DOI:10.2214/AJR.08.1048
AJR 2008; 191:W248-W255
© American Roentgen Ray Society
Terminal Bifurcation of the Biceps Brachii Muscle and Tendon: Anatomic Considerations and Clinical Implications
Berna Dirim1,2,
Sharon Sudarshan Brouha1,
Michael L. Pretterklieber3,
Klaus S. Wolff3,
Andreas Frank3,
Mini N. Pathria1 and
Christine B. Chung1
1 Department of Radiology, University of California, San Diego, San Diego, CA;
and Department of Radiology, VA San Diego Healthcare System, San Diego,
CA.
2 Present address: Radyoloji Servisi, Izmir Ataturk Egitim ve Arastirma
Hastanesi, Izmir, Turkey.
3 Department of Applied Anatomy, Center of Anatomy and Cell Biology, Medical
University of Vienna, Vienna, Austria.
Received April 10, 2008;
accepted after revision June 23, 2008.
This original research was presented as a scientific paper at the 2007
annual meeting of the Radiological Society of North America, Chicago, IL.
Address correspondence to B. Dirim
(bernadirim{at}gmail.com).
WEB
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Abstract
OBJECTIVE. The objective of our study was to describe the anatomic
variation of a bifurcated distal biceps tendon with MRI, histology, and
dissection in cadavers and to report the MR appearance of superimposed lesions
in a patient population with this anatomic variant.
MATERIALS AND METHODS. Visual and histologic examinations of the
distal biceps brachii tendon in eight sectioned fresh-frozen elbow specimens
were performed. Dissection of 17 elbow specimens was performed to describe the
distal biceps brachii tendon. In addition, all elbow MRI reports over a 3-year
period (n = 411) were retrospectively reviewed to determine the
presence of bifurcation of the distal biceps brachii tendon.
RESULTS. The distal biceps brachii tendon appeared bifurcated in 25%
of the sectioned specimens, and these findings were confirmed histologically.
The distal biceps brachii tendon was completely separable into two
components—that is, a short head and long head— throughout their
proximal to distal extent in 41.2% of the dissected specimens. The distal
biceps brachii tendon appeared bifurcated in 11.8% of 68 clinical cases that
showed distal biceps brachii tendon abnormalities or injuries. The following
patterns of injury were noted: complete rupture of both tendons (n =
1), complete rupture of the short head and normal insertion of the long head
(n = 2), complete rupture of the short head and partial tear of the
long head (n = 2), partial tear of both tendons (n = 2), and
complete rupture of the short head and tendinosis in the long head (n
= 1).
CONCLUSION. A bifurcated distal biceps brachii tendon is an anatomic
variant that arises from persistent division between the short head and long
head of the distal biceps brachii tendon and can be characterized with MRI.
Knowledge of a bifurcated distal biceps brachii tendon is important to
characterize injury to the components and to avoid pitfalls in imaging
diagnosis.
Keywords: anatomic variants • biceps brachii muscle • biceps brachii tendon • elbow injury • sports medicine
Introduction
Although abnormalities and injuries of the distal biceps brachii tendon are
less common than those of its proximal counterpart, the distal biceps brachii
tendon is subject to the same spectrum of abnormalities that requires not only
correct diagnosis but also accurate characterization to appropriately guide
therapy. There is no uniformly accepted system for the classification of
distal biceps brachii tendon injuries, and the complex soft-tissue and osseous
anatomy of this structure has not been addressed in a detailed fashion in the
literature. Injuries of the distal biceps brachii tendon can include
tendinosis and partial- and full-thickness tears
[1]. Distinguishing between
high-grade partial- and full-thickness tears of the distal biceps brachii
tendon on the basis of imaging findings or clinical examination results can be
challenging. Distal biceps brachii tendon rupture is relatively rare and has
been reported with an incidence of 1.2 occurrences per 100,000 persons per
year [2].
Successful surgical repair of a ruptured distal biceps brachii tendon is
predicated on an understanding of the anatomy of the distal biceps tendon and
its relationship to the radial tuberosity. Some anatomic aspects of the distal
biceps brachii tendon are described in classic anatomy texts. However, the
detailed anatomy of the distal biceps muscle and tendon and its relationship
to the radial tuberosity have received little attention.
The purpose of our study was to describe the detailed topography of the
distal biceps brachii tendon by stratigraphic dissection of embalmed specimens
and by MRI with histologic correlation of fresh elbow specimens. In addition,
we assessed the MR appearances of distal biceps brachii tendon injuries in a
patient population with a bifurcated terminal biceps brachii tendon. To our
knowledge, such detailed topographic analyses of the normal and injured distal
biceps brachii tendon have not been reported.
