Errors in the Three-step Test in the Diagnosis of Vertical Strabismus BURTON J. KUSHNER, MD

Abstract: The Parks three-step test is the standard for diagnosing which isolated cyclovertical muscle is palsied. It does not, however, tell the examiner if in fact one is dealing with a palsy of one cyclovertical muscle. Numerous other causes of vertical strabismus may have a positive Bielschowsky head tilt test. The use of the three-step test in these clinical situations may lead to incorrect diagnosis and treatment. These clinical conditions include contracture of the vertical recti, paresis of more than one vertical muscle, dissociated vertical divergence, pre­vious vertical muscle surgery, skew deviation, myasthenia gravis, and small nonparalytic vertical deviations associated with horizontal strabismus. Several diagnostic steps in addition to the three-step test are necessary to tell if one is in fact dealing with a palsy of a single cyclovertical muscle. Ophthalmology 96: 127-132, 1989

Parks1•2 has described a three-step test for the diagnosis

of an isolated cyclovertical muscle palsy based on the Bielschowsky head tilt phenomenon. This test has become standard for the diagnosis of vertical extraocular muscle palsies. This excellent test relies on the assumption that one is in fact dealing with a palsy of one cyclovertical muscle. It does not, however, tell the examiner if a patient in fact has a palsy of one cyclovertical muscle. Unless the examiner is cognizant of that fact and looks for other possible causes of vertical deviation, the three-step test may lead to incorrect diagnosis and possibly incorrect treatment. Other causes of vertical strabismus may er­roneously point to a palsy of one cyclovertical muscle if one relies on the three-step test. They include vertical de­viations due to contracture of the vertical recti, paresis of

Originally received: October 23, 1987. Revision accepted: August 30, 1988.

From the Pediatric Eye Clinic, University of Wisconsin Medical Center, Madison.

Presented at the American Academy of Ophthalmology Annual Meeting, Dallas, November 1987.

Reprint requests to Burton J. Kushner, MD, F4/336, Clinical Science Center, 600 Highland Ave, Madison, WI 53792.

more than one vertical muscle, dissociated vertical diver­gence, previous vertical muscle surgery, skew deviation, myasthenia gravis, and small nonparalytic vertical devia­tions associated with horizontal strabismus. Several ad­ditional diagnostic steps, beyond the three steps incor­porated in the Parks three-step test, are necessary to tell if one is in fact dealing with the palsy of a single cyclover­tical muscle.

CASE REPORTS

Case 1. A 46-year-old man sustained closed head trauma and was immediately aware of vertical and torsional diplopia. Results of motility examination showed a 10-prism diopter (PD) left hypertropia which increased to 25 PD in right gaze. On forced head tilt to the left, left hypertropia increased to 15 PD and on forced head tilt to the right it decreased to 5 PD, thus meeting the diagnostic criteria for a left superior oblique palsy by the three-step test (Fig I). He preferred to fixate with his right eye because of mild amblyopia in his left eye. Only upon checking his ocular rotations in the oblique fields of gaze and in upgaze was it evident that in fact he had a limitation of elevation of his right eye rather than a left superior oblique palsy (Fig 2). Results of subsequent examination confirmed abnormal forced ductions to elevation in his right eye. A secondary deviation was present

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Fig 1. Case I. The diagnostic fields of gaze as required by the three-step test. A left hypertropia increasing on right gaze and left head tilt would be diagnosed as a left superior oblique palsy. In all photographs, the patient was fixing with the right eye.

with right eye fixation. Radiographic investigation confirmed a blowout fracture of the right orbital floor. After surgical repair of the blowout fracture, he was orthophoric in the primary po­sition and his motility no longer mimicked a superior oblique palsy according to the three-step test.

Case 2. A 46-year-old man reported vertical, horizontal, and torsional diplopia after closed head trauma. Results of his ocular motility examination are represented in Figure 3. Based on the three-step test alone, a diagnosis of a right superior oblique palsy would be made. Only after measurement in the oblique fields of gaze was a small left hypertropia observed. The correct di­agnosis is a bilateral "almost masked" superior oblique palsy. Unilateral surgery for a right superior oblique palsy would prob­ably result in "unmasking" the palsy of the left superior oblique requiring secondary surgery.

Case 3. A 6-year-old boy had undergone bilateral medial rectus recessions for congenital esotropia at 8 months of age. Postop­eratively, he has had satisfactory horizontal alignment, but his parents notice an intermittent right hypertropia, particularly on left gaze. Results of motility examination showed a 5-PD dis­sociated right hypertropia (DVD) which increased 25 PD on left gaze. On forced head tilt to the right, the right hypertropia de­creased to 0 PD and on forced head tilt to the left it increased to 30 PD (Fig 4). He spontaneously assumed a head posture with 10° of right head tilt which eliminated his hypertropia. Results of funduscopic examination did not show objective tor­sion. Ductions and versions did not show any substantial un­deraction of any of the vertical muscles. Based on the three-step test criteria, one might diagnose this boy as having a left superior rectus paresis. On cover testing, however, it was evident that this is a dissociated hypertropia (does not follow Hering's law).

