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and operative reports is helpful to understand the patient’s current
gastrointestinal anatomy. Imaging with CTE or MRE and endoscopic
evaluation provide a preliminary “road map” of the distribution of
disease activity as well as any unsuspected entero-enteral fistulae,
contained perforations, and an overall estimate of small bowel
length. The optimal stoma site should be marked preoperatively
when a temporary or permanent stoma is likely.
The first step in any CD abdominal procedure is to thoroughly
examine the entire bowel. The bowel can be examined laparoscopically or via laparotomy, with the preoperative imaging and
endoscopic evaluation in mind, matching the preoperative findings
to the visual appearance of the bowel. The bowel must be visually
inspected, palpated digitally or through laparoscopic instruments,
and, if necessary, the lumen can be evaluated by passing a well-lubricated Foley or Fogarty balloon through the bowel and then retracting the partially inflated balloon to identify more subtle luminal
narrowings. Areas of small bowel disease usually display creeping
fat, wall thickening, and mesenteric thickening. Disease in the colon
may manifest more subtle external changes: mucosal disease can be
present with the external wall looking normal, hence preoperative
endoscopic evaluation is useful.
At the end of the examination, the surgeon should have a mental
road map of the gastrointestinal tract, with the total length of the small
bowel, the length and location of the diseased bowel, the phenotypic
appearance of the disease, and the presence of previous resections
and strictureplasties. Each diseased segment should be evaluated to
determine whether it is a candidate for strictureplasty, resection, or no
intervention in the case of a noncritical narrowing. The relationship
of multiple fibrostenotic strictures to one another must also be noted
to see whether they would need multiple simple strictureplasties, a
single intermediate or complex strictureplasty, a resection, or a combination of strictureplasties and resections. If abscesses or fistulae are
present, they must be computed in the surgical plan.
Gastroduodenal strictures are most often endoscopically accessible and can be treated with endoscopic dilation. When surgery
is indicated, short strictures throughout the first three portions of
the duodenum may be treated with the Heineke-Mikulicz strictureplasty, and strictures of the fourth portion of the duodenum may be
treated with the Finney strictureplasty by recruiting the first loop
of jejunum. These procedures are discussed later in this chapter. To
treat a duodenal stricture, the duodenum must be fully mobilized to
allow for a strictureplasty without tension. If a strictureplasty is not
feasible, a gastrojejunal bypass is a viable alternative.
Jejunal-ileal strictures may be addressed with a combination of
resection and strictureplasty techniques. Heineke-Mikulicz strictureplasty is the procedure of choice for short-segment strictures. Finney
strictureplasty is performed for longer-segment strictures. The
Michelassi strictureplasty is used for multiple sequential strictures.
These procedures are discussed later in this chapter.
Terminal ileum and colon strictures are usually the result of
inflammatory, nonpenetrating/nonstricturing or penetrating disease.
Therefore, a segmental resection is usually preferred. Occasionally,
Crohn’s terminal ileitis can be addressed with a modified Michelassi
strictureplasty.
Anastomotic strictures may be addressed with endoscopic dilation if endoscopically accessible. Anastomotic strictures that are not
amenable to endoscopic treatment can be addressed with resection
or strictureplasty. To perform a tension-free strictureplasty at the site
of a prior anastomosis, adequate mobilization of the intestinal loop
and lysis of adhesions must be performed. Anastomotic strictureplasty is safe and efficacious, but it is associated with a high rate of
recurrence (57%) when followed long term.
BOX 3 Strictureplasty Operative Strategy
• Anincisionismadealongthelengthofthestricture.
• Examinethemucosa,andperformabiopsyonanyareassus-
picious for dysplasia or carcinoma.
• Obtainexcellenthemostasis.
• Closetheenterotomywithabsorbableornonabsorbable
suture in one or two layers.
(Michelassi). Certain overarching principles are shared by all strictureplasty techniques:
■ After opening the bowel during the performance of a stricture-
plasty, the mucosal surface of the affected and neighboring bowel
must be evaluated for disease severity and presence of dysplasia/
carcinoma. Suspicious areas must be biopsied for frozen-section
analysis. If dysplasia or malignancy is confirmed, the strictureplasty is aborted in favor of an oncologic resection.
■ Excellent hemostasis is critical. Bleeding from a strictureplasty
site is one of the most common and troubling postoperative
complications. Bleeding is usually self-limited, but occasionally
requires blood transfusions. For persistent bleeding originating
from a strictureplasty within reach of an endoscope, endoscopic
techniques can be employed to achieve hemostasis. Selective
mesenteric angiography with intraarterial vasopressin infusion
effectively controls most episodes of bleeding originating from
strictureplasties that are not accessible with endoscopic techniques. In the presence of multiple suture lines (strictureplasties,
anastomoses), India ink blue dye can be injected at the time of
selective mesenteric angiography for subsequent intraoperative
localization of the bleeding.
■ Minimally invasive approaches to surgery can be utilized during
the performance of a strictureplasty either completely intracorporeally with effective laparoscopic or robotic suturing skills or
in a hybrid fashion by mobilizing and exteriorizing the affected
segment through a small incision in the abdominal wall.