Materials and Methods
Stratigraphic Dissection of Embalmed Specimens
Stratigraphic dissection of 17 anatomic elbow specimens (seven left elbows,
10 right elbows; nine male cadavers and eight female cadavers; mean age at
death, 75 years) fixed with a mixture of formol and carbolic acid was
performed. To avoid sampling and observer bias, the elbows were randomly
selected from available cadavers by anatomy assistants not involved in the
research group. Only separated single elbows were then transferred and
dissected by the authors.
During each step of stratigraphic dissection, each specimen was
photographed. To distinguish the several parts of the biceps brachii muscle in
the embalmed specimens, we used differently colored vessel loops. Thus, the
long head—or caput longum musculi bicipitis brachii—was marked
with a red vessel loop, its short head—or caput breve musculi bicipitis
brachii—with a blue loop, and the distal biceps brachii tendon with a
white vessel loop. If long and short head contributions could be identified in
the biceps brachii tendon, they were highlighted by a white–red and
white–blue vessel loop, respectively.
MRI, Visual Inspection, and Histologic Analysis of Fresh-Frozen Elbow Specimens
Eight fresh-frozen anatomic specimens of human elbows from seven persons
(two left elbows, six right elbows; age range at the time of death,
60–83 years; mean age, 74 years) were obtained. Frontal and lateral
radiographs of each anatomic specimen were obtained to ensure that the elbows
were not affected by surgical alterations or significant pathologic
abnormalities as determined in consensus by two authors with 30 and 10 years
of experience, respectively, in interpreting musculoskeletal radiographs. The
cadaveric specimens were immediately frozen at –40°C (Bio-Freezer,
Forma Scientific). The specimens were later allowed to thaw for 24 hours at
room temperature before MRI. The elbow specimens were obtained and used
according to institutional guidelines, and informed consent for research was
obtained from relatives of the deceased.
MR images were acquired with a 1.5-T superconducting magnet (Signa, GE
Healthcare) and a small standard flexible surface coil (Flex Coil, Medical
Advances). All cadaveric elbows were imaged in the coronal, transverse, and
sagittal planes. The MRI protocol consisted of T1-weighted spin-echo sequences
(TR/TE, 466.7/10.0) in sagittal, coronal, and transverse planes. To acquire
high-spatial-resolution images, a section thickness of 2.5 mm, intersection
gap of 0.5 mm, field of view of 13 cm, and data acquisition matrix of 256
x 224 were used.
After completion of MR scanning, the fresh elbow specimens were frozen
again at –40°C (Forma Bio-Freezer, Forma Scientific) for more than
120 hours. The frozen specimens were then sectioned using a band saw into 3-mm
slices in the axial (n = 3), coronal (n = 2), and sagittal
(n = 3) planes corresponding closely to the sections at MRI. After
the debris had been rinsed from the surface of the specimens, the sections
were thawed and then photographed under floodlighting with a digital camera
(Nikon Coolpix 990). To describe the anatomic appearance of the distal biceps
brachii tendon from the musculotendinous junction to the radial insertion, the
findings on MR images of each specimen were compared with the findings derived
from visual inspection of the cadaveric slices by three authors.
To analyze the composition of the fibers of the distal biceps brachii
tendon, histologic samples of this structure were collected from four elbow
specimens. Samples were chosen on the basis of findings at visual inspection
of the sectioned fresh-frozen elbow specimens. Two of these specimens appeared
to have a bifurcated distal biceps brachii tendon and two other specimens
appeared to have a one-bundle distal biceps brachii tendon. In each of the
four specimens, the tendon was analyzed at two levels: first, at the insertion
of the tendon in the radius; and, second, at a point midway between the
musculotendinous junction and the distal tendinous attachment site.
For histologic analysis, specimens were suspended in a 10% formalin
solution. Samples were embedded in paraffin and sectioned further into
5-µm-thick slices. Histologic slices were stained with H and E stain and
analyzed at light microscopy (magnification, x2–x4), by an
orthopedic pathologist with 30 years of experience. A pathologist and
radiologist together recorded whether the distal biceps brachii tendon
appeared bifurcated and recorded its histologic nature at both of the sites
chosen for analysis.
