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The alleged transmigration of the long tendon of the biceps brachii.

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T H E ALLEGED TRANSMIGRATION O F THE LONG
TENDON O F THE BICEPS BRACHII
RODERICK MALCOLM NEALE
Department of Anatomy, Stanford University
TEN FIGURES
It is generally accepted that the tendon of the long head of
the biceps brachii (caput longum BNA), referred to as the
long tendon in this article, develops outside the capsule of
the shoulder joint but migrates through the capsule during
later fetal development. Barcleen ('33) for example said that
"the long tendon of the biceps lies primitively outside the
capsule of the shoulder joint, but in some of the higher
mammals has come to lie within the capsule." A similar point
of view was expressed by Dwight ( '30), Hepburn ( '31),
Chiarugi ('at;), Testut ('ll), Fiek ( '04), Stolowsky (1899),
Le Double (1897) and Macalister (1889).
Most, if not all of these incidental and textbook statements
seem to have been based upon the original observations of
Hermann Welcker (1878), who examined fetal and adult
stages of this tendon in a number of specics. In some of
these species he found it outside of the capsule of the adult
shoulder joint. I n others it was closely attached to the under
surface of the capsule, and in still others it lay free in the
articular cavity. However, his work on the human fetus was
limited to what is discussed in the extract given below.
Since Welcker has been cited as authority for the belief that
the long tendon of the biceps develops outside the shoulder
joint and passes through the capsule during fetal development
in man, it seems advisable to quote him verbatim. He wrote :
205
206
RODERICH MALCOLM NEALE
Nach diesen Refunden wiirde kaum ein Zweifel bleiben, dass
auch bci dem Menschen dieselbe Entwicklung stattfindct ; doch
gelnng es mir, dies direct nachzuweisen. Bci einem menschlichen Embryo von etwa 3 Monaten (Lange vom Scheitel zum
Steisse 62mm, Lange des Armes voii der Scbulter bis zu den
FingerspitZen 33mm) fand ich den intracapsuliiren Theil der
Bicepssehne in einer Falte der Synovialliaut ljcgen (vergl.
Fig. 4a). Das Celenk wurde von hinten gcofket und rnit der
Scheere yuer durchschnitten, und der untere Abschnitt der
Kapsel untcr der Loupe untersucht. Bei Manipulirung mit
der Nadel sieht man, dass die zur Sehne tretende Synovialhautduplicatur nahczu auf dic Mitte dcr Sehne trifft; das
Nesotenontium ist ziemlich knapp und noch etwas breit.
Dasselbe lasst sich mittels der Nadel beliebig spannen, man
sieht deutlich die von beiden Sciten von der Sehnc zur Kapsel
tretenden Synovialhautfalten.
Rei einem zweiten menschlichen Embryo (RumpEinge
72mm, Armlhge 37mm) war der Befund (Fig. 4b) wesentlich
derselbe, doch fand sich die Unterminirung der Sehne hier
fast einzig langs ihrer lateralen Seite.
Ein dritter Embryo (Rumpflinge 82mm) zcigte die Ricepssehne bereits rings umgreifbar.
(The use of the word ‘doch’ in the first sentence is perplexing
but I can offer no explanation for it.)
It should be noted that Welclrer did not say that he saw the
long tendon of the biceps outside of the capsule of the shoulder
joint in the human fetus but concluded that in the human
fetus, the tendon migrates through the capsule, apparently
because he saw the former attached to the under surface of
the latter by a fold of synovial membrane in a 62-mni. (V.B.)
and a 72-nim. (V.B.) fetus, and also because he had found it
in various positions in different species. That Welcker did
not adequately dcmonstrate that the tendon migrates through
the capsule of the shoulder joint is not stated by those who
cited his work. I n Keibol and Mall’s Xanual of Human
Embryology, f o r example, Bardeen ( ’10) wrote :
During fetal development the tendon of the long head of the
biceps sinks in through the capsule of the joint. For a time
it is covered by a layer of synovial mcmbrane which attached
it to the capsule, but in the third or fourth month it becorncs
free in the joint cavity (Welckcr, 18iS).
ALLEGED TRAXSIvIIGRATION O F BICEPS TENDON
207
As far as I know, there are no reports in the literature
giving the relationships of the long tendon of the biceps while
it is outside the capsule of the shoulder joint or discussing
the process by which it penetrates the joint capsule. This
investigation was undertaken, at the suggestion of Doctor
hfeyer, to determine the position of the long tendon in the
human fetus particularly in relation to the capsule of the
shoulder joint in different stages of fetal development, and
to determine by what process it obtains the intracapsular
position.
