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Variability in the composition of the sphincter of oddi. A possible factor in the pathologic physiology of the biliary tract

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VARIABILITY IN T H E COMPOSITION O F THE
SPHINCTER OF ODDI. A POSSIBLE FACTOR
I N THE PATHOLOGIC PHYSIOLOGY O F
THE BILIARY TRACT
B. L. KREILKAMP AND E. A. BOYDEN'
Department of Anatomy, University of Minnesota, Minneapolis
FOUR FIGURES
Slthough previous studies of the development of the
choledocho-duodenal junction in the human fetus have indicated that the sphincter choledochus is the principal occluding
mechanism a t the intestinal end of the common bile duct
(Schwegler and Boyden, '37), clinical reports of the reflux
of contrast media into the pancreatic duct in choledochotomized patients have raised anew the question as to whether
the sphincter of the ampulla, when present, may not occasionally play the major role in obstructing the flow of bile. One
might, indeed, attribute the reflux to local edema or hyperplasia of the major papilla-either of which processes could
block the orifice and create a common channel between bile
it not that reflux occurs too
and pancreatic ducts-were
frequently to be explained on this basis ; namely in approximately one-fifth of choledochotomized patients (Leven, '38 ;
Colp and Doubilet, '38). Accordingly, it has seemed desirable
to extend the series of embryological studies being conducted
in this laboratory to adult material and to obtain, if possible,
some information regarding the variability of the component
parts of the sphincter of Oddi.
'The technical work upon which this paper is based was carried out by B. L.
Kreilkamp. The senior author (E. A. Boyden) is mainly responsible for this
account and f o r the sketches.
485
486
B. L. KREILKAMP AND E. 'A. BOYDEN
MATERIAL AND METHODS
The postnatal material consisted of twenty-five specimens
of that portion of the duodenum which includes the major
and minor papillae, together with the attached portion of the
head of the pancreas. The age distribution ranged from 1to
71 years. The material was obtained from routine autopsies
through the kindness of Drs. J. S. McCartney and Robert
Hebbel of the Department of Pathology, and N. D. Schofield
of the Department of Anatomy. Twelve specimens were used
for dissection of the major papilla and all twenty-five for
dissection of the minor .papilla (a report of which is now
being prepared).
The successful preparation of this material involved a
modification of the maceration methods hitherto employed in
studying this complex musculature. After some experimentation, the best fluid was found to be a 20% nitric acid solution.
Into this the strip of duodenum was placed, after being
stretched and affixed to a small wax plate by glass pins. The
length of time required for maceration varied with the age
of the specimen ;usually 24 to 48 hours sufficed. The specimens
were then placed in water. With the aid of a binocular dissecting microscope, the mucosa and submucosa were stripped
from the interior surface of the gut and the pancreatic tissue
from the exterior surface. Due to the delicacy of these preparations, it was found expedient to toughen the fine muscle
fibers before completing the dissection ; accordingly, the
macerated specimens were placed in 20% formalin, or Bouin's
solution for 1 or 2 days and then dissected. Thus, by successive maceration, preliminary dissection, fixing and then
further dissection, it was possible to separate the connective
tissue from the hardened muscle fibers without destroying fine
muscle bands or their attachments.
OBSERVATIONS
1. F i b e r s of t h e choledocho-duodenal aperture
Before discussing the sphincters it is necessary to point
out certain general changes in this region that have taken
VARIABILITY O F SPHIXCTEB OF ODD1
487
place between birth and maturity. Of these the most noticeable is the change in the gridiron-shaped aperture through
which the bile duct and associated pancreati3c duct enter the
wall of the duodenuni. I n the fetus this consists of a broad,
Fig. 1 External surface of macerated preparation of rlloledocho-duodennl
junction of a n adult as seen through window cut in logitadinal muscle of duodenum
a f t e r pancreas and adventitia have been cleared away. ( X 4.5). Fen. chol., eye4iaped cleft in circular musclc of gut (drawn in solid black) ; Hiat., hiatus in
longitudinal muscle of g u t ; D. chol., common bile duct ; D. pane., pancreatic duct;
Margo sup. and inf., upper and lower margins of fenestra through which the ducts
a r e entering the duodenal wall; R’, RL,hands of muscle reinforcing the corners of
the fenestra; C1, @, C4, hands of muscle connecting ducts t o margins of fenestra
and hiatus; Sph. cliol. sup., that portion of sphincter of bile duct lying outside the
fenestra; Fasc. long., the left longitudinal fascicle (the right is hidden by the
“ C ” fibers).
