Abstract
To describe the historical evolution of the role of lasers in effecting therapeutic changes in the four acellular membranes of the eye. Over the past 50 years, iterative developments have been instituted in lasers used for various forms of eye surgery predominately on the basis of data generated in early experiments in the 1960s to determine thresholds for damage and their incorporation in codes of practice for laser safety. The evolutionary steps are described. Excimer laser technology resulted in the generation of the new field of laser refractive surgery with over 40 million individuals now having undergone procedures such as photorefractive keratectomy and LASIK. Developments in lasers used for various forms of retinal surgery have undergone changes involving shorter and shorter pulse durations together with changes in beam energy distribution with implications for potential intervention in AMD prophylactically. Lasers have made a major impact on surgical treatment on all four acellular membranes of the eye but particularly Bowman’s membrane in refractive surgery, where it has been demonstrated that it can be removed without significant consequences for eye health or vision.
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References
Sanders MD . The Bowman Lecture Papilloedema: the pendulum of progress. Eye 1997; 11: 267–294.
James RR . British Masters of Ophthalmology Series 16 Sir William Bowman. Br J Opthalmol 1925; 9: 481–494.
Dickens C In: Schlicke P, (ed). The Oxford Companion to Charles Dickens: Anniversary Edition. Oxford University Press: Oxford, UK, 2011.
Mayhew H . London Labour and the London Poor: Volume I–IV. Griffin, Bohn and Co.: London, UK, 1861.
Jerrold B, Doré G . London: A Pilgrimage. Grant & Co.: London, UK, 1872.
Woodham-Smith C . Florence Nightingale. Constable: London, UK, 1950.
Dickens C . Tale of Two Cities. Chapman & Hall: London, UK, 1859.
Fisher R . The influence of age on some ocular basement membranes. Eye 1987; 1: 184–189.
Bowman W . Lectures on the Parts Concerned in the Operations on the Eye, and on the Structure of the Retina, Delivered at the Royal London Ophthalmic Hospital, Moorfields, June 1847. Longman, Brown, Green and Longmans: London, UK, 1849.
Duddell B . A Treatise of the Diseases of the Horny-Coat of the Eye, and the Various Kinds of Cataract. J Clark: London, UK, 1729.
Descemet J . An Sola Lens Crystallina Cataractae Sedes?. Paris, 1758.
Demours P, Lettre de M, Demours àM Petit,...: en réponse à sa critique d'un rapport sur une maladie de l'oeil survenue après l'inoculation de la petite vérole; contenant de nouvelles observations sur la structure de l'oeil, quelques remarques générales de pratique relatives aux maladies de cet organe 1767.
Daremberg Ch, Ruelle É. On the Naming of the Parts of Man P153 Paris from the Original Greek, Rufus (100AD) 1879.
Scheiner CSJ Oculus hoc est: Fundamentum opticum [6], dealing with the physiological optics of the eye printed in Innsbruck by Daniel Bauer in 1619.
Zinn J . Descriptio Anatomica Oculi Humani. Goettingen, Germany, 1755.
Boerhaave H . Dr Boerhaave’s Academical Lectures on the Theory of Physic: Being a Genuine Translation of his Institutes and Explanatory Comment, Collated and Adjusted to Each Other, as they were Dictated to his Students at the University of Leyden. W Innys: London, UK, 1745.
Bruch CLW . Untersuchungen zur Kenntnis des kornigen Pigments der Wirbeltthiere. Zurich, Switzerland, 1844.
Marshall J, Grindle CF . Fine structure of the cornea and its development. Trans Ophthalmol Soc UK 1978; 98 (3): 320–328.
Marshall J, Hussain AA, Starita C, Moore DJ, Patmore AL . The retinal pigment epithelium. In: Marmor MF, Wolfensberger TJ, (ed). The Retinal Pigment Epithelium. Oxford University Press: New York, NY, USA, 1998 pp 669–692.
Germundsson J, Karanis G, Fagerholm P, Lagali N . Age-related thinning of Bowman’s layer in the human cornea in vivo. Invest Ophthalmol Vis Sci 2013; 54 (9): 6143–6149.
Einstein A . Zur Quantentheorie der Strahlung (On the quantum mechanics of radiation). Phys Z 1917; 18: 121–128.
Gordon J, Zeiger H, Townes CH . The maser—new type of microwave amplifier, frequency standard, and spectrometer. Phys Rev 1955; 99: 1264.
Maiman TH . Nature 1960; 187: 493–494.