Clinical Cases
All elbow MRI reports from two patient populations over a 3-year period
(2004–2006) were retrospectively reviewed. Institutional review board
approval was obtained for review of these clinical cases. A total of 411 elbow
MR studies were performed during the study period, of which 68 were reported
to show a distal biceps brachii tendon injury or injuries. All studies with a
diagnosis of distal biceps brachii tendon injury were reviewed by three
radiologists trained in musculoskeletal imaging in consensus.
MR images were acquired using one of two 1.5-T superconducting magnets
(Excite, GE Healthcare; or Magnetom Vision, Siemens Medical Solutions). The
MRI protocol of the clinical cases consisted of T1-weighted spin-echo, proton
density–weighted, and short T1 inversion recovery–weighted
sequences in the axial plane; a short T1 inversion recovery–weighted
sequence in the sagittal plane; and a fat-suppressed proton
density–weighted sequence in the coronal plane.
In the 68 elbow MR studies with a diagnosis of distal biceps brachii tendon
injury, the biceps brachii tendon was surveyed from its musculotendinous
junction to its distal radial attachment site; the contributions of the short
head and long head were noted to determine whether tendon bifurcation was
present and, if so, its degree. In cases in which the distal biceps brachii
tendon appeared bifurcated the distal tendinous contributions of the short
head and long head of the distal biceps brachii muscle were surveyed for
evidence of tendinosis, partial tears, and complete tears using standard MRI
criteria. The criterion for complete tendon rupture was absence of the short
head, long head, or both heads of the distal biceps brachii tendon fibers at
the site of insertion on the radial tuberosity. Partial tears were diagnosed
on the basis of an abnormal tendon diameter and the presence of increased
intratendinous signal intensity paralleling that of fluid. Tendon diameter was
judged subjectively and was classified as either increased or decreased
compared with the diameters of the more proximal segments of the distal biceps
brachii tendon. Tendinosis was diagnosed on the basis of the presence of
increased intratendinous signal intensity that did not parallel joint fluid or
of an abnormal tendon diameter.
Abnormalities to the short and long heads of the biceps tendon were
localized through the application of three criteria based on the existing
literature and our experience with dissected specimens: first, following the
course of the tendon abnormality proximally to the level of the
musculotendinous junction; second, ulnar (short head) versus radial (long
head) location of the tendon; and, third, distal and anterior (short head)
versus proximal and posterior (long head) attachment site to the radial
tuberosity [3,
4]. The fluid in the
interosseous bursa of the elbow and in the bicipitoradialis bursa was
investigated and documented in all elbow MR examinations of the patients.
Results
Stratigraphic Dissection of Embalmed Specimens
Musculotendinous junction and "goose quill"—In
the anatomic dissections of 17 elbow specimens, we attempted to separate the
two muscle bellies and explore the distal extent of their tendons to the
ultimate site of insertion, noting the presence and degree of individual short
and long head components throughout the course. We found that at the
myotendinous junction separation of both bellies was hindered by a partial
decussation of the muscle and tendinous fibers. We termed this area
"goose quill" because of its resemblance to a goose's feather
(Fig. 1). The goose quill had a
median length of 2.0 cm (interquartile range 1, 1.0–1.6 cm;
interquartile range 3, 2.7–3.0 cm).
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Fig. 1 —Photograph of dissected cadaveric elbow shows area of
decussation of fibers of both muscle bellies that we termed "goose
quill" (GQ). CBB = caput breve musculi bicipitis brachii, CLB = caput
longum musculi bicipitis brachii.
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Bicipital aponeurosis—In most cases (94.1%), the bicipital
aponeurosis (i.e., lacertus fibrosus) was formed by superficial tendinous
fibers arising from both muscle bellies
(Fig. 2). In one case, the
short head formed a flat and strong bicipital aponeurosis reaching the medial
side and inserting via the antebrachial fascia on the dorsal border of the
ulna. In 5.9% (1/17) of the specimens, fibers of only the short head of the
biceps brachii tendon contributed to the bicipital aponeurosis. In 76.5% of
the specimens, the bicipital aponeurosis showed a single insertion on the
medial side of the forearm. Its fibers intermingled with the reinforced part
of the antebrachial fascia covering the superficial flexors of the
forearm.
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Fig. 2 —Embalmed specimen of adult human left cubital fossa. Biceps
brachii muscle with its tendon and bicipital aponeurosis have been dissected.
Note that bicipital aponeurosis (lacertus fibrosus [LF]) is formed by fibers
of long (caput longum musculi bicipitis brachii [CLB]) and short (caput breve
musculi bicipitis brachii [CBB]) heads of biceps brachii muscle. TB indicates
tendon of biceps brachii muscle inserting into radial tuberosity.
