The Role of Funduscopy and Fundus Photography in Strabismus Diagnosis GAIL V. MORTON, CO, NEIL LUCCHESE, MD, BURTON J. KUSHNER, MD

Abstract: Fundus photographs taken in 66 patients with vertical strabismus were analyzed in a blind study with respect to ocular torsion. The objective presence or absence of ocular torsion was then correlated with the patient's clinical diagnosis. The presence or absence of objective ocular torsion as seen in fundus photographs had a sensitivity of 0.86 and a specificity of 0.96 for diagnosing the presence of oblique dysfunction, and a sensitivity of 0.96 and specificity of 0.83 for diagnosing the presence of normal oblique function. [Key words: diagnostic, cyclotropia, funduscopy, fundus photography, hypertropia, motility restrictions, obliques, strabismus, torsion.] Ophthalmology 90:1186-1191, 1983

In 1856 von Graefe reported that vertical macular dis­placement could be observed ophthalmoscopically in a patient with incyclotropia. 1 Locke2 described shifting of the blind spot in the visual field of patients with A and V patterns as well as vertical ocular muscle imbalances. Levine and Zahoruk3 using fundus photography studied the disc-fovea relationship in patients with vertical muscle pareses.

Since the obliques have a greater torsional action than the vertical recti,4 the presence of substantial ocular torsion suggests oblique dysfunction. Although the double Mad­dox rod test is an excellent test for subjective torsion, sensory adaptations may make a subjective determination of ocular torsion inconsistent with the objective deter­mination of ocular torsion as has been pointed out by Guyton and von Noorden.s Also, in some patients the double Maddox rod test cannot be used. Children are often incapable of reliable sUbjective responses. Patients without binocularity may not be able to appreciate si­multaneously the red and white Maddox rod. Patients with a very large horizontal or vertical deviation may have difficulty determining when the red and white lines are in fact parallel due to the large distance between them.

From the Department of Ophthalmology, University of Wisconsin Medical School, Madison, Wisconsin.

Presented at the Eigh:ty-seventh Annual Meeting of the American Academy of Ophthalmology, San Francisco, California, October 3D-November 5, 1982.

Reprint requests to Gail V. Morton, CO, Department of Ophthalmology, Clinical Science Center, 600 Highland Avenue, Madison, WI 53792.

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Since 1975, one of us (BJK) has been routinely doc­umenting the objective presence or absence of ocular torsion as seen ophthalmoscopically in patients with ver­tical strabismus, and has felt it is a useful diagnostic ob­servation. No data exists, however, as to the accuracy, reproducibility, or clinical usefulness of the objective de­termination of ocular torsion.

The purpose of this study was to evaluate the repro­ducibility of a technique of assessing the presence of ob­jective torsion by fundus photography in a blind manner, and to determine if the objective assessment of ocular torsion is a clinically useful diagnostic test.

METHOD AND MATERIALS

This study consists of 66 patients with vertical stra­bismus in whom we took fundus photographs for the objective documentation of ocular torsion. In all but one patient both eyes were photographed. This included 34 fellow eyes with normal ocular filotility in patients with uniocular motility problems. Eight patients were pho­tographed both before and after surgery.

Photographs were taken through a dilated pupil ap­proximately 20 minutes after instillation of two drops of tropacamide. We used the standard Zeiss fundus camera equipped with the chin rest and head support. The pho­tographer took care to observe that the patient's head was straight while being photographed, however, no spe­cial head brace, bite bar, nor leveling device was used.

0161-6420/83/1000/1186/$1.10 © American Academy of Ophthalmology

MORTON, et al • ROLE OF FUNDUSCOPY AND FUNDUS PHOTOGRAPHY

Fig 1. Photograph of an intorted fundus. The fovea lies above the geo­metric center of the disc.

Fig 3. Photograph of a fundus showing no torsion. The range of the position of the fovea in the absence of torsion lies between the black lines.