Zaret MM, Breinin GM, Schmidt H, Ripps H, Siegal IM, Solon LR . Ocular lesions produced by an optical maser (laser). Science 1961; 134: 1525–1526.
Marshall J, Mellerio J . Histology of the formation of retinal laser lesions. Exp Eye Res 1967; 6 (1): 4–9.
Marshall J, Mellerio J . Pathological development of retinal laser photocoagulations. Exp Eye Res 1967; 6 (4): 303–308.
Marshall J . Thermal and mechanical mechanisms in laser damage to the retina. Invest Ophthalmol 1970; 9 (2): 97–115.
Marshall J, Mellerio J . Laser irradiation of retinal tissue. Br Med Bull 1970; 26 (2): 156–160.
Smart D, Manson N, Marshall J, Mellerio J . New ocular hazard of mode locking in CW lasers. Nature 1970; 227 (5263): 1149–1150.
Marshall J, Mellerio J . Disappearance of retino-epithelial scar tissue from ruby laser photocoagulations. Exp Eye Res 1970; 12 (2): 173–174.
Environmental Heath Criteria 23. Lasers and Optical Radiation. World Health Organisation: Geneva, Switzerland, 1982.
Blinding Laser Weapons. In: Doswald-Beck L (ed). Reports of the Meetings of Experts Convened by the International Committee of the Red Cross on Battlefield Laser Weapons 1989–91. Geneva, 1993.
Marshall J, Hamilton AM, Bird AC . Intra-retinal absorption of argon laser irradiation in human and monkey retinae. Experientia 1974; 30 (11): 1335–1337.
Marshall J, Hamilton AM, Bird AC . Histopathology of ruby and argon laser lesions in monkey and human retina. A comparative study. Br J Ophthalmol 1975; 59 (11): 610–630.
Marshall J . Lasers in ophthalmology: the basic principles. Eye (Lond) 1998; 2 (Suppl): S98–S112.
McHugh JD, Marshall J, Ffytche TJ, Hamilton AM, Raven A, Keeler CR . Initial clinical experience using a diode laser in the treatment of retinal vascular disease. Eye (Lond) 1989; 3 (Part 5): 516–527.
Watts GK . Ruby laser damage and pigmentation of the iris. Exp Eye Res 1969; 8 (4): 470–476.
McHugh JDA, Marshall J, Capon M, Rothery S, Raven A, Naylor RP . Transpupillary retinal photocoagulation in the eyes of rabbit and human using a diode laser. Lasers Light Ophthalmol 1998; 2 (2): 125–143.
Marshall J, Raven A, Welford W, Ness K. Surface erosion using lasers. US Patent No. 4 941 093, 1990 (filed in 1986).
Trokel SL, Srinivasan R, Braren B . Excimer laser surgery of the cornea. Am J Ophthalmol 1983; 96 (6): 710–715.
Marshall J, Trokel S, Rothery S, Schubert H . An ultrastructural study of corneal incisions induced by an Excimer laser at 193 nm. Ophthalmology 1985; 92 (6): 749–758.
Marshall J, Trokel S, Rothery S, Krueger RR . A comparative study of corneal incisions induced by diamond and steel knives and two ultraviolet radiations from an excimer laser. Br J Ophthalmol 1986; 70 (7): 482–501.
Marshall J, Trokel S, Rothery S, Krueger RR . Photoablative reprofiling of the cornea using an excimer laser: photorefractive keratectomy. Lasers Ophthalmol 1986; 1: 21–48.
Munnerlyn CR, Koons SJ, Marshall J . Photorefractive keratectomy: a technique for laser refractive surgery. J Cataract Refract Surg 1988; 14 (1): 46–52.
O'Brart DP, Gartry DS, Lohmann CP, Muir MGK, Marshall J . Excimer laser photorefractive keratectomy for myopia: comparison of 4.00- and 5.00-millimeter ablation zones. J Refract Corneal Surg 1994; 10 (2): 87–94.
O'Brart DPS, Corbett MC, Verma S, Heacock G, Lohmann CP, Muir MGK et al. Effects of ablation diameter, depth, and edge contour on the outcome of Excimer laser photorefractive keratectomy (abstract). J Refract Surgery 1995; 11: S285.
Corbett MC, Marshall J . Corneal haze after photorefractive keratectomy. A review of etiological mechanisms and treatment options. Lasers Light Ophthalmol 1996; 7 (4): 173–196.