Case 4. A 30-year-old man had undergone previous surgery for a right superior oblique palsy. This consisted of an 8-mm

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recession of the right inferior oblique and a 3-mm recession of the left inferior rectus. He has a residual right hypertropia which increased on right gaze and on right head tilt (Fig 5). Eight degrees of right excyclotropia is present. Based on the three-step test criteria, one might diagnose a left inferior oblique palsy. In fact, this patient has a residual right hypertropia secondary to a right superior oblique palsy which was surgically undercorrected pre­viously.

Case 5. A 5-year-old boy had a 50-PD esotropia associated with a 4-PD right hypertropia in the primary position. The right hypertropia increased on right gaze and on left head tilt (Fig 6). Ductions and versions showed no significant overactions or un­deractions, and objective torsion was not present on funduscopic examination. Based on the three-step test criteria, one might diagnose this child as having a left inferior oblique palsy. In fact, he does not have paralytic strabismus, but a small non paralytic vertical deviation associated with horizontal strabismus.

Case 6. A 70-year-old hypertensive woman reported a sudden onset of vertical diplopia. It began after a momentary loss of consciousness which was preceded by several minutes of dizziness and disorientation. Results of examination showed a 15-PD right hypertropia which increased on left gaze and on right head tilt (Fig 7). No cyclotropia was present with the double Maddox rod test. Ductions and versions did not show any significant under­action or overaction. Based on the three-step test criteria, one might diagnose this patient as having a right superior oblique palsy. The correct diagnosis is a skew deviation.

Case 7. A 45-year-old woman complained of intermittent vertical diplopia with fatigue. Results of motility examination showed a left hypertropia in the primary position which was variable in amount. It increased on right gaze and on left head tilt suggesting a diagnosis of a left superior oblique palsy by the three-step test. Based on the variability, as well as the history of

KUSHNER • THREE-STEP TEST

worsening symptoms with fatigue, a Tensilon test was performed which confirmed the suspected diagnosis of myasthenia gravis.

DISCUSSION

The classic explanation for the positive Bielschowsky head phenomenon is depicted in Figure 8. In the hypo­thetical case of the right superior oblique palsy on forced head tilt to the right, the right superior oblique and right superior rectus (both intorters) are both stimulated. Be­cause the superior oblique is palsied, it does not oppose the elevating action of the superior rectus, and the right hypertropia increases. Case 1 had a tight right inferior rectus secondary to a blowout fracture. In the head erect position, because the patient fixated with his right eye, excessive innervation was necessary to the right superior rectus to bring the eye into the primary position because of its tight antagonist. On forced head tilt to the left, the right superior rectus and superior oblique (intorters) are inhibited. Possibly, the right superior rectus, in this case, proportionately loses more of its vertical effect than the right superior oblique, leading to an increase in the hy­pertropia depicted in Figure 1. Although it is a simplifi­cation to try and explain the head tilt results by focusing on a single muscle pair, this is possibly part of the expla­nation for the positive forced head tilt difference some­times observed in the cases with tight vertical muscles. I have seen six patients with tightness of the inferior rectus (3 secondary to blowout fracture, 3 secondary to endocrine ophthalmopathy) who were mistakenly diagnosed as hav­ing superior oblique palsy in the unaffected eye because the examiner relied solely on the three-step test. Several of these patients had undergone surgery in the nonaffected eye for a superior oblique palsy. Although Jampolsky3

has pointed out that patients with abnormalities of the inferior rectus rarely show a positive forced head tilt dif­ference, all six of these patients were unusual, in that they used the affected eye for fixation because of asymmetric visual acuity. This undoubtedly caused alterations in the neural input to all of the vertical muscles.

These diagnostic errors appear more likely to occur if the patient is fixing with the affected eye. Typically, one must be on the lookout for this phenomenon if the patient does not have symmetric best-corrected visual acuity. A simple test for the presence of a secondary deviation is helpful in determining if the patient is fixing with the involved eye. The patient looks at a fixation light while a red glass is placed before either eye. He is instructed to alternately look at the red light and the white light and report if the separation is greater when he looks at either of the two lights. If it is, a secondary deviation is present when he is fixing with the eye with which he reports a greater image separation. In addition, routine tests to diagnose restrictions of ocular movements (forced duc­tion, active forced generation, and differential intraocular pressure) are important.

Fig 2. Case I. Upgaze fields confirming limitation of elevation of the right eye. The correct diagnosis is right inferior rectus tightness secondary to orbital floor fracture.

