The neurofibrovascular bundle of the inferior oblique muscle as its ancillary origin.

22 Pages·2005·4.05 MB·English

THE NEUROFIBROVASCULAR BUNDLE OF THE INFERIOR
OBLIQUE MUSCLE AS ITS ANCILLARY ORIGIN
BYDavidR. Stager, MD
ABSTRACT
Purpose: To establish that the neurofibrovascular bundle (NFVB) ofthe
inferior oblique muscle (IO) has ligamentous qualities that enable it to
function as an ancillaryorigin tothe muscle. Also, to showthatthe NFVB
does function as the ancillary origin for the IO muscle, particularlywhen
recessing andanteriorlytransposingits insertion.
Methods: Fresh (no formaldehyde preservative) cadaver and patient eyes
were studied anatomically, histologically, and physiologically. Eighteen
orbits were dissected to isolate the IO, the inferior rectus (IR), and the
NFVB to demonstrate the linear course of the NFVB and its adjacent
fibrousbands. Theshapeofthemusclewasdocumented. Coronalsections
ofthetwowhole,intactorbitswereanalyzedhistologically. Lightandelec-
tron microscopic sections ofanautopsyspecimen andasurgical specimen
were used to evaluate the capsule ofthe NFVB and the adjacent fibrous
bands nearthe anteriorportion ofthe NFVB andtheir attachment tothe
IR and 10 muscle capsules. The elastic modulus was measured in six in
situ and six in vitro cadaver NFVB specimens and in six in vivo surgical
cases atthe time ofdenervation ofthe NFVB. Foradditional comparison,
four in vitro cadaver superior oblique tendons were similarly tested. Six
eyes that developed recurrent IO overaction following an anterior trans-
position procedure were surgically explored to determine what structure
was servingas its ancillaryorigin.
Results: Gross anatomic and microscopic studies showed a linear orienta-
tion ofthe NFVB with adjacent fibrous bands anteriorlyjoining the IO
and IR muscle capsules. The surgical specimens ofthe anteriorportionof
the NFVB showabout 50% nerve and50% fibrocollagenous capsulewith
the collagen fibers alignedparallel tothe NFVB. The elastic moduluswas
highest (stiffest) in surgical specimens ofthe NFVB and in situ cadaver
NFVB, followed by in vitro cadaver NFVB and, finally, in vitro cadaver
superior oblique tendon. In patients who have undergone anterior trans-
position surgery, the NFVB served as the ancillaryorigin ofthe IO.
TR.AM. OPHTH. SOC.VOL.XCIV, 1996
1074 Stager
Conclusions: Thenameofthe neurovascularbundleshouldbechangedto
the NFVB, since it has a prominent fibrocollagenous capsule and it is
encased in fibrous tissue bands anteriorly. The NFVB has a linear course
intheorbitfromtheapextothe 10muscleandisrelativelystiff. Theasso-
ciatedfibrousbandextendsposteriorlyfromtheIOmusclecapsule,encas-
ingthe nerve anteriorly andattaching3 to 7 mm posteriorly into the cap-
sule ofthe IR. The NFVB binds the midposteriorportion ofthe IO pos-
teriorly. Itsligamentous qualitiesenabletheNFVBtofunctionasanancil-
laryorigin forthe 10.
INTRODUCTION
Althoughtheinferior oblique muscle (IO) hasbeen extensivelystudied, it
has not been reported as having an ancillary origin byway ofits nerve.'-'0
Described as a neurovascular bundle (NVB), the nerve (Fig 1) is essen-
tially a neurofibrovascular bundle (NFVB). Little is known about the
NFVB's orbital course and its anatomic and physiologic properties that
FIGURE 1
Ventral viewofglobe inprimaryposition illustrating relationship between inferioroblique
muscle (A), neurofibrovascular bundle (B), inferior rectus muscle (C), and fibrous tissue
bands(D).
NeurofibrovascularBundleofthe InferiorOblique 1075
maystructurally determine the function ofthe I0."I'- The need to identi-
fy an ancillary origin for the temporal portion of the IO muscle has
increased in importance overthe last 17years with the advent ofanterior
transposition (AT) surgerytoweaken the frequent overaction ofthis mus-
cle.
