Document 135226

SEMINAR
Seminar
Diverticular disease of the colon
Neil Stollman, Jeffrey B Raskin
Colonic diverticulosis refers to small outpouchings from the colonic lumen due to mucosal herniation through the
colonic wall at sites of vascular perforation. Abnormal colonic motility and inadequate intake of dietary fibre have been
implicated in its pathogenesis. This acquired abnormality is typically found in developed countries, and its prevalence
rises with age. Most patients affected will remain entirely asymptomatic; however, 10–20% of those affected can
manifest clinical syndromes, mainly diverticulitis and diverticular haemorrhage. As our elderly population grows, we
can anticipate a concomitant rise in the number of patients with diverticular disease. Here, we review the incidence,
pathophysiology, clinical presentation, and management of diverticular disease of the colon and its complications.
Diverticulosis of the colon is quite frequent in developed
countries and prevalence rises with age. Although up to twothirds of people older than age 80 years are affected, most
remain asymptomatic. The causes of colonic diverticula
include alterations in colonic wall resistance, disordered
colonic motility, and dietary deficiencies, especially fibre.
Clinical manifestations of this disorder range from nonspecific intermittent abdominal pain to potentially lifethreatening complications such as diverticulitis or
haemorrhage. CT scanning and colonoscopy are important
in diagnosis and management. Here, we review
epidemiology, causes, clinical presentation, and management of diverticular disease of the colon.
Epidemiology
Prevalence of colonic diverticulosis is difficult to measure
because most patients are asymptomatic. In early
(1920–1940) autopsy and barium enema series, rates of
2–10% were reported.1 Data show a substantial rise in
colonic diverticula within the past few decades. Prevalence
of diverticular disease increases with age, from less than 10%
in people younger than age 40 years to 50–66% in patients
older than age 80 years.1–3 No sex differences seem to exist.
Diverticulosis has been labelled a disease of western
civilisation because of its striking geographic variability. The
disorder is rare in rural Africa and Asia, with the highest
prevalence seen in the USA, Europe, and Australia.1 Within
a given country, the incidence of colonic diverticula can vary
in ethnic groups—eg, in Chinese inhabitants of Singapore,
incidence was reported to be 0·14 cases per million
population per year versus 5·41 cases in Europeans.4
Urbanisation within a country over time can also lead to a
rise in prevalence of diverticulosis. Follow-up in Singapore
has indicated colonic diverticulosis in 19%, an increase
Lancet 2004; 363: 631–39
See Personal account page 640
Division of Gastroenterology, San Francisco General Hospital, and
University of California San Francisco, San Francisco, CA, USA
(N Stollman MD); and Division of Gastroenterology, University of
Miami School of Medicine, Jackson Memorial Medical Center,
Miami, FL, USA (Prof J B Raskin MD)
Correspondence to: Dr Neil Stollman, Division of Gastroenterology,
San Francisco General Hospital, 1001 Potrero Avenue, Suite 3-D,
San Francisco, CA 94110, USA
(e-mail: [email protected])
THE LANCET • Vol 363 • February 21, 2004 • www.thelancet.com
attributed mainly to dietary changes.5 Results of series of
symptomatic diverticular disease in Africa have shown a
rising incidence in increasingly urbanised communities.6,7
Cases of complicated diverticulitis have risen 50% in
Finland in the past two decades, an increase attributed to an
ageing population and reduced fibre consumption.8
Although much of the epidemiological research mentioned
is simply descriptive, understanding and assessing these
noted trends could yield insight into pathogenesis of the
disorder and help to predict disease course and
complications.
Pathological anatomy
Colonic diverticula typically form in parallel rows between
the taeniae coli because of weakness of the muscle wall at
sites of penetration of the vasa recta supplying the mucosa.
In European and US populations, diverticula arise mainly in
the distal colon, with 90% of patients having sigmoid colon
involvement and only 15% having right-sided
diverticula.3,9–11 This finding is in contrast to that seen in
Asian populations, in which right-sided involvement is more
prominent.5,12
Diverticula vary from solitary findings to many hundreds.
They are typically 5–10 mm in diameter but can exceed
2 cm. An entity of giant colonic diverticula has been
described with sizes up to 25 cm. Most are single, located in
the sigmoid colon, and asymptomatic, but can present with
infection, obstruction, or perforation.13
Search strategy and selection criteria
Sources of information included: authors’ published work and
research; and original research, reviews, and practice
guidelines identified by computer database search—eg,
MEDLINE, LexisNexis, The Cochrane Library, and Science
Citation Index. Most recent publications were prioritised.
Search terms included: “diverticulosis”, “diverticulitis”,
“diverticular disease”, “diverticular hemorrhage”,
“gastrointestinal bleeding”, “diverticular abscess”,
“diverticular fistula”, “colonoscopy”, “endoscopy”,
“epidemiology”, “pathogenesis”, “motility”, “fiber”,
“computerized tomography”, “CT-scanning”, “surgery”,
“laparoscopic”, “ultrasound”, “ultrasonography”, “barium
enema”, “contrast enema”, “NSAID”, and “non-steroidal
anti-inflammatory”, with Boolean operators AND and OR.
Human and animal studies in the English language were
reviewed and manually crossreferenced.
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Mesentery
Artery
Diverticulum
Contraction
Contraction
Pressure
tracing
Figure 1: Segmentation of colon by contractions producing
little bladders
Modified from reference 24 with permission of the Royal College of
Surgeons of England, 1964.
Although diverticulosis is an acquired disorder, findings
of observational studies suggest that the disease pattern—
eg, right-sided, pancolonic—might be established early on
and then remain constant, rather than increasing over time
in number and extent. In sequential studies with barium
enema, no progression of disease has generally been noted
in most patients.14 In fact, two distinct forms of
diverticulosis might exist: one discernible by muscle
thickening, mainly in the left colon, and associated with
perforation and diverticulitis; the other due to a diffuse
connective tissue abnormality, resulting in pancolonic
diverticulosis and a propensity for bleeding.15 This
possibility could, in part, account for anatomic differences
described between European and US patients and those
from Asia.
