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SPECIAL ARTICLE

Subtotal Cholecystectomye“Fenestrating” vs
“Reconstituting” Subtypes and the Prevention of
Bile Duct Injury: Definition of the Optimal Procedure
in Difficult Operative Conditions
Steven M Strasberg, MD, FACS, Michael J Pucci, MD, FACS, L Michael Brunt, MD, FACS,
Daniel J Deziel, MD, FACS

Less than complete cholecystectomy has been advocated for difficult operative conditions for more than 100 years. These op-
erations are called partial or subtotal cholecystectomy, but the terms are poorly defined and do not stipulate whether a remnant
gallbladder is created. This article briefly reviews the history and development of the procedures and introduces new terms to
clarify the field. The term partial is discarded, and subtotal cholecystectomies are divided into “fenestrating” and “reconstitut-
ing” types. Subtotal reconstituting cholecystectomy closes off the lower end of the gallbladder, reducing the incidence of post-
operative fistula, but creates a remnant gallbladder, which may result in recurrence of symptomatic cholecystolithiasis. Subtotal
fenestrating cholecystectomy does not occlude the gallbladder, but may suture the cystic duct internally. It has a higher incidence
of postoperative biliary fistula, but does not appear to be associated with recurrent cholecystolithiasis. Laparoscopic subtotal
cholecystectomy has advantages but may require advanced laparoscopic skills. (J Am Coll Surg 2016;222:89e96.  2016
by the American College of Surgeons. Published by Elsevier Inc. All rights reserved.)

Laparoscopic cholecystectomy is a well-established proce- technique, in which the funnel-shaped infundibular-cystic


dure with clear benefits for patients over open cholecystec- duct junction is the rationale for identification, is much
tomy. However, it is associated with an increased rate of easier to achieve than CVS. However, biliary inflammatory
bile duct injury. Biliary injuries occur more commonly fusion and contraction can make the common bile duct
when operations are made more difficult due to the pres- resemble the cystic duct when this technique is used,3
ence of severe acute and/or chronic inflammation. Under and this increases the chance of biliary injury. The CVS
these conditions, secure ductal identification by the critical method protects against injury because when the CVS
view of safety (CVS) may be very challenging because CVS has not been achieved after a reasonable trial of dissection,
requires clearing of the inflamed hepatocystic triangle in the surgeon is more likely to realize that conditions are too
order to demonstrate the cystic duct, cystic artery, and difficult to proceed in the usual manner and opt for a
the cystic plate. It is a rigorous method, but as we have pre- different approach before a biliary injury occurs. It is
viously stressed,1,2 this is actually one of the strengths of the good that the CVS method prevents biliary injury, but if
CVS method of identification. The infundibular there is to be an effective and safe method of dealing
with difficult gallbladders, it must include a safe and effec-
tive bail-out technique when CVS cannot be attained. By
Disclosure Information: Nothing to disclose. safe we mean without bile duct injury and by effective we
Disclosures outside the scope of this work: Dr Brunt receives research sup-
port grants from Gore and Karl Storz Endoscopy.
mean without need for a second operation. Otherwise
This article is a work product of the SAGES Safe Cholecystectomy Task the surgeon will be tempted to push on with a risky dissec-
Force 2015. tion in the hepatocystic triangle in order to avoid a second
Received July 28, 2015; Revised September 27, 2015; Accepted September procedure or perform a cholecystostomy, which will usu-
28, 2015. ally necessitate a second operation. Stated otherwise, it is
From the Section of Hepato-Pancreato-Biliary Surgery (Strasberg) and the commendable when surgeons reach the decision that it is
Section of MIS Surgery (Brunt), Washington University in St Louis, St
Louis, MO; the Division of General Surgery, Thomas Jefferson University unsafe to proceed with a total cholecystectomy, but obvi-
Hospital, Philadelphia, PA (Pucci); and the Department of General Sur- ously there should be a good way to finish the procedure
gery, Rush University Medical Center, Chicago, IL (Deziel). when its time “to get out of Dodge.”
Correspondence address: Steven M Strasberg, MD, FACS, Washington
University in Saint Louis, 4990 Children’s Place, Suite 1160, Box 8109, Paradoxically, 2 of the most useful “bail out” proceduresd
Saint Louis, MO 63110. email: strasbergs@wustl.edu partial cholecystectomy and subtotal cholecystectomydare

