Expert Review Examination of the Fundus Colin Chu1 and John Salmon2 ……………………………………………………………………………………………………………………………………..

The Journal of Clinical Examination 2007; 2: 7-14

Abstract Fundoscopy with a direct ophthalmoscope is the most commonly used technique for examining the posterior segment of the eye by non-ophthalmologists. However, medical practitioners and students often do not feel confident with ophthalmoscopy, despite it being an essential skill with relevance to many areas of medicine. In this review, we present a routine which is logical, pragmatic and adheres to the established principles of clinical examination. It is based on original research papers, textbook accounts and clinical experience. Word Count: 2345 Key words: Fundoscopy, direct ophthalmoscope, clinical examination. Address for correspondence: [email protected] Author affiliations: 1Medical student, University of Oxford. 2Consultant Ophthalmologist, Oxford Eye Hospital, John Radcliffe Hospital, Oxford. …………………………………………………………………………………………………………………………………….. Introduction Hermann von Helmholtz presented his newly developed Augenspiegel (eye-mirror) to the assembled Physical Society of Berlin in December 1850.[1] For the first time, observation of the retina and optic disc became possible and it revolutionised the study and treatment of eye disease. The scale of his achievement was recognised by the Heidelberg Ophthalmological Society, which in 1858 awarded Helmholtz a silver cup. Upon it was the inscription, ‘To the creator of a new science, to the benefactor of mankind, in thankful remembrance of the invention of the Ophthalmoscope.[2,3] Other devices have subsequently arisen, such as the indirect ophthalmoscope and the slit-lamp, but the direct ophthalmoscope still exists in a modern form and remains part of everyday medical practice. In this article we hope to justify the need for further education, discuss correct technique according to the principles of clinical examination and end by examining its diagnostic place and the relation of ophthalmoscopy to other methods of assessment.[4] Need for Further Training Ophthalmoscope ownership, technique and routine application are all variables affecting the value of direct fundoscopy as a clinical tool. In a study of over 200 Canadian medical students, only 64% actually owned an ophthalmoscope. Moreover, 47% of senior medical students reported that they felt only ‘a little’ or ‘not at all’ confident in direct fundoscopy on an undilated eye.[5]

A similar result was reflected in a British study in which 43% of General Practitioners reported being ‘uneasy’ or ‘very uneasy’ using the direct ophthalmoscope.[6] In addition, a study of Scottish junior doctors revealed that only 18.5% routinely performed ophthalmoscopy.[7] Clearly, there is a need for education to increase the use of this fundamental skill. How to Perform Direct Fundoscopy The ophthalmoscope has multiple uses in the examination of the eye. It can provide a light source for testing pupillary reflexes, gauging if there is a narrow angle or revealing corneal pathology when combined with a cobalt blue filter and fluorescein drops. It can also be used to elicit the red reflex and to perform fundoscopy – the focus of this review. The fundus is defined as the optic nerve head, retina, macula and accompanying blood vessels at the posterior pole of the eye. It is the main target of the direct ophthalmoscope, which can only give a monocular view of up to 6º of field, magnified about 15 times.[8] (Figure 1) Although we will mention some diseases and their associated signs in passing, our emphasis in this review is on the examination routine. Our scheme for direct fundoscopy is presented in two parts preparation (Table 1) and examination (Table 2). This is expanded upon in the commentary below.

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When dilating the pupils, the main fear is of precipitating an attack of acute angle-closure glaucoma. The risk is exceptionally small and estimated at no more than 1 per 20,000 people if using tropicamide alone, so it should not be allowed to compromise a thorough view of the fundus.[11] It has even been argued that if a person is prone to angle-closure, it is better for it to occur in a healthcare setting rather than spontaneously.[12] Patients should also be warned that for up to 4 hours their ability to drive may be compromised, although the extent is an issue of contention.[13,14] 2. Technical Preparation There are many different brands of direct ophthalmoscopes, but most have similar features. A labelled example is shown in Figure 2 and a guide to the common apertures available is shown in Table 4.

C

Table 1 Preparation for direct fundoscopy.

A B D

E

1. Introduction a) Ask the patient to remove their glasses, but contact lenses can be left in. b) Dilate their pupils if not contraindicated and wait as appropriate.