Cause and pathogenesis
Colonic wall resistance
Early gross descriptions of diverticular colons typically
noted thickening of muscle wall and shortening of the
taeniae coli, with resultant concertina-like bunching of
haustral folds. Although muscle contraction is noted,
routine histology has not generally indicated muscle
hypertrophy. Findings of electron microscopic studies have
shown that diverticular colonic walls consist of structurally
normal muscle cells but elastin deposition is amplified by
more than 200% in muscle cells in the taenia coli compared
with those without diverticula.16 Elastin is laid down in a
contracted form, resulting in shortening of the taenia coli
and bunching of circular muscle. Age-related changes in
collagen composition could have a causal role in weakening
of wall resistance. An increase in type III collagen synthesis
has been described.17,18 Further, changes in collagen
crosslinking have been shown in animal and human
models.19,20 The importance of gut wall connective tissue is
underscored by early development of diverticula in patients
with connective tissue disorders such as Marfan’s and
Ehlers-Danlos syndromes.21
Disordered motility
In the 1960s, Arfwidsson22 did manometry on patients with
or without sigmoid diverticula and showed higher resting,
postprandial, and neostigmine-stimulated luminal pressures
in diverticular patients than in controls. Painter and
colleagues23,24 confirmed these findings in response to
neostigmine or morphine in individuals with sigmoid
diverticula
(intraluminal
hypertension)
and
did
simultaneous cineradiography. Painter suggested a theory of
segmentation in which contraction of the colon causes a
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series of discrete “little bladders” (figure 1). He proposed
that this segmentation had a physiological role in
delaying of transport and augmentation of water
reabsorption but could also generate excessively high
pressures within every bladder, favouring herniation.
This effect might be amplified by dietary fibre
deficiency.25 Subsequently, patients with symptomatic
diverticulosis have been shown to have higher motility
indices than either asymptomatic patients or healthy
controls.26 High right-sided pressures have also been
recorded in patients with right-colon diverticulosis,
suggesting that abnormal motility could also have a role
in
pathogenesis
of
proximal
diverticula.27
A
preponderance of excitatory cholinergic nerves and a
diminution of action of non-adrenergic, non-cholinergic
inhibitory nerves by nitric oxide have been noted in
diverticular colons compared with controls.28 These
findings suggest that an imbalance in usual excitatory and
inhibitory influences could favour enhanced tonicity.
Whether altered motility and intraluminal hypertension
are a cause of disease or symptoms, or an effect of same,
is uncertain.
Dietary fibre
The geographic variability of diverticular disease and
correlation with a western diet have long suggested a
dietary factor as fundamental in pathogenesis of the
disorder. Burkitt and Painter1 were the most eloquent
proponents of this theory, labelling diverticulosis a
deficiency disease that, like scurvy, could be avoided
with dietary changes. They recorded transit times and
stool weights from more than 1200 individuals in the
UK and rural Uganda.29 The UK patients, eating a low
fibre diet, had transit times of about 80 h and mean stool
weights of 110 g/day. By contrast, rural Ugandans,
eating very high fibre diets, had times of 34 h and
weights of more than 450 g/day. The longer transit time
and smaller stool volumes were thought to increase
intraluminal pressure, predisposing to diverticular
herniation. As reasonable as this hypothesis seems,
results of studies in western populations comparing
transit times and stool volumes in patients with and
without diverticular disease have failed to show
significant differences. Nonetheless, corroborative data
in animals do exist, most notably in rats fed diets of
various fibre content throughout their lifespan.30 45% of
rats on the lowest fibre diet developed diverticula
compared with only 9% of those fed the highest fibre
diet. Furthermore, in another animal model, high fibre
diets protected against collagen crosslinking and were
associated with reduced frequency of diverticulosis.19
Uncomplicated diverticulosis
Most patients, perhaps 75–80%, with anatomical
diverticulosis will remain asymptomatic throughout their
lifetime. Of the few who develop complications,
diverticulitis—and its difficulties such as abscesses,
fistulas, or obstruction—is the most usual manifestation,
followed by diverticular haemorrhage, both of which are
addressed below.
The asymptomatic patient
Asymptomatic diverticular disease is frequently an
incidental finding during assessment of a patient for
another reason, such as routine screening for colon
cancer. No treatment or follow-up needs to be offered to
this large population, most of whom will remain
asymptomatic, although findings of one study suggested a
possible prophylactic benefit of a high-fibre diet. In a
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prospective study of 51 529 US male health professionals
followed up for more than 4 years, 385 new cases of
symptomatic diverticular disease were identified.31 A
significant inverse association was recorded between
dietary fibre intake and risk of development of clinically
evident diverticular disease. Insoluble fibre from fruits
and vegetables was noted to be more protective than
cereal fibres.32 These results provide support for a recommendation that patients with asymptomatic diverticular
disease might benefit from increasing their fruit and
vegetable fibre intake, a stance endorsed by the American
Dietetic Association.33
The symptomatic patient
Patients can present with non-specific abdominal
complaints—eg, lower abdominal pain, usually leftsided—and subsequently be shown to have diverticulosis
coli; a causal relation is sometimes difficult to establish.
Such patients do not usually manifest signs of inflammation, such as pyrexia or neutrophilia, which could
indicate diverticulitis. Pain is generally exacerbated by
eating and diminished with defecation or flatus, which
suggests colonic wall tension due to raised intraluminal
pressure. Patients might also report other symptoms such
as bloating or constipation. Assessment can indicate
fullness or mild tenderness in the left lower quadrant,
but frank rebound or guarding should be absent.
A guaiac-positive stool in this setting should never be
attributed to diverticulosis without complete colonic
assessment. Findings of laboratory studies should be
normal.
Diagnostic modalities
For years, barium enema was the standard investigation
in diverticulosis patients, and although it provides
information on number and location of colonic
diverticula, it cannot discern clinical relevance. However,
inaccurate findings have been reported in nearly a third
of patients with diverticulosis.34 This disorder has, in the
past, been regarded as a contraindication to colonoscopy
for fear of causing a perforation.35,36 Further data and
extensive clinical experience, however, have shown that
colonoscopy is safe in this population, although the
diverticular colon can be difficult to examine because of
spasm, luminal narrowing, and fixation.37
Treatment
Brodribb38 did a randomised double-blind trial of a highfibre diet in 18 patients with symptomatic diverticular
disease. A significant placebo effect was noted at
1 month; however, by 3 months, a significant reduction
in bowel symptoms was seen in patients on the high-fibre
diet. These findings suggest that patients should
gradually increase their dietary fibre over weeks, and be
aware that their symptoms might initially worsen before
they improve, which could take months. In a subsequent
study,39 no improvement in symptom endpoints was
reported despite a decline in transit times and increases
in stool weight and frequency. Despite these conflicting
data, some amelioration of symptoms in patients with
uncomplicated disease can be reasonably expected with a
high-fibre diet.
Hypermotility of the diverticular colon suggests that
anticholinergic or antispasmodic drugs might improve
symptoms by diminishing muscular contraction.
Nonetheless, no adequately controlled therapeutic trials
have shown a benefit. No rationale exists for use of
antibiotics or narcotic analgesics in uncomplicated
diverticular disease.
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Complicated diverticular disease
Diverticulitis
Diverticulitis is the most usual clinical complication of
diverticular disease, affecting 10–25% of patients with
diverticula.3 The process by which diverticulitis arises has
been likened to that of appendicitis, with a diverticulum
becoming obstructed by inspissated stool in its neck.40
This faecalith abrades the mucosa of the sac, causing
inflammation and expansion of usual bacterial flora, with
diminished venous outflow and localised ischaemia.