ª 2016 by the American College of Surgeons. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jamcollsurg.2015.09.019


All rights reserved. 89 ISSN 1072-7515/16
90 Strasberg et al Subtotal Fenestrating Cholecystectomy J Am Coll Surg

Figure 1. Endoscopic retrograde cholangio-pancreatograms (ERCP)


in 2 patients who had subtotal reconstituting cholecystectomies
and became symptomatic again. Gallbladder remnants were iden-
tified by ERCP as enlarged areas at the end of the cystic duct. Right
figure inset shows that stones had reformed or were retained.

not clear and well-defined operations. Even the terms par-


tial and subtotal are imprecise because they fail to encom-
pass an essential element in these operations, which is
Figure 3. Transabdominal ultrasound of a patient who had a cho-
whether a functional remnant gallbladder may result as
lecystectomy nearly four years before developing recurrent biliary
a consequence of performing these procedures. In 1966, colic. A small remnant gallbladder with a retained or reformed stone
Bodvall and Overgaard4 defined “gallbladder remnant” was identified (solid arrow) with acoustic shadow (dashed arrow).
as a wider part of the free end of the cystic duct that gives
the appearance of a diminutive gallbladder.4 Today, (MRCP) (Fig. 2), or by ultrasound (Fig. 3). The func-
remnant gallbladders may be diagnosed by ERCP tional remnant gallbladder may communicate with the
(Fig. 1), magnetic resonance cholangiopancreatography remainder of the biliary tree just as the parent gallbladder
does. Stones can form or be retained within these rem-
nants and may cause recurrent biliary colic and all of
the usual complications of cholecystolithiasis.The poten-
tial consequences of leaving a gallbladder remnant are
well known. Bodvall and Overgaard4 attributed the first
report of clinically significant complications of gallbladder
remnants after cholecystectomy to Florken in 1912,5 and
summarized literature to 1966. The subject was reviewed
again in 2009 by Pernice and Andreoli.6 A brief summary
of the literature, which is mostly composed of small case
series or case reports, is that gallbladder remnants may
become symptomatic and require excision in a second
operation at any time from shortly after the initial opera-
tion to many years later. The latter is an important point
because most publications dealing with the outcomes of
less than complete cholecystectomy have short patient
follow-up times and therefore, may underestimate the
consequences of leaving a gallbladder remnant. Further-
more, operations to remove remnant gallbladders may
be difficult, so procedures that do not result in remnant
gallbladders are more desirable than those that do (Fig. 4).
Excellent recent systemic reviews of outcomes of proce-
dures reported in papers under the terms partial or subtotal
Figure 2. Magnetic resonance image (MRCP) of remnant gall- cholecystectomy by Henneman and colleagues7 and Elshaer
bladder (GB). and associates8 are available. The purpose of this paper is
Vol. 222, No. 1, January 2016 Strasberg et al Subtotal Fenestrating Cholecystectomy 91