2 LHT 2 RHT 15 RHT

~ T / 2 RHT +-- 7 RHT ---+ 15 RHT

2 ET Subjective

/ 1 \ Excyclo: OD 12'

2 RHT 4 RHT 8 RHT OS 5' 10 ET

~ TILT R: TILT L: 12 RHT 2 RHT

Fig 3. Case 2. Ocular motility of a patient with bilateral asymmetric superior oblique palsy. The small left hypertropia (LHT) is only present in an oblique field of gaze and would not be diagnosed by the three-step test. RHT = right hypertropia; ET = esotropia; R = right; L = left; OD = right eye; OS = left eye.

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Fig 4. Case 3. Patient with a dissociated right hypertropia (A) which increased on left gaze simulating right inferior oblique overaction (8). On head tilt right, the deviation decreases (C), and on head tilt left, the deviation increases (D). Based on the three-step test this might appear to be a left superior rectus palsy.

10 RHT +-- 8 RHT __. 5 RHT

~ TILT R: TILT L: 15 RHT 2 RHT

Fig 5. Case 4. Ocular motility of a patient with residual vertical deviation after pre­vious surgery for a right su­perior oblique palsy. The three-step test incorrectly di­agnoses this as a left inferior oblique palsy. RHT = right hypertropia; R = right; L =left.

A vertical muscle palsy may be bilateral but so asym­metric that the misalignment caused by the milder paresis may not be evident on right or left gaze, or head tilt. Most typically, this occurs with bilateral asymmetric superior oblique palsy, in which case the palsy of the lesser affected superior oblique is said to be "masked. "4 It is sometimes

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50 ET +-- 50 ET

6 RHT 4 RHT

TILT R: 0 HT

__. 50 ET

2 RHT

TILT L: 6 RHT

Fig 6. Case 5. Ocular motility of a patient with a nonpar­alytic vertical deviation as­sociated with horizontal stra­bismus. Based on the three­step test, this patient would be incorrectly diagnosed as having a left inferior oblique palsy. ET = esotropia; RHT = right hypertropia; R = right; L = left; HT = hy­pertropia.

necessary to check for a reversal of the hypertropia in the oblique fields of gaze. Measuring strabismus in the oblique fields of gaze can be technically difficult. Nevertheless, at least a qualitative cover test in the oblique fields is essential to help rule out a bilateral asymmetric superior oblique palsy.

KUSHNER • THREE-STEP TEST

12 RHT +--- 15 RHT -+ 18 RHT 6 ET 4 ET 6 ET

~ TILT R: TILT L: 18 RHT 12 RHT

Subjective:

No

Cyclotropla

Fig 7. Case 6. Ocular motility of a patient with a skew deviation. Based on the three-step test, a right superior oblique palsy would be incorrectly diagnosed. RHT = right hypertropia; ET = esotropia; R = right; L = left.

@ SR~

~.o-IR-

Fig 8. Diagrammatic representation of right superior oblique palsy (SO) with head tilt test to the right. The two intorters in the right eye (right superior rectus [SR] and right superior oblique) are stimulated. Because the right superior oblique is paretic the elevating action of the right su­perior rectus is unopposed and the eye elevates. IR = inferior rectus; 10 = inferior oblique.

Jampolsky3 has pointed out that superior rectus con­tracture is a common cause of a positive Bielschowsky head tilt test. I have seen two patients with superior rectus restriction ( 1 secondary to endocrine ophthalmopathy and 1 secondary to superior orbital fracture) who were thought to have paresis of the contralateral inferior oblique based on the three-step test.

Jampolsky3 has pointed out that DVD characteristically increases on forced head tilt to the contralateral side. Also, it is common for DVD to increase in adduction, partie-

Fig 9. For the orthophoric patient on forced head tilt right, the right superior rectus (SR) and right superior oblique (SO) (both intorters) are both stimulated. The elevating action of the superior rectus is cancelled by the depressing action of the superior oblique, and no vertical deviation is created (A). For an esotropic patient on forced head tilt to the right, equal stimulation to the right superior rectus (SR) and right superior oplique (SO) will result in a right hypotropia because the esotropic right eye is further in the field of the vertical action of the superior oblique (depression) than the superior rectus (B). For an exotropic patient on forced head tilt to the right, equal stimulation of the right superior rectus (SR) and right superior oblique (SO) will result in elevation of the right eye because the exotropic eye is further in the field of vertical action of the right superior rectus (elevation) than the right superior oblique (C).

