Brown Syndrome


Continuing Education Activity

True Brown syndrome is due to congenital causes, with a constant limitation of elevation and a positive traction test secondary to a tight superior oblique tendon. Pseudo-Brown syndrome encompasses acquired and intermittent cases, as well as cases not due to superior oblique muscle-tendon pathology. This activity highlights the role of the interprofessional team in managing patients suffering from Brown syndrome.

Objectives:

  • Describe the etiology of Brown syndrome.
  • Outline appropriate processes for the evaluation of Brown syndrome.
  • Review management options available for Brown syndrome.
  • Identify conditions similar to Brown syndrome and how to differentiate these conditions, and highlight the role of the interprofessional team in providing the best patient outcomes.

Introduction

Dr. Harold Brown first described eight cases of a new ocular motility condition, which presented with restricted elevation in adduction, among other features in 1949.[1][2] The clinical features were similar to those of an inferior oblique palsy, although there was minimal superior oblique muscle overaction. During surgery, Brown discovered a shortened tendon sheath of the superior oblique tendon, which was thought to restrict passive elevation movement in the adducted field. Hence the initial name of "superior oblique tendon sheath syndrome" was used. After extensive further investigation, it was demonstrated that key clinical features were a V or Y pattern strabismus, divergence in upgaze, downdrift in adduction, and a positive forced duction test for ocular elevation in the nasal field.[1] It can be acquired or congenital and is caused by damage to the trochlea of the superior oblique muscle tendon, an abnormality of the superior oblique tendon itself, abnormalities of the tissue around the rectus extraocular muscles (the rectus pulleys), or a congenital abnormality of the superior oblique muscle itself.[3][4]  

The terminology regarding Brown syndrome has varied and was often confusing. For this review, true Brown syndrome is due to congenital cause, with a constant limitation of elevation and a positive traction test secondary to a tight, superior oblique tendon. Pseudo-Brown syndrome encompasses acquired and intermittent cases, as well as cases not due to superior oblique muscle-tendon pathology.[5] Diagnosis is often challenging, and a thorough history and clinical examination are necessary to determine etiology and management.

Etiology

The consensus is that dysfunction of the superior oblique tendon-trochlear complex results in Brown syndrome. The condition is commonly divided into primary congenital and acquired causes. Acquired cases can be further classified into inflammatory, traumatic, or iatrogenic, although many different causes have been identified and are listed below for completeness.[1][6]

Congenital Brown Syndrome

  1. The tight, superior oblique anterior tendon sheath
  2. Short superior oblique muscle and tendon
  3. Nodule on the superior tendon
  4. Anomalous innervation

Acquired Brown Syndrome

  1. Systemic disease
  2. Dysthyroid disease
  3. Enteropathic arthropathy
  4. Hurler-Scheie syndrome
  5. Hypogammaglobulinemia
  6. Juvenile rheumatoid arthritis
  7. Rheumatoid arthritis
  8. Sjogren syndrome
  9. Systemic lupus erythematosus

Ophthalmic Disease

  1. Blepharoplasty
  2. Glaucoma implant in the superior nasal quadrant
  3. Orbital floor fracture
  4. Retinal encircling band
  5. Sinus surgery/sinusitis
  6. Superior oblique tuck
  7. Trochleitis
  8. Neoplasm superior nasal orbit
  9. Trauma to the superior or nasal orbit, e.g., canine tooth syndrome

Other Causes

  1. Cyclic Brown syndrome
  2. Idiopathic
  3. Inflammatory click syndrome
  4. Tenosynovitis of the superior oblique
  5. Cardiopulmonary resuscitation
  6. Postpartum

Epidemiology

Raynor and Hiatt in the 1970s estimated Brown syndrome to occur in 1 in 450 of strabismus cases.[1] When considering vertical muscle abnormalities, the incidence becomes higher; Urist et al. found 23 patients with Brown syndrome from a total of 226 patients with vertical muscle paresis, all with positive traction tests.[7] 