Bacteria may breach the mucosa and extend the process
through the full wall thickness, ultimately leading to
perforation.41 Extent and localisation of the perforation
will establish its clinical behaviour. Microperforations can
remain contained by pericolic fat and mesentery and cause
small pericolic abscesses. Large perforations can result in
an extensive abscess, which could continue around the
bowel wall and form a large inflammatory mass or extend
to other organs. Free perforation into the peritoneum
causing frank peritonitis can be life-threatening but is rare.
Clinical features
People with diverticulitis generally present with left lower
quadrant pain, indicating the propensity for this disorder
to arise in the sigmoid colon in western countries,
although individuals with redundant sigmoid colons can
manifest suprapubic or right-sided pain. Asian patients
have predominantly right-sided diverticula and will usually
present with right lower quadrant pain.42 Pain may be
intermittent or constant and is sometimes associated with
a change in bowel habits.43 Haematochezia is rare,
although anorexia, nausea, and vomiting can arise.
Physical examination usually discloses localised tenderness
and, occasionally, a palpable mass. Bowel sounds are
typically depressed but can be normal in mild cases or
enhanced in the presence of obstruction. Rectal
examination may reveal tenderness or a mass, especially
with a low-lying pelvic abscess. Fever is present in most
patients, although hypotension and shock are unusual.
White blood cell count is sometimes raised.43
The differential diagnosis of this presentation includes
acute appendicitis, especially in Asian patients or those
with redundant sigmoid colons.42 Aphthous ulcers,
anorectal involvement, and chronic diarrhoea suggest a
possible diagnosis of Crohn’s colitis. Colon carcinoma,
like diverticulosis, affects colons of ageing westerners, and
a causal relation has been postulated. Most probably,
colon cancer and diverticulosis are both results of the same
environmental effects, mainly dietary. Chronic symptoms
of weight loss or bleeding should raise suspicion for
carcinoma. Surgical investigation and resection could be
necessary to make a precise diagnosis. In uncomplicated
cases, elective colonoscopy after acute inflammation has
resolved will allow for exclusion of malignant disease.
Elderly people with diverticulosis are also at risk for
ischaemic colitis. Features helpful to differentiate between
these disorders include presence of thumbprinting on
abdominal radiographs and haematochezia, both
suggesting ischaemia. Gynaecological disorders, such as
ruptured ovarian cysts, ovarian torsion, ectopic pregnancy,
or pelvic inflammatory disease, can resemble acute
diverticulitis in female patients. Pelvic ultrasound can be
helpful in obtaining an accurate diagnosis. Other forms of
colitis, such as pseudomembranous or amoebic, can also
mimic diverticulitis.
Diagnostic modalities
Most patients with diverticulitis present with signs and
symptoms sufficient to justify clinical diagnosis and
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Figure 2: Barium enemas of manifestations of diverticulitis
(A) Acute diverticulitis with oedema (arrow) of the bowel wall. (B) Intramural sinus tract (arrow) in acute diverticulitis. (C) Confined perforation or abscess
(arrow) in acute diverticulitis. All figures courtesy of Javier Casillas.
institute empiric treatment, although a thorough physical
examination and basic laboratory studies, such as white
blood cell count, should be done in patients coming to
clinical attention. Further studies should be reserved for
individuals in whom diagnosis remains uncertain,
response to empiric treatment is suboptimal, or a
complication is suspected.
Chest and abdominal radiographs should generally be
done in patients with clinically significant abdominal pain.
A chest radiograph taken while the patient is upright can
aid detection of pneumoperitoneum and help to assess
cardiopulmonary status. Abdominal radiographs can show
abnormal findings in 30–50% of patients,44,45 which
include small or large bowel dilation or ileus,
pneumoperitoneum, bowel obstruction, or soft-tissue
densities suggesting abscesses.
Contrast enemas—once the diagnostic standard—are
limited by the fact that diverticulitis is mainly an
extraluminal process. If they are to be undertaken, watersoluble contrast material should be used and a lowpressure single-contrast study done. Findings deemed
highly suggestive of diverticulitis include extravasated
contrast material outlining an abscess cavity, intramural
sinus tract, or fistula (figure 2).9,46 Absence of any
diverticula should provoke reconsideration of the
diagnosis. In retrospective analyses, contrast enema has
been shown to have a sensitivity of 62–94%, with falsenegative results in 2–15%.47,48
CT scanning has an increasing role in diagnosis,
and should be regarded as the diagnostic procedure of
choice. Abdominal and pelvic scanning is done with
intravenous, oral, and rectal contrast. Criteria suggestive
of diverticulitis include pericolic infiltration of fatty tissue,
colonic wall thickening, and abscess formation (figure 3).
In many trials comparing CT with barium enema in
suspected diverticulitis, sensitivities for CT of 93–98%
and specificities of 75–100% have been consistently
reported, significantly more accurate than contrast
enemas.46,49–51
Because of risk of perforation from either the device or
air insufflation, endoscopy is generally avoided in initial
assessment of the patient with acute diverticulitis. Its
use should be restricted to situations in which diagnosis
of diverticulitis is unclear. In such cases, limited
sigmoidoscopy with minimum insufflation can be helpful
to exclude other diagnoses, such as inflammatory,
infectious, or ischaemic colitis.
Treatment
Need for admission is the initial decision to be made in
uncomplicated diverticulitis, which is based on patient’s
presentation, their ability to tolerate oral intake, severity
of illness, comorbid disease, and adequate outpatient
support. Outpatients should be treated with a clear liquid
diet and a broad-spectrum oral antibiotic with activity
against anaerobes and gram-negative rods (in particular,
Escherichia coli and Bacteroides fragilis).52 Symptomatic
improvement should generally be evident within 2–3 days,
at which time diet can be slowly advanced. Antibiotic
treatment should be continued for 7–10 days. Patients
needing admission should have clear liquids or nothing by
mouth and intravenous fluids. Intravenous antibiotics
should be started, aimed mainly at colonic anaerobic and
gram-negative flora.52 Improvement of symptoms should
Figure 3: CT scans of manifestations of diverticulitis
(A) Contained abscess (arrow) in severe sigmoid diverticulitis. (B) Large air-containing abscess (arrow) in subacute diverticulitis. (C) Large diverticular
abscess (arrow) with penetration into retroperitoneal structures and extending through abdominal wall into subcutaneous tissue. All figures courtesy of
Javier Casillas.
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be expected within 2–4 days, at which point diet can be
advanced. If improvement continues, patients may be
discharged to complete a 7–10 day oral antibiotic course.