O'Brart DP, Lohmann CP, Klonos G, Corbett MC, Pollock WS, Kerr-Muir MG et al. The effects of topical corticosteroids and plasmin inhibitors on refractive outcome, haze, and visual performance after photorefractive keratectomy. A prospective, randomized, observer-masked study. Ophthalmology 1994; 101 (9): 1565–1574.
Verma S, Corbett MC, Marshall J . A prospective randomized, double-masked trial to evaluate the role of topical anesthetics in controlling pain after photorefractive keratectomy. Ophthalmology 1995; 102 (12): 1918–1924.
Buratto L, Ferrari M, Rama P . Excimer laser intrastromal keratomileusis. Am J Ophthalmol 1992; 113 (3): 291–295.
Pallikaris IG, Papatzanaki ME, Siganos DS, Tsilimbaris MK . A corneal flap technique for laser in situ keratomileusis. Human studies. Arch Ophthalmol 1991; 109 (12): 1699–1702.
Shortt AJ, Allan BD, Evans JR . Laser-assisted in situ keratomileusis (LASIK) versus photorefractive keratectomy (PRK) for myopia. Cochrane Database Syst Rev 2013; 1: CD005135 (review).
Petzing JN, Tyrer JR . Recent developments and applications in electronic speckle pattern interferometry. J Strain Anal Eng Des 1998; 33 (2): 153–169.
Sheikh Ibrahim J, Petzing JN, Tyrer JR . Deformation analysis of aircraft wheels using speckle shearing interferometry. Proc Inst Mech Eng Part G 2004; 218: 287–295.
Knox Cartwright NE, Tyrer JR, Marshall J . Age-related differences in the elasticity of the human cornea. Invest Ophthalmol Vis Sci 2011; 52 (7): 4324–4329.
Abahussin M, Hayes S, Knox Cartwright NE, Kamma-Lorger CS, Khan Y, Marshall J et al. 3D collagen orientation study of the human cornea using X-ray diffraction and femtosecond laser technology. Invest Ophthalmol Vis Sci 2009; 50 (11): 5159–5164.
Jaycock PD, Lobo L, Ibrahim J, Tyrer J, Marshall J . Interferometric technique to measure biomechanical changes in the cornea induced by refractive surgery. J Cataract Refract Surg 2005; 31 (1): 175–184.
Knox Cartwright NE, Tyrer JR, Jaycock PD, Marshall J . Effects of variation in depth and side cut angulations in LASIK and thin-flap LASIK using a femtosecond laser: a biomechanical study. J Refract Surg 2012; 28 (6): 419–425.
Durrie DS, Slade SG, Marshall J . Wavefront-guided Excimer laser ablation using photorefractive keratectomy and sub-Bowman's keratomileusis: a contralateral eye study. J Refract Surg 2008; 24 (1): S77–S84.
Reinstein DZ, Archer TJ, Gobbe M . Accuracy and reproducibility of cap thickness in small incision lenticule extraction. J Refract Surg 2013; 29 (12): 810–815.
Koller T, Seiler T . Therapeutic cross-linking of the cornea using riboflavin/UVA. Klin Monbl Augenheilkd 2007; 224 (9): 700–706 (review; in German).
Knox Cartwright NE, Tyrer JR, Marshall J . In vitro quantification of the stiffening effect of corneal cross-linking in the human cornea using radial shearing speckle pattern interferometry. J Refract Surg 2012; 28 (7): 503–508.
Tomita M, Yoshida Y, Yamamoto Y, Mita M, Waring G IV . In vivo confocal laser microscopy of morphologic changes after simultaneous LASIK and accelerated collagen crosslinking for myopia: one-year results. J Cataract Refract Surg 2014; 40 (6): 981–990.
Seven I, Dupps WJ . Patient-Specific finite element simulations of standard incisional astigmatism surgery and a novel patterned collagen crosslinking approach to astigmatism treatment. J Med Dev 2013; 7 (4): 0409131–0409132.
Kanellopoulos AJ, Pamel GJ . Review of current indications for combined very high fluence collagen cross-linking and laser in situ keratomileusis surgery. Indian J Ophthalmol 2013; 61 (8): 430–432 (review).
Marshall J, Hersh P, Muller D . Corneal Collagen Cross-Linking. eBook Avedro Inc: Waltham, MA, USA, 2013.
Ugarte M, Hussain AA, Marshall J . An experimental study of the elastic properties of the human Bruch's membrane–choroid complex: relevance to ageing. Br J Ophthalmol 2006; 90 (5): 621–626.
