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Journal of Visceral Surgery (2014) xxx, xxx—xxx

Available online at

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REVIEW

The management of lower gastrointestinal

bleeding
Y. Marion a,d,∗, G. Lebreton a,d, V. Le Pennec b,d,
E. Hourna b,d, S. Viennot c,d, A. Alves b,d

a
Service de chirurgie digestive, centre hospitalier universitaire, avenue de la Côte-de-Nacre,
14000 Caen, France
b
Service de radiologie, centre hospitalier universitaire, avenue de la Côte-de-Nacre, 14000
Caen, France
c
Service de gastro-entérologie, centre hospitalier universitaire, avenue de la Côte-de-Nacre,
14000 Caen, France
d
Université de Caen, faculté de médecine, 14000 Caen, France

KEYWORDS Summary Lower gastrointestinal (LGI) bleeding is generally less severe than upper gastroin-
Lower testinal (UGI) bleeding with spontaneous cessation of bleeding in 80% of cases and a mortality
gastrointestinal of 2—4%. However, unlike UGI bleeding, there is no consensual agreement about management.
bleeding; Once the patient has been stabilized, the main objective and greatest difficulty is to identify the
Angiography; location of bleeding in order to provide specific appropriate treatment. While upper endoscopy
Endoscopy; and colonoscopy remain the essential first-line examinations, the development and availability
Video capsule of angiography have made this an important imaging modality for cases of active bleeding; they
endoscopy; allow diagnostic localization of bleeding and guide subsequent therapy, whether therapeutic
Enteroscopy; embolization, interventional colonoscopy or, if other techniques fail or are unavailable, surgery
Surgery directed at the precise site of bleeding. Furthermore, newly developed endoscopic techniques,
particularly video capsule enteroscopy, now allow minimally invasive exploration of the small
intestine; if this is positive, it will guide subsequent assisted enteroscopy or surgery. Other
small bowel imaging techniques include enteroclysis by CT or magnetic resonance imaging. At
the present time, exploratory surgery is no longer a first-line approach. In view of the lesser
gravity of LGI bleeding, it is most reasonable to simply stabilize the patient initially for sub-
sequent transfer to a specialized center, if minimally invasive techniques are not available at
the local hospital. In all cases, the complexity and diversity of LGI bleeding require a multidis-
ciplinary collaboration involving the gastroenterologist, radiologist, intensivist and surgeon to
optimize diagnosis and treatment of the patient.
© 2014 Elsevier Masson SAS. All rights reserved.

∗ Corresponding author. Service de chirurgie digestive, centre hospitalier universitaire, avenue de la Côte-de-Nacre, 14000 Caen, France.
E-mail address: marion-y@chu-caen.fr (Y. Marion).

http://dx.doi.org/10.1016/j.jviscsurg.2014.03.008
1878-7886/© 2014 Elsevier Masson SAS. All rights reserved.

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Introduction
Lower gastrointestinal (LGI) bleeding is defined as bleeding
whose origin is located downstream of the duodeno-jejunal
junction at the ligament of Treitz, thus including the small
intestine, colon, rectum or anus. Clinical manifestations are
melena or hematochezia. We speak of obscure LGI bleed-
ing when one or more episodes of bleeding occur for which
no site of origin is identified by standard endoscopy, and
of occult gastrointestinal bleeding when no gross blood is
observed by the patient or clinician yet there is evidence
of bleeding manifested by iron-deficiency anemia with no
identified extra-intestinal source of blood loss.
In recent years, diagnostic and treatment modalities
have developed considerably for use by gastroenterologists,
radiologists and surgeons. However, the main problem of LGI
bleeding remains the identification of the source rather than
the treatment of bleeding.
General
Epidemiology
LGI bleeding represents 20% to 25% of all gastrointestinal
bleedings [1]. Epidemiological studies are rare. North Amer-
ican studies have estimated the annual incidence in adults
at 21—27 per 100,000 population [2,3]. LGI bleeding occurs
more frequently in men than in women (24.2% vs. 17.2%,
P < 0.001) and more often in the elderly than in young sub-
jects (∼200-fold increase in the 9th decade compared to
the 3rd decade of life) [3]. This increased incidence is
explained by the increasing prevalence of diverticulosis and
angiodysplasia with age [2]. The mortality of LGI bleeding is
estimated at 2—4% in various series [2,4].
A prospective epidemiological study carried out in France
in 2007 by the National Association of General Hospital Gas-
troenterologists identified 1333 patients with LGI bleeding.
The mean age was 72 ± 16 years; ASA (American Society of
Anesthesiologists) score was 2.5 ± 0.9 and 50% of patients
had an ASA of 3. Use of a predisposing medication was found
in nearly 75% of patients (34% antiplatelet agents, 22% anti-
vitamin K agents, 11% non-steroid anti-inflammatory drugs
[NSAID], 7% heparin) [5].
Etiologies
In specifying the frequent and problematic causes, the
prevalence of various etiologies is purely illustrative given
the great variability of results in the literature [1,6—8].
Moreover, despite all diagnostic testing, the source of bleed-
ing cannot be identified in approximately 10% of patients
[9].
Colorectal lesions
Between 60 and 80% of LGI bleeding originates in the colon
and rectum [1,6,7,9,10].
Diverticular bleeding
Diverticular bleeding, which accounts for 20—50% of LGI
bleeding, occurs due to erosion of small arteries in the wall
of the diverticulum [2,5]. Diverticular bleeding stops spon-
taneously with conservative medical treatment in 85% of
cases. The incidence of re-bleeding is low, less than 15%
after an initial episode, but as high as 50% after a second
episode. In recent years, the location of the bleeding diver-
ticulum is more commonly described in the sigmoid and
descending colon in contrast to earlier descriptions impli-
cating the right colon [11].
Angiodysplasia
Angiodysplasia consists of single or multiple abnormalities
in the gastrointestinal wall consisting of vascular ectasia of
the mucosal capillaries communicating with dilated and tor-
tuous submucosal veins. The typical endoscopic appearance
is a 2—5 mm flat bright red lesion with regular contours and
a round or stellate shape. They are located mainly in the
right colon and cecum (80%) but may also affect the small
intestine (15%) or stomach. The pathophysiology of their
formation is poorly understood at present [12].
They are responsible for 3—10% of cases of LGI bleeding
in various series [1,12], but account for 50—60% of bleeding
of small bowel origin, especially among the elderly [13].
Bleeding stops spontaneously in approximately 90% of cases,
but the risk of re-bleeding is high: 26% at 1 year and 45% at
3 years in the series of Richter et al. and Junquera et al.
[14,15].