For this investigation human fetuses and embryos preserved in formalin and varying in Vertex-Breech length from
13 t o 66 mm. were used. In the larger fetuses blocks of tissues
were obtained as follows. With the aid of a dissecting niicroscope the skin and subcutaneous tissues were removed from
the upper one-half of the arm and from the shoulder region
by thc use of forceps and a dissecting needle. The attachment
of the deltoid muscle to the humerus was cut and the muscle
reflected medially to expose the capsule of the shoulder joint
and enable me to identify the biceps muscle. This was then
cut in its upper third and the proximal portion freed from the
surrounding connective tissue. The attachment of the tendon
of the short head to the muscle was also cut, leaving a small
amount of the muscle attached t o the long tendon. The latter
was included in the block of tissue which was removed for
purposes of identification of the long tendon in the sections
made f o r microscopic study. A portion of the vault of the
capsule of the shoulder joint, several millimeters in width to
either side of the tendon, was removed from the rest of the
capsule with a sharp knife. I n order that the relationships
of the long tendon to the internal surface of the capsule might
not be disturbed, the cuts through the capsule mere carried
into the cartilaginous head of the humerus. The block of
tissue removed hence was composed of a portion of cartilage
from the head of the humerus and the overlying capsule of
the shoulder joint with the long tendon. This material was
embedded in paraffin and cut into serial sections 1 2 i-1 thick.
208
RODERICK MALCOLM NEALE
In the smaller fetuses, another method of obtaining blocks
of tissue for sectioning was used, in order to avoid disturbing
the relationships of the long tendon and the capsule. I n
these specimens the shoulder girdle was removed from the
trunk by cutting the miiscular attachments and the clavicle,
and the brachium was divided transversely in its lower third.
By this means, a block of tissue was obtained in which the
shoulder joint and its surrounding structures lap undisturbed.
The proximal two-thirds of the brachium were included in
order that the long tendon could be identified positively in
serial sections by following it to its attachment t o the biceps
muscle. This tissue was embedded in paraffin and cut into
serial sections 1211 thick. The two smallest embryos were
embedded in their entirety and serially sectioned. All of the
tissues were stained with Delafield 's hcrnatoxylin and counterstained with alcoholic eosin.
From the large number of sections studied, those shown
in the photographs (figs. 1 to 10) were selected as best illustrating the relationships of the long tendon t o the capsule
of the shoulder joint during the pertinent period of the embryonic and fetal development of these structures.
F o r the purposes of this investigation, fetuses older than
the one shown in figure 2 were felt to be unnecessary, for the
only change from this to adult state is an increase in size of
all the structures through growth and a complete disappearance of the fold of synovial membrane, the so-called mcsotcnontium of Welcker,l extending from the upper surface of
the tendon to the under surface of the overlying capsule. I n
fetuses younger than the one from the sections for figures 9
and 10 were obtained, the joint capsule had not formed and the
long tendon could not be identified.
Figure 2 is a frontal section through the shoulder joint of
a 66-mm. fetus. The long tendon (lo) is seen lying over the
head of the humerus, just distal to its insertion into the
supraglenoid lip of the scapula. The capsule of the joint is
Listea in dietionaries as the mesotenonium, mesotendineum, mesotenon and
mesotendon.
ALLEGED TRAA-SNIGRATIOIT
O F BICEPS TENDOK
209
well developed and the tendon lies intra-articularly hut is xot
free within the articular cavity, being attached to the under
surface of the capsule by a fold of synovial membrane.
Figure 3, wliich is in the same plane of section as figure 2,
shows the relationships present i n a 51-mm. fctus. There is
Fig. 1 I’hotograph of the head of the left humerus of a
Notc tlic sulcuq in the cartilage of the head of thc humerus.
of the biceps i n seen i n the lower part of thc figure and has
reveal the sulcus under it which mag, in part, be a post-mortem
full term infant.
Tlic long tendon
bcen reflerted t o
impression. X 3 .
a well-developed joint capsule and the long tendon is intraarticular. A comparison of the two figures shows that in
figure 2 many of the fibers making up the mesotenonium hare
disappeared, but they are clearly seen in figure 3 extending
from the upper surface of the tenclori t o the under surface
of the overlying capsule.
THE ANATOhLlC4L RhCORll, TOL.