Heineke-Mikulicz Strictureplasty (Fig. 1)
Short strictures are best treated with a Heineke-Mikulicz strictureplasty, a technique derived from the Heineke-Mikulicz pyloroplasty
performed for pyloric stenosis. The Heineke-Mikulicz strictureplasty
is appropriate for strictures up to 5 cm in length.
First, two 3-0 sutures, either nonabsorbable or absorbable, are
placed on each side of the bowel at the midportion of the stricture
to act as stay sutures. A longitudinal enterotomy is made over the
stricture on the antimesenteric side of the bowel, extending 1 to
2 cm beyond the length of the stricture proximally and distally into
STRICTUREPLASTY
TECHNIQUES (BOX 3)
The technical difficulty of strictureplasty varies from simple (Heineke-Mikulicz) and intermediate (Finney) to complex
FIG. 1 Heineke-Mikulicz strictureplasty. The longitudinal enterotomy is
closed transversely to reconstruct a more widely patent lumen.
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FIG. 2 Modified Gambee stitch. First the stitch penetrates all layers
of the bowel wall from the serosa to the luminal mucosa approximately
0.5 cm from the cut edge. The mucosa of the other limb is traversed out
of the bowel lumen, and then the mucosa of the first side is traversed
back into the bowel lumen. Finally, on the other limb, the stitch penetrates all layers of the bowel wall from the luminal mucosa to the serosa
approximately 0.5 cm from the cut edge. (From Shureih SF, Wilson TH Jr,
Howard WH. Modified Gambee stitch. Safe, easy and fast modification. Am J Surg.
1981;141:304.)
nondiseased bowel. The stay sutures are then pulled perpendicular
to the long axis of the bowel, lining up the enterotomy to be closed
transversely. The closure may be performed in one or two layers. For
a one-layer closure, the Gambee stitch (Fig. 2), using an absorbable
suture, ensures appropriate approximation of the mucosa and serosa
while leaving the blood supply intact between sutures and is particularly well-suited to strictureplasty. For a two-layer closure, a running
absorbable inner layer is followed by an interrupted Lembert nonabsorbable suture outer layer.
A Sasaki modification of the Heineke-Mikulicz strictureplasty
technique (Fig. 3) can be applied to two short-segment strictures in
very close proximity. The enterotomy is created along the antimesenteric border through both strictures and the intervening healthy
segment of intestine. The resulting longer enterotomy is then closed
transversely after tailoring the end of each transected stricture.
The Moskel-Walske-Neumayer strictureplasty (Fig. 4) is another
modification of the Heineke-Mikulicz strictureplasty that applies
a V-Y advancement flap closure to address the disparity in size
between a very dilated proximal bowel and a nondilated distal bowel.
The enterotomy is created along the antimesenteric border of the
stricture extending into a Y shape on the antimesenteric border of
the dilated bowel just proximal to the stricture. The Y-flap of the
proximal dilated bowel is advanced into the strictured area and
closed in a transverse fashion.
The Judd strictureplasty is a variation of the Heineke-Mikulicz
strictureplasty used when the strictured segment also includes a fistula opening. This technique can be used when the fistula opening is
located on the antimesenteric side of the bowel. The anti-mesenteric
longitudinal incision is made to include the fistula opening. The
fistula opening is debrided, leaving healthy tissue, and the enterotomy is closed transversely using the described Heineke-Mikulicz
technique.
S
N
S
Finney Strictureplasty (Fig. 5)
The Finney strictureplasty is also derived from the homonymous
pyloroplasty technique. The Finney strictureplasty is appropriate for
strictures 5 to 12 cm in length or for a similar-length segment with
multiple short strictures closely grouped together with intervening
short segments of dilated bowel.
The strictured segment is folded creating a U-shape loop. A
rigid stricture that lacks the pliability to fold onto itself may require
folding normal bowel onto diseased bowel. The two limbs of the U
are sutured together in a side-to-side fashion. Interrupted Lambert
FIG. 3 Sasaki modification of the Heineke-Mikulicz strictureplasty can be
applied to a segment that contains two short segment strictures (S) with a
short intervening segment of normal (N) or dilated bowel.
sutures are placed close to the facing mesenteric borders forming
the posterior outer layer, extending 1 to 2 cm beyond the length
of the stricture proximally and distally. A longitudinal enterotomy
is created just above the stitches. The side-to-side anastomosis is
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FIG. 6 The Jaboulay strictureplasty is a modification of the Finney stric-
tureplasty that excludes the segment of the stricture that is not amenable
to suturing.
FIG. 4 Moskel-Walske-Neumayer strictureplasty is a modification of the
Heineke-Mikulicz strictureplasty that can be used to address a size mismatch of the dilated proximal segment of small bowel and the strictured
segment of small bowel. The longitudinal enterotomy along the stricture is
extended into a Y-shaped enterotomy on the dilated proximal bowel and
closed transversely by advancing the apex of the Y into the most distal
point of the enterotomy. (From Tichansky D, Cagir B, Yoo E, etal. Strictureplasty
for Crohn’s disease: meta-analysis. Dis Colon Rectum. 2000;43:911–919.)
