State Susan
D. Wall,
MD
#{149} Bronwyn
Jones,
FRACP,
O
toimmune
disease,
as well
as for
or-
gan
transplantation, has combined with the acquired immunodeficiency syndrome epidemic to increase greatly the incidence of opportunistic infections
and
other
complications tract. Consefluoroscopic and
the gastrointestinal quently,
barium
cross-sectional imaging bred to address these no longer uncommon. overlap
exists,
patterns
that
there
can
of
tai-
studies problems Although are
direct
radiographic
the diagnosis
to an opportunistic infection and sometimes to a specific pathogen. This article describes and illustrates
the radiographic
findings
of gas-
with Candida albicans, cytomegalovirus, Cryptosporidium spp, herpes simplex virus, Mycobacterium tuberculosis, M avium-intracellulare, and human trointestinal
superinfection
immunodeficiency
virus.
trointestinal
tract
Other
gas-
complications
of
immunosuppression are discussed, including graft-versus-host disease following bone marrow transplantation, typhlitis, and pseudomembranous colitis. Index terms: Acquired drome (AIDS), 70.2518 Colitis, 75.20 #{149}Enteritis, 7120 #{149}Gastrointestinal Herpes
simplex,
Mycobacteria, Radiology
I
From
70.20
70.203 1992;
immunodeficiency synCholangitis, 76.20 74.20 #{149}Esophagitis, tract, infection, 70.20 #{149} Grafts, infection #{149}
#{149} State-of-art
reviews
185:327-335
the Department
of Radiology,
Univer-
of California, San Francisco, Veterans Administration Medical Center, 4150 Clement St. San Francisco, CA 94121 (S.D.W.), and the Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins Medical
sity
Institutions,
Baltimore
1992; revision requested ceived July 2; accepted requests to S.D.W. C
RSNA,
1992
(B.J.).
Received
April
May 22; revision reJuly 6. Address reprint
Host: and Other
10,
infections
PPORTUNISTIC
of the
Complications’ plantation,
has combined
gastrointestinal tract have occurred with increasing frequency over the past decade, and now they are no longer considered uncommon.
acquired drome greatly
This is so because of the expanded population of immunocompromised
the gastrointestinal tract. of this article is to describe
patients. The “immunocompromised host” is a term used to describe son with increased susceptibility opportunistic pathogens due
graphic
qualitative
are
or quantitative
a perto to a
defect
of
iatrogenic
immune
suppression
of
medicine the patient
does not in general more susceptible to bacterial infection, as it has less impact on B-lymphocyte function. Also, antibiotics will eradicate the most aggressive bacteria. Rather, the relative T-ce!1 depression reduces the host’s defense against opportunistic organisms. An opportunistic organism is one of low virulence that is present in normal mucosa and/or skin flora or it is a microbial agent that is generally maintained in a latent state not causing disease. Organ failure no longer dooms a patient to early death, as the success with kidney, liver, lung, heart, bone marrow, and pancreas transplantation continues to progress with remarkable speed. Regimens to counteract organ transplant rejection are
most effective transplantation,
if begun
or even
at the
before,
time
of
and
they must be given for the life of the graft. Hence, the recipient will always be at increased risk to the consequences of immunosuppression. In the decade since the early 1980s, the increasing use of immunosuppressive therapy for cancer and autoimmune disease, as well as for organ transII III
II II 1111111111 IIIIIIIIIIHIIII
11111111III
with
the
immunodeficiency syn(AIDS) epidemic to increase the incidence of opportunistic
infections
one or more components of the norma! immune defense mechanism. A!though the defect may be congenital, acquired defects predominate as an increasing byproduct of current diseases and/or modern approaches to their treatment. A relative T-cell depression predominates, and so the modern render
Art
FRCR
Gastrointestinal Tract in the Immunocompromised Opportunistic Infections In the decade since the early 1980s, the increasing use of immunosuppressive therapy for cancer and au-
ofthe
and
other
complications
manifestations
patients.