lengthwise hiatus in the longitudinal muscle superimposed
upon a n underlying transverse, eye-shaped fenestra in the
circular muscle (pl. 2, Schwegler and Boyden, ’37-11). I n
the adult (figs. 1 and 2) these slits have become narrower
and are partly filled by camouflaging bands of muscle that
488
B. L. IiREJLIiAMP A N D E. A. BOYDER
have grown in from tlie margins. These bands vary in
different specimens but may be classified as follows :
1. Fibers reinforciqzg the apertures iq~t k dulodeiaaL wall.
The most conspicuous of these are bunclles passing from the
upper margin of the feriestra to blend either with fibers on tlie
deeper surface of the longitudinal muscle of the gut ( R , fig.
1-an external view of the window) or with tlie clceper side
Fig. 2 External surface of another macerated preparation. ( X 4.5). In this
specimen the lower portion of the hiatus, 1Iiat. ( ? ) , is completely filled in by n
growth of fibers t h a t is largely postnatal, aiid the right side of the lower margin
of the fenestra, Margo inf. ( P ) , is split into two wings. R3,R4,bands of muscle
reinforcing the corners of the choledochal aperture; C', C3, C4, bands connecting
the ducts or papilla with the margins of tlie apertnre. See text for detailed
description.
of the circular muscles forming the lower margin of tlie
window (R2, fig. 1; R2, figs. 3 and 4-views of the ~vinc~ow
from the mucosal side). Apparently they represent an estensive postnatal developinent of fetal strands similar to
those designated X1 and X2 by Schwegler and Boyden, '37-11
(see fig. 4 [p. 281 of these authors). Such strands are
VARL4BILITY O F SPHINCTER O F ODD1
489
especially well developed in a cliimparizce fetus now being
studied by one of US.^
A secorid group is illustrated by fibers that begin on the
exterior of the duodenum as fibers of the lateral margins of
the longitudinal hiatus of the gut wall (R“, fig. 2 ) then insert
either 011 the mucosal surface of the inferior margin of the
wirido~v (R“, figs. 3 and 4) or upon tlic exterior surface of
the margo inferior (Ed,fig. 2). I n the fetus the R3 bands
are presumably represented by some of the fibers labelled
X3 (fig. 13, Schwegler and Boyden, ’3i-111, p. 215).
911 four of these types are t o be identified only vaguely in
the fetus, and represent an unsuspected, postnatal expansion
and filling in of hiatus and fenestra. None of these strands
appears t o have been described in adults. Since their fnnctioii seenis t o be to reinforce the corners of the window aiid
to prevent splitting, we have named them Reinforcing ( “ R ” )
fibers. They occurred in eleven out of the twelve major papillae
dissected.
