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Review Article
Albinism: Particular Attention to the Ocular Motor System
Richard W. Hertle
ABSTRACT Access this article online Website: The purpose of this report is to summarize an understanding of the ocular motor system in www.meajo.org patients with albinism. Other than the association of vertical eccentric gaze null positions DOI: and asymmetric, (a) periodic alternating nystagmus in a large percentage of patients, the 10.4103/0974-9233.114804 ocular motor system in human albinism does not contain unique pathology, rather has Quick Response Code: “typical” types of infantile ocular oscillations and binocular disorders. Both the ocular motor and afferent visual system are affected to varying degrees in patients with albinism, thus, combined treatment of both systems will maximize visual function.
Key words: Albinism, Ocular Motor System, Visual Function
INTRODUCTION categories of regional hypopigmentation involving neuroectoderm (ocular albinism [OA]), neural crest (albinoidism), or both lbinism is a genetic condition of hypopigmentation caused (oculocutaneous albinism). In OA, there is hypopigmentation Aby an abnormality in melanin pigment production. The of ocular neuroectoderm (iris and retinal pigment epithelium) absence or reduction of melanin has a severe impact on the that manifests clinically with iris transillumination, macular development of the eye and visual system, such that persons hypoplasia, chorioretinal hypopigmentation, photophobia, and with albinism display a variety of ophthalmic deficits, including nystagmus. The term albinoidism is applied to a condition in foveal hypoplasia, translucency of the iris, nystagmus, reduced which hypopigmentation is limited to tissues of neural crest visual acuity and an abnormal decussation pattern at the optic origin (skin, hair, and iris stroma). Unlike patients with OA, chiasm.1,2 The characteristic, which is thought to distinguish those with albinoidism do not manifest macular hypoplasia, albinism from other visual disorders resulting in foveal nystagmus, photophobia, or decreased vision.2,4 hypoplasia and other disorders of hypopigmentation is the abnormal routing of visual pathways from the eye to the brain.1,3 EPIDEMIOLOGY Clinically, it is this abnormality in conjunction with phenotypic evaluation and ophthalmic examination that has been used to Albinism can affect people of all ethnic backgrounds. diagnose albinism. Approximately one in 17,000 people have one of the types of albinism.3,5 Prevalence of the different forms of albinism Albinism is not a single entity; it encompasses a heterogeneous varies considerably worldwide. OCA1 has a prevalence of group of congenital hypomelanotic disorders. Using one system approximately 1 per 40,000 in most populations but is very of classification oculo-cutaneous albinism (OCA1A), being the uncommon among African-Americans.3,5 In contrast, OCA2 is most severe type, is characterized by a complete lack of melanin the most common type of albinism in African OCA patients.3,5 production throughout life, while the milder forms OCA1B, The overall prevalence of OCA2 is estimated to be 1:36,000 in OCA2, OCA3 and OCA4 show some pigment accumulation over the USA, but is about 1:10,000 among African Americans.3,5 It time. These disorders can also be classified into three general affects 1 in 3,900 of the population in some parts of the Southern
The Children’s Vision Center, Akron Children’s Hospital, Akron, Northeast Ohio Medical Universities, Rootstown, Ohio, United States Corresponding Author: Dr. Richard W. Hertle, 300 Locust St., Suite 490, Akron, Ohio 44302, United States, E-mail: [email protected]
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Hertle: Eye Movements and Albinism