The patient fixated on the internal fixation device within the camera. Kodacolor 25 ASA film was used for all photographs. Early in the study four photographs were taken of each eye; however, the reproducibility of the findings in the multiple photographs made it apparent that this was not necessary. For the majority of patients in the study, two photographs were taken of each eye at each photographic sitting. Averaging the multiple pho­tographs was not necessary because in all cases there was no discrepancy between the multiple photographs. Only one photograph of each eye from each photographic ses­sion was used to comprise our series of 139 photographs.

All of the photographs were evaluated separately by two of the authors (GYM and NL) who were unfamiliar with the clinical diagnosis. Each photograph was rated as being intorted, normal, or extorted. We used the fol­lowing criteria in our assessments. Eyes were considered intorted if the fovea was located above the geometric center of the disc (Fig I), eyes were considered extorted

Fig 2. Photograph of an extorted fundus, where the fovea lies below the inferior margin of the disc.

ifthe fovea was below the bottom of the disc (Fig 2), and eyes were considered normal if the fovea lay in an area between the geometric center and the bottom of the disc (Fig 3). These are readily identifiable landmarks facili­tating the assessment of ocular torsion by funduscopy. For those eyes in which the fovea was right on the border between normal or torted, a rating of borderline intorted or borderline extorted was used. In cases where the two observers differed, a third observer (BJK) graded the pho­tographs in a similarly blinded manner. The assessment recorded was the one in which two of the three observers concurred. We then compared the objective funduscopic determination of torsion to the clinical diagnosis of each patient to determine the clinical usefulness of this test. To be considered consistent with the clinical diagnosis, the objective fundus torsion rating had to meet the fol­lowing criteria: (J) the fundus had to be rated normal in eyes without oblique dysfunction; (2) eyes with superior oblique overaction or inferior oblique underaction had to be rated intorted or borderline intorted; and (3) eyes with superior oblique underaction or inferior oblique overaction had to be rated extorted or borderline extorted.

RESULTS

The two observers agreed on the objective assessment of torsion in 91 % of the photographs. Those cases in which the observers differed were instances in which one observer thought the fundus was borderline torted and the other did not. In no instance did one observer think that torsion was definitely present while the other thought it was definitely not present.

A comparison of the objective funduscopic determi­nation of torsion to the expected presence of torsion based on the patient's clinical diagnosis is seen in Table 1. Sev­enty-three of the 84 eyes that clinically showed oblique

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Table 1. Comparison 01 Clinical Diagnosis and Objective Determination of Torsion

Fundus photograph Rating

Intorted Borderline Intorted Normal Borderline Extorted Extorted

Clinically Underacting Extorters or Overacting Intorters

No. of Eyes

26 10 4

dysfunction were rated as torted or borderline torted giving a sensitivity of 0.86 for the determination of torsion. Sev­enty-three of the 76 eyes rated as intorted or borderline torted, in fact had oblique dysfunction, giving a specificity of 0.96 for the determination of torsion. Fifty-two of the 55 eyes with clinically normal oblique function were rated as normal giving a sensitivity of 0.95 for the determination of normal oblique function. Fifty-two of the 63 eyes rated as normal, in fact had normal oblique function, giving a specificity of 0.83 for the determination of normal oblique function.

If we consider the borderline torted eyes as representing true torsion, our parameters are similar to those outlined by Bixenman and von Noorden6 for the disc-fovea re-

Clinically Normal Torsional Muscles

No. of Eyes

52 3

Clinically Underacting Intorters or Overacting Extorters

No. of Eyes

7 10 27

lationship in normal subjects. There were ten photographs rated as borderline intorted. All of these patients clinically showed oblique dysfunction indicating true intorsion. There were 13 photographs rated as borderline extorted. Of these, ten patients clinically showed oblique dysfunc­tion indicating true extorsion. Three were fellow eyes with normal ocular motility and are considered false pos­itives.