2. Fibers connecting t h e margins o f t h e aperture w i t h the
papilla. Closely associated with the reinforcing fibers but of
different function are what may be termed Connecting (“C”)
fibers. These bundles, likewise becoming fully identifiable
only postnatally, attach the major papilla or ducts to the
tunica niuscularis of the gut. One group (Cl,fig. l)-comparable, perhaps, to the “ F fibers” of Henderickson-leaves
the lateral margin of the hiatus and joins the bile duct just
before the latter enters the fenestra. Other bundles (C2,
figs. 1 and 2) pass from the external surface of the inferior
margin of the fenestra to join the longitudinal fascicles of
the papilla. Still a third type (C3, figs. 3 and 4) arises from
the iiiucosal surface of the inferior margin of the fenestra,
* The term “ X fibers” was originally employed by Hendriekson (1898) t o
designate (among othcis) certain fibers that pass from the circular niuscle (of
the superior margin of the nindow) t o the longitudinal fascicles of the sphincter of
Oddi. Some of those labelled x’ and x2 i n figure 4 (cited above) may well become
the “ X fibers” (our “C-fibers”) of the adult. Others undoubtedly differentiate
into what we have designated “R fibers.” I n fetal stages it is not possible t o trace
them t o their terminations or t o sce in wIiic11 direction they will grow.
490
B. L. KREILKAMP A N D E. A. BOYDEN
and after passing beneath the papilla to the opposite side
either joins the longitudinal fascicles of the papilla or
surings around to blend with its intrinsic circulai- muscles
( ~ 3 ,fig. 2).
Some of tliese bundles represent tlie “variant
K fibers ” of Hendrickson.
A fourth type (P,
figs. 1 aiid 2 ) passes from the exterior
surface of tlie superior margin of the fenestra to join tlie
longitudinal fascicles of the (same o r ) opposite side of the
papilla. These correspond to the “ X fibers” of Hendrickson
(loc. cit., fig. 29). We have not displayed them further, since
they are so clearly shown by that author. All four groups of
“ C fibers ” are primarily criss crossing bundles, and their
function, judging froiii their origin on the margins of the
aperture, is to erect the papilla and t o tie it to the intestinal
wall.
I n concluding this section, it is obvious from a comparison
of figures 1 arid 2 that there is much variation in the degree
to which the choledochal aperture in the duodenal wall becomes filled, postnatally, with camouflaging bundles. I n some
specimens tlie “R fibers” surround the bile duct so thickly
as to render it more subject t o compression by duodenal contraction than in others. But physiologically this compression
must be relatively unimportant, since the segment of the
duct subject to compression is very short-in which respect it
differs greatly from that of most laboratory mammals
(Boyden, ’37) where the overlapping of duodenal musculature is such a s t o usually mask the action of the sphincter
of Oddi (Sandblom, Voegtlin and Ivy, ’35). I n choledocliotomized patients, however, simultaneous recording of biliary
flow and duodenal pressures has demonstrated that pain
accompanying spastic closure of the biliary outlet (induced,
for instance by sudden increase of intra-biliary pressure) is
due not to spasm of the duodenum but to contraction of the
sphincter itself (Eel-ghand Layne, ’40) .3 It is to the musculaSee also Layne and Rergh (’40). To be sure, McGowan et al. (’38) have
shown t h a t in eertaiu intractable eases of biliary dyskinrsia, pain is accompanied
hy a risr in intra-duodenal pressure, but such pain they attribute t o local spasms
of the duodenum, caused 1 , :I~ disrasrd sphincter of Oddi.
VARIABILITY O F SPHINCTER O F ODD1
491
ture of the papilla, therefore, that one must look for variations of practical significance, as outlined in the following
section of this paper.
2. T h e sphimters of
the major papilla
In fetal stages Schwegler and Royden found a well-developed sphincter clioledoclius encircling tlie common bile duct
from a position just outside tlie fenestra (compare figs. 1
and 2) to the junction with the pancreatic duct. Around {lie
junction of the two ducts and extending nearly to the orifice
of the ampulla was a less compact sheath of delicate circular
fibers, the sphincter ampullae. No fibers were found completely encircling the pancreatic duct. Since tlie muscular
sheath of the bile duct was much thicker than that of the
ampulla, and the ampulla of the fetus was in process of
i i i v o l ~ t i o n ,it
~ was assumed that the principal occluding
mechanism-the one responsible for the filling of the gall
bladder-must
be the sphincter choledochus. The present
maceration studies confirm this, but in two out of twelve
adults a well-developed sphincter ampullae was observed.