part of Africa.3,5 OCA3 or Rufous oculocutaneous albinism has A number of inherited diseases with nystagmus show a been reported to affect 1:8,500 individuals in Africa, whereas combination of immunological and pigmentation defects.11-20 it is very rare in Caucasians and Asiatic populations.3,5 Recently, Chediak-Higashi, Hermansky-Pudlak, Griscelli, and mutations in a fourth gene were shown to be the cause of paroxysmal autonomic instability with Dystonia syndromes are albinism, OCA4, and were reported to explain the disease in all autosomal diseases with these characteristics. The molecular approximately 5-8% of German patients with albinism but 18% links between immunodeficiencies and albinism reflect the of Japanese patients.6 fact that both melanosomes and secretory lysosomes are not secreted normally. Chediak-Higashi syndrome, a disease Clinical description characterized by repeated infections and albinism, shows the All types of OCA and OA have similar ocular findings, including presence of abnormally large lysosomes and melanosomes, various degrees of early onset nystagmus, hypopigmentation of suggesting that melanosomes are not secreted normally, and iris and retinal pigment epithelium, foveal dysplasia, ametropia, supporting a functional link with the secretory lysosomes of strabismus and reduced best-corrected visual acuity [Figure 1]. hematopoietic cells.21 Photophobia and light interference may be prominent. The abnormal crossing of chiasmatic, post-chiasmatic fibers can be Diagnostic methods demonstrated by monocular visual evoked potentials. The diagnosis of OCA is usually based on clinical findings of hypopigmentation of the skin and hair, in addition to the Because albinism is often associated with decreased vision, characteristic ocular symptoms.1,3,22-25 However, due to the nystagmus, and refractive errors, recognition visual acuity may clinical overlap between the OCA subtypes, other testing vary depending on an eccentrically induced head position, such as molecular, electrophysiological or radiological may be accuracy of glasses prescription, and experience of the visual necessary.1,3,22-25 Molecular genetic testing of tyrosinase (TYR) acuity tester. Reliance on fixation preference testing, such and OCA2 are available on a clinical basis, while at present, as Teller acuity cards, to assess vision has been required for analysis of tryparedoxin peroxidase gene (TYRP1) and Ter patients younger than 2 years.7 Sweep visual evoked potential macrodomain organizer matS-binding protein gene (MATP) is (VEP) testing is a novel technique that can be used to assess on research basis only.1,3,22-25 visual acuity in pre-verbal patients with albinism.8 Reports have demonstrated a correlation between binocular grating acuity Increased crossing of optic nerve fibers in the chiasm is one of and future letter recognition acuity in patients with ocular and the most consistent findings in albinism in all species.26,27 In oculocutaneous albinism.9 Studies demonstrates that sweep humans, it has been found to be highly specific and asymmetries VEP testing can be used as a predictive tool for recognition in visual evoked potentials are very helpful as a diagnostic acuity in patients with albinism.3,8,10 It has been reported that tool for albinism. While the great majority of children with Teller acuity over-estimates recognition acuity in children with albinism show crossed hemispheric asymmetry on visual evoked albinism. Because albinism is a rare diagnosis, most published potentials, occasional all otherwise classic albinism show no studies that compare grating with recognition acuity involve evidence of hemispheric asymmetry.26,27 small patient numbers.3,8,10 Individuals with mild ocular or oculocutaneous albinism are often misdiagnosed as having idiopathic Infantile Nystagmus Syndrome (INS). The finding of subtle signs of ocular hypopigmentation in some infantile nystagmus and anomalous head postures (AHPs) [Figure 2] syndrome patients with good vision has led to speculation that patients with idiopathic INS may actually be heterozygous for albinism. Simon et al. have demonstrated that when patients with INS are carefully examined, many show iris transillumination, blunting of the macular reflex, and chorioretinal hypopigmentation consistent with albinism.28 In evaluating the INS patient, it is critical to perform a careful slit lamp examination with the room lights turned off, the door closed, and a retro-illumination through a thin, axial light beam to detect basal iris transillumination. Varying degrees of macular hypoplasia (absence of the foveal pit, absence of macula lutea pigment, absence of normal
Figure 1: Typical appearance of skin, hair, lashes and eyes of patient with oculo- macular pigment epithelial hyperpigmentation, and passage cutaneous albinism 1. Complete iris transillumination is also illustrated of retinal vessels through the fovea), together with other