Our objective assessment of torsion is grouped by clin­ical diagnosis in Table 2. The grading of fundus photog­raphy was inconsistent with the clinical diagnosis in only 14 eyes for an overall accuracy of89%. This included the three normal fellow eyes rated as borderline extorted. In addition, there were two eyes with mild superior oblique

Table 2. Clinical DiagnosiS of Eyes Photographed

Photographs Photographs Total Eyes Consistent with Inconsistent with

Diagnoses Tested Clinical Diagnosis Clinical Diagnosis

1. Bilateral SO palsy 8 7 1 2. Unilateral SO palsy 16 15 1 3. Comitant large HT 4 4 0 4. Elevation in adduction due to restriction:

Normal obliques 6 6 0 10 overaction 2 2 0

5. Ilird nerve palsy 3 3 0 6. Oblique dysfunction with large horizontal deviation 3 3 0 7. XT with HT without oblique dysfunction 3 3 0 8. Dissociated hypertropia:

Normal obliques 4 4 0 10 overation 4 4 0 SO overaction 10 10 0

9. A patterns: Normal obliques 4 4 0 SO overaction 22 18 4

10. V patterns: 10 overaction 10 5 5

11 . SR palsy 1 1 0 12. 10 palsy 1 1 0 13. Primary 10 overact ion 2 2 0 14. Primary SO overalion 2 2 0 15. Normal fellow eyes 34 31 3

TOTAL 139 125 14

Legend: SO = superior oblique; HT = hypertropia; 10 = inferior oblique; XT = exotropia; SR = superior rectus.

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MORTON, et al • ROLE OF FUNDUSCOPY AND FUNDUS PHOTOGRAPHY

pareses that did not demonstrate identifiable objective torsion. One patient had only 2 diopters of hypertropia in the primary position and only 10 diopters of hyper­tropia in the contralateral side gaze fields. The other was a patient with a bilateral asymmetric superior oblique palsy in whom objective torsion could only be seen in the more paretic eye. The lesser paretic eye was only 4 diopters hypertropic in the field of the ipsilateral superior oblique. The remaining nine inconsistencies involved "A" and "V" patterns, which clinically showed oblique over­action but did not show objective torsion in the fundus photographs. This was our largest source of inconsisten­cies.

DISCUSSION

From the clinical perspective, there were several in­stances where the objective documentation of torsion proved useful in the diagnosis of vertical muscle problems. In asymmetric bilateral superior oblique palsy, the palsy in the lesser affected eye can be "masked" by the large hypertropia in the other eye. Bilateral objective torsion indicates that both superior obliques are palsied. In our own study three of the four patients with bilateral "masked" superior oblique palsies had bilateral objective torsion.

In long-standing unilateral superior oblique palsy with spread of comitance the deviation becomes similar in all fields of gaze and isolating the paretic muscle may be difficult. These patients often clinically appear similar to those with large comitant-hypertropias, not due to oblique dysfunction. In all such patients in our study, the objective determination of torsion was accurate in separating these two types of patients.

Patients with dissociated vertical divergence (DVD) may show elevation in adduction when the eye is dis­sociated by the nose. This may be hard to distinguish clinically from inferior oblique overaction. Patients with DVD do not demonstrate objective torsion when the eye is in the primary position unless there is coexisting inferior oblique overaction. The presence or absence of inferior oblique overaction coexisting with DVD was diagnosed successfully on fundus photography in all patients in the study with DVD. For the purpose of interpreting the data in this study, a patient was clinically felt to have DVD with normal oblique function if weakening the superior rectus eliminated the elevation in adduction. Patients were clinically felt to have inferior oblique overaction if a recession of the inferior oblique eliminated the elevation in adduction. One would not expect weakening the in­ferior oblique to eliminate the elevation caused by DVD.

Objective funduscopic determination of torsion was useful in diagnosing oblique dysfunction combined with a large horizontal deviation, such as a IIIrd or VIth cranial nerve palsy. It was also useful in diagnosing patients with a nonparetic large angle exotropia associated with a hy­pertropia not due to oblique dysfunction. In such patients it is sometimes difficult to observe the eyes in the field

of action of the obliques due to the large horizontal de­viation. In our study fundus photographs helped docu­ment the presence of oblique dysfunction in all nine pa­tients of this type. Patients with third cranial nerve palsy showed intorted fundi, since the intorsion ofthe superior oblique was unopposed.