The
of
The purpose the radio-
seen
radiographic
esophagitis, enteritis, and to the various opportunistic
in such patterns
colitis
of
due
pathogens will be described first. These pathogens include Candida albicans, cytomegalovirus, herpes simplex virus, Cryptosporidium spp, and mycobacteria, both typical and atypical. Then, AIDS-specific problems of the gastrointestinal tract will be described, followed by a discussion of the gastrointestinal problems associated with bone marrow transplantation and graft-versus-host disease (GVHD). Discussion of other general
complications
of the gastrointestinal
tract associated with immunosuppression will follow, including typhlitis and pseudomembranous colitis. The radiographic manifestations of the tumors associated with immunosuppression are discussed elsewhere (1). The patterns noted with these pro-
cesses
are important
because
barium
radiography, as well as computed tomography (CT), can be instrumental in the assessment of possible opportu-
nistic tion
infections, can
provide
and their
identifica-
the
of the initial (2-5). Also,
basis AIDS
diagnosis of clinical these imaging studies can guide endoscopic biopsy and be used to evaluate complications and monitor the progress of therapy. Barium fluoroscopic studies, in particular, can be helpful in evaluating the immuno-
Abbreviations: AIDS ciency syndrome, CMV ELISA = enzyme-linked GVHD = graft-versus-host man immunodeficiency rium
avium-intracellulare.
acquired
= =
immunodefi-
cytomegalovirus, immunosorbent
assay,
disease, HIV = huvirus, MA! = Mycobacte-
compromised
patient who has dysphagia, odynophagia, abdominal pain, diarrhea, symptoms of intermittent obstruction, or gastrointestinal bleeding (6).
portunistic
infectious
Herpesvirus
spp,
agents
such
virus
as
both
typi-
spp.
typically
is dem-
in the is caused most often by C albicans (7). Oral involvement (thrush) usually accompanies diffuse esophageal dis-
onstrated by multiple, small shallow ulcerations (10). Often they are diamond shaped. Ulceration may be isolated or there may be small clusters of scattered ulcers. The remainder of the
ease.
esophageal
ing
esophagitis patient
of the esophagus abnormality of typical of Candida commonly is seen is due to other op-
CMV, and Mycobacterium
cal and atypical Herpes simplex
ESOPHAGITIS Opportunistic immunocompromised
Focal ulceration without surrounding the mucosa is not esophagitis, but it when esophagitis
Dysphagia
is the usual
complaint,
and
less common.
present-
odynophagia
is
Radiographic
findings
irregularity
involving
the proxi-
mal, as well as distal, portion of the esophagus. Clinical progression to moderate disease will cause a nodular thickening of the esophageal folds. A “shaggy” or “cobblestone” appear-
ance is typical as barium fills the interstices among the scattered irregular plaques of monilial colonies and necrotic debris. Such a radiographic tern in an immunocompromised
allows
the initial
diagnosis
However,
cause
are typical regardless of the cause of immune depression. Early disease is demonstrated at double-contrast barium esophagography by diffuse mu-
cosal
mal.
pathost
to be es-
tablished preclude confirmation
with sufficient certainty to the necessity of endoscopic prior to the initiation of therapy (8). Deep ulceration may be superimposed among the diffuse mu-
cosal plaques when disease is severe (Fig 1), and occasionally gastritis is present as well (Fig 2). Diffuse in-
can
mucosa
most
severe
multiple
can
lesions
to distinguish
from
radiographically
may become though
large
some
of the
with
can occur
Dissemination mation
solid
including
will result
4).
in the for-
of “microabscesses”
organs
the
intramural (9) and stricture, or diffuse (Fig in the
of the abdomen.
CT en-
hanced with intravenous contrast material then demonstrates numerous small ( < 0.5 cm) foci of low attenuation, most notably in the liver but sometimes also in the spleen and kid-
neys.
Such
junction
a pattern
with
thickening, disseminated
diffuse
#{149} Radiology
esophageal
wall
is highly suggestive candidiasis when
in an immunocompromised 328
at CT, in conof noted
patient.
of the
a
gas-
trointestinal tract usually involves primarily the proximal small bowel (duodenum and jejunum). Typically, it causes regular fold thickening (Fig 7) and often manifests with markedly
increased
small
bowel
secretions.
latter is an important diagnostic at both barium radiography and
The sign CT.