Young RW . The Bowman Lecture, 1982. Biological renewal. Applications to the eye. Trans Ophthalmol Soc UK 1982; 102 (Part 1): 42–75.
Bindewald A, Bird AC, Dandekar SS, Dolar-Szczasny J, Dreyhaupt J, Fitzke FW et al. Classification of fundus autofluorescence patterns in early age-related macular disease. Invest Ophthalmol Vis Sci 2005; 46 (9): 3309–3314.
Grindle CF, Marshall J . Ageing changes in Bruch's membrane and their functional implications. Trans Ophthalmol Soc UK 1978; 98 (1): 172–175.
Bird AC, Marshall J . Retinal pigment epithelial detachments in the elderly. Trans Ophthalmol Soc UK 1986; 105 (Part 6): 674–682 (review).
Moore DJ, Hussain A A, Marshall J . Age-related variation in the hydraulic conductivity of Bruch's membrane. Invest Ophthalmol Vis Sci 1995; 36 (7): 1290–1297.
Starita C, Hussain AA, Pagliarini S, Marshall J . Hydrodynamics of ageing Bruch's membrane: implications for macular disease. Exp Eye Res 1996; 62 (5): 565–572.
Hussain AA, Rowe L, Marshall J . Age-related alterations in the diffusional transport of amino acids across the human Bruch's–choroid complex. J Opt Soc Am A 2002; 19 (1): 166–172.
Guo L, Hussain AA, Limb GA, Marshall J . Age-dependent variation in metalloproteinase activity of isolated human Bruch's membrane and choroid. Invest Ophthalmol Vis Sci 1999; 40 (11): 2676–2682.
Weber BHF, Vogt G, Pruett RC, Stöhr H, Felbor U . Mutations in the tissue inhibitor of metalloproteinases-3 (TIMP3) in patients with Sorsby's fundus dystrophy. Nat Genet 1994; 8: 352–356.
Capon MR, Marshall J, Krafft JI, Alexander RA, Hiscott PS, Bird AC . Sorsby's fundus dystrophy. A light and electron microscopic study. Ophthalmology 1989; 96 (12): 1769–1777.
Kumar A, El-Osta A, Hussain AA, Marshall J . Increased sequestration of matrix metalloproteinases in ageing human Bruch's membrane: implications for ECM turnover. Invest Ophthalmol Vis Sci 2010; 51 (5): 2664 70.
Hussain AA, Lee Y, Marshall J . High molecular-weight gelatinase species of human Bruch's membrane: compositional analyses and age-related changes. Invest Ophthalmol Vis Sci 2010; 51 (5): 2363–2371.
Hussain AA, Lee Y, Zhang JJ, Marshall J . Disturbed matrix metalloproteinase activity of Bruch's membrane in age-related macular degeneration. Invest Ophthalmol Vis Sci 2011; 52 (7): 4459–4466.
Chew EY, Klein ML, Clemons TE, Agrón E, Ratnapriya R, Edwards AO et al. No clinically significant association between CFH and ARMS2 genotypes and response to nutritional supplements: AREDS Report Number 38. Ophthalmology 2014 e-pub ahead of print 24 June 2014 doi:10.1016/j.ophtha.2014.05.008.
Marshall J, Bird AC . Retinal receptor disorders without known metabolic abnormalities. In Garner A, Klintworth GK, (eds). Pathobiology of Ocular Disease. Marcel Dekker: New York, NY, USA, 1982 pp 1167–1220.
Sundaram V, Moore AT, Ali RR, Bainbridge JW . Retinal dystrophies and gene therapy. Eur J Pediatr 2012; 171 (5): 757–765.
Pearson RA, Hippert C, Graca AB, Barber AC . Photoreceptor replacement therapy: challenges presented by the diseased recipient retinal environment. Vis Neurosci 2014; 19: 1–12.
Sarks SH . Ageing and degeneration in the macular region: a clinico-pathological study. Br J Ophthalmol 1976; 60 (5): 324–341.
Ahir A, Guo L, Hussain AA, Marshall J . Expression of metalloproteinases from human retinal pigment epithelial cells and their effects on the hydraulic conductivity of Bruch's membrane. Invest Ophthalmol Vis Sci 2001; 43 (2): 458–465.
Zhang JJ, Sun Y, Hussain AA, Marshall J . Laser-mediated activation of human retinal pigment epithelial cells and concomitant release of matrix metalloproteinases. Invest Ophthalmol Vis Sci 2012; 53 (6): 2928–2937.