Figure 1 A retinal photograph of the normal fundus of a left eye. A: The optic disc, B: The macula, C: Superior vascular arcade, D: Inferior vascular arcade, E: An approximation to the maximum area of view obtained with a direct ophthalmoscope. 1. Introduction and Pupillary Dilatation Generally the patient’s glasses should be removed, unless they have an unusually large refractive error. Contact lenses should be left in. The examination is enhanced by undertaking ophthalmoscopy in a darkened room. The pupil will dilate slightly if the patient is asked to look in the distance. If the view of the posterior pole is inadequate, the pupil should be pharmacologically dilated, unless contraindicated. (Table 3) This improves the view from 15% of the fundus to 50%.[9] Tropicamide (1%) drops are generally regarded as the safest agent and can be supplemented with 2.5% Phenylephrine drops to enhance mydraisis.[10] A single drop is often all that is needed but a darkly pigmented iris generally requires a second drop and will take more time to dilate than a lightly pigmented iris.

2. Technical Preparation a) Darken the room. b) Check the ophthalmoscope: - Set the dial to 0 Dioptres. - Choose the appropriately sized aperture. c) Sit at the same eye level as the patient. 3. Patient Instruction a) Warn the patient: - That you will need to come very close to their eye. - That the light will be bright and possibly uncomfortable. b) Instruct them to fixate at a discrete point behind you and add ‘even if I get in the way’. c) Use your right eye with the ophthalmoscope held in your right hand to examine the patient’s right eye and vice-versa.

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Table 2 The examination process. 4. The Red Reflex - Start by examining the eye 50cm away and observe the reflection of the retina and underlying choroid. 5. The Optic Disc a) Maintain your view of the red reflex, move closer and place the thumb of your free hand on the patient’s forehead. b) Approach the eye at about 15º to the visual axis and to within about 2-3cm of the eye. Use the thumb on the patient’s forehead to stabilise yourself. c) Locate the optic disc, following the blood vessels back to their source as a guide. d) Use the lenses to bring the optic disc into sharp focus. This can be best done by using the edge of the disc as a reference point. 6. The Vasculature and Retina a) Angle the light beam to follow the vasculature out into the four main quadrants, also observing the surrounding retina. b) Ask the patient to look in the 8 cardinal directions, which will bring the different areas of the peripheral retina into view.

If the pupils are pharmacologically dilated, then the largest aperture on the ophthalmoscope should be used. In the instances where the pupil is not dilated, using a small aperture will minimise pupillary constriction. Reflection of light off the cornea can also interfere with obtaining an adequate view. Most modern ophthalmoscopes will use polarised light to overcome this and if necessary using a smaller aperture will reduce the glare further, however this is at the expense of retinal illumination. Start with the lens wheel at 0 Dioptres. Most direct ophthalmoscopes contain a series of lenses of varying refractive correction. They will either be convex (positive and black numbers*) or concave (negative and red numbers) to correct hypermetropia and myopia respectively. Increasing the strength of concave (negative) lenses shifts the point of focus further away from the viewer and towards the posterior pole of the eye.[15] These lenses are ‘dialled in’ using the index finger. * British ophthalmoscopes occasionally have the opposite notation so that black numbers (to correct myopia) are concave/minus. To coincide with the level of the optic disc, it is also important to sit at the same eye-level as the patient.

7. The Macula a) Finally, reduce the intensity of the light or switch to a smaller aperture if possible. b) Ask the patient to ‘look directly into the light’. This should bring the macula into view.

Table 3 Contraindications to pupillary dilatation

1) The patient requires neurological observations. 2) The patient has an old style of lens implant that is tethered to the iris. 3) There is a high risk of precipitating acute angle-closure glaucoma. 4) Patient refusal.

Figure 2 A standard direct ophthalmoscope, shown from behind (left) and from the front. (right). A: Cushioned brow rest, B: Viewing aperture, C: Lens wheel, D: Lens strength indicator, (typically red is negative and black positive) E: Rotating dimmer and on/off switch, F: Front light opening, G: Red-free filter switch, H: Aperture selection dial.

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Large aperture

Medium aperture

Small aperture

For standard use with dilated pupils

For undilated pupils or paediatric use

For use when viewing the macula

Slit

Red-free filter

Cobalt blue filter

To assess depth when viewing the retina or for use as a slitlamp

For assessment of the retinal nerve fibre layer and vasculature

For use with fluorescein, which will glow green in corneal defects

Table 4 Standard aperture settings.