gallbladder. Due to difficult conditions, he removed the


gallbladder such that “the hardened posterior wall and
the part of the bladder lying next to the cystic duct
remained.” He sewed the remaining gallbladder over on
itself, with a strip of gauze as a drain. This seems to be
the first description of a modification of cholecystectomy
due to difficult operative conditions in which the intent
was to remove as much of the gallbladder as possible
without dissecting the inflamed hepatocystic triangle.
The idea was to deal with the gallbladder problem in 1
operation while avoiding the risk of a major biliary or
vascular injury. The next development of subtotal chole-
cystectomy occurred not because of the problem of the
difficult gallbladder, but due to the problem of postoper-
Figure 4. Intraoperative photograph at conclusion of laparoscopic
ative bile leakage and bleeding from the liver bed after
dissection to free a remnant gallbladder (GB) in a patient who had
become symptomatic after a previous subtotal cholecystectomy. routine elective total cholecystectomy. Pribram,12,13 from
Berlin, described a technique in which the gallbladder
to clarify the procedures that have been described under the was bivalved along its longitudinal axis, stones were
terms partial and subtotal cholecystectomy in respect to removed, and then thermal ablation of both portions of
whether they are associated with a potentially functional the gallbladder wall was performed. The technique con-
remnant gallbladder and then to propose new terms that sisted of a deep destruction of the wall down to the serosa.
more appropriately depict what is actually done in these The preserved flaps of serosa were folded and sutured
procedures. We believe that clarification of the procedures together to reperitonealize the liver bed. Pribram did
and what they are called will help surgeons choose what not perform any anatomic resection in these cases, nor
type of procedure to select and will also facilitate clinical did he use this method to avoid dissection in the region
studies in this area. Based upon referrals to our centers of the cystic duct in the difficult gallbladder. In fact, he
we strongly suspect that many surgeons still believe that recommended ligation and division of the cystic duct
no good option between cholecystostomy and total chole- and the cystic artery external to the gallbladder, as in total
cystectomy is available and that anything less than a com- cholecystectomy. Variations on Pribram’s technique,
plete cholecystectomy may result the need for as second which included actual removal of the free portion of the
procedure. As noted earlier, this belief may encourage the gallbladder wall and ablation of the remaining portion
surgeon to push on with dissection in the hepatocystic attached to the liver, were recommended by Thorek14 in
triangle when there is danger in doing so, or to do a chol- Chicago and by Bailey and Love15,16 in London. A free
ecystostomy when a more satisfactory procedure is availa- graft of omentum or falciform ligament was sutured
bleeone that will take care of the patient’s problem in a over the remnant gallbladder on the liver. As did Pribram,
single operation. Part of the lack of awareness of options however, these surgeons also divided the cystic duct and
seems to be the confusing terminology. An effective, reli- artery.
able, standard, widely known, and accepted operation The idea of less than complete cholecystectomy for the
needs to be available when the CVS cannot be achieved. specific purpose of dealing with difficult operative condi-
The CVS is only 1 part of COSIC (culture of safety in cho- tions during cholecystectomy was advanced by Estes,17 of
lecystectomy),1,9 and a reliable bail-out operation is another Bethlehem, PA, in 1938. In an operation for gangrenous
key component of safety. These operations may also be cholecystitis on 25 patients, which he termed partial cho-
helpful when cholecystectomy is difficult due to associated lecystectomy, the gallbladder was incised longitudinally and
hepatic cirrhosis.10 the wall of the gallbladder was excised up to the point that
it was attached to the liver. The part attached to the liver
itself was left behind and the free cut edge of the gall-
A BRIEF HISTORY OF OPERATIONS IN WHICH bladder was oversewn. The remaining mucosa was treated
ONLY A PART OF THE GALLBLADDER IS with iodine. Estes specifically stated that the cystic duct
REMOVED was not sutured or ligated and that no part of the gall-
In 1898, Hans Kehr11 operated on a 27-year-old woman bladder was sutured together to produce a closed cystic
with acute cholecystitis, intending to extirpate the structure, ie, a gallbladder remnant.17 Recovery was
92 Strasberg et al Subtotal Fenestrating Cholecystectomy J Am Coll Surg