Roider J, Brinkmann R, Wirbelauer C, Laqua H, Birngruber R . Retinal sparing by selective retinal pigment epithelial photocoagulation. Arch Ophthalmol 1999; 117 (8): 1028–1034.
Plunkett M, Hussain A, Marshall J. Retinal Regeneration. US Patent No. 8 562 595 (WO2008049164), 2010 (filed in 2007).
Marshall J, Clover G, Rothery S . Some new findings on retinal irradiation by krypton and argon lasers. In Birngruber R, Gabel V-P, (eds). Laser Treatment and Photocoagulation of the Eye. Springer: Berlin, Germany, 1984 pp 21–37.
Pelosini L, Hamilton R, Mohamed M, Hamilton AM, Marshall J . Retina rejuvenation therapy for diabetic macular edema: a pilot study. Retina 2013; 33 (3): 548–558.
Guymer RH, Brassington KH, Dimitrov P, Makeyeva G, Plunkett M, Xia W et al. Nanosecond-laser application in intermediate AMD: 12-month results of fundus appearance and macular function. Clin Exp Ophthalmol 2014; 42 (5): 466–479.
Naumann GO . The Bowman Lecture. Eye (Lond) 1995; 9 (Part 4): 395–421 (review).
Gorovoy MS . Descemet-stripping automated endothelial keratoplasty. Cornea 2006; 25: 886–889.
Fankhauser F, Kwasniewska S . Clinical effects of the Nd:YAG laser operating in the photodisruptive and thermal modes: a review. Ophthalmologica 2003; 217 (1): 1–16 (review).
Shah A, Spalton DJ, Gilbert C, Vasavada A, Boyce JF, Minassian D et al. Effect of intraocular lens edge profile on posterior capsule opacification after extracapsular cataract surgery in a developing country. J Cataract Refract Surg 2007; 33 (7): 1259–1266.
Zhang JJ. Treatment solution and method for preventing posterior capsule opacification by selectively inducing detachment and death of lens epithelial cells. Patent No. 2 499 195 (WO/2004/026288), 2004 (filed 28 August 2003).
Acknowledgements
In putting together a manuscript of this kind summarising work that has taken place over almost 50 years, there are a huge number of individuals and institutions that have contributed and should be thanked. This work was financially supported by the following: Action Medical Research; Ann Allerton Fund; British Eye Research Foundation; British Retinitis Pigmentosa Society; Deutsche Forschungsgemeinschaft; Dr Hans and Mrs Gertrude Hirsch and Fight for Sight Small Grant Award; European Economic Community Concerted Action Biomedical and Health Research Programme; Fight For Sight; Frost Charitable Trust; Guide Dogs for the Blind Association; Iris Fund for Prevention of Blindness; JP Moulton Charity Trust; Lady Allerton Research Foundation; Macular Disease Society; Macula Society (USA); Medical Research Council; Ministry of Defence; National Eye Research Council; NIHR Moorfields Biomedical Research Centre; National Lottery Charities Board; Pocklington Foundation; PPP Healthcare Medical Trust; Research (Endowments) Committee, UMDS; Royal College of Surgeons Ophthalmic Research Fund; Royal National Institute for the Blind; Royal Society; Sembal Trust; South Devon and Cornwall Institution for the Blind; Special Trustees of St Thomas’ Hospital; United States Air Force; Wellcome Trust; Williams Fellowship for Medical and Scientific Research of the University of London; and Worshipful Company of Clothworkers. I thank the following commercial entities where collaborative or joint work was undertaken and funded: Alcon, Avedro, Diomed, Ellex, IntraLase, Keeler, Light Sciences Corporation, LensX, Pharmacia, Retica, Schwind, Summit Technology, and TEVA Pharmaceutical Industries Ltd. I am especially grateful to the Frost Trust who created my second chair in ophthalmology and have funded it for the past 23 years at both St Thomas’s Hospital (King’s College London) and the Institute of Ophthalmology (University College London). I would like to thank all my friends, colleagues, and students over the past 50 years for creating such a fantastic environment of intellectual challenge friendship. I would particularly like to thank the people who did all the work, my PhD and MD students whose efforts contributed to numerous papers, and many of whom are now professors with their own students in countries throughout the world. Finally, I would like to thank Ann Patmore for all her efforts, expertise, and particularly her patience for putting up with my obsessional attitudes in relation to papers and presentations.
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Marshall, J. The 2014 Bowman Lecture—Bowman’s and Bruch’s: a tale of two membranes during the laser revolution. Eye 29, 46–64 (2015). https://doi.org/10.1038/eye.2014.240
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