Horizontal restrictions of eye movement may produce an elevation or depression in adduction simulating an oblique dysfunction. Ifno oblique dysfunction is present, objective torsion is not present in the primary position. If there is oblique dysfunction in addition to a horizontal restriction, objective torsion is present in the primary position. In all six patients in our study with vertical deviations in adduction, secondary to horizontal restric­tions, but with normal oblique function, objective torsion was not present. In the two patients with elevation in adduction associated with horizontal restriction, but with true oblique dysfunction, the fundi appeared torted.

The presence of torsion has been reported in patients with pareses of the vertical recti.2

,3 The relative anterior­posterior course of these muscles would suggest that their being paretic would have minimal effect on ocular tor­sion.7 Although it is possible that the vertical recti do have a significant torsional action, another explanation may explain the cycloptropia reported with paresis of these muscles. If, for example, the superior rectus is pa­retic, a large hypotropia would be present. If the involved eye is brought into the primary position to test for ob­jective cyclotropia, an excessive amount of elevation would be required from the inferior oblique muscle. This could have the effect of creating a secondary excyclotropia due to the excyclorotary effect of the inferior oblique. Similarly, if there is a paretic inferior rectus, the excessive depression required from the superior oblique muscle to bring the eye into the primary position could result · in an incyclotropia. One patient seen by us subsequent to this consecutive series of patients shed light on this issue. The patient had undergone surgery for ptosis on his left eye as a young child. It consisted of a transposition of the superior rectus into the upper lid (Motais-Berke pro­cedure).8 After surgery he developed a large left hypo­tropia. When examined by us at age 29, he demonstrated 20 diopters ofleft hypotropia in the primary position and appeared to have a marked left superior rectus palsy. He reported 70 of subjective left excyclotropia with the double Maddox rod test. We performed a transposition of the left medial rectus and the left lateral rectus to the original site of the left superior rectus insertion (Knapp proce­dure).9 Intraoperative forced duction testing was normal in the left eye. After surgery his ocular motility was sub­stantially improved and he demonstrated only 5 diopters of left hypotropia in the primary position. He reported no subjective cyclotropia after surgery with the double Maddox rod test. Fundus photography postoperatively demonstrated 50 of correction of left excyclotropia as compared to the preoperative fundus appearance (Figs 4, 5). The difference between the 50 of objective correction of torsion and the 70 subjective correction of torsion is explainable by the inaccuracies of subjective torsion test­ing.5 One would not expect vertical displacement of both

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Fig 4. This is the preoperative fundus photograph of a patient with a superior rectus palsy and extorsion secondary to a Motais-Berke pro­cedure. The macula is located at an angle of 21 ° below the disc.

the medial and lateral recti in the same eye to produce any torsional change. Correction of the excyclotropia seen in this patient after horizontal rectus muscle surgery would suggest that the preoperative excyclotropia was due to excessive innervation of the ipsilateral inferior oblique needed to bring that eye into the primary position for fundus photography.

Patients with "A" and "V" patterns were our greatest source of inconsistencies. Analysis of the patients with "A" and "V" patterns in whom the fundus photographs were inconsistent with the clinical assessment of oblique function did not reveal any common characteristics. The operative results were no different with respect to pattern reversals after surgery or postoperative oblique overactions or underactions in patients with "inconsistent" ratings, when compared to the patients in whom the torsion rat­ings were "consistent" with their clinical assessment. The reason for the high degree of inconsistencies in patients with "A" and "V" patterns is not clear.