FIG. 5 Finney strictureplasty. The stricture is folded into a U-shape, and a
side-to-side anastomosis is created between the proximal and distal portions of the stricture.
constructed with an inner layer of running absorbable suture, reinforced by an anterior outer layer of interrupted Lambert sutures.
If the bowel quality of the stricture is not suitable for suturing, a
Jaboulay strictureplasty (Fig. 6) is a modification of the Finney strictureplasty in which a side-to-side anastomosis is created between
the uninvolved healthy bowel proximal and distal to the stricture,
leaving the strictured segment in place as a short bypassed segment.
This side-to-side anastomosis can also be created using a stapler
device. One concern specific to the Jaboulay strictureplasty is that
the short-bypassed segment may lead to long-term issues of bacterial
overgrowth, septic complications, and malignant degeneration.
Michelassi Strictureplasty or Side-to-Side
Isoperistaltic Strictureplasty (Fig. 7)
The side-to-side isoperistaltic strictureplasty (SSIS) preserves long
segments of bowel that otherwise would be resected leading to major
FIG. 7 Michelassi strictureplasty (side-to-side isoperistaltic stric-
tureplasty). Long strictures or multiple consecutive strictures can be
treated with side-to-side isoperistaltic strictureplasty. The involved segment
and associated mesentery are divided to allow for the two segments to
align alongside one another and create an isoperistaltic side-to-side anastomosis. (From Tichansky D, Cagir B, Yoo E, etal. Strictureplasty for Crohn’s disease:
meta-analysis. Dis Colon Rectum. 2000;43:911–919.)
loss of intestinal absorptive capacity. Segments of bowel greater than
12 cm containing a single long stricture or a series of shorter strictures in close proximity to one another over a long intestinal segment
may be addressed with SSIS.
The bowel and the mesentery are divided at the midpoint of the
segment of bowel intended for the strictureplasty. The proximal and
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distal loops of the diseased bowel are brought alongside each other to
overlap in a side-to-side isoperistaltic fashion, lining up the stenotic
areas of one loop against the dilated areas of the other loop as much
as possible. The two limbs are approximated with interrupted nonabsorbable Lambert sutures, forming the posterior outer layer of the
ultimate closure. A longitudinal enterotomy is then made just above
the sutures along the length of each of the two intestinal loops. The
ends of the bowel are spatulated to avoid creating blind ends. Luminal hemostasis is obtained with suture ligation and electrocautery.
The inner layer of running full-thickness absorbable sutures starts
with two sutures at the middle of the posterior suture line and each
progresses anteriorly as a continuous Connell stitch. An anterior
outer layer of interrupted seromuscular sutures completes the twolayer closure. Thick and friable mesentery may restrict the mobility
of the small bowel and thereby limit the ability to transect and slide
the proximal intestinal loop alongside the distal intestinal loop, precluding creation of an SSIS.
If the transection of the intestine and the mesentery cannot be
performed at the midpoint of the diseased loop and one resulting loop is shorter than the other, normal bowel can be recruited
into the anastomosis when aligning the two limbs. The Michelassi
strictureplasty can also be combined with resection of very severely
diseased segments. If the middle of the diseased loop of intestine
is severely affected by a long, rigid stricture that is not amenable
to creating a safe anastomosis, that segment can be resected before
sliding the proximal and distal loop alongside each other and creating the SSIS (Fig. 8A). Similarly, if one end of the diseased loop
of intestine is severely affected, that segment can be resected, and
FIG. 8 (A) Resection side-to-side isoperistaltic strictureplasty (SSIS). The severe stricture located in the middle of the diseased loop can be resected
before sliding the proximal and distal loops alongside each other and performing the SSIS. (B) Side-to-side-to-end SSIS. The severe stricture located at one
end of the diseased loop can be resected, and the SSIS can be anastomosed to the uninvolved bowel in an end-to-end fashion. (C) End-to-side-to-side-toend SSIS (SSIS with two discontinuous bowel loops). Severe strictures located in the middle and at either end of the diseased loop can be resected before
performing the SSIS using the discontinuous diseased loops and then creating an end-end anastomosis at each end of the SSIS (Michelassi II). SBR, small
bowel resection. (From Lowenfeld L, Michelassi F. Managing stricturing Crohn’s disease: Resect? Strictureplasty? Dilate? J Laparoendosc Adv Surg Tech A. 2021;31[8]:881–
889.)
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the side-to-side strictureplasty can be anastomosed to the distal or
proximal uninvolved bowel (Fig. 8B). When three severely fibrotic
and deformed bowel segments are separated by two strictured segments, the Michelassi II strictureplasty can be employed (Fig. 8C).
After resection of the three severely diseased segments located in
the middle and at either end of the diseased loop, the remaining two
discontinuous segments are used to perform an SSIS, according to
the original description. Finally, each of the two ends of the SSIS is
then anastomosed with the proximal and the distal bowel fashioning
an end-to-side-to-side-to-end strictureplasty.