Brown syndrome is more common in females in numerous studies, with 10% demonstrating bilaterality.[8][2] Brown syndrome has also been associated with Duane syndrome and crocodile tears, congenital ptosis, and Marcus Gunn syndrome.[9][10]

Pathophysiology

The superior oblique tendon has a transparent and avascular capsule, similar to the capsule, which envelops tendons of the other extraocular muscles. Parks discovered the tendon and Tenon capsule has a sleeve arrangement, which permits movement of the superior oblique through the trochlea in a telescoping manner.[6] The majority of primary congenital and a significant proportion of acquired Brown syndrome cases are due to anomalies in the superior oblique tendon and/or trochlear apparatus. Helveston et al. described four components of the trochlea: a cartilaginous "saddle," an intracochlear portion of the superior oblique tendon, a fibrovascular sheath around the tendon, and a dense fibrous section that secures the trochlear saddle to the medial wall of the orbit.[11] 

A bursa-like structure between the tendon's vascular sheath and the trochlear saddle was also revealed, and any excess fluid accumulation or deposition in this space can result in limitation of movement through the trochlear tunnel. Helveston et al. hypothesized that this was the cause of the "click" in acquired Brown syndrome.[11] Modern high-resolution orbital imaging studies have investigated the size and contractility changes in the superior oblique muscle, which is hypothesized to cause the abnormal mechanical loading found in Brown syndrome.[12] Evidence now suggests that much of the coordination of extraocular muscle innervations is determined by orbital biomechanics, although there is also extensive debate regarding the correct theory governing muscle movement.[13][14][15][16]

History and Physical

The reported clinical features associated with Brown syndrome have not changed significantly since the initial studies.[2] Von Noorden described in detail variable features which are not always present.[2][6] The hallmark sign is a limited elevation in adduction. If there is a severe restriction, then a down shoot in the adduction of the affected eye (s) can also be present. A positive, forced duction test confirms the diagnosis. A hypotropia can sometimes be present in the primary position, often proportional to the restriction severity. An abnormal head posture consisting of a chin up and a contralateral face turn to avoid the hypotropia allows for binocular fusion and comfortable vision. Patients who have acquired Brown syndrome, especially in adulthood, will be more likely to experience diplopia when tropic. Systemic features can also be present in the acquired Brown syndrome of inflammatory etiology, i.e., superonasal orbital pain and tenderness on movement or palpation.[17][18][19] An audible "click" on the ocular movement can be heard.[20] The history and certain physical findings are dependent on the etiology of Brown syndrome and will determine the evaluation and management strategies.

Clinical Features

  • Deficient or absent elevation in adduction
  • Normal or minimal elevation deficiency in the abduction
  • Mild elevation deficit in primary position
  • Positive forced duction test
  • Minimal or no superior oblique overaction

Variable Features

  • Down shoot in adduction
  • V-pattern due to divergence in up gaze
  • Widening of the palpebral fissure in adduction
  • Anomalous head posture (chin up and contralateral face turn)
  • Hypotropia in primary position

Evaluation

Following a detailed history, the clinical evaluation should include a thorough examination of ocular motility. Clinical features of Brown syndrome will be sought, and a forced duction test conducted. This can be performed with a local topical anesthetic (the patient may experience discomfort), or it can be performed with the patient anesthetized in theatre. A positive test is demonstrated by restriction of passive elevation in adduction of the affected eye. Retroplacement of the globe with forceps during attempted passive elevation in adduction will stretch the superior oblique muscle, accentuating the restriction of Brown syndrome. Dependent on the etiology, further imaging or laboratory investigations may become necessary, e.g., radiological imaging in cases of traumatic Brown syndrome and referral to medical teams for management of inflammatory causes may be warranted.