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Hertle: Eye Movements and Albinism
Figure 2: A composite illustration of the typical differences in the photographic Figure 3: Illustration of typical anomalous head posturing in patients with albinism. appearance of a normal optic in disc (top) and patient with albinism (bottom) Many patients have a chin-down posture associated with a vertical eccentric gaze nystagmus null position, although horizontal head/face turns dominate
signs of ocular hypopigmentation, suggest the diagnosis of disorders because the disturbances have highly varied causes and albinism. However, isolated foveal hypoplasia may also occur as present different clinical pictures. Eye-movement abnormalities a hereditary condition in children with normal pigmentation. of supranuclear origin are characterized by gaze palsies, tonic Other valuable clinical signs of albinism are often overlooked. gaze deviation, saccadic and smooth pursuit disorders, vergence For example, patients with albinism have a positive angle abnormalities, nystagmus, and saccadic oscillations. Supranuclear kappa that is usually absent in patients with idiopathic INS. disorders such as nystagmus in infancy and childhood result Studies have suggested a characteristic optic disc appearance from brain dysfunction above the level of the ocular motor in albinos consisting of a small, cupless disc, with temporal nerve nuclei. entrance and situs inversus of the vessels, an oblique long axis of the disc26 [Figure 3]. In 1985 Collewijn suggested a subdivision of albinos into three classes of oculomotor behavior. Class I was characterized by Other ocular and systemic hypopigmentation disorders should vigorous spontaneous nystagmus (of the pendular unidirectional be considered in the differential diagnosis of albinism. Creel et jerk or bidirectional jerk type), the absence of true horizontal al. have reported asymmetrical hemispheric VEPs in patients optokinetic nystagmus (OKN) but the presence of the ability with Prader-Willi syndrome (a condition characterized by to control the direction of gaze in an imprecise way. In Class II hypotonia, hypomentia, hypogonadism, and hyperphagia).29 there is a vigorous unidirectional jerk nystagmus that reverses Aland Island eye disease (Forsius-Eriksson syndrome) is a form in direction spontaneously or as a result of visual stimulation. of ocular hypopigmentation associated with electroretinographic Moving stimuli typically elicited inverted pursuit, the smooth findings of congenital stationary night blindness.15 Other ocular eye movements having a direction opposite to that of the and systemic hypopigmentation disorders such as Waardenburg stimulus movement. Class III is characterized by very little or syndrome and phenylketonuria also lack the hemispheric VEP no spontaneous nystagmus and virtually normal oculomotor asymmetry seen in albinism. responses.30
THE OCULAR MOTOR SYSTEM There are several types of nystagmus usually seen in infancy. The most common are those in the INS (INS, aka Eye movements bring visual stimuli to the fovea, maintain “congenital” nystagmus). Others are the nystagmus called foveal fixation of stationary and moving targets during head Fusion Maldevelopment Nystagmus syndrome (FMNS, aka movements, assist with body orientation in space and during latent/manifest latent nystagmus [LMLN]) and the pendular motion. These movements are performed by the ocular motor nystagmus of the Spasmus Nutans syndrome. The nomenclature system that consists of ocular motor nerves and nuclei in recommended by the Classification of Eye Movement the brainstem originating in the cerebral cortex, cerebellum, Abnormalities and Strabismus Working Group is referred in this vestibular structures, and the extraocular muscles. Anatomically, report as it eliminates the confusing and misleading terminology the ocular motor system may be divided according to location of the classical names found in the literature.31 The nystagmus into infranuclear, nuclear, internuclear, and supranuclear comprised in the INS is usually present at birth or noted in components. It is important to distinguish between supranuclear, early infancy during the various sensitive periods defining the internuclear, nuclear and infranuclear (orbital, cranial nerves) development of visual fixation and it persists throughout life.