Results
In one of the largest systemic reviews and meta-analysis of 23 series
on strictureplasty, including 1112 patients and 3259 strictureplasties, Yamamoto et al. reported that the most commonly performed
strictureplasty was the Heineke-Mikulicz strictureplasty (81%),
and strictureplasties are most often performed in the jejunoileal
region (94%). The mean number of strictureplasties performed
during one operation was 3 (range 1–21). The majority of patients
underwent simultaneous resection and strictureplasty (61%). These
observations have remained constant despite the widespread use of
biologics and the development of complex strictureplasty techniques
to address extensive CD in the past two decades (Heineke-Mikulicz
82.6%, jejunoileal 99.7%, simultaneous resection 73.7%). In a paper
reviewing the 25-year experience with SSIS, Michelassi et al. found
that 24% of patients who underwent strictureplasty for jejunoileitis
underwent one or more SSIS procedures, and of the patients who
underwent SSIS, 47% required additional small bowel resection
away from the site of strictureplasty, and 45% required at least one
synchronous conventional strictureplasty.
Yamamoto et al. reported a 13% overall complication rate following jejunoileal strictureplasty.
4% of cases, with 78% of septic complications related to the strictureplasty site and 44% of patients experiencing postoperative sepsis
requiring laparotomy. The risk of postoperative hemorrhage requiring at least 2 units of packed red blood cells was 3%, probably as a
result of creating a suture line in thick, diseased bowel. Most were
successfully managed nonoperatively, only 6% requiring laparotomy.
Only 2% of patients developed postoperative ileus, and 1% developed
postoperative bowel obstruction. Of the patients who developed
bowel obstruction, 27% required laparotomy. Emergency surgery,
intraabdominal abscess, low hemoglobin, hypoalbuminemia, preoperative weight loss, and older age were significant risk factors for
postoperative complications. In a meta-analysis including 32 studies
with a total of 1616 patients and 4538 strictureplasties, Campbell
et al. found that the incidence of early or late complications after a
conventional (Heineke-Mikulicz, Finney) or nonconventional (SSIS)
strictureplasty was similar (early complications 15% vs. 8% and late
complications 29% vs. 17%, respectively).
Large studies and meta-analyses support strictureplasty as at least
an equivalent alternative to resection in the treatment of CD. For
extensive CD, use of the Michelassi strictureplasty may help avoid
postoperative short gut syndrome. In the paper reviewing the 25-year
experience with SSIS, Michelassi et al. showed that the median length
of spared bowel was 52.5 cm (range: 20–280), equal to 17% of bowel
length (range, 4.3%–40%).
In terms of disease recurrence following strictureplasty, Yamamoto reported a 5-year recurrence rate following strictureplasty
of 28%, with only a 3% site-specific recurrence rate. Comparing
recurrence rates after strictureplasty and resection is challenging
because these operations are usually performed in two different
groups of patients who may have a different risk for recurrence:
6
Septic complications occurred in
strictureplasties are performed in fibrostenotic CD, while resections
are performed in all types of CD (fibrostenotic, inflammatory, and
penetrating). How much the phenotype of the disease influences
the recurrence rate is poorly understood. Yet, from available data,
it seems that the site-specific operation-free interval is similar for
patients who undergo resection or strictureplasty.
SUMMARY
No treatment is curative in CD, and there is no medical therapy to
prevent or reverse stricturing disease. Stricturing CD most commonly occurs in the small intestine and, over time, can lead to
small bowel obstruction. While small bowel resection appropriately
addresses a first incidence of obstruction at a single site, bowel preservation must be prioritized in the treatment of recurrent, extensive,
and multifocal CD to avoid or delay the occurrence of short gut syndrome. Strictureplasty techniques alleviate strictures and preserve
small bowel absorptive surface. Different strictureplasty techniques
have been developed to address the variety of disease presentations.
The safety profile of strictureplasty is good, making the technique
safe. In terms of disease recurrence, the site-specific operation-free
interval is similar for patients who undergo resection or strictureplasty. Strictureplasty can be used as a complement to medical therapy, endoscopic treatments, and surgical resection. These treatments
may be used simultaneously, sequentially, and repeatedly.
S u g g e S t e d R e a d i n g S
Bislenghi G, Fieuws S, Wolthuis A, etal. Positioning strictureplasty in the
treatment of extensive Crohn’s disease ileitis: a comparative study with
ileocecal resection. Int J Colorectal Dis. 2021;36(4):791–799.
Campbell L, Ambe R, Weaver J, Marcus SM, Cagir B. Comparison of con-
ventional and nonconventional strictureplasties in Crohn’s disease: A systematic review and meta-analysis. Dis Colon Rectum. 2012;55(6):714–726.
Fichera A, Lovadina S, Rubin M, Cimino F, Hurst RD, Michelassi F. Patterns
and operative treatment of recurrent Crohn’s disease: a prospective longitudinal study. Surgery. 2006;140(4):649–654.
