exposure to SHS was associated with a thinner global p-RNFL by 4.4 μm (P < .001). Reduced p-RNFL was also associated with increased numbers of smokers in the family (β = −3.40, P < .001) and increased quantity of SHS (β = −0.22, P < .001).

      Conclusions

      Exposure to SHS in children was associated with a thinner p-RNFL. A thinner p-RNFL may increase the risk of irreversible visual impairment in the future. Our results provide evidence to recommend that children avoid exposure to SHS.
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      References

        • Campos M.W.
        • Serebrisky D.
        • Castaldelli-Maia J.M.
        Smoking and cognition.
        Curr Drug Abuse Rev. 2016; 9: 76-79
        • Nita M.
        • Grzybowski A.
        Smoking and eye pathologies. A systemic review. Part II. Retina diseases, uveitis, optic neuropathies, thyroid-associated orbitopathy.
        Curr Pharm Des. 2017; 23: 639-654
        • Law S.M.
        • Lu X.
        • Yu F.
        • Tseng V.
        • Law S.K.
        • Coleman A.L.
        Cigarette smoking and glaucoma in the United States population.
        Eye (Lond). 2018; 32: 716-725
        • Thornton J.
        • Edwards R.
        • Mitchell P.
        • Harrison R.A.
        • Buchan I.
        • Kelly S.P.
        Smoking and age-related macular degeneration: a review of association.
        Eye (Lond). 2005; 19: 935-944
        • Rong S.S.
        • Peng Y.
        • Liang Y.B.
        • Cao D.
        • Jhanji V.
        Does cigarette smoking alter the risk of pterygium? A systematic review and meta-analysis.
        Invest Ophthalmol Vis Sci. 2014; 55: 6235-6243
        • Kelly S.P.
        • Thornton J.
        • Edwards R.
        • Sahu A.
        • Harrison R.
        Smoking and cataract: review of causal association.
        J Cataract Refract Surg. 2005; 31: 2395-2404
        • Thornton J.
        • Kelly S.P.
        • Harrison R.A.
        • Edwards R.
        Cigarette smoking and thyroid eye disease: a systematic review.
        Eye (Lond). 2007; 21: 1135-1145
        • Solberg Y.
        • Rosner M.
        • Belkin M.
        The association between cigarette smoking and ocular diseases.
        Surv Ophthalmol. 1998; 42: 535-547
        • Teo K.K.
        • Ounpuu S.
        • Hawken S.
        • et al.
        Tobacco use and risk of myocardial infarction in 52 countries in the INTERHEART study: a case-control study.
        Lancet. 2006; 368: 647-658
        • Ong E.K.
        • Glantz S.A.
        Tobacco industry efforts subverting International Agency for Research on Cancer’s second-hand smoke study.
        Lancet. 2000; 355: 1253-1259
        • Janson C.
        • Chinn S.
        • Jarvis D.
        • et al.
        Effect of passive smoking on respiratory symptoms, bronchial responsiveness, lung function, and total serum IgE in the European Community Respiratory Health Survey: a cross-sectional study.
        Lancet. 2001; 358: 2103-2109
        • Klonoff-Cohen H.S.
        • Edelstein S.L.
        • Lefkowitz E.S.
        • et al.
        The effect of passive smoking and tobacco exposure through breast milk on sudden infant death syndrome.
        JAMA. 1995; 273: 795-798
        • Oberg M.
        • Jaakkola M.S.
        • Woodward A.
        • Peruga A.
        • Pruss-Ustun A.
        Worldwide burden of disease from exposure to second-hand smoke: a retrospective analysis of data from 192 countries.
        Lancet. 2011; 377: 139-146
        • Egebjerg Jensen K.
        • Jensen A.
        • Nohr B.
        • Kruger Kjaer S.
        Do pregnant women still smoke? A study of smoking patterns among 261,029 primiparous women in Denmark 1997-2005.
        Acta Obstet Gynecol Scand. 2008; 87: 760-767
        • Martinez-Frias M.L.
        • Rodriguez-Pinilla E.
        • Bermejo E.
        • Grupo Periferico del E.
        Tobacco smoking during pregnancy in Spain: an analysis according to years, autonomous communities and maternal characteristics [in Spanish].