One of these specimens is shown in figure 3 A, a view of the
mucosal surface of the papilla after removal of the mucosa.
The sphincters choledochus and yauzcreaticus. In this specimen (fig. 3 A ) the bile and pancreatic ducts, after emerging
from the fenestra, run parallel throughout the upper threefifths of the papilla. As tlie bile duct lies chiefly on tlie
mucosal side of the papilla, the fibers on that side are chiefly
fibers of the sphincter choledochus. The two mounds are
large “glandular convolntions’ ’ (Gl.) exposed by dissection,
each surrounded by its own circular fibers as described bv
illatsuno, ‘23). Near the junction of tlie ducts (fig. 3 B)
When first formed the embryonic ampulla is eoextenisve with the duodenal
portion of the bile passage; in later fetal months it occupies only the terminal
5 2 t o 83% of the passage (cf. table 1, Schwegler and Boyden, ’37-1); in the
adult it has disappeared in all but 57% of 1001 individuals (Baggenstoss, ’38)’
a n d jn all but 2070 of adults it lias been reduced to 2 inin. or less in length (Mann
and Giordano, ’23).
492
B. L. IiKEILIiAMP SND E. A. BOYDEN
the papilla has been snipped off, revealing both a sphinctcr
pancreaticus and a sphincter choledochus, the two interlacing
here and there in a manner suggesting the “figwre 8” described by Nuboer (’31). Schwegler and Boydeii ( ’3i-111)
were unable to find such an arrangement in the fetus, and as
a true sphincter pancreaticus was found in only four out
Fig. 3 Mucosal surface of major papilla of specimen shown in figure 2, illustrating
maximum development of sphincter ampullae. ( x 4.5). A-Papilla lying in natural
position after renioval of mucosa. R-Papilla
elevated, with distal half snipped
off, to show underlying fibers and the relation of sphincters t o ducts. Gl., glandular
masses exposed by maceration and dissection; C3 and RZ,R3, bands of “connecti n g ” and “reinforcing” fibers; Spli. amp. (fig. 3 E ) , beginning of spllinctcr nmpullae. ( F o r detailed description see text.)
VARIABILITY O F SPHINCTER O F ODD1
493
of our twelve macerated preparations of the major papilla,
this “figure 8” niust represent a variation of the prevailing
pattern.
The sphinctei. ampullae. Around the two ducts, just before
they unite to form the ampulla (Sph. amp., fig. 3 B), there is
a peripheral sheath of muscle fibers encircling both ducts.
This is the beginning of the sphincter ampullae. This junctional sheath was found to be a constant feature in fetal
stages (compare figs. 17 and 21, Schwegler and Boyden,
’37-111), but whereas it soon dwindled into an insignificant
layer in the fetus (loc. cit., fig. 18), in this adult specimen it
continues nearly to the end of the papilla as a well-developed
sphincter of the ampulla (figs. 3 and 4).5
The fact that it is a sig-nificant muscle in only one-sixth
of these macerated preparations supplies a possible explanation for that reflux of contrast media from one duct to another
which occurs in about one-fifth of choledochotomized patients
(as noted above). Unfortunately, through a misunderstanding,
the autopsy numbers of these twelve specimens were not kept,
so it is impossible t o say whether or not these patients had
exhibited any biliary distress. I n any case, a satisfactory
solution of the problem would require the examination by
maceration methods of the papillae of deceased clioledocliotomized patients known to have exhibited reflux phenoniena.G
’Porsio ( ’31), i n comparing the musculature of this region in adults with that
of infants of 2, 6, and 9 to 1 2 months, also stresses the great delicacy of the sheath
around the infant ampulla and the pancreatic duct as compared with that encircling the common bile duct-a distinction which he finds maintained in adults. But
his explanation-ilainely t h a t the spiiicter choledochus is more robust because i t
receives so many fibers from the inferior margin of the window t h a t it is t o be considered as a n emanation from the circular muscle of the intestine-is not supported
by embryological evidence (Schwegler and Boyden, ’37). Apparently what
attracted his attention away from the i n situ, iiieseiicliymal origin of the sphincter
were the groups of connecting fibers similar to those which we have displayed in
figures 1 t o 4 (Cz, C3).