The AT operation was first mentioned by Guibor,6 Prangen,'7 and
Lloyd,'8 who described the procedure as a recession. Gobin'9 and others20
reported "anteriorpositioning" the 10 to weaken the muscle. Apt and
Branson2"firstidentifiedandadvocatedanteriortranspositionofthe IOby
modifying a standard 10-mm recession of the muscle. They and Scott22
believed the procedure enhanced the recession because it brought the
insertion closer to the plane ofthe origin. Elliott and Nankin23 reported a
procedure to bringthe JO muscle insertion to apointjust anterior to the
lateral border ofthe inferior rectus (IR) muscle insertion.Although they
intendedtofurtherweakenthe 10 muscle, theyfoundahighincidence of
limitation of elevation (antielevation effect). Soon after, it was reported
thattheir methodconvertedthe IO to adepressororan "antielevator."'425
Theprocedurehasbecomeverypopularbecauseiteffectivelyweakensan
overacting IO muscle and also prevents or improves dissociated hyper-
tropia.26-32
The antielevator mechanism has not been adequately explained.30'32
Shiftingtheinsertion fromwellposteriortotheequatortowellanteriorto
the equator does not change the 10 muscle's origin. The origin remains
just posterior to the inferior orbital rim nasally, well anteriorto the equa-
torofthe globe. Forthe temporal portion ofthe JO to act as a depressor
following the AT procedure, another structure located in the midportion
ofthe 10 must serve as an ancillary origin. Some investigators2'27'28 specu-
latethatLockwood's ligamentandsurroundingtissuearethatancillaryori-
gin. Stager and colleagues3"6 suggested that the origin is the NFVB ofthe
IO. Theirstudies didnotdirectlyevaluate the NFVB, butits effectonthe
position ofthe 10 in primarygaze and upgaze was looked at radiographi-
cally. Ziffer and associates37 called the evidence inconclusive. No one has
demonstrated that the NFVB functions as an ancillary origin. This
research was done to document NFVB characteristics that might deter-
mine its function as an ancillary origin ofthe IO bybinding the midpor-
tion ofthe IO tothe apexofthe orbit.
MATERIALS AND METHODS
Three studies were undertaken to ascertain the ligamentous qualities of
the NFVB and its potential to serve as an ancillary origin ofthe IO mus-
cle.
1076 Stager
CADAVER STUDIES
Atotalof18fresh (noformaldehydepreservative) cadaverorbitsweredis-
sected to isolate the IR, the IO, and the NFVB. Photographs were taken
to document the course of the NFVB. The NFVB's distance from the
orbitalapextothe JO myoneuraljunctionwascomparedwiththedistance
from the orbital apex to the 10 origin. Fibrous tissue bands surrounding
the NFVB anteriorlywerecarefullydissectedandanalyzed. Thechangein
the shape ofthe 10 muscle between its origin andinsertionwas also doc-
umented.
HISTOLOGIC STUDIES
Three types of studies were performed histologically: (1) Serial coronal
sections oftwo whole, intact orbits from the NFVB myoneural junction
posteriorly to the apex ofthe orbit were analyzed.?8 The position ofthe
NFVB with respect to the lateralborderofthe IRwas evaluated at 1-mm
intervals todeterminewhetherthe NFVBwas alinearorcircuitous struc-
ture. (2) Microscopic sections ofthe two intactorbital specimens andone
autopsy specimen from the IO-IR region of an 18-year-old male were
examined to evaluate the NFVB andthe surrounding fibrous bands ante-
riorlyandtheirattachmenttothe IRand10 musclecapsules. (3) Onesur-
gical specimen from the NFVB of a 6-year-old child was examined by
high-magnification light and electron microscopyto detect fibrous, colla-
gen, and elastic components ofthe capsule ofthe NFVB.
ELASTIC MODULUS STUDIES
The calculation ofYoung's elastic modulus permits the quantitative com-
parison of the elasticity of tissues. Young's modulus is inversely propor-
tional to the tissue elasticity and directly proportional to the tissue stiff-
ness. For a linear elastic structure, Young's elastic modulus, expressed in
Pascals (Pa), is the ratio ofstress divided by strain.39Stress is defined as
force perunit area. Strain is the relative change oflength from baseline.
Elastic modulus measurements were madeincadaverspecimens and
in surgical patients.
* The elastic modulus ofthe NFVB from cadaverswas determinedin situ
(n=6) and in vitro (n=6), with the NFVB separated from the encasing
fibrous tissue anteriorly. Forcomparison, theelasticmodulusofaninvitro
specimenofthesuperioroblique (SO)tendonwasmeasuredinfourofthe
same cadavers. The invitro studieswereperformed on excised tissue in a
muscle physiologylaboratory.
* A protocol was approved by institutional review board and informed
consent obtainedfromtheparents offourchildrenundergoingadenerva-
NeurofibrovascularBundleofthe InferiorOblique 1077
tion and extirpation procedure on their overacting IO muscles. The
NFVBs of six eyes were prepared for measurement ofan in vivo elastic
modulusatthetimeofdenervation.TheNFVBwasexposedbydissection,
and a hemostat, with one arm firmly attached to a 4-0 silk suture, was
placed across the NFVB (Fig 2). The NFVB was cut just distal to the
hemostat. The suture was then attached to a stress gauge. The strain on
the NFVB was determinedinincrements of10gtoamaximum of50gof
stress.
FIGURE2
Onemmposteriorto10muscle(A)neurofibrovascularbundle(NFVB),(B)isclampedwith
ahemostattowhichistiedasuture.NFVBisthencutandstressisincreasedbywayofsuture
attachedtoastressgaugefrom0to50ginplaneofverticalactionofinferiorrectusmuscle,
(C) Displacement of knot in suture measures strain on the NFVB. Arrow shows
2-mmdisplacementofknotwith50-gstress.