Treatment / Management

Observation and conservative management is the mainstay for most forms of Brown syndrome. Spontaneous improvement is common for acquired cases, although less common in congenital ones. Non-surgical treatment includes eye exercises and treatment of underlying causes, e.g., oral or local injection of corticosteroids for inflammation. Improvements after daily eye exercises have been reported in case series and reports. Both oral and injection of corticosteroids have been effective in cases of acquired Brown syndrome due to juvenile idiopathic arthritis. Steroid-sparing immunosuppressants, e.g., adalimumab, have been used successfully in isolated cases of Brown syndrome refractory to steroids or nonsteroidal anti-inflammatory drug therapy.[21] 

Surgical treatment is indicated if there is a hypotropia and/or symptomatic anomalous head posture in the primary position. If the patient finds the cosmetic appearance unacceptable, then this may be a relative indication for surgery. The goals of treatment are the improvement of binocular fusion in physiological fields of gaze and version normalization. Tenotomy of the superior oblique tendon has proved more effective than the removal of the tendon sheath. Severing the entire tendon can lead to unpredictable results, including causing a superior oblique palsy.[8] An ipsilateral inferior oblique recession with the tenotomy has been proposed by Parks and Eustis to reduce the effect of secondary superior oblique palsy.[22] Wright described the insertion of a silicone expander that elongated the superior oblique tendon and its effectiveness in 1991, which is in use today.[23][24] 

Medical grade silicone, e.g., retinal band, is inserted between cut ends of the superior oblique tendon and sutured in place without disruption of the floor of the tendon capsule. Another method of weakening the superior oblique is via a graduated recession, first proposed by Calderia in 1975 in treatment of A pattern strabismus with superior oblique overaction.[25] Moghadam et al. reported effective treatment of severe congenital Brown syndrome with a superior oblique tendon split lengthening technique.[26] Trochlea reconstruction and adhesiotomy have been used for cases of the acquired Brown syndrome, where this is the source of elevation limitation.[27]

Differential Diagnosis

The following are some important and common differentials that need to be considered while establishing the diagnosis of Brown syndrome:

  1. Inferior oblique palsy
  2. Orbital fracture
  3. Superior oblique overaction
  4. Congenital fibrosis syndrome
  5. Double elevator palsy
  6. Adherence syndromes

Superior oblique overaction, with or without inferior oblique palsy, will reveal free passive elevation with forced duction testing, and an "A" pattern on upgaze due to superior oblique overaction, in contrast to Brown syndrome. Orbital fractures can cause extraocular muscle entrapment and mechanical limitation of elevation. This can be differentiated from Brown by marked restriction of elevation in both abduction, adduction, and associated findings such as a history of trauma, infraorbital paraesthesia, or enophthalmos. Congenital fibrosis syndromes affect multiple extraocular muscles. The elevator can also be affected resulting in ptosis, which along with elevation deficiencies both in abduction and adduction, help to differentiate from Brown syndrome. Finally, in double elevator palsy (monocular elevation deficiency), the elevation deficiency in abduction is equal to or greater than that in adduction. Forced duction testing can be positive, and is accentuated by proptosis of the globe.

Staging

The severity of Brown syndrome can be graded as follows:

  • Mild: Restricted elevation in adduction, no hypotropia or down shoot in adduction
  • Moderate: Restricted elevation and down shoot in adduction, no hypotropia in primary position
  • Severe: Restricted elevation and marked down shoot in adduction with hypotropia present in primary position

Prognosis

The primary congenital Brown syndrome can be observed as many cases do result in spontaneous improvement. Furthermore, there is less a need for upgaze as the child grows, unless the final height is below average. Surgery is unpredictable, with subsequent procedures often necessary to treat an iatrogenic superior oblique palsy caused by tenectomy or tenotomy. Inflammatory causes are characterized by the ocular motility findings of Brown syndrome associated with pain, which can be localized to the affected trochlea region. Local tenderness on palpation is often present and can fluctuate with relapsing episodes. Peri-ocular corticosteroid injections to the affected area have been described with a good response.[28] 

Post-traumatic Brown syndrome has become less frequent in countries that have stricter road safety regulations. Surgical treatment, such as superior oblique tenotomy, often requires a second procedure on the ipsilateral and contralateral vertical recti and oblique muscles to improve the field of binocular vision.[29]

Complications

Intraoperative complications include excessive bleeding, lost muscle, perforation of the globe, and damage to surrounding ocular structures. Postoperative complications are scarring, under and over-correction, superior oblique palsy, need for further surgery, and implant extrusion (in cases of silicone tendon expander).