Mege D, Michelassi F. Michelassi II strictureplasty for Crohn’s Disease: A new
side-to-side isoperistaltic strictureplasty with discontinuous bowel loops.
Ann Surg. 2020;271(1):e1–e2.
Michelassi F. Side-to-side isoperistaltic strictureplasty for multiple Crohn’s
strictures. Dis Colon Rectum. 1996;39(3):345–349.
Michelassi F, Hurst RD, Melis M, etal. Side-to-side isoperistaltic stricture-
plasty in extensive Crohn’s disease: A prospective longitudinal study. Ann
Surg. 2000;232:401–408.
Michelassi F, Mege D, Rubin M, Hurst RD. Long-term results of the side-to-
side isoperistaltic strictureplasty in crohn disease: 25-year follow-up and
outcomes. Ann Surg. 2020;272(1):130–137.
Rottoli M, Tanzanu M, Manzo CA, etal. Strictureplasty for Crohn’s disease of
the small bowel in the biologic era: long-term outcomes and risk factors
for recurrence. Tech Coloproctol. 2020;24(7):711–720.
Sasaki I, Funayama Y, Naito H, Fukushima K, Shibata C, Matsuno S. Extended
strictureplasty for multiple short skipped strictures of Crohn’s disease. Dis
Colon Rectum. 1996;39:342–344.
Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classifi-
cation of inflammatory bowel disease: Controversies, consensus, and
implications. Gut. 2006;55(6):749–753.
Sayfan J, Wilson DAL, Allan A, Andrews H, Alexander-Williams J.
Recurrence after strictureplasty or resection for Crohn’s disease. Br J Surg.
1989;76(4):335–338.
Yamamoto T, Keighley MRB. Long-Term results of strictureplasty for ileo-
colonic anastomotic recurrence in Crohn’s disease. J Gastrointest Surg.
1999;3(5):555–560.
Yamamoto T, Fazio VW, Tekkis PP. Safety and efficacy of strictureplasty for
Crohn’s disease: a systematic review and meta-analysis. Dis Colon Rectum.
2007;50(11):1968–1986.
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Management of Small
Bowel Tumors
Ramy El-Diwany, MD, PhD, and John W. Harmon, MD
mall bowel malignancies are rare, difficult to diagnose, and have
few treatment guidelines. Because small bowel tumors present
S
with vague and common symptoms, it is imperative that the surgeon keep them on the differential for abdominal pain, obstruction,
and gastrointestinal (GI) bleed. However, the majority of patients
referred to surgeons for small bowel tumors have a suspicious mass
on imaging. Evidence-based guidelines on management of small
bowel malignancy are difficult to find, and given the rarity of these
lesions, there is little information in the literature to provide reference for clinical decision making.
PRESENTATION
The typical presenting symptoms of small bowel tumors are vague
and highly variable. Many patients with a known mass, discovered
following workup for GI bleeding or encountered incidentally on
imaging, present to surgeons as a referral from a primary care provider or a gastroenterologist. Others will present with colicky pain
from obstruction, either partial or complete, and will be found to
have a small bowel tumor during surgery. The mass itself can be intraluminal or circumferential, directly responsible for obstruction, or
can have surrounding fibrosis that results in stricture and adhesion to
the mesentery or retroperitoneum. GI stromal tumors (GIST) are frequently asymptomatic but can present with bleeding or obstruction.
Paraneoplastic symptoms such as weight loss and vague abdominal pain are concerning for malignant neoplasms like adenocarcinoma and lymphoma, particularly in the context of a known small
bowel mass; however, these nonspecific symptoms should prompt
broad investigations, as small bowel tumors are one of the rarer
malignancies. Neuroendocrine tumors (NETs) that are productive of
vasoactive amines can present with a wide range of symptoms, from
epigastric pain and ulcerations to flushing, sweating, and diarrhea.
However, most are asymptomatic and are found incidentally on
imaging workup for other conditions.
complete blood count to look for anemia or elevated white blood
cell count in the acute setting if signs of perforation are present.
Elevated liver enzymes or amylase suggest possible duodenal mass
or obstruction. Carcinoembryonic antigen (CEA) is often elevated in
small bowel adenocarcinoma but is not sensitive or specific. Serum
5-HIAA and chromogranin A should not be routinely tested unless
there is a strong clinical suspicion of NET based on symptoms or
imaging features.
Imaging
Upon presentation with obstructive symptoms, a computed tomography (CT) scan with IV contrast allows clinicians to visualize the
location of obstruction and possibly even the mass itself (Fig. 1).
Masses can be constricting, occasionally demonstrating an “apple
core” appearance with a circumferential constriction of the lumen.