The clinical significance of pancreatic reflux into the gall bladder has been
pointed out by Colp and Doubilet ( ‘38) who consider this a factor in the production
of non-perforative bile peritonitis and acute cholecystitis.
494
B. L. KREILKAMP AND E. A. BOYDEN
In concluding this account the senior author presents the
following classification of the muscles of the choledochoduodenal junction on the basis of what is now known about
fetal and adult stages:
Fig. 4
( x 23).
Photomicrograph of lower third of macerated papilla shown in figure 3 A.
Lum., lumen of ampulla filled with cellular debris; Sph. amp., sphincter
ampullae.
1. Muscles of t h e cl2oledocho-dzcodeizal a p e r t u r e
1. S u p e r i o r and inf erior margins of the choledochal
fenestra: These enclose the eye-shaped slit in the
circular layer of the tunica muscularis, through
which the ducts enter the intestinal wall. (They
impinge upon the ducts a t only one level; therefore
the ducts are not ensheathed by them as in common
laboratory mammals.)
2. “R-fibers” : bands “reinforcing” the angles of the
fcnestra, thereby preventing extension by splitting.
(These arise contemporaneously with the intrinsic
muscles of the ducts.)
VARIABILITY O F S P H I N C T E R O F 0L)I)I
495
3. “C-fibers”: bands “~oniiecting:’)~
the margins of the
hiatus and of the fenestra with the major papilla and
i t s ducts. (They arise contemporaneously with the
“R-fibers,” and serve both to erect the papilla and
to tie the ducts to the window).
2. Iqztriizsic muscles of t h e ducts and ampulla
1. f h c loihgitudiizal fascicles : two bundles running lengthwise of the papilla i n the intervals between the two
ducts. I n addition to “C-fibers” they contain bands
connecting different transverse levels of the ducts
and ampulla. (These serve mainly to shorten and
erect the papilla.)
2. tlie sphincter choledochus : An annular sheath of intrinsic muscle surrounding tlie bile duct from a
position just outside the window (superior portion
of sphincter) to its junction with the pancreatic
duct (inferior portion). (It obstructs the flow of
bile causing the latter to back u p into the gall bladder during the intervals between meals. Spasm
of this muscle may result in biliary dyskinesia.)
3. t h e sphiizcter pancreaticus : a n annular band around
the pancreatic duct just before it joins the bile
duct. Not definable in the fetus and present in only
one-third of adults.
4. t h e sphiitcter ampullae : a n annular sheath beginning
just before the junction of the ducts and continuing
down around the ampulla when the latter is present.
It occurs as a well-defined sheath in only one-sixth
of adults. (Spasm of this muscle inay cause reflux
of pancreatic juice into the biliary tract or of bile
into the pancreatic duct.)
SUMMARY
1. A perfected maceration technique applied to the tissues
of the human choledocho-duodenal junction has revealed the
existence of a new set of fibers that act to reinforce the eye-
496
B. L. IiREILI<ANP A N D E. A. BOYIIEK
shaped slit through which tlie bile and pancreatic ducts enter
the duodenal wall.
2. A sphiiicter pancreaticus was found in four of twelve
niajor papillae, and a well-developed sphincter ampullae in
only two of the twelve. A stroiig spliincter clioledoclius was
present in all cases.
3. The numerical correspondence between the incidence of
pancreatic reflux and the occurrence of a sphincter ampullae
raises the question a s to whether anatomical variation of the
coniponents of the sphiiicter of Oddi may not be a factor in
the pathological physiology of the biliary tract.
LITERATURE CITED
B ~GGE NST OSS , A. H. 1938 Major duodenal pipilki. Variations of patliologic
intrrest aud lesions of tlie macosa. Arch. P:itli., rol. 26, pp. 893-868.