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Distal biceps tendon—In 11.8% (2/17) of the specimens, only
the long head of the biceps tendon attached at the radial tuberosity. In 88.2%
(15/17) of the specimens, a common biceps brachii tendon composed of both the
short and long head components inserted at the radial tuberosity. In these
cases, the common biceps brachii tendon had two macroscopically identifiable
components representing the short head and long head. In 41.2% of these cases,
the short head and long head were completely separable into two components
along their course (Fig.
3).
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Fig. 3 —Photograph of dissected cadaveric radial tuberosity
(arrowheads) with insertion of tendon of biceps muscle. Note that
tendon inserts over whole plane of tuberosity and that in this case tendon
fibers can be assigned to individual muscle bellies—that is, more
proximally situated tendon springs off from long head and more distally
inserting tendon, from short head.
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MRI, Visual Inspection, and Histologic Analysis of Fresh-Frozen Elbow Specimens
Separation of the two muscle bellies (i.e., short head and long head) with
their distal continuation as individual tendons was seen in two of eight (25%)
specimens on MR images and visual inspection of the anatomic sections. MR
images of these two specimens revealed separable short head and long head
components from the musculotendinous junction to a point 3.3 cm distally in
one elbow specimen and 3.6 cm distally in the other elbow specimen. The
separation was best visualized on axial and coronal MR images. The short head
and long head of the distal biceps brachii tendon were separated by a linear
region of fat.
At the insertion to the radial tuberosity, the distal biceps brachii tendon
had the MRI appearance of a single bundle in both specimens. On visual
inspection, similar findings were apparent. These findings were confirmed on
histologic analysis in the region of the bifurcated distal biceps brachii
tendon in which the short and long heads were separated by a plane of fatty
tissue (Figs. 4A,
4B, and
4C). In six of eight (75%)
specimens, the distal biceps brachii tendon was seen as one bundle from its
proximal to distal extent at both MRI and visual inspection.
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Fig. 4A —Bifurcated distal biceps tendon in left elbow specimen of
male cadaver (age at death, 83 years). Axial spin-echo T1-weighted MR image
(A) and axial 3-mm-thick anatomic slice (B) show separated short
head (thin arrow) and long head (thick arrow) of distal
biceps tendon with fat (arrowhead). H = humerus.
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Fig. 4B —Bifurcated distal biceps tendon in left elbow specimen of
male cadaver (age at death, 83 years). Axial spin-echo T1-weighted MR image
(A) and axial 3-mm-thick anatomic slice (B) show separated short
head (thin arrow) and long head (thick arrow) of distal
biceps tendon with fat (arrowhead). H = humerus.
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Fig. 4C —Bifurcated distal biceps tendon in left elbow specimen of
male cadaver (age at death, 83 years). Photomicrograph of histologic section
shows fat cells (asterisk) between short head (S) and long head (L)
of bifurcated biceps tendon. (H and E, x2)
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Four histologic samples collected from two of the elbow specimens that
appeared to have a one-bundle distal biceps brachii tendon on MRI and visual
inspection served as a control group. The one-bundle appearance was confirmed
in one of the specimens. In the second specimen, however, fat and a thin,
fibrous tissue septum separated the central tendon into short head and long
head components on microscopic examination. Around the central separation
zone, the tendon fibers were smaller than their peripheral counterparts in
both the short head and long head (Figs.
5A,
5B, and
5C).
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Fig. 5A —One-bundle appearance of distal biceps tendon in left elbow
specimen of 74-year-old man at MRI and on visual inspection. Biceps tendon was
separated into short head and long head components on microscopic examination.
Axial spin-echo T1-weighted MR image (A) and axial 3-mm-thick anatomic
slice (B) show nonseparated, one-bundle short head (arrow). U
= ulna, R = radius.
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Fig. 5B —One-bundle appearance of distal biceps tendon in left elbow
specimen of 74-year-old man at MRI and on visual inspection. Biceps tendon was
separated into short head and long head components on microscopic examination.
Axial spin-echo T1-weighted MR image (A) and axial 3-mm-thick anatomic
slice (B) show nonseparated, one-bundle short head (arrow). U
= ulna, R = radius.
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Fig. 5C —One-bundle appearance of distal biceps tendon in left elbow
specimen of 74-year-old man at MRI and on visual inspection. Biceps tendon was
separated into short head and long head components on microscopic examination.