Severity criteria Ischemic colitis

The gravity of LGI bleeding is generally less severe than that
of UGI bleeding; hemorrhage ceases spontaneously in 80%
of cases [6]. Currently, there is no consensus definition of
the severity of LGI bleeding. Severity is assessed according
to its hemodynamic consequences, laboratory findings and
underlying patient condition [2,6]:
• systolic blood pressure <100 mmHg;
• pulse >100/min;
• hemoglobin <10 g/dL;
• need for more than six units of red blood cell transfusion
to restore satisfactory hemodynamics;
• co-morbidities and associated use of anticoagulants.
The assessment of severity is very important because it
is a determining factor in the plan of management.
Ischemic colitis includes all secondary erosive lesions due to
arterial or venous hypoxia of the wall of the colon and/or
rectum, whether acute or chronic. It accounts for 3—9% of
LGI bleeding [1].
Inflammatory colitis
This designation encompasses chronic inflammatory bowel
disease (IBD) (6—30% of LGI bleeding), infectious colitis, and
non-specific inflammatory colitis.
Other colonic etiologies
These include polyps and colorectal cancers, iatrogenic
causes (post-polypectomy), radiation proctitis and colitis,
colonic endometriosis, colorectal varices, among others.

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The management of lower gastrointestinal bleeding
Small intestinal lesions
Bleeding from the small intestine represents 2—9% of LGI
bleeding, but is the source of 45—75% of obscure LGI bleed-
ing [16].
Angiodysplasia
Angiodysplasia accounts for 50—60% of small intestinal
bleeding, especially in the elderly [13].
Meckel’s diverticulum
Meckel’s diverticulum is the most common congenital mal-
formation of the digestive tract (incidence 2—4%) [17]. This
embryonic remnant results from partial persistence of the
vitelline duct. Its presence is usually asymptomatic but is
associated with complications in 4—16% of cases [17]. Bleed-
ing is related to the presence of ectopic gastric mucosa
whose acid secretion causes ulceration and bleeding of the
adjacent small intestinal mucosa. This complication is par-
ticularly common in children, and progressively decreases
with age.
Other small intestinal etiologies
A non-exhaustive listing includes: small bowel tumor (mainly
stromal tumors), mesenteric arterial or venous infarction,
inflammatory enteritis (Crohn’s), infectious enteritis, and
radiation enteritis.
In patients under 50 years of age with LGI bleeding of
small bowel origin, the most common causes are Crohn’s
disease, Meckel’s diverticulum and small bowel tumors [18].
Anal lesions
Anal lesions account for 4—10% of LGI bleeding. Diagno-
sis requires careful clinical examination using an anoscope.
Internal hemorrhoids are the most common cause, but this
remains a diagnosis of exclusion until other lesions are ruled
out.
Other causes include anal cancers, fissures, perineal
manifestations of Crohn’s disease, and traumatic ulceration
(i.e., thermometers).
Gastroenterologic diagnosis and treatment
Upper esophago-gastro-duodenal endoscopy
Heavy UGI bleeding can present as frank rectal bleeding in
11% of cases; this requires that upper GI endoscopy be per-
formed to rule out an upper GI source of digestive bleeding
[6].
Recommendations: upper GI endoscopy is recommended
as the first examination for any gastrointestinal bleeding.
Colonoscopy
Colonoscopy plays an indispensable role in the management
of LGI bleeding due to the frequency of bleeding from colo-
rectal sites; it has the major potential advantage of playing
both diagnostic and therapeutic roles, even when bleeding is
not actively ongoing. However, the feasibility of emergency
colonoscopy, the optimal time interval before performance,
the need for bowel preparation, and the criteria for judg-
ing whether certain lesions are the source of bleeding have
been the subject of controversy.
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3
Diagnostic colonoscopy
The main problem is to establish that a visualized lesion
is actually the cause of bleeding: validating signs are the
visualization of active bleeding, of a blood clot overlying a
visible vessel or of a clot adherent to a diverticular ulcer-
ation or the neck of a diverticulum. Such lesions are also
associated with a risk of adverse prognosis and recurrent
bleeding [19,20]. The mere presence of blood in a given
colonic segment offers little informative value as to the
exact site of bleeding due to increased peristalsis associated
with LGI bleeding.
The diagnostic yield of emergency colonoscopy for LGI
bleeding is highly variable in the literature, ranging from
48—100% [6], but it approaches 74—100% in more recent
studies [21]. Optimal timing remains controversial but early
colonoscopy seems to increase the diagnostic and therapeu-
tic efficiency. Green et al. have shown that colonoscopy
within the first 12 hours allowed visualization of active
bleeding in 42% versus 22% at 72 h [22]. Jensen [19] also
showed that early endoscopy combined with endoscopic
therapy significantly reduced the risk of recurrence and the
need for surgery versus a control group, and allowed a signif-
icant reduction in the duration of hospitalization. However,
a more recent study by Laine et al. showed no significant
difference, probably due to lack of power [23].
Another controversy is the value of a bowel preparation.
The recommendations of the HAS (Haute Autorité de santé),
the AGA (American Gastroenterological Association) and
the ASGE (American Society for Gastrointestinal Endoscopy)
[10,24,25] favor oral bowel preparation whenever possible,
in order to improve visualization of small mucosal lesions
and to lessen the risk of endoscopic bowel injury. Three to
six liters of polyethylene glycol (PEG) should be ingested by
mouth over 4—6 hours, or instilled via a naso-gastric tube if
necessary, in association with enemas [25]. Colonic prepa-
ration reduces the risk of intestinal perforation due to poor
visibility and it also increases the likelihood of a complete
colonoscopy. Indeed, without bowel preparation, the cecum
is visualized in only 55—70% of cases [21]. After bowel prepa-
ration, Strate et al. obtained a definitive diagnosis in 91% of
cases [26]. However, conflicting results emerge from some
series, as Chaudry et al. [27] reported a 97% diagnostic yield
for emergency colonoscopy, even in the absence of oral
bowel preparation.
In the emergency setting, colonoscopy is still considered
a relatively safe procedure whose major complication is
colonic perforation. The literature review by Strate et al. of
four studies including 664 patients showed a 0.6% perfora-
tion rate for emergency colonoscopy versus 0.3% for elective
colonoscopy [26].
Therapeutic colonoscopy
Once a diagnosis has been established, a hemostatic proce-
dure can be performed colonoscopically in 8—37% of cases
[21]. The techniques of hemostasis vary depending on the
bleeding lesion. Significant technical progress in endoscopic