Some masses are polypoid, projecting intraluminally, and are better
visualized with oral contrast. Close evaluation of the contour of the
bowel is necessary to find submucosal lesions, and the keen surgeon should also thoroughly evaluate the mesentery for associated
enlarged nodes or a mesenteric-based mass. Occasionally, enlarged
nodes are the only sign of a nearby small tumor. A negative CT
should not rule out small bowel tumor, as they are not particularly
sensitive in this condition. However, CT does detect abnormalities in
up to 80% of patients who do have a small bowel tumor. CTs are also
valuable for staging nodes and metastatic lesions. Additional specialized imaging modalities such as octreotide or PET/DOTATATE
scans are helpful in localization of NETs and identification of multifocal and metastatic disease (Fig. 2). In some institutions, these scans
are routine before operative intervention.
Endoscopy
Esophagogastroduodenoscopy (EGD) can detect tumors into the
third portion of the duodenum and is an excellent tool to begin the
workup for GI bleed or other symptoms that are suspicious for GI
masses. Endoscopic ultrasound is a useful adjunct to standard EGD
Predisposing Conditions
Familial adenomatous polyposis (FAP), hereditary nonpolyposis
colon cancer (HNPCC) and Peutz-Jeghers syndrome (PJS) are
genetic cancer syndromes that predispose to small bowel malignancy. Crohn’s disease and celiac sprue, chronic inflammatory
conditions involving the small bowel, also predispose to small bowel
malignancy, and risk increases with increased severity and longer
duration of disease. Patients with cystic fibrosis have 19-times higher
incidence than the general population, with an additional 2- to 5-fold
higher risk following lung transplantation. Obesity, tobacco use, and
high dietary intake of red meat, smoked foods, alcohol, and refined
sugar have all been shown to have an association with small bowel
tumors, but the links between these risk factors and tumorigenesis
are not clear. In fact, the etiology of small bowel tumors that are not
associated with either chronic inflammatory diseases or genetic cancer syndromes is poorly understood.
Examination and Diagnostics for Patients Found to
Have Small Bowel Tumors
On physical examination, it is only rarely possible to palpate an
abdominal mass. Laboratory workup should include the standard
FIG. 1 Adenocarcinoma in the fourth portion of duodenum (arrow).
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A
C
B
D
E
but in the discussion of small bowel tumors is limited to evaluation of
duodenal lesions. For more distal evaluation, balloon-assisted deep
enteroscopy or push endoscopy techniques can be performed by
expert gastroenterologists and allow for visualization of most or even
all of the small bowel lumen. This, however, is only rarely employed
and only available in specialized centers. Video capsule endoscopy
(VCE) also affords the ability to evaluate the mucosal surface of the
FIG. 2 DOTATATE PET/CT scan demonstrating
focal uptake of somatostatin receptor tracer in primary neuroendocrine (A, B) small bowel tumor and
(C, D) liver metastasis. (E) Scintigraphy showing
primary tumor and liver metastasis. (Images courtesy
Javad Azadi, MD.)
entire small bowel, with an average of 30,000 images captured in the
small bowel alone during an examination. With the assistance of
neural networks and machine learning, the interpretation of these
studies is becoming more sensitive and specific, making them an
increasingly helpful tool for the investigation of small bowel tumors.
VCE does not allow for tissue diagnosis and is contraindicated in
patients with obstructive symptoms.
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MANAGEMENT
Benign
Several types of benign small bowel neoplasms exist, and all are
quite rare. Adenomas can be categorized as either villous, tubular, or
Brunner’s gland associated. As in colorectal cancer, some adenomas
have malignant potential. There are no firm guidelines regarding
management of these masses, but conventionally, the colorectal
cancer pathway is followed with endoscopic resection if possible.
Adenomas have increased malignant potential when associated with
FAP. The number, size, histology, and dysplastic characteristics of the
polyps should guide management using the Spigelman classification.
Surgical resection is warranted for large adenomas that are not
amenable to endoscopic resection, particularly if biopsy reveals villous features. Additionally, patients should be screened for synchronous colorectal lesions with colonoscopy.
Leiomyomas are small tumors that are present in the submucosa
of the small bowel. They are routinely small, firm, and well circumscribed. While they may cause obstruction and require resection
for this reason, their presence alone is not an indication for surgery.
Differentiating between leiomyosarcoma and leiomyoma can be
difficult, and often these lesions are surgically resected to rule out
malignant disease.
Lipomas are diagnosed relatively easily on CT due to their characteristic fatty density. Hamartomas associated with PJS should be
resected only if causing bleeding or obstructive symptoms. In addition to lipomas and hamartomas, fibromyxomas and ganglioneuromas do not require resection, although biopsy may be necessary for
diagnostic confirmation. Hemangiomas can be present along the
length of the small bowel. Fortunately, these are easily differentiated
on CT with IV contrast or magnetic resonance (MR) enterography
obviating the need for biopsy.
Malignant
Malignant tumors of the small bowel are rare, with an estimated
10,470 cases and an estimated 1450 mortalities in the United States
in 2018. Small bowel cancer comprises only 1% to 2% of GI malignancies. Because of the rarity of these cases and available retrospective data, there are very few guidelines available even worldwide for
treatment of small bowel malignancy, and those are routinely derived
from expert opinion based on analogous management of colon cancer. For this reason, each case should be evaluated on an individual
basis and overseen by a multidisciplinary oncology team including a
surgical oncologist.