direct

To look at the patient’s right eye, the examiner should hold the ophthalmoscope in the right hand and look through it with the right eye. (Figure 3) This is then reversed for the opposite side. Ideally, both eyes should be kept open, with the image suppressed in one eye. This is achievable with practice, but is by no means essential. 4. The Red Reflex Start by examining for the red reflex by shining the beam of light at the eye from about 50cm away.[17] There should be an orange-red glow from the choroid and overlying retina that fills the whole diameter of the pupil. (Figure 4) Opacities that obscure the reflex appear as dark shadows and can result from a variety of causes. (Table 5) The commonest cause is usually cataract, but other, more serious, pathologies can include retinal detachment, vitreous haemorrhage and intraocular tumours.[18] If required, the anterior segment can be brought into view by dialling in +10 Dioptres and thereby shifting the focus proximally.

ophthalmoscope

3. Patient Instruction Direct fundoscopy is an examination that requires the patient’s personal space to be entered. Considering that the normal reflex is to close the eyelids when an object approaches, special consideration should be given to gaining the patient’s cooperation and placing them at ease. Having gained consent, explain that the light may be slightly uncomfortable and that you need to come very close to get a detailed view. Strangely, it is quite common for patients (and doctors) to hold their breath. Telling the patient to keep both eyes open and breathing in a relaxed way may make things much easier for both parties.

Figure 3 How to hold the ophthalmoscope when performing fundoscopy.

The most important instruction is for the patient to fixate at a defined point horizontally directly in front of them*, essentially in the primary position. The instruction should be qualified with ‘even if I get in the way.’ [16] This action achieves two objectives. It stabilises the eye in a fixed position, as long as the point is well defined e.g. a particular letter on a Snellen chart, the tip of a door handle or a light switch. Focusing in the distance also abolishes the near reflex, which could otherwise cause pupillary constriction. *If the user is tall the sitting patient needs to look up slightly. Figure 4 A red reflex in a patient with aniridia.

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5. The Optic Disc While maintaining a view of the red reflex, move closer to the patient so that your free hand rests upon their forehead. One finger can then hold up the eyelid if required, while the thumb can be used to stabilise the ophthalmoscope. Approach at about 15° to the visual axis and move to within 2-3cm of the eye. This angle is intuitive, as one is essentially approaching along the direction of the blind-spot. The optic disc should be immediately visible. If only vasculature is seen, look at the main bifurcations which almost form ‘arrow-heads’ pointing towards the optic disc.[19] Table 5 What to assess in direct fundoscopy 1. Observe the red reflex Opacities are a feature of cataract, vitreous haemorrhage, corneal scar, retinal detachment and retinoblastoma. 2. Optic disc – Edge This is blurred and indistinct in papilloedema. 3. Optic disc – Colour If the disc is completely white or pale consider optic atrophy. 4. Optic disc – Cup-disc ratio If above 0.6 there is an association with glaucoma.

Once located, rotate the lens wheel to focus on the disc. As a reference point, use the disc edge and adjust the number of dioptres of correction until it is sharply focused. Generally, it is easier to scale up and down by trial and error than attempting to predict the refractive errors between yourself and the patient in advance. If there is no refractive error, then a small degree of divergence (negative and red numbers) will still be needed to shift the point of focus from the middle of the eye to the posterior disc. When looking at the optic disc, the edge, colour and cup-disc ratio should be observed. (Figure 1) Papilloedema is the commonest cause of an indistinct edge and may be secondary to raised intracranial pressure. (Figure 5) There may also be haemorrhages around the disc if this is of acute onset. The disc is normally a pale pink with a yellow cup. If the rim of the disc is pale then optic atrophy should be considered. (Figure 6) The physiologic cup is a small depression in the centre of the optic disc. The ratio of the diameter of the cup to the diameter of the disc is a marker associated with chronic glaucoma. (Figure 7) The cup-disc ratio is normally under 0.3 and is generally best measured in the vertical dimension.[20]

5. Venous Pulsations The presence of pulsations generally excludes raised intracranial pressure. 6. Vasculature – Arteries ‘Silver wiring’ and arterial thinning are associated with hypertensive change. 7. Vasculature – Veins Tortuous and ‘beaded’ veins are seen in diabetic retinopathy. 8. Vasculature – Vein and artery crossing points Arteriovenous ‘nipping’ where the vein is indented is a feature of hypertensive retinopathy.

Figure 5 Papilloedema

9. Observe the retina - Haemorrhage, exudate and neovascularisation are signs of diabetic retinopathy. - Discrete, raised lesions can be metastases, primary melanoma or retinoblastoma. - Scars may be iatrogenic or secondary to inflammatory disease. 10. Observe the macula - Macular oedema or exudate can be seen with diabetic maculopathy or neuroretinitis. - Drusen are associated with age-related macular degeneration.