Mesenteric lymphadenopathy is uncommon in patients with cryptosporidiosis, although some patients may
one
or a cluster of several ulcers. Mycobacterium aviumintracellulare (MAI) has been noted to cause discrete ulceration of the esophagus (14), but this is uncommon. Mycobacterium tuberculosis recently has been reported to cause marked abnor-
Occasionally,
mality
in the esophagus
(15). Disease
have demonstrated esophagomediastinal communication. There may be sinus tract formation from the esophageal lumen to the necrotic lymph node. Esophagobronchial communication has been seen, as well. A few patients have demonstrated esopha-
formation of diffuse pseudodiverticula which can be focal
diar-
mu-
cult
plications
Cryptosporidiosis
a severe
L of fluid
cosa may be present with early CMV esophagitis, the typical pattern is of a diffusely normal mucosal background
lymph
simulation of a mass lesion (Fig 3). Antifungal treatment of Candida esophagitis can be effective, and complete healing without residua can result. However, com-
day.
cause
( > 2.0 cm). Al-
irregularity
mediastinal
of the
it can
loss of 10-17
(Fig 5)
necrotic
because
with
ulcer usually is isolated and often is located near the gastroesophageal junction. Typically shallow in its early stage, the CMV ulcer
sionally an isolated lesion of monilial organisms and necrotic denuded epithelium is demonstrated. Radiographic diagnosis then is more diffi-
occa-
AIDS,
rhea
Biopsy
from
but
with
follow-
In patients
to confirm esophagitis. severe ulceration is
to progress
is characteristic,
immunosuppressed
transplantation.
that
appears
volvement
were
ing organ
radio-
candidiasis.
and culture are necessary the diagnosis of herpes CMV esophagitis causes odynophagia. Discrete
demonstrated (11-13). The
is nor-
infection
plaquelike
be difficult
graphically
often
who
and there involvement
infected,
nodes,
is contiguous transmural of the esophagus. Find-
ings at barium
radiography
and CT
goesophageal similarly can
fistulas. Actinomycosis cause severe esophageal
disease
diffusely
and well (Fig
with
thickened
deep intramural as esophagoesophageal 6).
sinus
folds
tracts, as fistulas
ENTERITIS
esophagus.
spp is a small
pro-
Cryptosporidium tozoan that has to cause enteritis
been noted frequently in immunocompro-
mised
especially
AIDS
patients, (16).
was reported
Prior
to the
rarely
Figure 1. Severe Candida esophagitis. Barium esophagogram demonstrates typical findings of severe esophageal candidiasis with focal deep ulceration in the distal
those
with
epidemic,
among
patients
it
Note
the
diffusely
abnormal
background mucosa, which appears nodular and irregular due to the filling of barium among the interstices of the plaques of monilial organisms and necrotic debris. Contrast
this
with
the
typical
(CMV) ulceration noted ma! mucosal background.
cytomegalovirus
on an otherwise
November
nor-
1992
have
shotty human
retained
the
small
( < 0.5
cm),
lymph nodes of uncomplicated immunodeficiency virus (HIV)
disease.
With
long-standing
disease,
gastric, distal small bowel, and even colonic involvement can be noted. Numerous radiographic abnormalities are demonstrated in patients with AIDS who are infected with MAI. The small bowel is thought to be the portal of entry of this atypical mycobacterium. Hence, enteritis is not surprising (Fig 8). Barium radiography generally demonstrates irregular fold thickening and mild dilatation, often involving the middle and distal small bowel more than the proximal segments. Fine nodularity of the mucosa may be present. Enteritis due to MAI may be referred to as pseudo-Whipple disease because of the resemblance both histologically and radiographically. Gram-negative bacilli and material positive for periodic acidSchiff and acid-fast stain are demon-
strated Figure
2.
Gastric
candidiasis.