67,
NO
2 4XD SVPPLEVENT Y O 2
In the transverse srction throngh the shoulder joint of a
35-mm. fetus (fig. 4), thc well-dcvcloyed ai-ticula~.capsule is
t ~ t t i ~ ( * lto
~ ~tt1l 1 ~scapula arid surrounds the outer surface of
th(1 head of tlie humci.us. The loiig tcndon lies against the
inter.nnl snrfnce of t l capsulc
~
hut is not fret. iii the wrti~iilar
t*ilT7it?-.
It is circuiiiwribecl and surronnderl hp a free zoiit'
clxcrpt on il IS uppcr snrfacc w h c ~ etlrc synovial att~olirricrit
to the capsule is situated. The fold 01 syriovial menihriine
surrounding the tendon mtl wt.hic+ stlpilrates it from the ai-ticula18 c+avity is iiiclicatecl by a thin layer below the teiidoti i n
figure 4.
The loiig tmdoii of a somewhat ;vomiger fetus is sho~viiin
oblique section at its insertion into the supraglenoitl lip of'
tbr scalnda in figure 5. This frontal section from ii 41-mni.
fetus shows the tendon below the capsule hut still attaelietl
t o it by a fold of synovial niemht~ane,a s i n the previous spticinim. Tlic c a l m & is well-dcfinccl atid thcre are iio g:'aps in
tlic continuity of the coniieclive tissue fibers composing it.
The tciidon also is N ~.5'e11-(iefined
striictnre and easily iclrntitied. The fragments seen in thc articular cavity are pirces
of cw*tiluge detac~liedfrom the humwus a i d sca1)ulw duriug
l)r('l)ilt'atioo.
Figtiw G is a photocrayli of a transvcrsc. scclion f'rom a
25-mm. l'ctus at a point above tlic bicipital ~ I W O V Cand sliows
the tendon lying o r e r the head of the humerus. There is R
deep wulcus i n thc cartilage of the head of the Iiurnerns undertitiatli tlic tclnclon, which lies henewtli the capsule. Some
Fig. 2 Photograph of a n approximatel. frontal sectioii o f the right shoiilder
of x 66 mm. (V,K.) f e t u s : a. the joint capsule : h, thc long tmdon of the hicepq,
c, the licad of th e humeriis. X 100.
Fig. 3 Photograph o f aii approYirnatelp frontal section of the right shoulder
of II 31 m r u . (V.B.) f r t u s : a, the jnint repsule; ti, the long tcrrdon of thr biceps;
c, tilt. head of thc humerus. Eiinning from the tendon to the under siirfacr of
the capsule are th c fihers which foriii the fold o f syriorial iurwlirnne or
' mrsntenontiuiii ' of Welckcr. X 100.
Fig. 4 Pliotograph u f a: trans1 ersc scetion of the left shoulder of a 45-mm.
( V . K . ) fctufi: a, t h e joint eapsulc; h, n cross section of t h e long tendon of tht,
bitcps; e, the head of the humerus: cl, the, t i p of t h e rornvoid process; r, tlic.
joint e:tulty ; f , thr. qcapula. h'otc the synoui:rl menibr:inr Irolding thc teriiion
tu the under s u r f a w o f the capsule. X 50.
211
Figures 2 t o 4
Fig. 3 I’liotograpli of an approxiniatcly frontal section o f t h e right shoulder
of :I 41-nini. (V.13.) f e t u s : a, the joint e:rpule; b, t h e long teiidon of tlrc biwpw
at i t 8 insertioii i n t o thc supraglenoid lip of tlic scapula; c , t h e licail of the
humerus; e, tlre joint cavity; f , the sc:ipulii. X 12.5.
Fig. ci Photograph of a transwrse w c t i o r i of the right shoulder of a 35 mrn.
(1-23.) fetus: a, the joint capsule; b, a cross scction of the long teudon of tllr
biceps; c, tlir head of the hurrirrus; d, t h e cor:teuid proeess. X l 2 5 .
21 2
ALLEGED TRANSMIGRATTON O F BICEPS TENDON
213
fibers of connective tissue sarrouncl the tendon and attach
it to the under surface of the latter. These fibers are not
closely applied to the tendon but are loosely arranged abort
it, leaving a free space betweeii it and the head of the humerus.