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Hertle: Eye Movements and Albinism
Figure 4: Eye movement recording from patient with albinism and typical periodic Figure 5: Eye movement recording data of OS from patient with oculo-cutaneous alternating nystagmus performed under binocular conditions using velocity albinism performed under binocular conditions using data from the left eye data trace from the preferred right eye over 200 s illustrating a typical periodic, illustrating a typical asymmetry during a periodic type of rhythmic cycle with symmetric, oscillation with approximately 90 s of jerk right followed by 10-20 s of changes in the waveforms evident when the fast phase is to the left (pure jerk left slowing and direction change followed by 90 s of jerk left. Up is right (R), down is wave form) and to the right (jerk right with extended foveation). It is easy to see that left (L), upper trace is position and lower trace is velocity in both upper and lower this patient will have better vision and visual function during the jerk right phase of portions of the figure the cycle. OS = left eye, up is right (R), down is left (L), upper trace is position and lower trace is velocity
The syndrome consists of one or more types of characteristic waveforms, head turns, tilts, or oscillations.32-35 Two of the more particular associations of the INS and albinism include the predominant and underappreciated presence of an The nystagmus waveform in idiopathic INS (in which there eccentric vertical gaze null (chin-up or chin-down head posture), is no afferent visual pathway rerouting) is identical to the and the presence of spontaneous changing direction/intensity ones present in albinism, suggesting that anomalous afferent of the oscillation43 [Figures 2, 4 and 5]. pathway of the albino visual system interferes with ocular motor calibration in the same way as other congenital or early Most clinicians are familiar with the dynamic oscillation of infantile sensory system deficits and it is that similar anomalous acquired periodic alternating nystagmus (PAN). Acquired PAN ocular motor calibration that is primarily responsible for INS has a specific pattern identified by the presence of spontaneous in albinism.7,34,36-39 In addition to retinogeniculate, cortical, and nystagmus in the primary position, which beats horizontally in intracortical neural misrouting, albino animals have also been one direction for 1 or 2 min, followed by a quiet period, and found to have misrouting of their subcortical visual pathways, then reappearance of the nystagmus in the opposite direction which are intimately involved in optokinetic responses.40 for a similar length of time36,44-46 [Figure 4]. It is usually seen in Although numerous studies have described INS pathophysiology association with vestibulo-cerebellar disease, neurodegenerative and its effect on the visual system, its etiology remains elusive. conditions such as Friedreich’s ataxia, or vision loss.36,44-46 The Defects involving the saccadic, optokinetic, smooth pursuit, and dynamic neutral zone in INS varies spontaneously with time in fixation systems as well as the neural integrator for conjugate up to 1/3 of patients with albinism while fixating a static target. horizontal gaze have been proposed.7,34,36-39 Biomedical control Many of these albino patients with INS, exhibit an asymmetric, system models have reproduced this oscillation and it has been (a) periodic alternating nystagmus (APAN).34-36,38,47-49 Unlike attributed it to a “high gain instability” in the ocular motor acquired PAN, APAN is usually asymmetric, with unequal system. This loosely translates as an error in “calibration” of time periods of jerk nystagmus in each direction. APAN has the eye movement system during attempted fixation. Including all the characteristics of INS except that the null point shifts genetic predisposition, many clinical conditions are associated position in either a regular (periodic) or irregular (aperiodic) with the INS oscillation.41,42 pattern and is usually also asymmetric (unequal intervals of jerk nystagmus in each direction) [Figure 5]. This results in Regardless of its clinical associations, nearly all patients with changes in the intensity and/or direction of the nystagmus INS have infantile onset in common; we can deduce that this from seconds to minutes. APAN encompasses all idiosyncratic oscillation is most likely to occur in an immature ocular motor variations in intra- and inter-cycle timing and amplitudes; more system. The etiology is probably multifactorial but the final specific nomenclature can be applied when these characteristics common pathway may be interference with neural “cross talk” are known. The occurrence of APAN in INS was thought to between the developing sensory and motor systems during a be rare but many authors have reported otherwise.34-36,38,47-49 period of developmental sensitivity. There is also switching between accelerating and linear slow