hemostasis has been achieved in the last decade, partic-
ularly for immediate or delayed iatrogenic bleeding after
polypectomy or endoscopic mucosal resection, as well as for
a wide range of colorectal lesions such as bleeding divertic-
ula, angiodysplasia and post-radiation telangiectasia.
For diverticular hemorrhage, hemostatic modali-
ties include monopolar or bipolar electrocoagulation,
argon plasma coagulation (APC), submucosal injection of
epinephrine solution (SIES), occlusion of a visible vessel by
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hemostatic clips, or a combination of these techniques.
There are currently no recommendations in favor of one or
the other technique, but if SIES is selected, it should be
recognized that this treatment has only temporary effect,
and must be combined with clip occlusion or electrocoagu-
lation [6]. Bloomfeld’s report concerning thirteen patients
showed a 38% early recurrence rate within one month after
treatment with SIES with electrocoagulation and a 23%
late recurrence rate [28]. In a series reported by Jensen,
patients who were treated by SIES and electrocoagulation
had no observed recurrence compared with a 53% incidence
of recurrent bleeding for patients who did not undergo
endoscopic therapy [19].
For angiodysplasia, first-line treatment is based on APC
and bipolar electrocoagulation according to a recent review
[12], because these techniques allow a very superficial coag-
ulation with a low rate of perforation (<0.5%). The risk of
recurrence is estimated at 7—15%. No significant difference
could be shown in comparisons of the two techniques.
Recommendations: after upper endoscopy, colonoscopy
is the next essential examination for any LGI hemorrhage.
In addition to its diagnostic capability, it offers the advan-
tage of therapeutic intervention, even when bleeding is no
longer active. Preferably it should be preceded by colonic
preparation and performed as early as possible.
Video capsule endoscopy (VCE)
VCE is performed by swallowing a small encapsulated device
(11 × 26 mm, including a battery power source, a camera
for capturing images, a light source, and a radio transmitter
for transmitting images to a receiver worn on a belt by the
patient); images obtained as the capsule transits the small
intestine that can then be analyzed by computer.
Two meta-analyses and thirteen studies [29] showed
VCE to have a diagnostic sensitivity (Se) of 88—100% when
upper and lower endoscopy failed to provide a diagnosis,
with a negative predictive value (NPV) of 86—100%, and a
specificity (Sp) of 48—97%. The diagnostic yield of VCE is
estimated at between 38 and 93% [30]. This wide variabil-
ity of results is partly explained by marked improvement of
performance if the procedure is performed within 15 days
of bleeding (91% vs. 34%). Jones et al. have even suggested
that after an initial inconclusive VCE examination, repeti-
tion of VCE allowed localization of bleeding in 75% of cases
[31]. Current recommendations suggest that a second VCE
may be proposed after diagnostic failure of the initial study
[24,29].
For obscure LGI bleeding, significant predictors of a pos-
itive VCE study were: age >60 years, previous episodes of
bleeding, the number of transfusions required, inflammatory
bowel disease and repetition of a VCE study [32,33].
The feasibility of VCE was also evaluated in the
emergency setting for patients with initial hemodynamic
instability and/or need for transfusion; VCE was completed
within 48 hours after a negative endoscopic assessment. VCE
allowed the localization and identification of bleeding in
67% of cases and allowed endoscopic, surgical or radiological
treatment focused on the site of bleeding [34].
VCE is a non-invasive examination that is very useful for
diagnosis but without associated therapeutic possibilities.
One limitation of VCE is the failure to visualize the cecum
in 15% of cases, because the battery runs out of power too
soon [35]; the main complication is capsular retention in
1—2% of cases; while this requires enteroscopy or surgery
to correct, therapy at the identified bleeding site can
Please cite this article in press as: Marion Y, et al. The management of lower gastrointestinal bleeding. Journal of Visceral
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simultaneously be performed at this intervention [35]. If
intestinal stricture is suspected that might prevent capsule
migration, an absorbable test capsule test has been devel-
oped. Thirty hours after oral ingestion, passage of the device
is confirmed by CT; if it passes successfully, VCE can then be
performed [36].
Recommendations: the use of VCE has grown considerably
in recent years and it has become the examination of choice
if no source of bleeding is found on initial upper and lower
endoscopic assessment for LGI bleeding [1,24].
Push enteroscopy
Push enteroscopy using a pediatric colonoscope or an
enteroscope extends the reach of upper endoscopy for
another 15—160 cm beyond the ligament of Treitz.
This technique was initially developed to explore the
small intestine when gastro-duodenoscopy and colonoscopy
revealed no bleeding site; it has become obsolete since the
advent of the VCE and assisted enteroscopy. A meta-analysis
showed that the diagnostic yield of enteroscopy was 26%,
significantly lower than the 56% yield of VCE [37].
Assisted enteroscopy (AE)
AE is a new endoscopic technique developed since 2001,
initially with double balloon enteroscopy (DBE), then sin-
gle balloon enteroscopy (SBE) and most recently by spiral
enteroscopy. No significant difference has been shown
between the results of the three modalities and most stud-
ies focus on DBE [8]. This technique permits exploration of
the entire small intestine by an oral and/or anal approach
and also allows biopsies and therapeutic hemostasis.
AE and VCE have a similar diagnostic yield; the most
recent meta-analysis of 397 patients showed a diagnostic
yield of 57% and 60% respectively [8]. The two major advan-
tages of AE are that it permits biopsies or application of
hemostatic modalities; these were performed in approxi-
mately 27% of cases.
Its main limitation remains incomplete exploration in 71%
of cases. Other limitations include limited availability, the
need for anesthesia, and prolonged duration of the exami-
nation.
This is a safe technique with less than 1% incidence of
complications (gastrointestinal perforation [0.4%], pancre-
atitis [0.3%], and ileus) [8].
Recommendations: at present, the technique of AE has
not replaced VCE but constitutes a complementary tech-
nique, for second intention use; the best indication is for
treatment of small intestinal lesions identified by VCE [29].
Radiologic diagnosis and treatment
Diagnostic and interventional radiologic management has
evolved considerably over the last fifteen years due to
technological improvements, better diagnostic performance
of CT, and the therapeutic techniques of endo-arterial