Figure 6 Optic Atrophy

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Figure 7 Glaucomatous ‘Cupping’ with a Cup-Disc ratio of about 0.6. Spontaneous venous pulsations can also be looked for as the retinal vein emerges from the optic disc. This sign is subtle and is seen as an expansion of the whole vein during cardiac diastole. The sign is not present in about 12% of people, but is reliably absent in almost 100% of people with an intracranial pressure raised above 180 mmH2O.[21] Thus if seen, it is highly unlikely that the patient has significantly raised intracranial pressure at that moment in time.[22] 6. The Vasculature and Retina The main arcades of blood vessels emerge from the disc and head into the four main quadrants. By following these, an assessment of the state of the vasculature can be made. The retinal arteries are a brighter red than the veins and only three-quarters of the diameter, but characteristically reflect light as a bright stripe along their length.[9] A systematic method of assessment is to look first at the arteries, next the veins and then the arterio-venous crossing points.

The light beam can be angled to allow a peripheral view, but to see into the different regions, the patient should be asked to look in the 8 cardinal directions - essentially the four points of a compass and their intersecting diagonals. By gazing in a particular direction, the corresponding segment of the retina is brought into view. For example, asking the patient to look ‘down and to the left’ with their right eye will bring the lower left (inferior nasal) region into the central field of view.[15] This works for all eight regions and permits a thorough examination. 7. The Macula The macula is the avascular central region of the fundus and contains the central fovea. As such, it possesses the greatest density of cone photoreceptors, responsible for the highest acuity vision and colour perception. The area is exquisitely sensitive to light and examination can cause discomfort. The aperture on the direct ophthalmoscope should be reduced to a smaller setting and the intensity reduced if possible. As the normal point of fixation is over the fovea, by asking the patient to ‘look straight into the light,’ the macula should fall in the middle of the view. Again, pathology may be obvious, often in the form of drusen, exudate or haemorrhage. (Figure 9)

Whilst looking at the vasculature in the different regions, the surrounding retina can be simultaneously evaluated (Table 5). Haemorrhage, exudate, scars and other obvious ocular lesions should be seen. (Figure 8) Figure 9 Haemorrhage in the macular region in age-related macular degeneration. (Retinal Photograph)

Figure 8 Diabetic retinopathy with a pre-retinal haemorrhage. (Retinal photograph)

Comparison with other imaging modalities Is there still a role for the direct ophthalmoscope, and how does it compare to other imaging modalities? Certainly its use is advocated as a rapid and simple examination, particularly in a paediatric setting.[23] Also, the direct ophthalmoscope provides greater magnification to detect venous pulsations when considering raised intracranial pressure.[21] 12

Direct ophthalmoscopy is not the favoured technique in every setting. Prior to developing the UK national screening programme for diabetic retinopathy, studies found that although the specificity was higher (97% vs. 86%), the sensitivity was inferior to retinal photography (65% vs. 89%).[24] This has been mirrored in other studies.[25] Primary open-angle glaucoma is a leading cause of irreversible blindness and the direct ophthalmoscope has historically been important for the diagnosis and monitoring of disease progression. Recent studies have shown that semiautomated measurement devices may be preferable to direct observation and assessment of the vertical cup-to disc ratio.[26,27] There is a reasonable correlation between the two modalities, but the advantage of a computerised system is that inter-observer variability is reduced. This may be significant as when considering management a measurement error between two occasions may be interpreted as disease progression. Currently however, direct ophthalmoscopy is still relied upon. Computerised photography and scanning is expensive, not widely available and is still being validated. Conclusion Fundoscopy can appear daunting and there is a high level of unease regarding its use amongst many medical practitioners. However, the whole process can be confidently performed by following a logical succession of steps as set out in this review. To the non-specialist the direct ophthalmoscope will continue to remain both adequate and essential for the examination and diagnosis of the most common diseases of the eye. In a recent Christmas issue of the BMJ, Roger Armour also demonstrated how to build an working ophthalmoscope for less than £1, meaning that no doctor need now go without one on the grounds of cost.[28] It seems appropriate to finish as we started, with Helmholtz. He received many letters, including one which read, ‘Your Ophthalmoscope is excellent, but I cannot see anything with it.’ Invariably and pertinently, his reply was the same to all ‘Practice’.[2] References [1] Hirschberg J. The History of Ophthalmology. Blodi FC, trans. Bonn, Germany: JP Wayenbourg Verlag; 1992.