generally quite smooth and there were no persistent bile MEANING OF PARTIAL AND SUBTOTAL
fistulas. Arthur Lerner,18 of Winnipeg, in 1950 and Wil- CHOLECYSTECTOMY AND INTRODUCTION OF
liam McElmoyle,19 of Victoria, British Columbia, in FENESTRATING AND RECONSTITUTING AS
1954 described variations of this technique, intended MODIFYING TERMS
specifically for difficult cholecystectomies and again Partial in surgical terminology literally means removal of
without producing a closed cystic structure. Lerner a part of an organ. It is quantitatively a vague term that
described 2 cases of “partial cholecystectomy” in which can mean removal of a small or large part of the organ.
he resected the free wall of the gallbladder down to the Subtotal means removal of almost all of an organ. It is
cystic duct. He noted that the cystic artery would be less vague as to extent. Normally, a partial resection is
cut within or on the wall of the gallbladder as one less than a subtotal resection, as in the terms partial gas-
trimmed the inferior aspect of the gallbladder wall trectomy and subtotal gastrectomy. However, a review of
near the cystic duct and recommended oversewing the the literature showed that in regard to the gallbladder,
wall at that point to occlude the vessel. McElmoyle19 some authors use the term partial to describe a near total
described and illustrated, in a singularly clear fashion, excision7,18,21,23-26; others use the term subtotal to describe
the principles and technique of this operation when per- the same extent of resection.8,10,20,27-30 It is a source of
formed specifically for the prevention of bile duct or confusion that 2 terms are used for the same procedure.
vascular injury during a difficult cholecystectomy. No Furthermore, neither term indicates whether a gallbladder
attempt is made to dissect the cystic duct or artery remnant is produced as a result of the procedure. The lack
when inflammation obscures the neck of the gallbladder. of nomenclature relating to gallbladder remnants is also a
The gallbladder is opened and the redundant portions source of confusion, so much so that recent review articles
excised. The cystic duct and the portions of the body, on this subject have subclassified subtotal cholecystec-
neck, and infundibulum lying above and to the left tomies7 or pointed out the variations.8 Therefore, 2 ad-
side are left in situ as a “shield to the vulnerable struc- justments to terminology are required, the first to deal
tures.” The cystic duct is not closed; its mucosa is ablated with the overlapping terms partial and subtotal, and the
and a drain is placed. McElmoyle19 reported 23 cases second to introduce words that will indicate whether a
with excellent results and no biliary fistula. What Estes, particular technique leaves a remnant gallbladder or not.
Lerner, and McElmoyle all recognized was that a portion As a starting point, it is suggested that the term subtotal
of the gallbladder wall should intentionally be left should be preferred over the term partial to designate
behind as a buffer between the edge of the dissection the extent of this resection because subtotal is clearly
on the gallbladder and the dangerous hepatocystic trian- more accurate than partial. If only the top half or less
gle.19 This was the “shield” of McElmoyle, which fulfils a of the gallbladder is removed, which is not what is being
main principle of safety: to stay 1 step away from danger. discussed in this article, the term fundectomy would seem
McElmoyle’s description was particularly eloquent. appropriate. In that way, the term partial cholecystectomy
Bornman and Terblanche20 clearly described and illus- could be completely eliminated in reference to excision
trated a similar operation 30 years later using the name of the gallbladder. Secondly, to designate whether or
subtotal cholecystectomy, but gave the option of internal not a remnant gallbladder is produced by the procedure,
suture of the cystic duct or external suture over a probe it is proposed that that the modifiers fenestrating (no gall-
advanced into the cystic duct from within the bladder remnant produced [Fig. 5]) and reconstituting
gallbladder. (gallbladder remnant produced [Fig. 6]) be introduced
While these authors were describing their techniques, to describe these operations. Therefore, 2 types of subtotal
others were presenting a modification in which the lowest cholecystectomies would be recognized, namely, subtotal
portion of the gallbladder was resutured. This step was fenestrating cholecystectomy and subtotal reconstituting
done to avoid biliary fistula but may also result in the cre- cholecystectomy.
ation of a remnant gallbladder. Maingot,21 who contrib-
uted much to the performance of biliary surgery, and
Grey Turner,22 who recognized the seriousness of biliary SUBTOTAL CHOLECYSTECTOMY AND THE
injury, suggested a similar approach in 1936 and 1944, CYSTIC DUCT
respectively, which they dubbed partial cholecystectomy. As noted in the historical section, the cystic duct and ar-
Note that the terms partial and subtotal were used in tery were sometimes ligated external to the gallbladder
some cases to describe the same operation, and in neither when a less than complete cholecystectomy was per-
case did the terms indicate whether a remnant gallbladder formed early in the development of cholecystectomy.
was produced. But as emphasized by McElmoyle19 and others,17,18 this
Vol. 222, No. 1, January 2016 Strasberg et al Subtotal Fenestrating Cholecystectomy 93