Photomicrograph of histologic section shows thin, fibrous tissue septum
(short arrow) and fat tissue (asterisk) that separate distal
biceps tendon into short head (S) and long head (L) components. Around central
separation zone, tendon fibers (arrowheads) are smaller than
peripheral counterparts (long arrows) in both short and long heads.
(H and E, x4)
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Clinical Cases
On MRI studies, the distal biceps brachii tendon appeared bifurcated in
eight of the 68 (11.8%) elbows that had a distal biceps brachii tendon injury.
In all eight cases, the patients were men (six left elbows, two right elbows);
they ranged in age from 35 to 66 years, with a mean age of 48.5 ± 10.6
(SD) years.
The following patterns of injury were noted in patients with a
bifurcated-appearing distal biceps brachii tendon. In one of eight (12.5%)
cases, complete rupture of both the short and long heads of the distal biceps
brachii tendon was detected. In two of eight (25%) cases, complete rupture of
the short head of the distal biceps brachii tendon and normal insertion of the
long head were seen (Figs. 6A,
6B,
6C, and
6D). In two of eight (25%)
cases, complete rupture of the short head of the distal biceps brachii tendon
and a partial tear of the long head were present. In two of eight (25%) cases,
partial tears of both heads of the distal biceps brachii tendon were
identified (Figs. 7A,
7B,
7C,
7D,
7E, and
7F). In one of eight (12.5%)
cases, complete rupture of the short head of the distal biceps brachii tendon
and tendinosis in the long head were noted (Figs.
8A,
8B,
8C, and
8D).
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Fig. 6A —Complete rupture of short head and normal long head of
bifurcated distal biceps brachii tendon in left elbow of 61-year-old man. H =
humerus, U = ulna, R = radius. Sagittal short T1 inversion
recovery–weighted image shows complete rupture and proximal retraction
of short head of biceps brachii tendon (arrow) and fluid signal
filled into gap (arrowheads).
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Fig. 6B —Complete rupture of short head and normal long head of
bifurcated distal biceps brachii tendon in left elbow of 61-year-old man. H =
humerus, U = ulna, R = radius. Sagittal short T1 inversion
recovery–weighted image shows normal long head (arrows) and
fluid filled into gap (arrowheads) of ruptured short head of biceps
brachii tendon.
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Fig. 6C —Complete rupture of short head and normal long head of
bifurcated distal biceps brachii tendon in left elbow of 61-year-old man. H =
humerus, U = ulna, R = radius. Axial short T1 inversion
recovery–weighted image shows fluid filled into gap of ruptured short
head (thin arrow) and normal long head (thick arrow) of
biceps brachii tendon.
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Fig. 6D —Complete rupture of short head and normal long head of
bifurcated distal biceps brachii tendon in left elbow of 61-year-old man. H =
humerus, U = ulna, R = radius. Axial short T1 inversion
recovery–weighted image shows fluid signal (arrows) surrounds
normal radial attachment site of long head of biceps brachii tendon.
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Fig. 7A —Partial tear of both short head and long head of bifurcated
distal biceps brachii tendon in left elbow of 41-year-old man. H = humerus, U
= ulna, R = radius. Axial proton density–weighted MR image shows
proximal portions of both short (thin arrow) and long (thick
arrow) heads of bifurcated distal biceps brachii tendon.
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Fig. 7B —Partial tear of both short head and long head of bifurcated
distal biceps brachii tendon in left elbow of 41-year-old man. H = humerus, U
= ulna, R = radius. Axial proton density–weighted MR image shows some
fibers of short head (thin arrow) that finish at level of lacertus
fibrosus (arrowheads) and normal appearance of long head (thick
arrow) of biceps brachii tendon.
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Fig. 7C —Partial tear of both short head and long head of bifurcated
distal biceps brachii tendon in left elbow of 41-year-old man. H = humerus, U
= ulna, R = radius. Axial proton density–weighted MR image shows normal
signal in short head (double arrows) and long head (single
arrow) of biceps brachii tendon. Arrowheads indicate bicipital
aponeurosis.
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Fig. 7D —Partial tear of both short head and long head of bifurcated
distal biceps brachii tendon in left elbow of 41-year-old man. H = humerus, U
= ulna, R = radius. Axial short T1 inversion recovery–weighted image
shows high signal in attenuated short head (thin arrow) and
intermediate signal in normal-sized long head (thick arrow) of biceps
brachii tendon.