The occurrence of a sulcus in the cartilage of the head of
the humerus in a fetus is surprising. I understand that when
obscrved in the adult, such sulci have been attributed to wear
from or impressioiis of the long tendon over the head of the
humerus, but such an explanation is doubtful f o r it cannot
account for a sulcus such as seen in figure 6. This could be
regarded as resulting from interference with the growth of
the cartilage by the developing long tendon; and if sulci found
in the articular cartilage of the liunieral head, near the
tuberosities, are the result of developmental factors, one
should expect them t o bc present more frequently in the
infant than in the adult. To obtain evidence on this qucstion,
fifty humeri of infants a t term and fifty-five humeri of adults
from the dissecting room were examined. Among the fifty
humeri of infants, thirty-six males and fourteen females,
there were thirteen (26%) in which sulci in the cartilage of
the head of the humerus such a s represented in figure 1 were
observed. They were bilateral in ten instances, dextral alone
in two and sinistral alone in onc instance. Twelve sulci were
found in male specimens and oiie in a female. They wcrc
from $ to $ nim. deep, from 2 t o 3 mm. wide, and from 9 t o
12 mm. long.
Amoiig the fifty-five adult humeri there was only one
instance of it sulcus in the cartilage, continuing the intertubercular sulcus on t o the head of the humerus. This mas on
the left side in a male cadaver. The sulcus was about mm.
deep, about 6 mm. wide and about 30 mm. long and hence
may in part at least be a post-mortem impression.
Figure 7 shows that the relationships of the long tendon t o
the joint capsule are the same in the 30-mm. as in the 35-nim.
fetus (fig. G ) , except that the fibers of thc tendon are fewer
in number and are not so densely paclred together and that
there are fewer fibers composing the joint capsule in the
former.
Fig. i Photograph of ii transverse section of the left shoulder of a 30-mm.
(V.B.) fetus: it, the joint capsule; I), a cross section of the long tendon of the
biceps; c, the head of the humerus; d, the eoracoid prncess. x 125.
Fig. 8 Photograph of a transverse section of the right shoulder of a 28-nm.
(V.R.) fetus: a, the fibers of connective tissue which represent the joint capsule
at this stage; b, a cross sectinn of the long tendon of thc bicepq; c , the head of
the humerus; d, the eoracoid process. x 2'25.
214
Fig. 9 l’hotograph of :I transverse wetion of tlrr riglit shoulder of R 2 2 n m
(V.E.) embryo: a, t h e rnc~ccrwhyrir from u7hic.h thc c:ipsule of thP ,joint will tw
fortiled; b, R ermb scction of the long trndon of tlie biwps; I‘, tlie hr:ltl o f t h e
Iiuiiieruu; d, th c tip of the coracoid process. X 22.5.
Fig. 10 Same as figurc 9, except X 400. To i d c n t i f ? thr fihers inarkctl ( h ,
:is B u o s s scction of tlic long tendon (if the tiiccps, swial sections were followed
tlll thvw f h s were *(*riitci ;ittach t o the hiwps muscle.
215
I11 tlic tranbi-erse section of the shoulder joint of w 28-mm.
fetus (fig. 8), it may be seer1 that the fiber.; making np the
loiig tmdon caii be clearly cliffereiitiated fi*onithe siirrouridiiig
tissues. The teiidoii i s enclosctl within a slieath madr np of if
few f i h c ~ s o f circularly arraligetl connective tissue, not
closelp applietl to it, there being (.leal- hpac
teudon, which lies close to the liead of the hurnrrus and is separated from i t only b~ the fiberb of the coiinectire tissue sheath.
,\i
demarcated from thti surr~ounc3iiig mesen-
[lie Iiamerus wiid o v w t h e loiiji ttliidoIi arid hlencliiig with tlie
fibers of thc outer sidc of tlie ihcatli of the leiidon.
F'igurcs 9 and 10, which are from trniiwcrse sectioiis frorn
t he shoulder of a 22-11im. c m l r p , t-~prclwita v ~ r ye;uly stage
iii thc tleveloprnent of tlie structures concerned.
The joint
sl ractuws. I37 following it in serial scctioiis
from its attachinelit to the bicrps musclc', the sl ruclure 1al)elcd
( 1 ) ) in figures 9 and 10 caould he itlciitifjctl as tlie long teiidoii.
I1 is seen lyirig close to the hurncrws a i d is siiri~)iiiitledon
its ontei- surface by the mescnchynic from whicli iliv joint
capsule is j u s t begiiiuing to differ-cntiate.