embolization. At present, the bleeding scan using scintig-
raphy with radio-labeled RBC’s no longer plays a role in the
diagnosis of most cases of LGI bleeding.
CT angiography (CTA)
New techniques of rapid image acquisition coupled with the
high-speed injection of iodinated contrast (3—4 mL/sec) and
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The management of lower gastrointestinal bleeding
the increasing availability of this imaging technique now
allow access to rapid and effective CTA for management
of LGI bleeding. Performance of this examination consists
of three acquisition phases: a pre-contrast phase, an arte-
rial injection phase and a bowel wall enhancement phase
at 80—90 seconds after injection. The use of oral contrast is
not recommended. Detection of contrast extravasation will
help clarify the anatomic site of bleeding, helping to guide
the endoscopist or surgeon and/or specifically identify the
artery supplying this site for possible embolization. Bleeding
is characterized by spontaneous intra-luminal hyperintensity
or endo-digestive extravasation of iodinated contrast; this
can be visualized if the rate of bleeding exceeds 0.3 mL/min
[38].
In recent years, with the development of rapid acqui-
sition spiral CT scanners that can produce 16 to 64 slices
per second, several teams have investigated the role of CTA
in the management of LGI bleeding [39—41]. Initial stud-
ies have reported a diagnostic efficacy of 54—79% for the
localization of bleeding [39], 96% specificity, a positive pre-
dictive value of 95% and a negative predictive value of 100%
for patients with active bleeding [42]. Other advantages of
CTA are its ability to demonstrate enhancement anomalies
of the bowel wall and mesenteric fat, as well as anatomical
abnormalities such as tumors and diverticula.
CTA’s limitation lies in its decreased ability to detect the
source of GI bleeding if bleeding is not actively ongoing.
The sensitivity of CTA for detection of active bleeding is
91—92% versus only 45—47% for occult bleeding [43]. CTA is
indicated in the acute hemorrhagic period, if the patient’s
hemodynamic status permits.
Recommendations: for active bleeding, CTA is the exam-
ination of choice after endoscopies because of its high
diagnostic yield, its availability in most centers, and the
fact that it can be performed quickly after completion
of endoscopy, thus serving as a guide for interventional
colonoscopy, embolization or surgery. However, CTA has no
role in the management of chronic, obscure or occult bleed-
ing.
Arteriography
With the advent of multidetector CT angiography, arteriog-
raphy no longer plays a diagnostic role in the assessment of
GI bleeding after failure of endoscopic maneuvers; its use is
now reserved for therapeutic indications.
Arteriography can explore the celiac trunk, mesenteric
arteries and internal iliac arteries with selective cannula-
tion of their side branches. The main diagnostic criterion
is extravasation of iodinated contrast media into the diges-
tive lumen (flow rate > 0.5 mL/min) [21]; this identifies the
source of bleeding with certainty. Like CTA, the diagnostic
efficacy of arteriography is high if it is performed during
a period of active bleeding; its sensitivity for detection of
the bleeding site ranges from 40 to 86% in literature reports
[44] with a specificity of 100% [2]. Factors favoring success-
ful detection of a bleeding site by arteriography include:
hemodynamic instability, a 50% drop in hemoglobin, and
transfusion of >5 units of packed RBCs in 24 hours; however,
arteriography is not without complications; the incidence
is estimated at 9.3% (arterial puncture site complications,
contrast-related renal failure, etc.) [45].
If the arteriography is negative, some authors have
proposed the injection of heparin, vasodilators and throm-
bolytic agents in situ to increase the diagnostic yield of
angiography. In a retrospective study of 36 patients with
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5
recurrent LGI bleeding (after diagnostic failure of angiog-
raphy in 24 cases), this procedure allowed detection of
the bleeding site in eleven patients (31%) with no reported
complications [46]. These results seem surprising in terms
of morbidity and make these provocative techniques to
increase the sensitivity of arteriography controversial.
Arteriography also provides a route for therapeutic
embolization. Improvements in catheterization materiel
(miniaturization) and embolic agents (mechanical agents
such as coils, microparticles, and gelatin foam) allow a very
safe distal embolization. Intestinal ischemic complications
occur but are usually minimal and often self-limiting [42].
In a literature review that included 144 patients, the rate of
asymptomatic ischemia was 9% [9]. The hemostatic success
rate of arterial embolization varies between 44 and 91% [2]
recurrent bleeding in 14% [44]; in such cases, the patient
can undergo a second embolization procedure.
In addition, venous bleeding (bleeding gastrointestinal
varices complicating portal hypertension) can also bene-
fit from interventional radiology including the performance
of transhepatic portosystemic shunt (TIPS) combined with
selective venous embolization [47].
Recommendations: arteriography is indicated for ther-
apeutic purposes in LGI bleeding, after localization of an
active bleeding site by CTA and failure or inability to treat
the lesion endoscopically. Provocative injection of hep-
arin or other agents is controversial and requires further
study.
Bleeding scan: scintigraphy with radio-labeled
red blood cells
This method is sensitive provided that the bleeding rate is at
least 0.1 mL/min. It is more sensitive but less specific than
colonoscopy or angiography [2]. Like the other techniques,
it identifies active bleeding but has the advantage of being
able to locate a bleeding site as long as 24 hours after injec-
tion [44]. Its disadvantage is that the location of bleeding to
an area of overlapping bowel loops can fail to distinguish a
long sigmoid colon loop from the right colon [6]. The diag-
nostic yield of scintigraphy is highly variable in the literature
ranging from 41 to 94% [44] with an equally variable rate of
correct localization of 24—91% in various series [2]. Local-
ization is most accurate when bleeding is identified in early
images. Indeed, if the scan is positive at two hours, the loca-
tion accuracy is 95-100%; this falls to 57—67% if bleeding is
identified on images beyond two hours [6].
In some centers, particularly in the English-speaking
world, scintigraphy is performed as an initial test before
arteriography. It helps determine which patients will profit
from arteriography and allows the radiologist to focus on
the region of scintigraphy-detected bleeding with selective
angiography. In fact, initial scintigraphy increases the diag-
nostic yield of arteriography by a factor of 2.4 and probably
avoids performance of a non-contributory angiography if the