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Fig. 7E —Partial tear of both short head and long head of bifurcated
distal biceps brachii tendon in left elbow of 41-year-old man. H = humerus, U
= ulna, R = radius. Axial short T1 inversion recovery–weighted image
shows high signal in attenuated radial attachment site of long head of biceps
brachii tendon (arrows), which indicates partial tear.
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Fig. 7F —Partial tear of both short head and long head of bifurcated
distal biceps brachii tendon in left elbow of 41-year-old man. H = humerus, U
= ulna, R = radius. Axial short T1 inversion recovery–weighted image
shows high signal in attenuated radial attachment site of short head of biceps
brachii tendon (arrows), which indicates partial tear.
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Fig. 8A —Complete rupture of short head and tendinosis of long head of
bifurcated distal biceps brachii tendon in right elbow of 42-year-old man. R =
radius, U = ulna. Coronal fat-suppressed proton density–weighted MR
image shows high signal in moderately retracted, ruptured short head (thin
arrow) and normal appearance of long head (thick arrow) of
biceps brachii tendon.
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Fig. 8B —Complete rupture of short head and tendinosis of long head of
bifurcated distal biceps brachii tendon in right elbow of 42-year-old man. R =
radius, U = ulna. Coronal fat-suppressed proton density–weighted MR
image shows high signal in blank space of radial attachment area of complete
ruptured short head (arrowheads) and high signal in radial attachment
site of long head (arrow) of biceps brachii tendon.
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Fig. 8C —Complete rupture of short head and tendinosis of long head of
bifurcated distal biceps brachii tendon in right elbow of 42-year-old man. R =
radius, U = ulna. Axial short T1 inversion recovery–weighted image shows
high signal in moderately retracted, ruptured short head (thin arrow)
and moderate thickening and signal increase in long head (thick
arrow) of distal biceps brachii tendon.
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Fig. 8D —Complete rupture of short head and tendinosis of long head of
bifurcated distal biceps brachii tendon in right elbow of 42-year-old man. R =
radius, U = ulna. Axial short T1 inversion recovery–weighted image shows
fluid in blank space of radial attachment area of complete ruptured short head
(arrowhead) and radial attachment site of long head (arrow)
of biceps brachii tendon.
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In a single case, a partial tear of the long head of the distal biceps
brachii tendon was located at the level of the musculotendinous junction. In
all other cases of distal biceps brachii tendon injury with tendon
abnormalities of the short or long head, lesions were observed near the radial
tuberosity. In one of eight (12.5%) cases, some fibers of the short head
finished at the level of the bicipital aponeurosis
(Fig. 7C). Fluid in the
interosseous bursa was seen in all cases. Seven of eight (87.5%) cases had
fluid in the bicipitoradial bursa.
Four of the eight patients underwent surgery. We had access to operative
results for only two of the four. In one of these patients, the MRI findings
of a bifid distal biceps brachii tendon, total rupture of the short head, and
partial tear of the long head were confirmed. The rupture of the short head
was repaired into the radius with the EndoButton fixation technique
(continuous loop of polyester tape, Smith & Nephew). In the other patient
who underwent surgery of the bifid distal biceps brachii tendon, total rupture
of the short head and partial tear of the long head were confirmed, just as
the MR images indicated. The total rupture of the short head was repaired with
an interpositional graft from the flexor carpi radialis muscle. One patient
who had total rupture of the short head and a normal long head of the distal
biceps brachii tendon and one patient who had total rupture of the short and
long heads underwent surgery at outside hospitals and we could not obtain
access to the surgical reports. The other four cases were treated
conservatively.
Discussion
The biceps brachii muscle originates with its long head from the
supraglenoid tubercle and with its short head from the coracoid process of the
scapula. Both heads gradually become attached to each other while they descend
on the anterior aspect of the upper arm. Proximal to the level of the elbow
joint, again two tendons are formed by the incompletely united muscle bellies.
The partial coalescence of both heads is created by a crossover of several
muscle fiber bundles that we call "goose quill." The main tendon
of insertion formed by deep tendinous fibers originating from both heads
enters the cubital fossa on its lateral aspect and is attached to the radial
tuberosity. Furthermore, superficial tendinous fibers of both muscle bellies
form an aponeurotic sheet that reinforces the antebrachial fascia and is
attached via this fascia to the dorsal border of the ulna
(Fig. 9).