Thci relatioiiships of the long tendon of the hiceps to thti
cap sule of the slioultler j oint arid ot 11er neighboring s t ruet i i w s map lw summarized a s follov~s. Late in tlw second
month, acacording t o Strwter's ( '20) tahlrs, the long teiitloil
can be identified and tlic beginning of the formation of thcl
joirit capsule secii. A t illis timcl the teiicloii lies elosc t o tlrcl
humerus, aiid the fibers of thcl capbulc cxtciiid o ~ e its
r outclr
surface, thns enclosiiig jt brfore the joint c*;ivity is present.
During the first week of the third month, the tendon is eiiclosed
within a slieath of connective tissue fibers looselp arr:uipccl
around it. Onlj- the fibers of the syiovial sheath sscparate
the uiidcr surface of the tendon from the hnrneriis; and the
joint capsule to the uridcr surfacc of which tlic sheath of the
teiidori is attached, extends ovci' thc outtir surface of it. Hp
ALLEGED TRANSMIGRATION O F BICEPS TENDON
217
the middle of the third month, the joint cavity has appeared
and the tendon is surrounded by its sheath which separates
it from the joint cavity. The sheath is closely attached to the
under siirface of the capsule and is composed of cells and
fibers indistiiiguishable from those lining the joint cavity.
I n the third week of the third month the tendon shows considerable increase in size and its sheath is more closely applied t o it. The connection of the sheath of the tendon to the
capsule becomes less intimate because of an increase in the
length of the attachment uniting them. This separation of
the sheath of the tendon from the under surface of the capsule
continues, and late in the third month the attachment between
them has become much longer and thinner.
In all stages of development studied, the long tendon of
the biceps lay under, i.e., within and not without, the capsule
of the shoulder joint. I never found it even partly outside
of the capsule or in a position which made its relation to the
capsule doubtful. As soon as the tendon could be identified,
it lay next to the head of the humerus with the fibers of the
developing joint capsule over it. A primary extracapsular
position of the tendon with subsequent migration of it througli
the capsule to a secondary position within the joint cavity
hence has not been confirmed.
LTTERATURE CITED
BARDEEN,
C. R. 1910 Th e deveiopment of the skeleton and of the connective
tissues. Keibel and Mall’s Manual of Human Embryology, Lippjncott
Co., Philadelphia, p. 387.
1933 The museular system. hlorris’ Human Anatomy, 9th ed., P.
Blakiston’s Son and Co., Philadelphia, p. 447.
CIILIRUGI, G. 1936 Articolazione dell ’omero. Istituzioni di Anatoinia dell ’
Uomo, 2nd ed., Soeieta Editriee Lihraria, Milano, vol. 1, p. G83.
DWIGHT, T. 1930 Thc shoulder joint. Pirrsol’s Humnu Anatomy, 9th ed.,
Lipinrott Co., Philadelphia, p. 277.
FICK,R. 1904 Anatomie der Gelenke. Bardplehrn ’s Handbuch der Anatoniie
des hlenschen, Gustav Fischer, Jena, Bd. 2, Ahteilung 1, Tcil 1, 6. 185.
IIEPBURN,
D. 1931 The articulations or joints, rewritten bg D. M. Blair.
Cunningham’s Textbook of Anatomy, Gth ed., Wm. Wood and Co.,
New York, p. 334.
THE AKATOMICAL RECORD. VOL!. 67, NO. 2 A N D Sl3PPLEMEKT NO. 2
218
EODERICK 3lALCOLM NEALE
LE DOUBLE,A. F. 1897 119uscles du bras. Trait6 dea Variations d u Systeme
Musculaire de l'Homni?, Schleicher FrAres, Paris, T. 2, pp. 35-37.
MACALISTER,
A. 1889 A Textbook of Human Anatomy, P. Blakiston, Son and
Co., Philadelphia, p. 286.
STOLOWSKP,
A. 1899 Drei seltene Anomalien des M. biceps brachii.
Aiiatomische Hefte, Bd. 12, S. 330.
STREETER,
G. L. 1920 Six charts showing the corrclation between weight, size,
and menstrua1 age in the human fctus. Reprinted from Weight,
sitting height, head size, foot length and menstrual age of human
embryo. Contributions t o Embryology, XI, Carncgie Institution of
Washington, pub. no. 274.
TES'I'UT,L. 1911 Articulation scapulo-humerale. Trait6 d 'Anatomie Humaine,
6th ed., Octave Doin et Fils, Paris, T. 1, p. 519.
WETAKER,
H. 1878 Dic Einwanderung dcr Bieepssehne in das Schultergelenk.
d r e h i v f u r Aiiatomie und Physiologie, Jahrgang 1875, S. 20 and
(quotation) S. 27-28,
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