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phases in the two directions and asymmetries, even in those abnormal cross-talk from a defective sensory system to the patients who’s APAN was essentially periodic. The recognition developing motor system at any time during the motor system’s of both PAN and APAN is essential when surgery is being sensitive period [Figures 6 and 7]. This can occur from conception considered for either acquired nystagmus or INS. Abadi and due to a sensory defect (e.g., foveal, retinal dystrophy), during Pascal studied 25 subjects with oculocutaneous albinism (16 embryogenesis due a developmental abnormality (e.g., optic tyrosinase negative and 9 tyrosinase positive) and seven with nerve hypoplasia), or after birth during infancy (e.g., congenital OA (five x-linked and two autosomal recessive) and found that cataracts). This theory of the genesis of INS incorporates a 12 exhibited APAN.36 The nystagmus waveforms encountered pathophysiologic role for the sensory system in its genesis and during the APAN active phases were either jerk-with-extended- modification. While the set of physiologic circumstances may foveation or pseudocycloid, whereas a variety of oscillations differ, the final common pathway is abnormal calibration of the (including triangular and bidirectional) were evident during ocular motor system during its sensitive period. The primary the quiet phases. Gradstein et al. diagnosed APAN in 18 (9%) ocular motor instability underlying INS is the same but its of their 200 patients with infantile nystagmus, although most clinical and oculographic expression are modified by both initial had not been diagnosed49 with APAN before referral, despite and final developmental integrity of all parallel afferent visual changing nystagmus reported by referring clinicians. In those system processes. 18 patients, they found five to have ocular or oculocutaneous albinism and 16 had an alternating AHP. The APAN cycle was of The other childhood form of nystagmus reported in patients with variable duration, often with asymmetric right- and left-beating albinism is FMNS (FMNS, aka LMLN) which exhibits: A jerk components. Half of the patients showed a combination jerk nystagmus with either a linear or decreasing-velocity exponential and pendular waveforms in both phases. In another report, slow phase identical to that of gaze-paretic nystagmus; strabismus; the same authors found ocular oscillations consistent with INS alternating hyperphoria/dissociated vertical deviation; and evident in 24 of 27 patients with oculocutaneous albinism and pendular torsional nystagmus in primary position51-55 [Figure 8]. Hermansky-Pudlak syndrome (HPS) and half showed PAN. They The constantly present, conjugate, horizontal, jerk nystagmus concluded that most patients with HPS have INS, and many have increases in intensity by monocular occlusion, blurring, or PAN. Hosokawa et al. found periodicity in the time-frequency reducing image brightness. A jerk nystagmus with a linear distribution in 3 of 13 patients (23%) with albinism and INS.50 slow phase may be present when both eyes are closed. Rarely, the nystagmus is only evoked by the “pure” or “true” latent Hertle, et al. reported 78 patients with APAN and found that condition and occurs only with uniocular viewing (i.e., the other 46% had an associated diagnosis of oculocutaneous or OA34. eye being occluded). That is, there is no nystagmus when both Most of their patients had strabismus (72%) and an AHP (87%) eyes are viewing, but when one eye is occluded, jerk nystagmus with one-third having a visually preferred eye. The clinical head/ develops in both eyes, with the fast phases toward the uncovered face position was evenly split between those patients with a static eye, The term, “manifest latent nystagmus” was first defined head posture and a dynamic (alternating) posture. Interestingly, by Kestenbaum as being present with both eyes open but only those patients with strabismus were more likely to have a static one being used for fixation. Using eye movement recordings head posture, even with a periodic rhythm detected on eye- mild fusion maldevlopment nystagmus (FMNS) with both eyes movement recordings. viewing can usually be detected in those patients who may appear to have “pure” latent nystagmus clinically. True/pure Although, INS may result from a primary genetic defect directly affecting ocular motor calibration, it may also result from