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Fig. 9 —Schematic drawing illustrates anatomy of biceps brachii
muscle. Note different origins of both heads as well as formation of fiber
decussation in distal aspect of muscle, "goose quill" (GQ). To
different extents, long (caput longum musculi bicipitis brachii [CLB]) and
short head (caput breve musculi bicipitis brachii [CBB]) contribute tendinous
fibers for tendons of insertions. With main tendon (BT), muscle is attached to
radial tuberosity and with superficial aponeurotic layer, lacertus fibrosus
(LF), it reaches dorsal border of ulna.
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As the biceps brachii muscle extends from the scapula to the forearm, it
acts in the shoulder joint as well as in the elbow and radioulnar joints.
Acting on the shoulder joint, the biceps brachii muscle creates anteversion of
the arm, whereas acting on the elbow and radioulnar joints, it is a powerful
supinator of the forearm via its insertion on the radial tuberosity. This
movement is especially useful for screw driving. When the forearm is in the
supine position, the biceps brachii muscle—together with the brachialis
muscle and all the forearm muscles arising from the medial epicondyle of the
humerus—flexes the elbow.
Although abnormalities and injuries of the distal aspect of the biceps
brachii tendon have been reported to be relatively rare as compared with those
of the proximal aspect, successful treatment requires an understanding of
normal anatomy, anatomic variants, and patterns of abnormalities and injuries.
Contemporary anatomic descriptions of the biceps brachii muscle and the elbow
joint offer only a generalized description of the distal biceps brachii
tendon, bicipital aponeurosis, and insertion of the tendon at the radial
tuberosity [5,
6].
The anterior part of the distal biceps brachii tendon receives the fibers
of the short head and the posterior part, those of the long head. A twisting
of the tendinous fibers arising from the short head and long head and their
respective contribution to the anterior and posterior part of the distal
biceps brachii tendon, resulting in either distal or proximal insertion at the
radial tuberosity, have been described in anatomy texts and recently in the
orthopedics literature [3,
4,
6,
7]. The stratigraphic
dissections performed for our study allowed us to divide the biceps tendon
into three parts arranged from its proximal to distal extent: the goose quill
and musculotendinous junction, the bicipital aponeurosis, and the distal
portion of the biceps brachii tendon.
The goose quill structure has been described in neither the modern
[5,
6] nor the traditional
[8] anatomy literature, to our
knowledge. At the myotendinous junction, separation of both muscle bellies was
hindered by a partial decussation of the muscle and tendinous fibers. We
termed this area "goose quill" because of its resemblance to a
goose's feather. The goose quill contradicts the postulate that the tendon can
be split easily from the level of the muscle to the radial tuberosity. We
believe that the quill's function is to optimize the transformation of muscle
contraction into optimal flexion and supination at the same time by aligning
the power vector of the two muscle heads. Although the goose quill does not
facilitate identification of the short and long head components of the biceps
tendon to the bicipital aponeurosis, it does not obscure visualization of the
bifurcated distal biceps brachii tendon.
In 94.1% of the embalmed elbow specimens, the bicipital aponeurosis was
formed by superficial fibers originating from both muscle heads. Clear
distinction of their origins by mere blunt dissection was not possible. The
fibers could be separated artificially only by dissecting the tendon parallel
to the direction of its fibers with a scalpel. In 5.9% of the embalmed elbow
specimens, the bicipital aponeurosis was formed by superficial fibers
originating from only the short head. In one of the clinical cases (12.5%),
the short head alone comprised the bicipital aponeurosis. These findings
illustrate the importance of closely surveying the short head and long head of
the distal biceps brachii tendon throughout their distal extent because they
offer varying contributions not only to the distal tendon attachment but also
to the bicipital aponeurosis.
Investigators have suggested that in cases of biceps tendon injury anatomic
repair to both the distal tendon and the bicipital aponeurosis are required to
prevent the known complication of decreased range of elbow
motion—specifically, of supination
[3]. It is likely that during
the performance of elbow surgery the function of the bicipital
aponeurosis—that is, drawing the posterior border of the ulna medially
to elicit supination of the forearm—should be emphasized. Thus, by
repairing a disrupted bicipital aponeurosis accompanying a rupture of the
distal biceps brachii tendon, the traction on the ulna can be restored.
Although this concept has been introduced in current surgical research
[3,
9], suture fixation of the torn
bicipital aponeurosis is not proposed.
As we previously noted, in most dissected distal biceps brachii tendons in
our study, the distal tendon was composed of macroscopically distinct short
and long head components, with half being completely separate tendons.