Figure 5. Subtotal fenestrating cholecystectomy. (A) The free, peritonealized portion of the
gallbladder has been excised except for a lip at the lowest portion of the gallbladder. This acts as
a shield to protect against inadvertently entering the hepatocystic triangle (“Shield” of McEl-
moyle). The portion of the gallbladder adherent to the liver has been left in situ. Stones have
been extracted. The cut edge of the gallbladder may be oversewn. The mucosa is usually ab-
lated. The cystic duct may be closed from the inside with a purse-string suture (inset). The cystic
duct may be very short, and attempts to ligate the cystic duct outside the gallbladder may result
in injury to the common bile duct. (B) As in Figure 5A, except a portion of the gallbladder adherent
to the liver has been excised.

method is undesirable when a subtotal operation is per- occlusion of the cystic duct should be attempted only
formed in the presence of difficult operative conditions. from the interior of the gallbladder by a purse-string
In fact, to do so, the surgeon must use the infundibular suture, as described in 1 method by Bornman and
technique to display the cystic duct. As explained earlier, Terblanche.20 The suggested alternative method of
this method of identification may be unreliable in the advancing a probe into the cystic duct from the interior
presence of severe inflammation. Under these conditions, of the gallbladder to identify and ligate the cystic duct

Figure 6. Subtotal reconstituting cholecystectomy. (A) The free, peritonealized portion of the
gallbladder has been excised. The portion of the gallbladder adherent to the liver may be left situ
as in Figure 5A or partially excised as shown here. The lowest portion of the gallbladder is closed
with sutures or staples, reconstituting an intact lumen in which stones may reform. (B) As in
Figure 6A, except that only the lowest part of the gallbladder remains. As in Figure 6A, this is
closed, reconstituting an intact lumen in which stones may reform. Whether the subtotal cho-
lecystectomy is “fenestrating” or “reconstituting” depends on whether the lowest part of the
gallbladder is left open (fenestrating) or closed (reconstituting) and not on the amount of gall-
bladder that is left attached to the liver.
94 Strasberg et al Subtotal Fenestrating Cholecystectomy J Am Coll Surg