Fundus photography is a means of documenting find­ings that are visible ophthalmoscopically. With the ex­ception of those patients in whom the disc-foveal rela­tionship is close to the borderline for torsion, the deter­mination can be made with the indirect ophthalmoscope, provided that the examiner is careful to correct for the inverted image seen with that instrument. As seen with the indirect ophthalmoscope, the fovea lying above the superior margin of the disc indicates extorsion, and the fovea lying below the geometric center of the disc dem­onstrates intorsion (Fig 6). Funduscopy is useful when patients are either too young or uncooperative for fundus photography. In patients demonstrating a manifest nys­tagmus, particularly if it is rotary, fundus photographs may yield inaccurate interpretation of the presence of oblique dysfunction. When such patients are viewed with the indirect ophthalmoscope, one can easily see the fovea change rhythmically from an intorted to an extorted ap­pearance.

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Fig S. This is the postoperative fundus photograph of the patient in Figure 4 after a Knapp procedure. The macula is located at an angle of 16° below the disc, 5° less extorted than preoperatively.

Fig 6. Appearance of a right eye as seen through the indirect ophthal­moscope. Note the image is inverted. The fovea is in the normal position between the geographic middle of the disc and the superior disc margin. With extortion the fovea is above the superior horizontal line (black). With intorsion the fovea is below the inferior horizontal line (black).

REFERENCES

1. von Graefe A. Notizen vermischten Inhalts. 3: Ueber die ophthal· moscopische Beobachtung gewisser Augenmuskelwirkungen. Al­brecht von Graefes Arch Ophthalmol 1856; 2:322-9.

2. Locke JC. Heterotopia of the blind spot in ocular vertical muscle imbalance. Am J Ophthalmol1968; 65:362-74.

3. Levine MH, Zahoruk RM. Disk-macula relationship in diagnosis of vertical muscle paresis. Am J Ophthalmol 1972; 73:262-5.

4. Duke-Elder S. System of Ophthalmology. Vol 6: Ocular Motility and Strabismus. St Louis: CV Mosby, 1973; 117.

5. Guyton DL, von Noorden GK. Sensory adaptations to cyclodeviations. In: Reinecke RD, ed. Strabismus; Proceedings of the Third Meeting of the Intemational Strabismological AssOCiation, May 10-12, 1978, Kyoto, Japan. New York: Grune & Stratton, 1978; 399-403.

MORTON, et al • ROLE OF FUNDUSCOPY AND FUNDUS PHOTOGRAPHY

6. Bixenman WW, von Noorden GK. Apparent foveal displacement in normal subjects and in cyclotropia. Ophthalmology 1982; 89:58-62.

7. Duke-Elder S. System of Ophthalmology. Vol 6: Ocular Motility and Strabismus. St Louis: CV Mosby, 1973; 116.

8. Berke RN. An operation for ptosis utilizing the superior rectus muscle. Arch Ophthalmol 1949; 42:685-708.

9. Knapp P. The surgical treatment of double-elevator paralysis. Trans Am Ophthalmol Soc 1969; 67:304-23.

Discussion by

David L. Guyton, MD

The authors have very nicely documented the significance of ocular torsion in the diagnosis of cyclovertical strabismus. My own observations over the past 6 years agree entirely with theirs, with only one minor exception, or additional observation. Al­though acute third nerve palsies show intorsion as reported here, I tend to see the long-standing cases in my practice, and the intorsion has usually disappeared as partial recovery of the third nerve has occurred. Again, this is only a minor addition to the results reported.

What about the inconsistencies observed with A- or V-pat­terns? These were all cases showing oblique dysfunction, but not showing the expected extorsion or intorsion. These false negatives may be due to the fact that the range of normal torsion of the fundus is quite large. I have come to consider torsion normal if the fovea is level somewhere within the lower third of the disc. This is in good agreement with the study of normal fundi reported by Bixenman and von Noorden1 last year. Even this definition of normal torsion represents a range of 9°.2 A given patient, therefore, might start out with torsional position of the fundi near one end of the normal range, then develop significant bilateral oblique overaction, developing up to 15 ° oftrue cyclodeviation, but still showing so-called "normal" tor­sion. This wide range of normal torsion probably explains some of the inconsistencies in the present study.