Failure of conservative medical treatment warrants a
diligent search for complications, consideration of
alternative diagnoses, and surgical consultation. Most
patients admitted with acute diverticulitis will respond to
conservative treatment, but 15–30% will need surgery
during that time.9,48,53 Free perforation with generalised
peritonitis, although uncommon, carries a high mortality
rate (up to 35%) and needs urgent surgical intervention.9,48
For most patients who respond well to conservative
treatment, an important clinical question subsequently
revolves around likelihood of recurrence and role of
prophylactic surgical resection. Risk of recurrent
symptoms after an attack of acute diverticulitis has been
reported between 7% and 45%; a third is a reasonable
approximation.9,48,53 Recurrent attacks are less likely to
respond to medical treatment and have a high mortality
rate;48,53 thus, most authorities agree that elective resection
is indicated after two attacks of uncomplicated
diverticulitis.54–56 The risk-benefit analysis of such an
approach must be tailored with consideration of severity
and responsiveness of the episode, general health of the
patient, and risk of subsequent occurrence. Risk of
resection is an evolving factor, with reports of increasingly
favourable experiences with laparoscopic resections for
diverticular disease.57–62 This approach might reduce the
threshold for resection in some patients by lowering
operative morbidity. However, some patients will still have
symptoms after surgical resection.
Diverticulitis in special situations
Diverticulitis is seen in about 2–5% of people younger
than 40 years old,9,53 mainly in males.9,63,64 Disease is more
virulent in young patients, with 66–88% needing urgent
surgery during their initial attack, with a high risk of
recurrences or complications.9,63,65,66 Obesity can also be an
important risk factor in young people.67 For these reasons,
and because of the low operative risk of an elective
procedure in an otherwise healthy young patient, resection
is generally indicated after one well-documented episode
of uncomplicated diverticulitis.48,54 Others, however, have
questioned this assertion.56,68,69
Immunocompromised patients with diverticulitis may
present with more subtle signs and symptoms than those
who are immunocompetent and represent a difficult
diagnostic challenge. They are less likely to benefit from
medical treatment and have a higher rate of free
perforation, need for surgery, and postoperative mortality
than non-compromised patients.70,71 Because of this high
risk, some authorities have advocated elective resection
after one episode in an immunosuppressed individual.54
Complicated diverticulitis
Abscess
When perforation of a diverticulum takes place, a localised
phlegmon initially develops; further spread can lead to
formation of large local or distant abscesses. Clinical signs
suggesting abscess formation include a tender mass on
investigation or persistent fever despite an adequate trial
of antibiotics. When an abscess is suspected, CT scanning
is the best modality for making the diagnosis and following
its course.
Small pericolic abscesses can generally be treated
conservatively with continued antibiotics and bowel
rest.56,72 In patients in whom surgery is needed, a singlestage resection and anastomosis can generally be done.
For those with distant or unresolving abscesses, drainage
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is indicated. Surgery was previously the main option, but
CT-guided percutaneous drainage of abdominal abscesses
is now used in preference when feasible. The advantage of
percutaneous catheter drainage is rapid control of sepsis
and patient stabilisation. Further, drainage might eliminate
need for a two-stage procedure with interval colostomy,
instead allowing temporary palliative drainage and
subsequent single-stage resection.73,74
Fistulas
When a diverticular phlegmon or abscess extends or
ruptures into an adjacent organ, fistulas can arise, the most
typical being colovesicular.75 Such fistulas have a two to one
male predominance, attributable to protection of the
bladder by the uterus and 50% rate of hysterectomy in
female patients with colovesical fistulas. Pneumaturia and
faecaluria are suggestive signs.76 Cystoscopy, cystography,
and contrast radiographs or methylene blue studies can
show fistula tracts. Single-stage operative resection with
fistula closure can be undertaken in most patients.75,76
Colovaginal fistulas are the next most frequent,
representing about 25% of all cases.75 Passage of stool or
flatus via the vagina is pathognomonic. Frequent vaginal
infections or copious discharge should prompt consideration of a colovaginal fistula. Treatment is surgical
resection of the diseased colon with repair of the contiguous
organ.56 Coloenteric, colouterine, coloureteral, and
colocutaneous fistulas arise much less typically.
Obstruction
During an episode of acute diverticulitis, partial colonic
obstruction can happen because of relative lumenal
narrowing from pericolic inflammation or compression
from abscess formation. Colonic pseudo-obstruction can
also take place. Acute diverticulitis might cause small bowel
obstruction or ileus if a loop of small intestine becomes
incorporated into the inflammatory mass. These
presentations usually improve as inflammation subsides
with effective treatment; failure to do so should prompt
surgical consultation.
Recurrent episodes of diverticulitis, sometimes subclinical, can initiate progressive fibrosis and stricturing of
the colonic wall without persisting inflammation.
Ultimately, high-grade or complete obstruction can
happen, needing surgery. An insidious presentation with
non-specific symptoms is typical. Generally, a stricture with
uncertain cause is identified on barium enema. The
important issue is to distinguish between a diverticular
stricture and a stenosing neoplasm. Doctors should attempt
to make this differentiation by colonoscopy with biopsy, but
this procedure is not always possible.77 Strictures in which
malignant disease cannot be excluded should undergo
surgical en bloc resection. A trial of endoscopic treatment
with balloon dilation can be attempted in patients in whom
neoplasm is judged sufficiently excluded.78–80 Early work
with colonic metal stents has suggested that they might
have a role in colonic obstruction due to diverticular
disease. Stenting can provide temporary decompression,
allowing for bowel preparation and subsequent single-stage
resection without diversion.81,82
Haemorrhage
Important lower gastrointestinal bleeding can be caused
by diverticula, vascular ectasias, colitis, or neoplasms.10,83–85
Diverticular sources have been reported to be the most
typically identified cause, accounting for greater than 40%
of lower gastrointestinal bleeding episodes.86,87 Severe
haemorrhage can arise in 3–5% of patients with
diverticulosis.10,88,89 Despite the fact that most diverticula
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Figure 4: Endoscopic pictures of diverticulum
(A) Diverticulum with visible vessel. (B) Oozing during epinephrine injection. (C) Diverticulum post injection. All photos courtesy of Francisco C Ramirez.
are in the left colon in western individuals, the site of
bleeding may more often be located in the proximal
colon.10,88,90–93
Pathophysiology
Microangiography on resected specimens from patients
with bleeding diverticula shows intimal thickening and
medial thinning of the vasa recta as it courses over the
dome of the diverticulum.90 These changes arise
asymetrically towards the lumen and lead to segmental
weakening of the artery, predisposing to rupture. Factors
that initiate this arterial change are unknown, although
inflammation does not seem to be a contributing factor.
This finding accords with the clinical impression that
bleeding rarely complicates diverticulitis.
The association of use of non-steroidal antiinflammatories (NSAIDs) with ulcer disease and upper
gastrointestinal bleeding is well documented, but data
have also implicated these drugs in diverticular bleeding.