Neuroendocrine Tumors
Derived from enterochromaffin cells, known as Kulchitsky cells,
NETs are found throughout the crypts of Lieberkühn and are the
most common small bowel tumor. They are histologically characterized by cytoplasmic core granules most commonly containing chromogranin A, synaptophysin, and neuron-specific enolase
(Fig. 3). They often have the capacity to secrete clinically relevant
vasoactive monoamines, peptides, and hormones. Neuroendocrine
tumors are commonly referred to as carcinoid tumors and are the
most common tumors of small bowel, accounting for more than
20% of the malignant tumors in the small bowel. Although small
bowel NETs are often incidentally identified, many individuals
present with advanced disease. At presentation, 40% of individuals
will have multifocal tumors >2 cm, 70% will have invasion into the
muscularis propria and regional lymph nodes, and 50% will have
liver metastasis. Five-year cancer-specific survival in local staged
small bowel NETs is 95%; however, with nodal and distant disease,
this falls to 84% and 51%, respectively, with an overall survival of
32% in individuals with distant disease. Well-differentiated NETs are
characterized as grade 1 to 3 based on Ki-67 index (%) and mitotic
index/10 high-powered field (Table 1). GI NETs can occur anywhere
in the GI tracts; however, 35% to 45% of them occur in the small
intestine, and most are found within 60 cm of the ileocecal valve. On
CT scan, carcinoid lesions are hyperenhancing in contrast to adenocarcinomas that are only moderately enhancing. They tend to extend
through the serosa and can cause foreshortening of the mesentery
secondary to a desmoplastic reaction. Frequently, the primary small
bowel lesion is not visualized on imaging, and the presenting finding
is bulky mesenteric adenopathy.
The regional spread of carcinoid tumors necessitates en bloc
resection of the mass and mesentery, including an extensive lymphadenectomy, which is often more amenable to an open exploration
(Fig. 4). During the operation, it is important to inspect for mul-
ticentric disease and liver metastases. However, even if these are
present, it is still recommended to resect the primary lesion both
for local control and longevity. Evidence indicates that 90% of the
disease burden should be removed to yield the most durable symptomatic improvement, so any disease that seems resectable should
be targeted at the time of surgery. In patients with liver metastasis,
occasionally a staged approach to resection is implemented. Operative manipulation of carcinoid tumors has been associated with
hemodynamically significant surges in vasoactive peptides known
as carcinoid crisis, which is generally managed with high-dose
somatostatin analogues in addition to hemodynamic stabilization.
There is mixed evidence supporting the use of prophylactic somatostatin analogues for the prevention of carcinoid somatostatin
crisis, and the practice varies substantially among surgeons and
institutions. For duodenal carcinoid, endoscopic resection may be
possible for small lesions. Anterior wall duodenal lesions may be
directly excised with laparoscopic or open surgery. For select posterior lesions, local excision through an anterior duodenotomy to
expose the posterior wall is an excellent approach. When both an
anterior and posterior duodenotomy are performed, a gastrojejunostomy is recommended to avoid obstruction from narrowing of
the duodenum. A Fogarty balloon, introduced through the gallbladder or cystic duct and passed proximally through the ampulla, can
provide guidance during resection of tumors in the second portion
of the duodenum. A cholecystectomy is then performed. This avoids
opening the common bile duct. If the tumor is too close to the
ampulla to be safely resected, a pancreaticoduodenectomy may be
the only recourse.
Typical small bowel carcinoid resection removes 1 to 2 feet of
small bowel, with wide lymphatic mesenteric clearance. The mesenteric involvement of this disease is often underestimated and can
be misleading, necessitating more bowel resection than originally
anticipated in some cases. It is imperative that patients are counseled about the risks of extensive resection preoperatively. Cases
in which there is extensive involvement of small bowel mesentery
require careful deliberation, and in some cases, leaving mesenteric
disease behind is a disconcerting but necessary consideration to
avoid short-gut syndrome. The authors would like to emphasize
that while extensive resection should be considered for debulking
symptomatic, multifocal, or metastatic disease, the consequences
of a near-complete enterectomy, if less than 120 cm of small bowel
remained, certainly outweigh the benefits of resection for these cases.
Similarly, if the disease is extensive but relatively asymptomatic, with
heavy mesenteric involvement to the root, the OR may best be left
out of the treatment plan and systemic medical treatment with a
somatostatin analogue is warranted.
Both multiple endocrine neoplasia type I (MEN1) and neurofibromatosis predispose patients to small bowel NETs; however, these
occur primarily in the foregut, presenting as gastrinomas or somatostatinomas. The diagnosis and management of individual NETs is
discussed elsewhere in this textbook.
SMALL BOWEL 147
C
D
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BA
FIG. 3 Histology of NET. (A, B) Small bowel serosal invasion with surrounding normal small bowel mucosa (H&E, 2× and 20× magnification).
(C) Synaptophysin (20× magnification). (D) Chromogranin (20× magnification). (Images courtesy Neil Neumann, MD, PhD, and Sarah Umetsi, MD, PhD.)