scintigraphy is negative [2].
Scintigraphy with technetium labeled (99mTc) RBC’s
retains its indication for young patients in whom Meckel’s
diverticulum may be responsible for LGI bleeding [36].
Recommendations: while still widely used in Anglo-Saxon
countries, scintigraphy is not available in many centers, par-
ticularly for emergency use, and it requires more acquisition
time than CTA, leading to a preference for the latter. If
scintigraphy is available, it remains indicated in the young
patient for detection of Meckel’s diverticulum.
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CT enterography and MRI enterography [48]
CT enterography requires placement of a naso-jejunal tube
under fluoroscopic control; the tip should be positioned
beyond the duodeno-jejunal junction at the ligament of Tre-
itz. Enteroclysis is then performed injecting a continuous
flow of oral contrast agent (Barium diluted with mannitol,
PEG, or water); CT images are obtained with concomitant
injection of intravenous contrast. MRI enterography also
uses an oral contrast agent directly ingested by mouth along
with intravenous injection of gadolinium contrast.
The purpose of these two studies is to obtain an optimal
and sustained distension of the small intestine in order to
analyze its wall effectively throughout the duration of image
acquisition. MRI enterography has the advantage of avoiding
radiation exposure.
These are the two best radiological tests for diagnosis
of small intestinal transmural and extramural pathologies
the small bowel follow-through examination has become
obsolete [48]. These tests are commonly used in Crohn’s
disease to detect and assess areas of inflammatory activity
and to evaluate strictures and fistulae [49]. They are also
very effective for assessment of transmural and extramural
pathologies particularly small tumors [36].
For LGI bleeding, recent studies CT enterography, have
shown it to be effective in detecting causes of obscure LGI
bleeding [36]. However, Heo et al. have performed VCE after
negative CT enterography and have successfully identified
a lesion in 57% of patients. Agrawal et al. proposed the
inverse approach, i.e., performing CT enterography when
VCE was negative; in such cases, CT enterography revealed
no lesions [50]. Indeed, the main limitation of these tests is
their poor ability to explore the superficial mucosa, unlike
current endoscopic techniques (VCE or DBE). Angiodyspla-
sia or ulcerations are difficult to detect, yet they remain
the main causes of small intestinal bleeding in the elderly.
However, when luminal occlusion or risk factors for stricture
(Crohn’s disease, long-term NSAID use) are present, CT and
MRI enterography are preferable to VCE in order to avoid
bowel obstruction during the passage of the capsule.
Recommendations: CT or MRI enterography is indicated
for cases of obscure LGI bleeding, as long as there is reason
to suspect bowel obstruction or stricture.
Therapeutic surgical exploration
In most large centers, surgical consultation occurs second-
arily after initial management by the gastroenterologist
and/or intensivist, when it becomes evident that his opinion
or skills are required. Surgical consultation is requested if:
• bleeding is localized and surgery is necessary because of
the inability or failure of an endoscopic or radiological
treatment;
• bleeding is not localized, to discuss what surgical explo-
rations are possible;
• in emergency when faced with severe acute hemorrhage.
Localized bleeding
If preoperative investigations by the gastroenterologist
and/or radiologist have identified the bleeding site or if
endoscopic therapy and/or radiologically-guided therapy is
not feasible or has failed, a radical surgical procedure may
be necessary. The specific surgical procedure depends on the
Please cite this article in press as: Marion Y, et al. The management of lower gastrointestinal bleeding. Journal of Visceral
Surgery (2014), http://dx.doi.org/10.1016/j.jviscsurg.2014.03.008
site and the etiology of bleeding. The list of operations is as
varied as are the various causes of bleeding, including:
• for diverticular hemorrhage, segmental colonic resection
is the rule [11,25]: right hemicolectomy if bleeding is
identified on the right, left colectomy if the bleeding site
is localized on the left, but there is no role for subtotal
colectomy in this situation;
• for angiodysplasia, segmental resection of the offend-
ing digestive segment is performed [12], and similarly,
in the case of Meckel’s diverticulum where resec-
tion/anastomosis is performed [17];
• for adenocarcinoma of the small intestine, wide onco-
logic resection with distal and proximal margins of at least
5 cm is recommended combined with en bloc mesenteric
resection for loco-regional lymph node dissection [51].
Recommendations: the main indications for surgery for
LGI bleeding are: localized bleeding with failure or inability
to achieve hemostasis via endoscopic or radiologic interven-
tion, or the need for curative resection (tumor of the small
intestine or colon).
Unlocalized bleeding
The role of surgery in the control of LGI bleeding from an
unknown site raises many questions.
The role of exploratory laparotomy
With the development of diagnostic and therapeutic tech-
niques by the gastroenterologist and the radiologist, there
is currently little or no role for exploratory laparotomy.
If all investigations are non-diagnostic, one should
temporize, stabilizing the patient hemodynamically by
effective medical treatment, correcting coagulation disor-
ders, reviewing all the diagnostic tests and repeating them if
necessary. A first colonoscopy may be negative due to perfor-
mance under poor conditions such as poor bowel preparation
or due to spontaneous cessation of bleeding. Medical obser-
vation in the hospital is appropriate and is often useful,
permitting prompt repeat colonoscopy and/or CT angiogra-
phy; as stated above, these tests are more sensitive if they
are performed during active hemorrhage.
Recommendations: exploratory laparotomy should not be
performed for LGI bleeding.
Technique and indications for intra-operative
enteroscopy (IOE)
IOE is most commonly performed during laparotomy
although its use in conjunction with laparoscopy has been
reported [16]. IOE is performed by introduction of the
endoscope orally or trans-anally or by introduction of the
scope through an enterotomy under surgical guidance, or
by some combination of these techniques. Natural orifice
enteroscopy is less invasive but requires more time, and it
results in small intestinal and colonic distention that may
interfere with abdominal closure; IOE via enterotomy is fre-
quently incomplete [8]. Once the bleeding site is identified,
treatment tailored to specific findings is performed.
Literature reports have only small numbers and therefore
show a great variability in results. IOE achieves complete
visualization in 57—100%, with a diagnostic yield of 79% and