[2] Ravin J G. Sesquicentennial of the ophthalmoscope. Arch Ophthalmol. 1999 Dec;117(12):1634-8. [3] M’Kendrick JG. Hermann Ludwig Ferdinand von Helmholtz. London, England: T Fisher Unwin; 1899. [4] Jopling H. The principles of clinical examination. The Journal of Clinical Examination 2006 1: 3-6. [5] Gupta RR, Lam WC. Medical students' selfconfidence in performing direct ophthalmoscopy in clinical training. Can J Ophthalmol. 2006 41(2):16974. [6] Shuttleworth GN, Marsh GW. How effective is undergraduate and postgraduate teaching in ophthalmology? Eye 1997; 11 Pt 5:744-50. [7] Ang GS, Dhillon B. Do junior house officers routinely test visual acuity and perform ophthalmoscopy? Scott Med J 2002 47(3):60-3. [8] Olver J, Cassidy L. Ophthalmology at a Glance. Blackwell Publishing Ltd; 2005. [9] Snell RS, Lemp MA. Clinical Anatomy of the Eye. 2nd ed. Blackwell Science, Inc; 1998. p. 214230. [10] Pandit RJ, Taylor R. Mydriasis and glaucoma: exploding the myth. A systematic review. Diabet Med 2000 17(10):693-9. [11] Liew G, Mitchell P, Wang JJ, Wong TY. Fundoscopy: to dilate or not to dilate? BMJ 2006 332(7532):3. [12] Bhan KJ, Bastawrous A, Davey KG. Funduscopy: to dilate or not? Precipitation of angle closure may not be a disservice. BMJ 2006 332(7534):179. [13] Goel S, Maharajan P, Chua C, Dong B, Butcher M, Bagga P. Driving ability after pupillary dilatation. Eye. 2003 17(6):735-8. [14] Siderov J, Mehta D, Virk R. The legal requirement for driving in the United Kingdom is met following pupil dilatation. Br J Ophthalmol 2005 89(10):1379-80. [15] Riordan-Eva P, Whitcher JP. Vaughan & Asbury’s General Ophthalmology. 16th ed. McGraw Hill; 2004. p. 40-43. [16] Cozma I, Fraser S, Nambiar AK, Peter N, Spokes D. How to use an ophthalmoscope. Student BMJ 2004 12:309-348. [17] Khaw P-T, Shah P, Elkington AR. ABC of Eyes. 4th ed. BMJ Publishing group. 2004. p. 5-6.

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[18] McLaughlin and Levin The red reflex. Pediatr Emerg Care. 2006 22(2):137-40. [19] Orient JM. Sapira’s Art & Science of Bedside Diagnosis. 2nd ed. Lippincott Williams & Wilkins; 2000. p. 200. [20] Theodossiades J, Murdoch I. What optic disc parameters are most accurately assessed using the direct ophthalmoscope? Eye 2001 15(Pt 3):283-7. [21] Levin BE. The clinical significance of spontaneous pulsations of the retinal vein. Arch Neurol 1978;35:37-40. [22] McKee HD, Ahad MA. Spontaneous retinal venous pulsations can be present with a swollen optic disc. J Neurol Neurosurg Psychiatry 2004 75(6):941 [23] Sit M, Levin AV. Direct ophthalmoscopy in pediatric emergency care. Pediatr Emerg Care 2001 17(3):199-204. [24] Harding et al. Sensitivity and specificity of photography and direct ophthalmoscopy in screening for sight threatening eye disease: the Liverpool diabetic eye study. BMJ 1995 311:11311135. [25] Siu SC, Ko TC, Wong KW, Chan WN. Effectiveness of non-mydriatic retinal photography and direct ophthalmoscopy in detecting diabetic retinopathy. Hong Kong Med J 1998 4(4):367-370. [26] Wolfs RC, Ramrattan RS, Hofman A, de Jong PT. Cup-to-disc ratio: ophthalmoscopy versus automated measurement in a general population: The Rotterdam Study. Ophthalmology 1999 106(8):1597-601. [27] Watkins R, Panchal L, Uddin J, Gunvant P. Vertical cup-to-disc ratio: agreement between direct ophthalmoscopic estimation, fundus biomicroscopic estimation, and scanning laser ophthalmoscopic measurement. Optom Vis Sci. 2003 80(6):454-9. [28] Armour RH. Manufacture and use of home made ophthalmoscopes: a 150th anniversary tribute to Helmholtz. BMJ 2000 321(7276):1557-9. Acknowledgements We would like to thank A McKnight for his comments and advice. Conflicts of interest None.

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