Adenocarcinoma
More than a third of small bowel cancers are adenocarcinoma and
occur primarily in the duodenum. Unfortunately, because they are
relatively asymptomatic until they are large enough to be obstructive
or cause clinically evident bleeding, more than half of these tumors
present at advanced stages, a third with nodal spread, and a quarter
with distant metastases. Because of this, the 5-year survival following
diagnosis is only 20% to 40% in most cases. Surgical resection is the
TABLE 1 Gastrointestinal Neuroendocrine
mainstay of therapy, with a segmental resection and accompanying wide local excision of the mesentery to collect the nodal basin
(Fig. 5). For those at the terminal ileum, an ileocolectomy should be
performed. For duodenal lesions at the ampulla, a pancreaticoduodenectomy is necessary.
For unresectable primary disease, it is reasonable to perform a
palliative surgical bypass of the obstructive lesion. Palliative radiation for unresectable disease is usually not beneficial. Clinical trials
are ongoing to improve local and systemic control of unresectable
disease, and surgeons are encouraged to help patients seek out these
resources if possible.
Neoplasm Classification System
KI-67 INDEX
(%)
WELL-DIFFERENTIATED
NET GRADE 1 <3 <2
NET GRADE 2 3–20 2–20
NET GRADE 3 >20 >20
POORLY DIFFERENTIATED
NET GRADE 3 >20 >20
SMALL CELL TYPE N/A N/A
LARGE CELL TYPE N/A N/A
MIXED NEUROENDOCRINE
NEOPLASMS
Data from WHO classification of Tumors of Endocrine Organs, Fourth edition (2017).
MITOTIC
INDEX/10 HPF
FIG. 4 Ileocecal resection specimen with carcinoid tumor extending into
serosal surface with regional lymph node metastasis. (Image courtesy Neil
Neumann, MD, PhD, and Sarah Umetsi, MD, PhD.)
148 MANAGEMENT OF SMALL BOWEL TUMORS
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GIST
Mesenchymal tumors such as GISTs are most often found in the
stomach (>50%) but also develop in the small bowel, with 25% in the
jejunum. Derived from the interstitial cells of Cajal, they comprise
approximately 10% of small bowel tumors. About 20% to 30% of GISTs
are malignant at presentation, more often malignant when involving
the small bowel. On CT scan, they appear as smooth, well-defined
masses arising from the small bowel wall demonstrating exophytic
growth patterns and internal heterogeneity. They may have areas of
central hemorrhage or necrosis (Fig. 6). GIST rarely metastasize to
nodes or spread outside of the abdominal cavity but can be aggressive.
Metastases to the liver can present with multiple serosal-based nodules. The primary lesions are known for causing ulceration through
the mucosa, presenting with bleeding. GIST can be differentiated
from other sarcomas of smooth muscle by immunostaining for c-KIT.
Activating mutations of the KIT oncogene can be seen in over 80%
of GISTs. CT-guided biopsy is usually not necessary as radiographic
appearance is distinctive and resection is indicated.
A laparoscopic approach for resection of GIST is often ideal.
These tumors are exophytic, making them easier to locate than other
small bowel tumors during laparoscopic exploration, and as they
do not spread via lymphatics, lymphadenectomy is not required.
A short segmental enterectomy with only 2 cm margins is recommended. If the tumor is bulky or adjacent organ involvement is
suspected, preoperative imatinib can aid in shrinking the mass to
facilitate resection. Unfortunately, more than 50% of these masses
recur within 5 years. To prolong disease-free survival, high-risk
patients should be treated postoperatively with a minimum of 12 to
24 months of imatinib, and studies are ongoing regarding longer or
even indefinite treatment to prevent recurrence. High-risk features
include tumor size >2 cm, high mitotic index, poorly differentiated
cell type, presence of metastasis, and positive margin.
Sarcoma
Sarcoma, typically leiomyosarcoma, is rare, occurring most often in
the ileum. Five-year survival is approximately 50%. Radical surgical
excision is recommended if the primary disease is resectable. Similar
to adenocarcinoma, if the disease is deemed unresectable, surgical
bypass should be considered. Palliative radiation has a greater role
in sarcoma management compared with other small bowel tumors.
Lymphoma
The small bowel is the most frequently encountered extranodal site
for lymphoma. This tumor is usually non–Hodgkin-type lymphoma
and involves the small bowel mesentery more commonly than the
luminal surface. It is most common in the ileum, the most lymphoid-rich region of the small bowel. Clinicians should maintain
a high suspicion for other sites of involvement, as a solitary small
FIG. 5 Small bowel adenocarcinoma (A) intraoperative photo and (B) gross pathology. (B courtesy of Neil Neumann, MD, PhD, and Sarah Umetsi, MD, PhD).
AB
FIG. 6 (A) Gross pathologic appearance high-grade GIST invading distal pancreas. (B) Gross pathologic appearance of intraluminal portion of GIST. (Images
courtesy Neil Neumann, MD, PhD, and Sarah Umetsi, MD, PhD.)
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