therapeutic yield of 76% [16]. Previous identification of a
lesion by VCE improves the contribution of IOE; when VCE
was positive, 87% of lesions were identified versus 0% if VCE
was negative [16]. These results show the important role of
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The management of lower gastrointestinal bleeding
IOE when a lesion has been identified before the procedure.
Morbidity is 17%, predominantly post-procedure ileus; IOE
has a significant mortality of 5%, mainly due to multi-organ
failure with sepsis after recurrent bleeding [16].
IOE has long been considered the gold standard for
cases of obscure LGI bleeding because it was the only
examination that allowed complete endoscopy of the small
intestine. With the development of minimally invasive endo-
scopic techniques (VCE and AE) and radiologic ‘‘virtual
endoscopy’’, the small intestine can now be fully explored
without surgery and IOE is no longer indicated for purely
diagnostic purposes.
However, it remains useful and appropriate for intra-
operative identification of small intestinal bleeding sites
that are not accessible to standard endoscopic or
radiology-guided treatment or if they cannot be localized
intra-operatively without IOE because of the absence of an
externally visible lesion or if preoperative tattooing was not
performed.
Recommendations: IOE for purely diagnostic purposes
has been supplanted by VCE and AE. IOE is useful for
intra-operative identification during a surgical procedure if
specific preoperative marking has not been performed.
Severe acute hemorrhage
Indications and results of emergency surgery
It must be re-emphasized that 80% of LGI bleeding episodes
stop spontaneously [6]. In addition, the population of
patients who develop LGI bleeding are generally at increased
risk for surgical intervention (advanced age, high ASA
score, associated use of anticoagulant or antiplatelet med-
ications). The mortality rate associated with emergency
surgery is nearly 10% [2]. However, in a series of 215 patients
operated under these conditions, Gayer et al. showed that
mortality was lower if bleeding had been localized pre-
operatively thereby allowing elective surgery specifically
adapted to the etiology; here, the mortality was 3.3% versus
9.4% for bleeding that could not be localized preoperatively
[7]. These results underline the importance of preoperative
investigations to locate the site of bleeding.
Most cases of LGI bleeding, even when severe or recur-
rent, do not require surgery and can be controlled with
medical treatment or by endoscopic or radiology-guided
therapy. However, in exceptional cases, emergency surgery
may be necessary. According to the review by Farell et al.,
emergency surgery is indicated in the following four situa-
tions [2]:
• hemodynamic instability that persists despite optimal
resuscitation;
• persistent hemorrhage (requiring more than 6 units of
RBC transfusion) and inability to define the bleeding site
despite colonoscopy, push enteroscopy and CTA;
• active bleeding from a segmental intestinal lesion that is
amenable to surgical hemostasis;
• the patient who is in good general condition and who can
undergo surgery without unacceptable morbidity and with
reasonable life expectancy.
In this report, emergency surgery was performed in 18 to
25% of patients with LGI bleeding that required transfusion.
(Grade B) [2].
Recommendation: preoperative localization of the bleed-
ing site is essential. Emergency exploratory laparotomy and
salvage surgery have a high mortality and is rarely contrib-
utory.
Please cite this article in press as: Marion Y, et al. The management of lower gastrointestinal bleeding. Journal of Visceral
Surgery (2014), http://dx.doi.org/10.1016/j.jviscsurg.2014.03.008
7
If emergency salvage surgery without preoperative
localization is performed, what should the actual
procedure consist of?
Fortunately, this situation is exceptional; only an empirical
treatment approach can be proposed:
• with the patient positioned for either an abdominal or
perineal approach, the first step is a proctology exam to
eliminate a low rectal or anal cause (4—10% of LGI bleed-
ing). An anoscope and Parks retractors are necessary for
adequate visualization;
• midline laparotomy. There are no data in the literature to
assess the role of laparoscopy in this context. A careful
inspection and palpation of the entire GI tract down-
stream from the Treitz ligament should be performed.
The absence of blood in the small intestine confirms a
colorectal source, but its presence does not eliminate the
possibility of backflow of blood through an incompetent
ileocecal valve;
• upper endoscopy and colonoscopy should be repeated
intra-operatively: to increase the sensitivity of
colonoscopy, the surgeon can perform intra-operative
colonic lavage [9,21] and assist the endoscopist by
guiding the endoscope past tortuous curves. It should be
remembered that the cecum is visualized in only 55—70%
of emergency colonoscopies [21];
• if the source of bleeding is identified, appropriate surgery
is performed;
• finally, if despite all explorations, the bleeding cannot be
localized surgical management should be similar to that
for diverticular bleeding [25].
If the small intestine is cleared and if colonic diver-
ticula are present, data from the literature show that, in
the absence of a precise localization of the site of bleed-
ing, ‘‘blind’’ subtotal colectomy is the best treatment for
bleeding of colonic origin. However, this approach carries a
high mortality between 10% and 33% with a re-bleeding rate
between 0 and 8%. But these results are much better than for
segmental colectomy, which has a mortality rate between
20 and 57% and a rate of recurrent bleeding between 30 and
63% [25,52—54].
If there is blood in the small intestine but the remainder
of the examination is normal, two different situations may
be responsible:
• in an elderly patient with colonic diverticula, blood may
have refluxed backward from the colon. In view of the
epidemiology, a diverticular origin of bleeding is probable
and a subtotal colectomy is justified;
• the patient is young and/or there are no diverticula, no
specific resection can be recommended.
Recommendations: prior to embarking upon salvage
surgery, diagnostic tests should be repeated in the operating
room. If no specific bleeding site is identified but bleeding of
diverticular origin is probable, a subtotal colectomy should
be performed rather than a ‘‘blind’’ segmental colectomy.
Management of LGI bleeding in practice
Practical management of LGI bleeding depends on the sever-
ity of the hemorrhage and the availability of diagnostic and
therapeutic methods at the admitting facility. Endoscopic
and radiological techniques have improved to the point that
the site of bleeding can be localized in the majority of cases.
In addition, episodes of LGI bleeding are less serious than
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8 Y. Marion et al.