In a large prospective series of patients with lower
gastrointestinal bleeding (in whom 50% were diverticular), a bleeding risk with NSAIDs was reported that
was equal to that of duodenal ulcer.94 In the Health
Professionals Follow-up Study,95 regular NSAID use was
associated with raised risk of diverticular bleeding.
Whether patients with diverticulosis should be counselled
to avoid NSAIDs—as is done for ulcer patients—or use
COX2 selective agents—is still conjecture.
Clinical features
Clinical presentation of diverticular haemorrhage is
usually one of an abrupt painless onset. The patient can
have mild lower abdominal cramps or the urge to
defecate, followed by passage of voluminous red or
maroon blood or clots. While melaena can sometimes
happen with a slowly bleeding right colon lesion, the
arterial nature of diverticular bleeding makes this
presentation uncommon. Presence of colonic diverticula
should not be judged an adequate explanation for a
positive faecal occult blood test or as a cause of iron
deficiency anaemia. Haemorrhage ceases spontaneously in
70–80% of patients, and rebleeding rates range from 22%
to 38%.88,89,92 The chance of a third bleeding episode can
be as high as 50%, leading many doctors to recommend
surgical resection after a second bleeding episode, similar
to recommendations made for recurrent divericulitis.54,88
Diagnosis and management
Overall management of lower gastrointestinal bleeding is
beyond the scope of this review, but is described in other
636
articles.89,96 Fluid and blood product resuscitation needs
immediate attention. Exclusion of an upper gastrointestinal source by endoscopy is warranted, because
10–15% of patients with haematochezia will have an
upper gastrointestinal tract cause. Flexible sigmoidoscopy
is an appropriate initial approach to rule out an obvious
rectosigmoid lesion, and can be done either unprepared or
after enema administration. If no cause is identified,
further
assessment
with
non-invasive
(nuclear
scintigraphy) or invasive (angiography, colonoscopy)
techniques can be undertaken in an attempt to localise
and treat the bleeding source.
Scintigraphy has several theoretical advantages in
assessment of lower gastrointestinal bleeding. It is noninvasive and sensitive to bleeding rates as low as
0·1 mL/min. Furthermore, once labelled, red cells remain
active for up to 24 h, permitting repeat imaging in the
patient with intermittent bleeding.97 At best, however,
nuclear scans provide information only about the
anatomic site of bleeding, not its cause, and have no
therapeutic potential. Further, accuracy of predicting the
bleeding site has been questioned.98 In view of the high
sensitivity and relative simplicity of scintigraphy, however,
many centres use this method as a screening test before
angiography, to keep the number of negative angiograms
to a minimum and allow for selection of a specific artery
for injection.97
Angiography has a sensitivity for lower gastrointestinal
bleeding at a rate of 0·5 mL/min, although this value is
from animal work.83 An important use of diagnostic
angiography is to identify the site of bleeding with enough
accuracy to allow selective hemicolectomy, rather than
empirical subtotal colectomy, although accuracy has been
questioned.99 An additional role for angiography rests in
its therapeutic potential. Intra-arterial vasopressin can
control haemorrhage in more than 90% of patients.100
This treatment is usually only temporary, however,
because up to half of treated people will rebleed with
discontinuation of infusion. Nonetheless, even temporary
control of bleeding can allow semielective surgical
procedure in a well-prepared patient, rather than
emergency resection, with concomitant reduction in
surgical morbidity.100 Angiographic embolisation of very
distal bleeding branches (subselective) is also effective and
safe.101
For most patients, diverticular bleeding is self-limited.
Subsequent colonoscopy should be done to elucidate the
bleeding source and to exclude neoplasia.9,102–104 The role
of colonoscopy during episodes of lower gastrointestinal
bleeding is being defined.105,106 A rapid oral purge with
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SEMINAR
electrolyte solution to prepare the colon for emergent
colonoscopy has been shown to be safe and effective.107–109
In small series, endoscopy has been used to control acute
bleeding (figure 4).110–118 In a cohort of 48 patients with
lower gastrointestinal bleeding,118 ten had definite signs of
diverticular haemorrhage and were treated endoscopically, and none had recurrent bleeding. In a historical
control group of 17 patients not treated with
colonoscopy,119 nine had additional bleeding. Although
such treatment may be applicable to only a few patients
with lower intestinal bleeding, colonoscopic haemostasis
will probably have an increasing role in the future.
Surgery in lower gastrointestinal bleeding is usually
reserved until endoscopic or angiographic treatments fail.
Segmental resection is most usually done if the bleeding
site is clearly identified from a therapeutically unsuccessful angiographic or endoscopic procedure. Rebleeding
is seen in about 6% of patients.100 In people with persistent
bleeding and no angiographic or endoscopic identification
of a definite bleeding site, subtotal colectomy could be
needed.
Conflict of interest statement
None declared.
Acknowledgments
No funding was received for this Seminar.
References
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
Painter NS, Burkitt DP. Diverticular disease of the colon: a
deficiency disease of Western civilization. BMJ 1971; 2:
450–54.
Painter NS, Burkitt DP. Diverticular disease of the colon, a 20th
century problem. Clin Gastroenterol 1975; 4: 3–21.
Parks TG. Natural history of diverticular disease of the colon.
Clin Gastroenterol 1975; 4: 53–69.
Kyle J, Adesola A, Tinckler L, deBeaux J. Incidence of diverticulitis.
Scand J Gastroenterol 1967; 2: 77–80.
Lee YS. Diverticular disease of the large bowel in Singapore: an
autopsy survey. Dis Colon Rectum 1986; 29: 330–35.
Walker AR, Segal I. Epidemiology of noninfective intestinal diseases
in various ethnic groups in South Africa. Isr J Med Sci 1979; 15:
309–13.
Ogunbiyi OA. Diverticular disease of the colon in Ibadan, Nigeria.
Afr J Med Med Sci 1989; 18: 241–44.
Makela J, Kiviniemi H, Laitinen S. Prevalence of perforated sigmoid
diverticulitis is increasing. Dis Colon Rectum 2002; 45: 955–61.
Roberts PL, Veidenheimer MC. Current management of
diverticulitis. Adv Surg 1994; 27: 189–208.
Reinus JF, Brandt LJ. Vascular ectasias and diverticulosis: common
causes of lower intestinal bleeding. Gastroenterol Clin North Am
1994; 23: 1–20.
Slack W. The anatomy, pathology and some clinical features of
diverticulitis of the colon. Br J Surg 1962; 50: 185–90.
Chia JG, Wilde CC, Ngoi SS, Goh PM, Ong CL. Trends of
diverticular disease of the large bowel in a newly developed country.
Dis Colon Rectum 1991; 34: 498–501.
Levi DM, Levi JU, Rogers AI, Bergau DK, Wenger J. Giant colonic
diverticulum: an unusual manifestation of a common disease.