Additional variations in the distal biceps tendon included a distal tendon
that was composed solely of the long head, with the short head forming the
bicipital aponeurosis alone in one case. In the other case, the short head
formed the bicipital aponeurosis and provided an attachment to the coronoid
process. Such variations related to the formation of the biceps tendon
[6,
8] have not been described to
our knowledge.
The results are largely supported by the MRI–anatomic correlation
component of our study as well as the results of a recent study in the
orthopedics literature in which 10 of 17 embalmed dissected specimens had two
separate short and long head muscle bellies and distal tendons throughout
their entire course [4]. In
some cases, the anatomic variation of a bifurcated distal biceps brachii
tendon can be identified on MRI as well as by gross inspection and histologic
evaluation. In other cases, a bifurcation is present but is not identifiable
on MRI.
In applying the results of the dissection and MRI–anatomic
correlation components of our study to the retrospective review of clinical
images, a systematic approach to determine short versus long head involvement
in the setting of abnormalities or injuries to a distally bifurcated biceps
tendon can be established. Moreover, in applying this system, we were able to
characterize several patterns of distal tendon injury in the bifurcated
tendon.
We are aware of only a single case report that has described rupture of a
medial tendon in a patient with a bifurcated distal biceps brachii tendon. In
that case, a completely unfused and bifurcated distal biceps brachii
muscle–tendon unit was described at surgery and repaired
[10]. Before surgery, however,
a mistaken diagnosis of a complete rupture of the distal biceps brachii tendon
was made.
One of the limitations of our study is the small number of cadaveric
specimens. Although only eight fresh-frozen elbow specimens were sectioned, we
believe the findings are significant because we correlated our findings with
histologic analysis in specimens. In addition, dissection of 17 embalmed elbow
specimens was performed to describe the distal biceps brachii tendon.
We recognize that looking at consecutive MR studies to determine the
prevalence of a finding on MRI is better than looking only at cases with
abnormal findings. Although that strategy is ideal, the histologic component
of our study dictates that the true incidence will be underestimated. We chose
to look only at cases with abnormal findings.
Use of the flexed abducted supinated view while MRI was performed of the
frozen elbow specimens or the clinical cases might have helped better
visualize the distal biceps brachii tendon
[11]; however, the frozen
elbow specimens were sectioned in the axial, coronal, and sagittal planes,
corresponding closely to the sections at MRI. The findings on MR images of
each specimen were compared with the findings derived from visual inspection
of the cadaveric slices. The comparison between the findings on flexed
abducted supinated MR images of the elbow specimens with the findings derived
from visual inspection of the cadaveric slices in these three routine
sectioning planes was not possible. For the clinical cases, all elbow MR
studies with a diagnosis of distal biceps brachii tendon injury over a 3-year
period were retrospectively reviewed. Unfortunately, these MR images did not
include the flexed abducted supinated view. Therefore, we could not use the
flexed abducted supinated MRI view in our study. Although the MR studies were
performed to describe possible injury and the bifurcated appearance of the
distal biceps brachii tendon, adding the flexed abducted supinated view to the
MR examination may be helpful.
The other limitation of our study is the lack of operative correlation of
all clinical cases. Many of the patients were treated conservatively and two
patients were lost to follow-up.
In conclusion, although injury of the distal biceps brachii tendon is a
relatively uncommon event, its accurate diagnosis and precise characterization
are crucial for the appropriate clinical management and optimal outcome. The
results of the various components of our study have shown that anatomic
variations exist at the level of the musculotendinous junction of the biceps
tendon, the bicipital aponeurosis, and the distal tendon. We emphasize that
terminal bifurcation in the distal biceps brachii tendon is not rare and that
the presence of this anatomic variation can introduce pitfalls in imaging
diagnosis in the setting of an injury. We also have illustrated a variety of
superimposed abnormalities and injuries in the setting of the bifurcated
distal biceps tendon including partial tears, complete ruptures, and
tendinosis with variable involvement of the short and long heads in eight
clinical cases on MRI. These observations, combined with those detailed in
several recently published articles, may lead to new techniques to
anatomically repair the injured distal portion of the distal biceps brachii
tendon.
Acknowledgments
We thank Parvitz Haghighi for histologic examination of the anatomic
specimens, Donald L. Resnick for guidance, and Debra Trudell for performing
the MRI examinations and sectioning the anatomic specimens. We gratefully
acknowledge Eva B. Krammer for supplying additional specimens. We are also
very indebted to Elisabeth Sabaditsch-Wolff for critically reading the
manuscript.
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Abstract
Introduction