UGI bleeding with an 80% rate of spontaneous cessation of
bleeding and a lower mortality of 2—4% [2] versus 6—13%
[55]. It is therefore appropriate to stabilize the patient
hemodynamically for transfer to a larger center if expertise
in non-invasive diagnostic and therapeutic interventions is
not available locally. Similarly, if the bleeding has stopped
spontaneously and all investigations are non-contributory,
supportive medical management can be continued with rep-
etition of examinations if bleeding recurs.
While there is no clear consensus for management as
there is for UGI bleeding, the following course of man-
agement can be proposed based on an overview of all the
diagnostic and therapeutic modalities and in accordance
with the recommendations of the SFED (French Society of
Digestive Endoscopy), AGA and ASGE [1,10,24].
Acute lower gastrointestinal bleeding
As for any other source of bleeding, initial medical manage-
ment is of fundamental importance, including stabilization
of the patient’s hemodynamic condition, transfusion if nec-
essary, and correction of coagulation disorders to enable the
performance of necessary diagnostic explorations under safe
conditions (Fig. 1). Detailed history and physical examina-
tion including a rectal exam should be performed.
All patients with LGI bleeding should undergo initial
upper endoscopy and urgent colonoscopy after bowel prepa-
ration. If there is active ongoing bleeding, angiography also
seems indicated as an initial investigation. Currently, CTA
has many advantages: it is available in most centers, can
be performed quickly with a satisfactory diagnostic yield
when there is active bleeding, and helps to guide a ther-
apeutic colonoscopy or embolization. At this stage, the site
of bleeding has been localized in most cases.
If diagnostic studies are negative, continued efforts
should be made to locate the bleeding site rather than
resorting to ‘‘blind’’ exploratory surgery, which has a high
mortality and is likely to be non-contributory. VCE has grad-
ually emerged as a second-line modality for visualizing the
small intestine, even in the emergency setting [34]. Upper
endoscopy and colonoscopy should be repeated. In young
patients, the diagnosis of Meckel’s diverticulum must be
considered as well as inflammatory bowel disease or a neo-
plasm. A CT or MRI enterography and/or bleeding scan using
Tc99 m scintigraphy should be discussed on a case-by-case
basis.
Once the bleeding site has been identified, treatment is
based on interventional endoscopy or radiological emboliza-
tion depending on the respective technical difficulties and
availability of these modalities at the treating facility. If all
else fails, elective surgery is performed.
Emergency salvage surgery without localization of the
bleeding site has become exceptionally rare and should be
avoided as much as possible. If, unfortunately, it proves to
be necessary, the surgery is then empirical depending on
operative findings. Based on the hypothesis that the most
common cause of LGI bleeding is diverticulosis, performance
of a subtotal colectomy may be appropriate.
Chronic lower and/or upper GI bleeding
without hemodynamic instability
Initial assessment is performed with upper endoscopy and
colonoscopy (Fig. 2). CTA is not indicated because of its low
yield when bleeding is not active and its lower sensitivity
compared to endoscopy for this indication. If the tests are
non-contributory, management should be the same as for
occult LGI bleeding.
VCE is the investigation of choice if endoscopic assess-
ment fails to localize a bleeding site. If there is concern
about intestinal stricture or obstruction, then VCE is contra-
indicated and a ‘‘virtual enteroscopy’’ by either CT or MRI