Deterrence and Patient Education

Patient education, including the parents, can help with the management of the primary congenital Brown syndrome. Explanation of the etiology and need for surgical intervention, only when there is no improvement or symptoms, can help reassure patients. If patients are unconcerned by their compensatory head position and do not have diplopia, then conservative management is adequate. Treating the underlying cause of the acquired Brown syndrome, e.g., inflammatory causes, can lead to symptom relief. If surgery is indicated, detailed discussion with the patient regarding risks and benefits, including possible worsening of symptoms, is necessary before proceeding. Patients can also be provided with relevant educational material and directed to support groups, which can be beneficial to their wellbeing and outcome.

Pearls and Other Issues

Brown syndrome can be challenging to diagnose, with multiple etiologies possible in the acquired category. A thorough history and clinical evaluation are, therefore, essential. Observation and conservative management in primary congenital Brown syndrome can allow most patients time for spontaneous improvement to occur. Surgery can be reserved for patients who show no improvement; however, multiple surgeries are often required. Inflammatory causes of Brown syndrome could respond to local corticosteroid injection. Traumatic Brown syndrome is difficult to manage, often with disappointing results.

Enhancing Healthcare Team Outcomes

Evaluation of the patient with Brown syndrome requires an interprofessional approach, involving physicians, orthoptists, nurses, pharmacists, and ophthalmic technicians. The multidisciplinary health staff will guide the patient through any post-operative care with instructions on the correct administration of eye drops. They will also explain to the patient red-flag symptoms to be aware of, and the need to contact the team should he/she develop them. They will be part of the patient follow-up in an outpatient setting, assisting with visual acuity and orthoptic assessments. [Level 5]



(Click Image to Enlarge)
Left Brown syndrome with hypotropia in the primary position, limited elevation and downshoot in adduction.
Left Brown syndrome with hypotropia in the primary position, limited elevation and downshoot in adduction.
Contributed by Dr Lanxing Fu
Article Details

Article Author

Lanxing Fu

Article Editor:

Jahanzeb Malik

Updated:

2/3/2021 5:35:58 AM

PubMed Link:

Brown Syndrome

References

[1]

Wilson ME,Eustis HS Jr,Parks MM, Brown's syndrome. Survey of ophthalmology. 1989 Nov-Dec;     [PubMed PMID: 2694414]

[2]

Lee J, Management of Brown syndrome. Seminars in ophthalmology. 2008 Sep-Oct;     [PubMed PMID: 19085429]

[3]

Kaeser PF,Kress B,Rohde S,Kolling G, Absence of the fourth cranial nerve in congenital Brown syndrome. Acta ophthalmologica. 2012 Jun     [PubMed PMID: 22268674]

[4]

Yang HK,Kim JH,Kim JS,Hwang JM, Combined Brown syndrome and superior oblique palsy without a trochlear nerve: case report. BMC ophthalmology. 2017 Aug 25     [PubMed PMID: 28841851]

[5]

Coats DK,Paysse EA,Orenga-Nania S, Acquired Pseudo-Brown's syndrome immediately following Ahmed valve glaucoma implant. Ophthalmic surgery and lasers. 1999 May;     [PubMed PMID: 10334029]

[6]

Wright KW, Brown's syndrome: diagnosis and management. Transactions of the American Ophthalmological Society. 1999;     [PubMed PMID: 10703149]

[7]

Urist MJ, Head tilt in vertical muscle paresis. American journal of ophthalmology. 1970 Mar;     [PubMed PMID: 5418862]

[8]

von Noorden GK,Olivier P, Superior oblique tenectomy in Brown's syndrome. Ophthalmology. 1982 Apr;     [PubMed PMID: 7099550]

[9]

Anderson RL,Baumgartner SA, Strabismus in ptosis. Archives of ophthalmology (Chicago, Ill. : 1960). 1980 Jun;     [PubMed PMID: 7387509]

[10]