        Med Clin (Barc). 2005; 124: 86-92
        • Figueras F.
        • Meler E.
        • Eixarch E.
        • et al.
        Association of smoking during pregnancy and fetal growth restriction: subgroups of higher susceptibility.
        Eur J Obstet Gynecol Reprod Biol. 2008; 138: 171-175
        • Ip P.
        • Chung B.H.
        • Ho F.K.
        • et al.
        Prenatal tobacco exposure shortens telomere length in children.
        Nicotine Tob Res. 2017; 19: 111-118
        • Polanska K.
        • Jurewicz J.
        • Hanke W.
        Smoking and alcohol drinking during pregnancy as the risk factors for poor child neurodevelopment - a review of epidemiological studies.
        Int J Occup Med Environ Health. 2015; 28: 419-443
        • Herrmann M.
        • King K.
        • Weitzman M.
        Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment.
        Curr Opin Pediatr. 2008; 20: 184-190
        • Ashina H.
        • Li X.Q.
        • Olsen E.M.
        • Skovgaard A.M.
        • Larsen M.
        • Munch I.C.
        Association of maternal smoking during pregnancy and birth weight with retinal nerve fiber layer thickness in children aged 11 or 12 years: the Copenhagen Child Cohort 2000 Eye Study.
        JAMA Ophthalmol. 2017; 135: 331-337
        • Yuan N.
        • Li J.
        • Tang S.
        • et al.
        Association of secondhand smoking exposure with choroidal thinning in children aged 6 to 8 years: the Hong Kong Children Eye Study.
        JAMA Ophthalmol. 2019; 137: 1-9
        • Yam J.C.
        • Tang S.M.
        • Kam K.W.
        • et al.
        High prevalence of myopia in children and their parents in Hong Kong Chinese Population: the Hong Kong Children Eye Study [online ahead of print].
        Acta Ophthalmol. 2020; https://doi.org/10.1111/aos.14350
        • Cheung C.Y.
        • Li J.
        • Yuan N.
        • et al.
        Quantitative retinal microvasculature in children using swept-source optical coherence tomography: the Hong Kong Children Eye Study [Epub ahead of print].
        Br J Ophthalmol. 2018; https://doi.org/10.1136/bjophthalmol-2018-312413
        • Ojaimi E.
        • Rose K.A.
        • Smith W.
        • Morgan I.G.
        • Martin F.J.
        • Mitchell P.
        Methods for a population-based study of myopia and other eye conditions in school children: the Sydney Myopia Study.
        Ophthalmic Epidemiol. 2005; 12: 59-69
        • Guo Y.
        • Liu L.J.
        • Tang P.
        • et al.
        Outdoor activity and myopia progression in 4-year follow-up of Chinese primary school children: The Beijing Children Eye Study.
        PloS One. 2017; 12: e0175921
        • Scheuermann T.S.
        • Nollen N.L.
        • Cox L.S.
        • et al.
        Smoking dependence across the levels of cigarette smoking in a multiethnic sample.
        Addict Behav. 2015; 43: 1-6
        • Mohanty P.
        • Gujjari S.K.
        • Nakum C.G.
        Salivary free hemoglobin and lactate dehydrogenase as biomarkers for periodontal disease in smokers.
        Quintessence Int. 2019; 50: 428-434
        • Branstetter S.A.
        • Nye R.T.
        • Muscat J.E.
        Time to first cigarette of the day and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) in adult regular and non-daily smokers: (NHANES) 2007-10.
        Regul Toxicol Pharmacol. 2019; 108: 104454
        • Budenz D.L.
        • Anderson D.R.
        • Varma R.
        • et al.
        Determinants of normal retinal nerve fiber layer thickness measured by Stratus OCT.
        Ophthalmology. 2007; 114: 1046-1052
        • Dogan B.
        • Kazim Erol M.
        • Dogan U.
        • et al.
        The retinal nerve fiber layer, choroidal thickness, and central macular thickness in morbid obesity: an evaluation using spectral-domain optical coherence tomography.
        Eur Rev Med Pharmacol Sci. 2016; 20: 886-891
        • Dervisogullari M.S.
        • Totan Y.
        • Tenlik A.
        • Yuce A.