Figure 1. Management of acute lower GI bleeding. LGI = lower gastrointestinal; EGDScopy = esophago-gastro-duodenal endoscopy;
AE = assisted enteroscopy; VCE = video capsule endoscopy; eCT = CT enterography; eMRI = MRI enterography; Bleeding scan = 99mTc tech-
netium radio-labeled RBC scan.

Please cite this article in press as: Marion Y, et al. The management of lower gastrointestinal bleeding. Journal of Visceral
Surgery (2014), http://dx.doi.org/10.1016/j.jviscsurg.2014.03.008
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JVS-381; No. of Pages 11 ARTICLE IN PRESS
The management of lower gastrointestinal bleeding
Figure 2. Management of chronic LGI bleeding with no hemodynamic instability. LGI bleeding = lower gastrointestinal bleeding; Upper
endoscopy = esophago-gastro-duodenoscopy; AE = assisted enteroscopy; VCE = Video capsule enteroscopy; eCT = CT enteroscopy; eMRI = MRI
enteroscopy; Bleeding scan = Tc99 m radio-labelled RBC scan; IOE = intra-operative enteroscopy.
enterography is performed. In young patients, a bleeding
scan using 99mTc scintigraphy should be considered.
If all investigations are negative, upper endoscopy and
colonoscopy should be repeated.
If the source of bleeding still cannot be localized, treat-
ment should consist of supportive medical management with
repetition of all studies as appropriate.
Once a bleeding site has been identified, hemostatic
treatment by interventional colonoscopy or AE is performed.
If non-invasive approaches are not feasible or unsuccess-
ful, surgery focused on the identified site is then performed
with preoperative marking of the site during colonoscopy
or AE using clips or tattooing. If a small bowel bleeding
source is identified that cannot be marked preoperatively,
enteroscopy is performed intra-operatively.
Conclusions
There is no consensus regarding management of LGI bleed-
ing, but the primary goal in all cases is identification of
the bleeding site. In recent years, the development of
endoscopic and radiological techniques has allowed mini-
mally invasive exploration, which may allow subsequent or
simultaneous hemostatic therapy via colonoscopy or assisted
enteroscopy. If the bleeding is actively ongoing, emboliza-
tion will stop bleeding in most cases. In addition, surgery
still plays a role for bleeding from an identified site, or,
more rarely, in case of failure or inability to perform other
treatments.
In any event, the diversity and complexity of the manage-
ment of LGI bleeding require multidisciplinary consultation
for the most severe cases involving gastroenterologists,
radiologists, surgeons, and intensivists.
Please cite this article in press as: Marion Y, et al. The management of lower gastrointestinal bleeding. Journal of Visceral
Surgery (2014), http://dx.doi.org/10.1016/j.jviscsurg.2014.03.008
9
ESSENTIAL POINTS
The essential points are:
• lower gastrointestinal bleeding requires
multidisciplinary care involving intensivist,
radiologist, gastroenterologist and surgeon;
• the main objective is to localize the source of
bleeding;
• upper gastrointestinal endoscopy should
always be performed since bleeding from the
esophagus, stomach, or duodenum can present
as hematochezia when there is abundant UGI
bleeding;
• CT angiography (CTA) has gradually established its
role in the diagnosis of acute LGI hemorrhage in
patients with ongoing active bleeding due to its
timeliness and high diagnostic yield; this modality
has become increasingly available in most centers;
• intra-operative enteroscopy, formerly regarded as
the gold standard for occult LGI bleeding, has been
superseded by newer diagnostic techniques and
minimally invasive treatment techniques for small
intestinal bleeding: video capsule endoscopy,
enteral CT, enteral-magnetic resonance imaging
(MRI) and assisted enteroscopy;
• once the site of bleeding is located, most cases
of LGI bleeding can be treated by endoscopy or
interventional radiology. If such modalities fail
or are unavailable, elective surgical treatment is
recommended;
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10
• indications for urgent life-saving surgery has become
exceptional and should be avoided as much as
possible;
• the spontaneous cessation and the lesser gravity
of most cases of LGI bleeding (as opposed to UGI
bleeding) justifies patient transfer to a specialized
center after initial hemodynamic stabilization if the
site of bleeding cannot be localized and advanced
diagnostic techniques are not available at the first-
line hospital.
Disclosure of interest
The authors declare that they have no conflicts of interest
concerning this article.
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