Karsenti G,Karsenti D,Zaluski S,Mercadier B, [Association of Stilling-Duane syndrome and Brown's syndrome with crocodile tear syndrome and other congenital anomalies]. Bulletin des societes d'ophtalmologie de France. 1984 May;     [PubMed PMID: 6534598]

[11]

Helveston EM,Merriam WW,Ellis FD,Shellhamer RH,Gosling CG, The trochlea. A study of the anatomy and physiology. Ophthalmology. 1982 Feb;     [PubMed PMID: 7070784]

[12]

Suh SY,Le A,Demer JL, Size of the Oblique Extraocular Muscles and Superior Oblique Muscle Contractility in Brown Syndrome. Investigative ophthalmology     [PubMed PMID: 26397461]

[13]

Miller JM, EOM Pulleys and Sequelae: A Critical Review. Investigative ophthalmology     [PubMed PMID: 31800963]

[14]

Demer JL,Clark RA, Letter to the Editor of IOVS From Joseph L. Demer and Robert A. Clark Regarding Joel M. Miller,     [PubMed PMID: 32503051]

[15]

McLoon LK,Vicente A,Fitzpatrick KR,Lindström M,Pedrosa Domellöf F, Composition, Architecture, and Functional Implications of the Connective Tissue Network of the Extraocular Muscles. Investigative ophthalmology     [PubMed PMID: 29346490]

[16]

Miller JM, Understanding and misunderstanding extraocular muscle pulleys. Journal of vision. 2007 Aug 30;     [PubMed PMID: 17997665]

[17]

Eneh A,Johnson D,Schweitzer K,Strube YNJ, Brown's syndrome during pregnancy: a case report and review of literature. Canadian journal of ophthalmology. Journal canadien d'ophtalmologie. 2018 Dec     [PubMed PMID: 30503010]

[18]

Oral cancer screening--our continuing responsibility., , The Bulletin of the Philadelphia County Dental Society, 1977 Feb     [PubMed PMID: 26669341]

[19]

"Dental work--cheap"., Czarnecki ES,, The Bulletin of the Philadelphia County Dental Society, 1977 Feb     [PubMed PMID: 22491719]

[20]

White VA,Cline RA, Pathologic causes of the superior oblique click syndrome. Ophthalmology. 1999 Jul;     [PubMed PMID: 10406608]

[21]

Michels KL,Kurup SP,Curran ML,Alperin R,De Leon E,Mets-Halgrimson R, A case of acquired Brown syndrome treated with adalimumab. Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus. 2020 Jun     [PubMed PMID: 32087325]

[22]

Parks MM,Eustis HS, Simultaneous superior oblique tenotomy and inferior oblique recession in Brown's syndrome. Ophthalmology. 1987 Aug;     [PubMed PMID: 3658365]

[23]

Wright KW, Superior oblique silicone expander for Brown syndrome and superior oblique overaction. Journal of pediatric ophthalmology and strabismus. 1991 Mar-Apr;     [PubMed PMID: 2051286]

[24]

Radiotherapy in leukemia and lymphoma of children., Pinkel D,Hustu HO,Aur RJ,Smith K,Borella LD,Simone J,, Cancer, 1977 Feb     [PubMed PMID: 27485546]

[25]

Caldeira JA, Bilateral recession of the superior oblique in     [PubMed PMID: 24877301]

[26]

Moghadam AA,Sharifi M,Heydari S, The results of Brown syndrome surgery with superior oblique split tendon lengthening. Strabismus. 2014 Mar     [PubMed PMID: 24564724]

[27]

Kokubo K,Katori N,Kasai K,Hayashi K,Kamisasanuki T, Trochlea surgery for acquired Brown syndrome. Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus. 2014 Feb     [PubMed PMID: 24568984]

[28]

ADA comments on hospital staff controversy., Daun LG,, CDS review, 1977 Feb     [PubMed PMID: 28757707]

[29]

Aylward GW,Lawson J,McCarry B,Lee JP,Fells P, The surgical treatment of traumatic Brown syndrome. Journal of pediatric ophthalmology and strabismus. 1992 Sep-Oct;     [PubMed PMID: 1432513]