external to the gallbladder20 has the potential danger of remnants that required excision at a second procedure
advancing the probe into the common bile duct and had an internal diameter of only about 1 cm. Clearly,
mistakenly ligating that duct instead of the cystic duct. many important aspects of the outcomes of these opera-
This would be prone to occur when the cystic duct tions will not be known until large studies involving small
is very short, as may happen when it is effaced by a and large hospitals are available. This will not be possible
large stone. using administrative databases because for now, subtotal
cholecystectomy does not have its own CPT code.
The modern technique for performing these operations
SUBTOTAL FENESTRATING CHOLECYSTECTOMY is straightforward (Figs. 5 and 6). The gallbladder is
AND SUBTOTAL RECONSTITUTING opened along its long axis and emptied of stones,
CHOLECYSTECTOMY: ADVANTAGES, including removal of stones in the lumen of the gall-
DISADVANTAGES bladder neck and cystic duct if possible. Also, consider-
Subtotal fenestrating cholecystectomy has the advantage ation may be given to attempting imaging either via
that a remnant gallbladder is much less likely to result cholangiography through the lumen of the gallbladder
than if the lumen of the gallbladder is re-established at or with intraoperative ultrasound. In either the fenestrat-
Hartmann’s pouch, as in the reconstituting technique. If ing or reconstituting type of procedure, the portion of the
an ERCP were done immediately after a subtotal reconsti- gallbladder adherent to the liver is usually left in situ and
tuting cholecystectomy, an area at the end of the cystic ablated. The latter may be done with electrocautery, argon
duct wider than the cystic duct would be present and beam, or saline-linked radiofrequency ablation. Alterna-
the criterion of Bodvall and Overgaard4 for the existence tively, some or all of the gallbladder attached to the liver
of a gallbladder remnant would be fulfilled. Although may be removed (Figs. 5 and 6). When this is done, the
closing over Hartmann’s pouch results in a gallbladder gallbladder wall and cystic plate may be removed down
remnant, it was found, as might be expected, to reduce to bare liver, as shown in the diagrams, or the cystic plate
the incidence of postoperative bile fistula in the reviews may be left in situ. The cut edge of the gallbladder
of subtotal cholecystectomy by Henneman and col- adherent to the liver may be oversewn with a continuous
leagues7 and Elshaer and associates.8 However, although suture. In some cases, the gallbladder will be gangrenous.
bile fistula was more common with the fenestrating tech- If so, the gangrenous portion should be excised without
nique, these fistulas seem to resolve spontaneously in most extending the extent of the subtotal resection. In the fen-
cases.8 Those that do not may be associated with retained estrating procedure, the very bottom of the gallbladder
common bile duct stones and relieved endoscopically. lumen remains open to the peritoneal cavity. There will
Based on presently available information, it would seem be a “lip” or “shield” of gallbladder (Fig. 5), where the
that the fenestrating type of subtotal cholecystectomy cystic artery branches come onto the gallbladder and these
would be preferable, but knowledge in this area is very will be transected at that point. Oversewing the cut edge
incomplete. There certainly have been no head-to-head of the gallbladder here may be necessary, although when
comparisons of fenestrating vs reconstituting techniques. inflammation is severe, these vessels are sometimes throm-
Furthermore, the extent to which Hartmann’s pouch is bosed. The cystic duct may be sutured from the inside us-
resected is probably quite variable, and the effect of leav- ing fine sutures, although this is often not possible. The
ing different size remnants on the chance of developing area should be carefully drained with 1 or 2 closed suction
subsequent symptoms is unknown. In fact, there is no drains, depending on the extent of the contamination. In
good information regarding the incidence of symptomatic the reconstituting type, the lip is usually somewhat larger
gallbladder remnants after subtotal reconstituting or sub- and the lumen is closed by various means including su-
total fenestrating cholecystectomies. A recent meta- tures and staplers8 (Fig. 6). Note again that the procedures
analysis discussed this issue,8 but articles on the subject are not distinguished by the amount of gallbladder left
rarely provide long-term follow-up of patients, and gall- adherent to the liver, but by whether or not a closed
bladder remnants may become symptomatic years after remnant gallbladder is created.
subtotal cholecystectomy, so good data on this topic are
lacking. Possibly, there is a watershed in the reconstituting
subtotal cholecystectomy procedure in which so little of LAPAROSCOPIC VS OPEN SUBTOTAL
the gallbladder lumen is left that it is equivalent to CHOLECYSTECTOMY
occluding the lumen of the cystic duct from within the Based on the meta-analysis of Elshaer and coworkers,8 it
gallbladder. If so, it must be an occlusion very close to seems that a subtotal fenestrating cholecystectomy is
the cystic duct because some symptomatic gallbladder more likely to be done when an open approach is used.
Vol. 222, No. 1, January 2016 Strasberg et al Subtotal Fenestrating Cholecystectomy 95

Paradoxically, in their data, bile leaks were more common Analysis and interpretation of data: Strasberg, Pucci,
after a laparoscopic procedure. Possibly, this is due to the Brunt, Deziel
improved ability to suture the cystic duct orifice when the Drafting of manuscript: Strasberg, Pucci, Brunt, Deziel
procedure is done open. The ideal procedure in circum- Critical revision: Strasberg, Pucci, Brunt, Deziel
stances when the CVS cannot be achieved would have
several attributes, including the following:
Acknowledgment: The authors gratefully acknowledge the
1. Does not leave a remnant gallbladder that will become contribution made to this manuscript by Jennifer Brum-
symptomatic and require a later operation. baugh, MA, Webmaster and Medical Illustrator, Depart-
2. Has low morbidity due to bile fistula. If a fistula occurs ment of Surgery, Thomas Jefferson University, who
it should resolve spontaneously over a short period. produced Figures 5 and 6. The editors are also grateful to
3. Can be done laparoscopically. Dr Martin Hertl, MD, FACS, Rush University Medical
4. Can be done by a general surgeon without additional Center, for translation of reference 12.
fellowship training in hepato-pancreato-biliary or
minimally invasive surgery.
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