Am J Gastroenterol 1993; 88: 139–42.
Horner J. Natural history of the diverticulosis of the colon.
Am J Dig Dis 1958; 3: 343–50.
Ryan P. Changing concepts in diverticular disease. Dis Colon Rectum
1983; 26: 12–18.
Whiteway J, Morson BC. Elastosis in diverticular disease of the
sigmoid colon. Gut 1985; 26: 258–66.
Bode MK, Karttunen TJ, Makela J, Risteli L, Risteli J. Type I and
III collagens in human colon cancer and diverticulosis.
Scand J Gastroenterol 2000; 35: 747–52.
Stumpf M, Cao W, Klinge U, Klosterhalfen B, Kasperk R,
Schumpelick V. Increased distribution of collagen type III and
reduced expression of matrix metalloproteinase 1 in patients with
diverticular disease. Int J Colorectal Dis 2001; 16: 271–75.
Wess L, Eastwood MA, Edwards CA, Busuttil A, Miller A.
Collagen alteration in an animal model of colonic diverticulosis. Gut
1996; 38: 701–06.
THE LANCET • Vol 363 • February 21, 2004 • www.thelancet.com
20 Wess L, Eastwood MA, Wess TJ, Busuttil A, Miller A. Cross linking
of collagen is increased in colonic diverticulosis. Gut 1995; 37: 91–94.
21 Simpson J, Scholefield JH, Spiller RC. Pathogenesis of colonic
diverticula. Br J Surg 2002; 89: 546–54.
22 Arfwidsson S, Kock N, Lehmann L, Winberg T. Pathogenesis of
multiple diverticula of the sigmoid colon in diverticular diseases.
Acta Chir Scan Suppl 1964; 342: 1–68.
23 Painter NS, Truelove SC, Ardran GM, Tuckey M. Segmentation and
the localization of intraluminal pressure in the human colon, with
special reference to the pathogenesis of colonic diverticula.
Gastroenterology 1968; 54 (suppl): 778–80.
24 Painter NS. The aetiology of diverticulosis of the colon with special
reference to the action of certain drugs on the behavior of the colon.
Ann R Coll Surg Engl 1964; 34: 98–119.
25 Hodgson J. Effect of methylcellulose on rectal and colonic pressures
in treatment of diverticular disease. BMJ 1972; 3: 729–31.
26 Cortesini C, Pantalone D. Usefulness of colonic motility study in
identifying patients at risk for complicated diverticular disease.
Dis Colon Rectum 1991; 34: 339–42.
27 Sugihara K, Muto T, Morioka Y. Motility study in right sided
diverticular disease of the colon. Gut 1983; 24: 1130–34.
28 Tomita R, Fujisaki S, Tanjoh K, Fukuzawa M. Role of nitric oxide in
the left-sided colon of patients with diverticular disease.
Hepatogastroenterology 2000; 47: 692–96.
29 Burkitt DP, Walker AR, Painter NS. Effect of dietary fibre on stools
and the transit-times, and its role in the causation of disease. Lancet
1972; 2: 1408–12.
30 Fisher N, Berry CS, Fearn T, Gregory JA, Hardy J. Cereal dietary
fiber consumption and diverticular disease: a lifespan study in rats.
Am J Clin Nutr 1985; 42: 788–804.
31 Aldoori WH, Giovannucci EL, Rimm EB, Wing AL,
Trichopoulos DV, Willett WC. A prospective study of diet and the
risk of symptomatic diverticular disease in men. Am J Clin Nutr 1994;
60: 757–64.
32 Aldoori WH, Giovannucci EL, Rockett HR, Sampson L, Rimm EB,
Willett WC. A prospective study of dietary fiber types and
symptomatic diverticular disease in men. J Nutr 1998; 128: 714–19.
33 Marlett J, McBurney M, Slavin J. Position of the American Dietetic
Association: health implications of dietary fiber. J Am Diet Assoc
2002; 102: 993–1000.
34 Boulos PB, Karamanolis DG, Salmon PR, Clark CG. Is colonoscopy
necessary in diverticular disease? Lancet 1984; 1: 95–96.
35 Wolff W, Shinya H. Colonoscopy. N Engl J Med 1973; 288:
974–75.
36 Williams CB, Lane RH, Sakai Y. Colonoscopy: an air-pressure
hazard. Lancet 1973; 2: 729.
37 Anderson JC, Messina CR, Cohn W, et al. Factors predictive of
difficult colonoscopy. Gastrointest Endosc 2001; 54: 558–62.
38 Brodribb AJ. Treatment of symptomatic diverticular disease with a
high-fibre diet. Lancet 1977; 1: 664–66.
39 Ornstein M. Are fibre supplements really necessary in diverticular
disease of the colon? A controlled clinical trial. BMJ 1981; 282:
1353–56.
40 Berman LG, Burdick D, Heitzman ER, Prior JT. A critical reappraisal
of sigmoid peridiverticulitis. Surg Gynecol Obstet 1968; 127: 481–91.
41 Williams R, Davis I. Diverticular disease of the colon, 5th edn.
Philadelphia: Saunders, 1995.
42 Markham NI, Li AK. Diverticulitis of the right colon: experience
from Hong Kong. Gut 1992; 33: 547–49.
43 Ambrosetti P, Robert JH, Witzig JA, et al. Acute left colonic
diverticulitis: a prospective analysis of 226 consecutive cases. Surgery
1994; 115: 546–50.
44 Kourtesis GJ, Williams RA, Wilson SE. Surgical options in acute
diverticulitis: value of sigmoid resection in dealing with the septic
focus. Aust N Z J Surg 1988; 58: 955–59.
45 Morris J, Stellato TA, Lieberman J, Haaga JR. The utility of
computed tomography in colonic diverticulitis. Ann Surg 1986; 204:
128–32.
46 Doringer E. Computerized tomography of colonic diverticulitis.
Crit Rev Diagn Imaging 1992; 33: 421–35.
47 Shrier D, Skucas J, Weiss S. Diverticulitis: an evaluation by computed
tomography and contrast enema. Am J Gastroenterol 1991; 86:
1466–71.
48 The standards task force of the American Society of Colon and Rectal
Surgeons. Practice parameters for sigmoid diverticulitis: supporting
documentation. Dis Colon Rectum 1995; 38: 126–32.
49 Hulnick DH, Megibow AJ, Balthazar EJ, Naidich DP, Bosniak MA.
Computed tomography in the evaluation of diverticulitis. Radiology
1984; 152: 491–95.
50 Cho KC, Morehouse HT, Alterman DD, Thornhill BA. Sigmoid
diverticulitis: diagnostic role of CT—comparison with barium enema
studies. Radiology 1990; 176: 111–15.