Figure 6: Eye-movement video and recording from an 86 year-old patient with Figure 7: Patient with albinism and unidirectional direction jerk Infantile Nystagmus albinism and Infantile Nystagmus syndrome. The recording illustrates conjugate, jerk syndrome (INS) waveforms with change in direction with changing eye fixation with extended foveation waveforms. Notice that after the 2 s mark the nystagmus (INS with “latent component”). Note the accelerating slow phases; R-right; L-left. improves due to a null position in immediate left gaze. On the figure, up is right, Figures, by convention, eye motion to the right up and to the left down, OD = right down is left eye, OS = left eye, Sec = seconds
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Figure 8: Eye movements (position and velocity) of albino patient with Fusion Figure 9: Eye movement recordings from the null position before (left panels) and Maldevelopment Nystagmus syndrome (FMNS) and changing Nystagmus jerk after (right panel) eye muscle surgery in a patient with albinism showing significant direction to the direction of the fixing eye (note linear and decreasing velocity slow favorable changes in foveation without a significant change in frequency phases typical of FMNS)
FMNS “latent nystagmus vera” is uncommon.51-55 The intensity transcutaneous vibratory or electronic stimulation of the face of FMNS decreases when visual attention declines and increases and neck, injection of botulinum toxin, and a variety of surgical during attempted fixation. FMNS may clinically resemble other procedures. Excepting those treatments that directly improve types of nystagmus (e.g., INS with a latent component) and visual acuity (spectacle and contact lens correction of refractive require eye-movement recordings to differentiate it. errors), all these treatments have in common a desired effect of reducing the nystagmus intensity directly or indirectly, The prevalence of strabismus averages 53% in patients with allowing for an increase in visual acuity. In a review of a total of albinism but varies depending on the phenotype or genetic 361 patients undergoing surgical repositioning of the eyes for diagnosis, with a prevalence of almost 100% in patients OCA1. INS from 21 reports in which vision was measured both pre- The most common forms are basic comitant esotropia or operatively and post-operatively, 273 (76%) had improved vision exotropia, although all motor components of the Infantile after the surgery.34,38,63-71 There are specific reports showing an Esotropia syndrome have been reported, i.e., dissociated improvement in 1 or greater LogMar in OCA patients after deviations, apparent over- or under-action of the obliques, extraocular muscle (EOM) surgery72 [Figure 9]. alphabet patterns. There are also reports of frequent saccadic intrusions in patients with albinism, the sizes of which were CONCLUSIONS correlated with velocities of steady drifts in fixations.56 Other than the association of vertical eccentric gaze null positions TREATMENT and APAN in a large percentage of patients, the ocular motor system in human albinism does not contain unique pathology, Other aspects of visual functions have been reported affected in rather has “typical” types of infantile ocular oscillations and patients with OCA and INS, both with and without diagnosed binocular disorders. This summary emphasizes that both the sensory system deficits.3,57-61 These include contrast sensitivity, ocular motor and afferent visual system are affected to varying color vision, motion perception, temporal luminance, contour degrees in patients with albinism, thus combined treatment of interaction, smooth pursuit and OKN.3,57-61 Despite foveal both systems will maximize visual function. hypoplasia, spectacle correction should be encouraged in children with albinism, since improved visual acuity and ocular REFERENCES alignment and reduction of abnormal head positions are among 1. Dorey SE, Neveu MM, Burton LC, Sloper JJ, Holder GE. The the recognized benefits. Children with albinism may similarly clinical features of albinism and their correlation with visual appreciate improved vision from INS surgery and from eye evoked potentials. Br J Ophthalmol 2003;87:767-72. muscle surgery which improves the ocular oscillation and 2. Summers CG. Albinism: Classification, clinical characteristics, secondary torticollis.34,39,43,62 and recent findings. Optom Vis Sci 2009;86:659-62. 3. Grønskov K, Ek J, Brondum-Nielsen K. Oculocutaneous albinism. Orphanet J Rare Dis 2007;2:43. Numerous treatments have been described for INS. These 4. Proudlock F, Gottlob I. Foveal development and nystagmus. include dietary manipulation, drugs, contact lenses, prisms, Ann N Y Acad Sci 2011;1233:292-7. biofeedback, intermittent photic stimulation, acupuncture, 5. Ohlsson J, Villarreal G, Sjöström A, Abrahamsson M, Sjöstrand
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Hertle: Eye Movements and Albinism
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