BERGH,GEORGES.,A K D JOIIS A. LAYNE1940 A demonstration of the independent contiaction of the sphincter of the common bile duct in
human subjects. A m . ,I. Pliysiol. (In press.)
BOYDEN,
E. A. I937 Tlie sphincter of Oddi in iiian and certain repieseutative
maminals. Suig., ~ o l .1, pp. 2.5-37.
1940 The clioledoclio- and pancicatico duodenal junctions i i i tlie
chimpanzee. Aiint. Cec., ~ o l .76 (Suppl. 2 ) , p. 9.
COLP, RALPII, AND HENRYDOURILET1938 :i The clinical signiikince of
pancreatic reflux. Ann. Surg. 1.01. 108, pp. 243-262.
___.1938 b The operative iiicidence of paiicieatic ieflux iu cliolelitliiasi~.
Surg., vol. 4, pp. 837-846.
I~ENDRICRSON,
WILLIAM F. 1898 A study of the musculature of the entirextra-liepatic biliary system, including that of the duodenal portion
of the common bile duct and of the sphincter. Jolins Hopkins Hospital
Bull., vol. 9, pp. 221-232.
LAYNE,JOHN A., A N D GEORGE
8. BERGH 1940 An exprrimental study of paiu iu
the human biliarp trnct induced by spasm of the spliincter of Oddi.
Surg. Gyu. and Ohst., vol. 70, pp. 18-24.
LEVAN,
N. LOGAN 1938 Reflux into the niajor pancreatic duct during cholangiography. Proc. Soc. IGxp Biol. and Med., vol. 38, p. 808.
MPGOWAN, JOHN
M., P A U L A. ICNEPPER, WALTMAN WALTERSA N D ALBERT A1.
SNELL 1838 Tlie relation of spasm of the second portion of tlie
duodenum to biliaiy colic. Surg. Gyn., and Obst., vol. 66, pp. 979-987.
M m N , F. C., AND A. 8.GIORDANO1923 The bile factor i n pancreatitis. Arch.
Surg., vol. 6, pp. 1-30.
MATSUNO,YOSHIMITSU 1923 Ueber die Muskulatur iles Ductus Choledochus.
Virchom’s Arch. f . path. Anat., Rd. 247, S. 208-215.
-R;UBOFT~, J . P. 1931 Studien uher das extr:ilirl,atisclieli Gallen\\.zffssystc~~~.
11.
Der Bau der Muskeln und de4 clastiwlieii Gewebcs in deli norinalen
cxtrahepatischen G;il!enmegeu. Fraiikf. Zeitsclir. f. Path., Rd. 41,
S. 198-249.
VARIABILITY O F S P H I N C T E R O F ODD1
497
1931 Coiitributo alla struttura della porzione intraparictale
del dotto coledoco e del dotto pancreatic0 dell’uomo, con speciale
riguardo allo sfintere di Oddi. (Con 13 figure intercalate nel testa).
Arch. Ital. di Anat. e di Embriol., vol. 29, pp. 127-155.
S A S D B L O I f , PIIILIP, If‘. I>. VOEGTLIN A N D A. c. I V Y
1935 The effect Of
cliolccptokinin 011 the choledocho-duodenal mechanism (sphincter of
Oddi). Am. J. Physiol., vol. 113, pp. 175-150.
SCHWTRGLER,
JR.,R. A., A N D E. A. BOYDEN1937 The development of the pars
intestinalis of the common bile duct in the human fetus, with special
reference to the origin of the ampulla of Vater and the sphincter of
Oddi. I. The involution of the ampulla. Anat. Rec., vol. 67, pp. 441466.
1937 JI. The early development of the musculus proprius. Ihid.,
~ 0 1 .68, pp. 17-41.
- 1937 111. The composition of t h e inusculus proprius. Ibid., pp.
193-220.
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