637
SEMINAR
51 Ambrosetti P, Jenny A, Becker C, Terrier TF, Morel P. Acute left
colonic diverticulitis: compared performance of computed
tomography and water-soluble contrast enema: prospective evaluation
of 420 patients. Dis Colon Rectum 2000; 43: 1363–67.
52 Chow A. Appendicitis and diverticulitis. Philadelphia: Lippincott,
1994.
53 Parks TG. Natural history of diverticular disease of the colon: a
review of 521 cases. BMJ 1969; 4: 639–42.
54 Stollman NH, Raskin JB. Diagnosis and management of diverticular
disease of the colon in adults: ad hoc practice parameters committee
of the American College of Gastroenterology. Am J Gastroenterol
1999; 94: 3110–21.
55 Kohler L, Sauerland S, Neugebauer E. Diagnosis and treatment of
diverticular disease: results of a consensus development conference.
Surg Endosc 1999; 13: 430–36.
56 Wong WD, Wexner SD, Lowry A, et al. Practice parameters for the
treatment of sigmoid diverticulitis: supporting documentation.
Dis Colon Rectum 2000; 43: 290–97.
57 Franklin ME Jr, Dorman JP, Jacobs M, Plasencia G. Is laparoscopic
surgery applicable to complicated colonic diverticular disease?
Surg Endosc 1997; 11: 1021–25.
58 Smadja C, Sbai Idrissi M, Tahrat M, et al. Elective laparoscopic
sigmoid colectomy for diverticulitis: results of a prospective study.
Surg Endosc 1999; 13: 645–48.
59 Kockerling F, Schneider C, Reymond MA, et al. Laparoscopic
resection of sigmoid diverticulitis: results of a multicenter study.
Surg Endosc 1999; 13: 567–71.
60 Berthou JC, Charbonneau P. Elective laparoscopic management of
sigmoid diverticulitis: results in a series of 110 patients. Surg Endosc
1999; 13: 457–60.
61 Stevenson A, Stitz R, Lumley J, Fielding G. Laparoscopically
assisted anterior resection for diverticular disease: follow-up of
100 consecutive patients. Ann Surg 1998; 227: 335–42.
62 Lauro A, Alonso Poza A, Cirocchi R, et al. Laparoscopic surgery for
colon diverticulitis. Minerva Chir 2002; 57: 1–5.
63 Konvolinka CW. Acute diverticulitis under age forty. Am J Surg 1994;
167: 562–65.
64 Acosta JA, Grebenc ML, Doberneck RC, McCarthy JD, Fry DE.
Colonic diverticular disease in patients 40 years old or younger.
Am Surg 1992; 58: 605–07.
65 Freischlag J, Bennion RS, Thompson JE Jr. Complications of
diverticular disease of the colon in young people. Dis Colon Rectum
1986; 29: 639–43.
66 Chautems RC, Ambrosetti P, Ludwig A, Mermillod B, Morel P,
Soravia C. Long-term follow-up after first acute episode of sigmoid
diverticulitis: is surgery mandatory? A prospective study of
118 patients. Dis Colon Rectum 2002; 45: 962–66.
67 Schauer PR, Ramos R, Ghiatas AA, Sirinek KR. Virulent diverticular
disease in young obese men. Am J Surg 1992; 164: 443–46.
68 Reisman Y, Ziv Y, Kravrovitc D, Negri M, Wolloch Y, Halevy A.
Diverticulitis: the effect of age and location on the course of disease.
Int J Colorectal Dis 1999; 14: 250–54.
69 Spivak H, Weinrauch S, Harvey JC, Surick B, Ferstenberg H,
Friedman I. Acute colonic diverticulitis in the young.
Dis Colon Rectum 1997; 40: 570–74.
70 Perkins JD, Shield CF 3rd, Chang FC, Farha GJ. Acute diverticulitis:
comparison of treatment in immunocompromised and
nonimmunocompromised patients. Am J Surg 1984; 148: 745–48.
71 Tyau ES, Prystowsky JB, Joehl RJ, Nahrwold DL. Acute diverticulitis:
a complicated problem in the immunocompromised patient.
Arch Surg 1991; 126: 855–58.
72 Ambrosetti P, Robert J, Witzig JA, et al. Incidence, outcome, and
proposed management of isolated abscesses complicating acute
left-sided colonic diverticulitis: a prospective study of 140 patients.
Dis Colon Rectum 1992; 35: 1072–76.
73 Schechter S, Eisenstat TE, Oliver GC, Rubin RJ, Salvati EP.
Computerized tomographic scan-guided drainage of intra-abdominal
abscesses: preoperative and postoperative modalities in colon and
rectal surgery. Dis Colon Rectum 1994; 37: 984–88.
74 Stabile BE, Puccio E, van Sonnenberg E, Neff CC. Preoperative
percutaneous drainage of diverticular abscesses. Am J Surg 1990; 159:
99–104.
75 Woods RJ, Lavery IC, Fazio VW, Jagelman DG, Weakley FL.
Internal fistulas in diverticular disease. Dis Colon Rectum 1988; 31:
591–96.
76 McBeath RB, Schiff M Jr, Allen V, Bottaccini MR, Miller JI,
Ehreth JT. A 12-year experience with enterovesical fistulas. Urology
1994; 44: 661–65.
77 Forde KA, Treat MR. Colonoscopy in the evaluation of strictures.
Dis Colon Rectum 1985; 28: 699–701.
78 Kozarek RA. Hydrostatic balloon dilation of gastrointestinal stenoses:
a national survey. Gastrointest Endosc 1986; 32: 15–19.
638
79 Manten H, Zara J, Rakin J. Balloon dilation of rectosigmoid
strictures: transendoscopic approach. Gastrointest Endosc 1986; 32:
164.
80 Oz MC, Forde KA. Endoscopic alternatives in the management of
colonic strictures. Surgery 1990; 108: 513–19.
81 Tamim WZ, Ghellai A, Counihan TC, Swanson RS, Colby JM,
Sweeney WB. Experience with endoluminal colonic wall stents for
the management of large bowel obstruction for benign and
malignant disease. Arch Surg 2000; 135: 434–38.
82 Paul L, Pinto I, Gomez H, Fernandez-Lobato R, Moyano E.
Metallic stents in the treatment of benign diseases of the colon:
preliminary experience in 10 cases. Radiology 2002; 223: 715–22.
83 Potter GD, Sellin JH. Lower gastrointestinal bleeding.
Gastroenterol Clin North Am 1988; 17: 341–56.
84 Boley SJ, DiBiase A, Brandt LJ, Sammartano RJ. Lower intestinal
bleeding in the elderly. Am J Surg 1979; 137: 57–64.
85 Gostout CJ, Wang KK, Ahlquist DA, et al. Acute gastrointestinal
bleeding: experience of a specialized management team.
J Clin Gastroenterol 1992; 14: 260–67.