A NORMAL

~

B ESOTROPIC

~

c EXOTROPIC

eo

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ularly if there is associated inferior oblique overaction. Thus, a patient with DVD in the right eye may be expected to show an increase in the hypertropia on left gaze and on left head tilt. From this, one might diagnose a left superior rectus paresis based on the three-step test criteria. Often a patient with DVD will assume a spontaneous head tilt to fuse, as was characterized by case 3. To avoid erroneous diagnosis of DVD, one must assess the hyper­tropia by cover test rather than by light reflex alone. On cover test, the dissociated nature of the deviation (does not follow Hering's law) will be evident.

Surgically weakened muscles may behave on the three­step test like any other muscles which are relatively paretic. Presumably, if appropriate vertical muscle surgery had been previously performed to correct for a vertical stra­bismus, the muscle which had been surgically weakened should have been one with an opposite action as the one which was relatively underacting preoperatively (i.e., sur­gically weakening an inferior oblique if the ipsilateral su­perior oblique is underacting). Thus, after such an oper­ation there will be two vertical muscles with opposite ac­tions with varying degrees of underaction. In such a circumstance, the three-step test may be unpredictable. Case 4 was representative of this.

Moore and Cohen5 studied the results of forced head tilt testing on patients with horizontal strabismus. They found that there were typically small changes in vertical alignment on forced head tilting in patients with no evi­dence of vertical muscle paresis. They found that patients with esotropia typically showed each eye elevating on contralateral tilt and depressing on ipsilateral tilt. Patients with exotropia typically showed elevation on ipsilateral tilt and depression on contralateral tilt. They attributed these findings to the relative differences in the vertical action of the oblique muscles and vertical recti when the eye is either abducted (exotropic) or adducted (esotropic) (Fig 9). This type of deviation can be differentiated from a true vertical muscle paresis in several ways. Ocular ro­tations typically do not show as substantial limitations or overactions as seen with vertical muscle pareses. Also, patients wi~h an oblique muscle palsy tend to have a sub­stantial difference in the vertical deviation between right and left gaze. Although these patients do have a difference on right and left gaze, and therefore may meet the criteria for a particular vertical muscle palsy according to the three-step test, the differences between right and left gaze tend to be small. Also, these patients typically do not spontaneously assume a head tilt to fuse, nor do they exhibit objective or subjective torsion. The presence of a large horizontal deviation with a relatively small vertical deviation should alert the clinician to this entity. Case 5 was representative of this phenomenon.

Although a skew deviation is typically a comitant ver­tical deviation secondary to central nervous system insult,

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I

horizontal incomitance and a positive head tilt test may be present. In a review of 100 cases of skew deviation, Keane6 reported that many of the patients met the three­step criteria for superior oblique palsy. Usually, a skew deviation shows other signs to suggest that it is not a palsy. Typically, the amount ofincomitance found with a skew deviation is substantially less than that associated with a vertical muscle palsy. Also, the amount and direction of cyclotropia may be inconsistent with the vertical muscle palsy diagnosed by the three-step test. Ocular rotations frequently do not show as much overaction or underaction as seen in a vertical muscle palsy.

Myasthenia gravis can present as an isolated palsy of any extraocular muscle and will respond on three-step testing accordingly. Although theoretically this is a palsy of an extraocular muscle, the underlying disease makes it worthy of special attention. History of acquired diplopia without a specific predisposing event, variability, and ex­acerbation of symptoms with fatigue may suggest this di­agnosis. When in doubt, a Tensilon test should be per­formed.

The following additional steps are necessary when using the three-st~p test to determine if one is in fact dealing with an isolated palsy of a cyclovertical muscle.

( 1) Testing for the presence of a secondary deviation, particularly if visual acuity is unequal.

(2) Assessment of ocular rotations of both eyes in the diagnostic fields of gaze.

(3) Qualitative cover testing in the oblique fields of gaze.

( 4) Determination if the hypertropia is of the dis­sociated type (does not follow Hering's law).

(5) History of previous surgery. ( 6) History or findings to suggest a skew deviation

or myasthenia gravis.

REFERENCES

1. Parks MM. Isolated cyclovertical muscle palsy. Arch Ophthalmol 1958; 60:1027-35.

2. Bielschowsky A. Lectures on motor anomalies of the eyes. II. Paralysis

of individual eye muscles. Arch Ophthalmol1935; 13:33-59.

3. Jampolsky A. Management of vertical strabismus. In: Crawford JS,

Flynn J, Haik BG, et al. Pediatric Ophthalmology and Strabismus: Transactions of the New Orleans Academy of Ophthalmology. New

York: Raven Press, 1986; 141-71. 4. Kraft SP, Scott WE. Masked bilateral superior oblique palsy: clinical

features and diagnosis. J Pediatr Ophthalmol Strabismus 1986; 23: 264-72.

5. Moore S, Cohen RL. The head tilt test in horizontal strabismus. Am

Orthopt J 1987; 37:105-8. 6. Keane JR. Ocular skew deviation: analysis of 100 cases. Arch Neurol

1975; 32:185-90.