1078 Stager
* Four patients (six eyes), who years earlier had received the classic AT
procedure oftheir 10 muscle insertion and then developed recurrent IO
overaction, wereevaluatedtodeterminewhichstructurewas actingasthe
ancillaryorigin ofthe 10, the intermuscular septal tissue surroundingthe
IO plus the muscle's attachment to Tenon's capsule (often referred to as
Lockwood'sligament), ortheNFVBanditsassociatedfibrousbands. Each
IO muscle was disinserted and placed on stretch with 10 g offorce. The
changeinthepositionoftheinsertionalendofthe IOwasthennoted, first
afterlysingthe surroundingintermuscular septaltissues thatattachto the
IO muscle capsule, except for that portion immediately surrounding the
NFVB. A second measurement was then noted after cutting the NFVB
andits surrounding fibrous bands at the myoneuraljunction (Fig 3). The
process was reversed in one eye by cutting the NFVB first and the sur-
roundingattachedintermuscular septum last.
10tgms
c
C
FIGURE3
Identification ofsource ofancillaryorigin forinferioroblique (IO) muscle (A) in eye that
underwent anteriortransposition procedure. IOwas disinserted andplaced under 10 gof
stress.Displacement(leftposition)aftercuttingintermuscularseptalattachmentswasonly2
mmpriortolysis ofneurofibrovascularbundle (NFVB) (B). AftercuttingNFVB (B) (right
position),samestressonsutureindisinsertedIOmuscleincreaseddisplacementtoanaver-
ageof13.8mm.Sutureinmusclewaspulledinplaneofverticalactionofinferiorrectusmus-
cle(C).
NeurofibrovascularBundle ofthe InferiorOblique 1079
RESULTS
CADAVER STUDIES
Figure 4 reveals that the course ofthe NFVB is linear and not circuitous
in orientation alongthe temporal side ofthe IR muscle as itcourses from
the orbital apex to its myoneuraljunction in the JO muscle. Postmortem
changes reduced the volume ofthe globe and the orbit, and subsequent
tissue collapse may alter the course of the NFVB (J. L. Demer, H. E.
Grossniklaus, personal communications). However, the origin ofthe JO
muscle on the bony orbit does not shift posteriorly with postmortem
orbital shrinkage, andit should always be fartheranteriorlyfrom the apex
ofthe orbit than is the myoneuraljunction ofthe NFVB, which is direct-
ed 370 posterior from the origin. In the cadaver specimens, the NFVB's
distancefromtheapexoftheorbittoitsmyoneuraljunctionwas Ito3mm
lessthanthe distance fromtheorbitalapextotheoriginofthe IO muscle.
Average length ofthe NFVB was 27mm.
Figures 5 and 6 demonstrate the anterior fibrous tissue bands that
encase the NFVB as it approaches the myoneural junction. The fibrous
bandswerepresentinallthecadaverspecimenstoavariableextent. Gross
dissectionrevealedthatthefibroustissueadjacenttothe NFVB originates
anteriorlyfrom the IO muscle capsulartissues nearthe attachment ofthe
NFVB tothe IO muscle. Itextends posteriorly about 3 to 8 mm to attach
to the IR muscle capsule 17to 22 mm posteriortoits insertion.
The shape ofthe 10 muscle specimens was noted (Fig 7). The ante-
rior and posterior borders were not parallel. Rather, the posterior border
peaked posteriorly at the NFVB junction, causing the conspicuous
fusiform expansion ofthe muscle atthis site.
HISTOLOGIC STUDIES
Serialmicroscopicsectionstakenfromtwointactorbitspecimens at 1-mm
intervals from the 10 muscle posteriorto the apexofthe orbit,where the
distance was measured between the NFVB and the lateral border ofthe
IR (Fig8), showedthatthe NFVBwasprimarilylinearandnotcircuitous.
A0.5- to 1-mm temporal bowingoccurred anteriorlyonthe specimen.0
Microscopic sections ofthe intact orbital specimens and the autopsy
specimen ofan 18-year-old male revealed two segments offibrous tissue,
the tightly packed capsule and the surrounding sheets of fibrous tissue.
The adjacent fibrous tissue was composed offibrous bands surrounding,
butmostnasalto,thedistal8mmoftheNFVB.Thesefibroustissuebands
appeartofusewiththe JO musclecapsuleanteriorlyandwiththe IRmus-
cle capsule posteriorly 17 to 22 mm posterior to the IR muscle insertion.
1080 Stager
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ofinero obiu mucl lge
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NeurofibrovascularBundleofthe InferiorOblique 1081
FIGURE5
Cadaverdissectionofneurofibrovascularbundle(B)withfibroustissuebands(D)extending
frominferioroblique muscle (A)capsulenearmyoneuraljunctiontoinferiorrectus muscle
(C)capsule3to7mmposteriorly.
1082 Stager
_M j g D k t!-tt.., .
Cadaver dissection ofdistalportion ofneurof.i.r.v!s'ubfuardl (B.t adjacetfibrou
bands D)separated Ths fbost.issu badsfor poteio adeiofinferio obique
neirrc_s()msl
(Aan asls