86 Peura DA, Lanza FL, Gostout CJ, Foutch PG. The American
College of Gastroenterology bleeding registry: preliminary findings.
Am J Gastroenterol 1997; 92: 924–28.
87 Longstreth GF. Epidemiology and outcome of patients hospitalized
with acute lower gastrointestinal hemorrhage: a population-based
study. Am J Gastroenterol 1997; 92: 419–24.
88 McGuire HH Jr, Haynes BW Jr. Massive hemorrhage for
diverticulosis of the colon: guidelines for therapy based on bleeding
patterns observed in fifty cases. Ann Surg 1972; 175: 847–55.
89 Zuckerman GR, Prakash C. Acute lower intestinal bleeding: part II—
etiology, therapy, and outcomes. Gastrointest Endosc 1999; 49:
228–38.
90 Meyers MA, Alonso DR, Gray GF, Baer JW. Pathogenesis of
bleeding colonic diverticulosis. Gastroenterology 1976; 71: 577–83.
91 Casarella WJ, Kanter IE, Seaman WB. Right-sided colonic
diverticula as a cause of acute rectal hemorrhage. N Engl J Med
1972; 286: 450–53.
92 McGuire HH Jr. Bleeding colonic diverticula: a reappraisal of
natural history and management. Ann Surg 1994; 220: 653–56.
93 Wong SK, Ho YH, Leong AP, Seow-Choen F. Clinical behavior of
complicated right-sided and left-sided diverticulosis. Dis Colon
Rectum 1997; 40: 344–48.
94 Wilcox CM, Alexander LN, Cotsonis GA, Clark WS. Nonsteroidal
antiinflammatory drugs are associated with both upper and lower
gastrointestinal bleeding. Dig Dis Sci 1997; 42: 990–97.
95 Aldoori WH, Giovannucci EL, Rimm EB, Wing AL, Willett WC.
Use of acetaminophen and nonsteroidal anti-inflammatory drugs:
a prospective study and the risk of symptomatic diverticular disease
in men. Arch Fam Med 1998; 7: 255–60.
96 Zuccaro G Jr. Management of the adult patient with acute
lower gastrointestinal bleeding. Am J Gastroenterol 1998; 93:
1202–08.
97 Alavi A, Ring EJ. Localization of gastrointestinal bleeding:
superiority of 99mTc sulfur colloid compared with angiography.
AJR Am J Roentgenol 1981; 137: 741–48.
98 Hunter JM, Pezim ME. Limited value of technetium 99m-labeled
red cell scintigraphy in localization of lower gastrointestinal
bleeding. Am J Surg 1990; 159: 504–06.
99 Cohn SM, Moller BA, Zieg PM, Milner KA, Angood PB.
Angiography for preoperative evaluation in patients with lower
gastrointestinal bleeding: are the benefits worth the risks?
Arch Surg 1998; 133: 50–55.
100 Browder W, Cerise EJ, Litwin MS. Impact of emergency
angiography in massive lower gastrointestinal bleeding. Ann Surg
1986; 204: 530–36.
101 Gordon RL, Ahl KL, Kerlan RK, et al. Selective arterial
embolization for the control of lower gastrointestinal bleeding.
Am J Surg 1997; 174: 24–28.
102 Shinya H, Cwern M, Wolf G. Colonoscopic diagnosis and
management of rectal bleeding. Surg Clin North Am 1982; 62:
897–903.
103 Tedesco FJ, Waye JD, Raskin JB, Morris SJ, Greenwald RA.
Colonoscopic evaluation of rectal bleeding: a study of 304 patients.
Ann Intern Med 1978; 89: 907–09.
104 Irvine EJ, O’Connor J, Frost RA, et al. Prospective comparison of
double contrast barium enema plus flexible sigmoidoscopy v
colonoscopy in rectal bleeding: barium enema v colonoscopy in
rectal bleeding. Gut 1988; 29: 1188–93.
105 Forde KA. Colonoscopy in acute rectal bleeding. Gastrointest Endosc
1981; 27: 219–20.
106 Deyhle P, Blum A, Nuesch H. Emergency coloscopy (sic) in the
management of acute perianal hemorrhage. Endoscopy 1974; 6:
229–32.
THE LANCET • Vol 363 • February 21, 2004 • www.thelancet.com
SEMINAR
107 Jensen DM, Machicado GA. Diagnosis and treatment of severe
hematochezia: the role of urgent colonoscopy after purge.
Gastroenterology 1988; 95: 1569–74.
108 Jensen D, Machicado G, Tapia J. Emergent colonoscopy in patients
with severe hematochezia. Gastrointest Endosc 1983; 29: 177.
109 Caos A, Benner KG, Manier J, et al. Colonoscopy after Golytely
preparation in acute rectal bleeding. J Clin Gastroenterol 1986; 8:
46–49.
110 Mauldin JL. Therapeutic use of colonoscopy in active diverticular
bleeding. Gastrointest Endosc 1985; 31: 290–91.
111 Johnston J, Sones J. Endoscopic heater probe coagulation of
the bleeding colonic diverticulum. Gastrointest Endosc 1986; 32:
160.
112 Savides TJ, Jensen DM. Colonoscopic hemostasis for recurrent
diverticular hemorrhage associated with a visible vessel: a report of
three cases. Gastrointest Endosc 1994; 40: 70–73.
113 Foutch PG, Zimmerman K. Diverticular bleeding and the pigmented
protuberance (sentinel clot): clinical implications, histopathological
THE LANCET • Vol 363 • February 21, 2004 • www.thelancet.com
correlation, and results of endoscopic intervention. Am J Gastroenterol
1996; 91: 2589–93.
114 Bertoni G, Conigliaro R, Ricci E, Mortilla MG, Bedogni G,
Fornaciari G. Endoscopic injection hemostasis of colonic diverticular
bleeding: a case report. Endoscopy 1990; 22: 154–55.
115 Kim YI, Marcon NE. Injection therapy for colonic diverticular
bleeding: a case study. J Clin Gastroenterol 1993; 17: 46–48.
116 Andress HJ, Mewes A, Lange V. Endoscopic hemostasis of a bleeding
diverticulum of the sigma with fibrin sealant. Endoscopy 1993; 25: 193.
117 Witte JT. Band ligation for colonic bleeding: modification of
multiband ligating devices for use with a colonoscope.
Gastrointest Endosc 2000; 52: 762–65.
118 Hokama A, Uehara T, Nakayoshi T, et al. Utility of endoscopic
hemoclipping for colonic diverticular bleeding. Am J Gastroenterol
1997; 92: 543–46.
119 Jensen DM, Machicado GA, Jutabha R, Kovacs TO. Urgent
colonoscopy for the diagnosis and treatment of severe diverticular
hemorrhage. N Engl J Med 2000; 342: 78–82.
639