A recent case illustrated this point nicely. With a definite right superior oblique palsy, the right fundus appeared normal, and the left fundus appeared borderline intorted. Clearly the right superior oblique palsy had caused extorsion of the right eye, but with the right fundus starting off from a borderline intorted appearance, the amount of extorsion produced was not enough to move the fundus out of the so-called normal range.

Not all inconsistencies can be explained, however. Although the authors report no instance of grossly abnormal torsion with­out oblique overaction in their 139 eyes, I have seen three such cases in the past 6 years, with no explanation for this finding.

The authors' data confirm3 two important points that should be emphasized. First, patients with dissociated vertical deviation do not show abnormal torsion, at least when photographed or when examined with the indirect ophthalmoscope at low light intensity. If abnormal torsion is present in a patient with DVD, overacting obliques are present as well. The torsional position of the fundi, therefore, can often help determine the proper surgical approach for such patients. Ifboth problems are present, they should both be addressed at the same surgery.

Secondly, the authors make no distinction between primary overaction and secondary overaction of the inferior oblique as far as extorsion of the fundus is concerned. This is because both forms of overaction show extorsion of the fundus. If there has been confusion regarding this in the past, it has been because

From the Wilmer Ophthalmological Institute, The Johns Hopkins University School of MediCine, Baltimore, Maryland.

a distinction has not been made between anatomical torsion of the fundus and subjective torsion as measured by the double Maddox rod test, Lancaster red-green test, or other subjective test. These two measures of torsion can be entirely different, primarily because of sensory adaptations that can occur to sub­jective torsion.

Children are able to reorient their retinal meridians physi­ologically, at the cortical level. Overacting inferior obliques de­veloping in childhood often produce 15 to 20° of anatomical extorsion, but the double Maddox rod test with these patients always shows no subjective torsion. Adults cannot adapt easily to subjective torsion, but can learn to interpret the world as straight, or level, with time.

In a study that I reported with von Noorden in 1978,4 34 patients with anatomical cyclodeviations were tested for sub­jective cyclodeviation by the double Maddox rod test. Those patients who had acquired their anatomical cyclodeviation by the age of 6 showed no subjective torsion, whereas those patients acquiring their cyclodeviation after the age of 6 all showed sig­nificant subjective torsion.

It follows that subjective measures of cyclodeviations may be unreliable because of sensory adaptations. Anatomical cy­clodeviations, on the other hand, are more reliable, with only the fairly wide range of normal to take into account.

One last point should be made. Most ophthalmologists are not used to looking for abnormal torsion of the fundus. This is partly because of the disorientation caused by the inversion and reversal of the image formed by the indirect ophthalmoscope. In the indirect ophthalmoscope view, the fovea should be some­where level with the upper third of the disc. What is important to remember is that if the indirect ophthalmoscope view appears extorted, the eye is extorted, and if the indirect ophthalmoscope view appears intorted, the eye is intorted. If this is not imme­diately obvious to the ophthalmologist, I daresay that the ophthalmologist has missed the significance of torsion on fundus exam all these years. I heartily join Dr. Kushner and his associates in encouraging each ophthalmologist to start looking for torsion, and I congratulate the authors for their excellent documentation of abnormal torsion of the fundus as an important objective sign in strabismus diagnosis.

References

1. Bixenman WW, von Noorden GK. Apparent foveal displacement in normal subjects and in cyclotropia. Ophthalmology 1982; 89:58-62.

2. Guyton DL. Clinical assessment of ocular torsion. Am Orthopt J 1983; in press.

3. Guyton DL. Discussion of: Bixenman WW, von Noorden GK. Apparent foveal displacement in normal subjects and in cyclotropia. Ophthal­mology 1982; 89:62.

4. Guyton DL, von Noorden GK. Sensory adaptations to cyclodeviations. In: Reinecke RD, ed. Strabismus; Proceedings of the Third Meeting of the Intemational Strabismological Association, May 10-12, 1978, Kyoto, Japan. New York: Grune & Stratton, 1978; 399-403.

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