        • Guler E.
        Effect of smoking on retina nerve fiber layer and ganglion cell-inner plexiform layer complex.
        Cutan Ocul Toxicol. 2015; 34: 282-285
        • El-Shazly A.A.
        • Farweez Y.A.T.
        • Elewa L.S.
        • Elzankalony Y.A.
        • Farweez B.A.T.
        Effect of active and passive smoking on retinal nerve fibre layer and ganglion cell complex.
        J Ophthalmol. 2017; 2017: 6354025
        • Yang T.K.
        • Huang X.G.
        • Yao J.Y.
        Effects of cigarette smoking on retinal and choroidal thickness: a systematic review and meta-analysis.
        J Ophthalmol. 2019; 2019: 8079127
        • Pueyo V.
        • Guerri N.
        • Oros D.
        • et al.
        Effects of smoking during pregnancy on the optic nerve neurodevelopment.
        Early Hum Dev. 2011; 87: 331-334
        • Tariq Y.M.
        • Pai A.
        • Li H.T.
        • et al.
        Association of birth parameters with OCT measured macular and retinal nerve fiber layer thickness.
        Invest Ophthalmol Vis Sci. 2011; 52: 1709-1715
        • Peng P.H.
        • Hsu S.Y.
        • Wang W.S.
        • Ko M.L.
        Age and axial length on peripapillary retinal nerve fiber layer thickness measured by optical coherence tomography in nonglaucomatous Taiwanese participants.
        PLoS One. 2017; 12: e0179320
        • Delcourt C.
        Early exposure to secondhand smoking and ocular health-insights from latest-generation optical coherence tomographic imaging [Online ahead of print].
        JAMA Ophthalmol. 2019; https://doi.org/10.1001/jamaophthalmol.2019.4185
        • Jain V.
        • Jain M.
        • Abdull M.M.
        • Bastawrous A.
        The association between cigarette smoking and primary open-angle glaucoma: a systematic review.
        Int Ophthalmol. 2017; 37: 291-301
        • Niven T.C.S.
        • Azhany Y.
        • Rohana A.J.
        • et al.
        Cigarette smoking on severity of primary angle closure glaucoma in Malay patients.
        J Glaucoma. 2019; 28: 7-13
        • Nita M.
        • Grzybowski A.
        Smoking and eye pathologies. A systemic review. Part I. Anterior eye segment pathologies.
        Curr Pharm Des. 2017; 23: 629-638
        • Pérez-de-Arcelus M.
        • Toledo E.
        • Martínez-González M.Á.
        • Martín-Calvo N.
        • Fernández-Montero A.
        • Moreno-Montañés J.
        Smoking and incidence of glaucoma: the SUN Cohort.
        Medicine (Baltimore). 2017; 96: e5761
        • Bsteh G.
        • Berek K.
        • Hegen H.
        • et al.
        Serum neurofilament levels correlate with retinal nerve fiber layer thinning in multiple sclerosis.
        Mult Scler. 2020; 26: 1682-1690
        • Costello F.
        • Burton J.M.
        Retinal imaging with optical coherence tomography: a biomarker in multiple sclerosis?.
        Eye Brain. 2018; 10: 47-63
        • Gordon-Lipkin E.
        • Chodkowski B.
        • Reich D.S.
        • et al.
        Retinal nerve fiber layer is associated with brain atrophy in multiple sclerosis.
        Neurology. 2007; 69: 1603-1609
        • Iseri P.K.
        • Altinas O.
        • Tokay T.
        • Yuksel N.
        Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease.
        J Neuroophthalmol. 2006; 26: 18-24
        • Chen R.
        • Clifford A.
        • Lang L.
        • Anstey K.J.
        Is exposure to secondhand smoke associated with cognitive parameters of children and adolescents?—a systematic literature review.
        Ann Epidemiol. 2013; 23: 652-661
        • Pagani L.S.
        Environmental tobacco smoke exposure and brain development: the case of attention deficit/hyperactivity disorder.
        Neurosci Biobehav Rev. 2014; 44: 195-205
        • Levy R.J.
        Carbon monoxide pollution and neurodevelopment: a public health concern.
        Neurotoxicol Teratol. 2015; 49: 31-40