Barium
exami-
nation of the stomach in an elderly woman with no other cause of immunosuppression demonstrates a large penetrating ulcer (arrows) on the greater curve. Endoscopic biopsy revealed C albicans.
at biopsy
pria,
as is seen
(17).
Radiographic
demonstrates of the
small
copy,
and
of the
bowel
often
of segments
at barium
is due
pro-
disease
evaluation
separation this
lamina
in Whipple
to the
fluoros-
teric lymphadenopathy that is typical of this entity. Lymphadenopathy due to MA! may be more extensive in the mesentery than it is in the retroperitoneum (18). Enlarged lymph nodes in patients with MAI usually are small to moderate in size (1.0-1.5 cm), and
sometimes
a central
area
of low
atten-
uation will be present. One publication has noted M tuberculosis to be present more often than MA! when the enlarged nodes have central low attenuation (19). Occasionally, lymphadenopathy due to MA! can be bulky. MA! of the gastrointestinal tract typically causes enteritis. Occasionally, esophageal
ulceration
can
but colitis is uncommon. nated
MA!
scess
can
in solid
cause
be seen,
Dissemimultifocal
organs
ab-
of the abdomen.
Contrast material-enhanced CT demonstrate focal low-attenuation lesions in the liver and sometimes
spleen.
CT-guided
needle abnormal nostic.
aspiration lymph
will the
percutaneous
fine-
of such lesions or of nodes will be diag-
mesen-
COLITIS CMV
tients
in immunosuppressed
causes
colitis
more
pa-
frequently
than it does enteritis. Early disease in the colon may be notable at doublecontrast barium radiography by means of a pattern of discrete, small, well-defined nodules much like that seen with lymphoid nodular hyperplasia. However, it is present diffusely throughout the entire colon and not isolated to the right colon. Culture at
this
stage
often
will
be positive.
Mod-
erate disease is noted on the basis of diffuse superficial ulceration (aphthous lesions) on a background of otherwise normal mucosa (Fig 9). Deep ulceration is seen in more severe disease. CT at that stage will demonstrate thickening of the wall of the cecum and usually also of the terminal ileum (20). Although disease may be limited to a pattern of typhlitis, wall thickening may be present throughout the more distal colon, and sometimes the entire colon is involved. Diffuse involvement occurs in a continuous fashion, and intervening skip areas of normal colon are not seen. With bolus administration of intravenous contrast medium, enhancement of the mucosa, as well as 3.
4.
Figures 3, 4. (3) Focal esophageal candidiasis. Barium esophagogram demonstrates a single mass lesion causing a large irregular filling defect in the upper esophagus. The mucosa is norma! throughout the remainder of the esophagus. Endoscopic biopsy demonstrated a mass of monilial plaque and necrotic debris. (4) Monilial stricture of the esophagus. A long, irregular stricture of the esophagus is demonstrated at barium swallow examination in a patient with a bone marrow transplant who has been treated for severe Candida esophagitis. Vt1iim
1R
.
Miirrikcr
serosa,
may
be noted.
Often
the
thick-
ened colonic wall is abnormally low in attenuation at CT, indicating edema. Infiltration of the pericolonic fat is common at this stage, and ascites may be present. Lymphadenopa-
thy is not a predominant
feature
of .-.
CMV there
colitis. When may be focal
rhage within and edematous Occasionally, intramural ing ischemia
disease is severe, areas of hemor-
the
thickened, colonic wall with advanced
nodular, (Fig 10). disease,
air may be noted, and infarction.
indicatPlain ra-
diography of the abdomen will demonstrate findings typical of toxic megacolon, with an air-distended transverse
and
proximal
colon.
Nod-
ules of edematous mucosa, or both,
or hemorrhagic may be noted.
orrhage, colonic can be the cause with HIV disease
perforation, or both of death in patients and severe CMV
colitis. with
Diagnosis, biopsy,
which
can be made
is important
treatment
with
Hem-
because
ganciclovir
(9-[1,3-
dihydroxy-2-propoxymethyl] nine,
DHPG),
fourths
gua-
is effective
of patients
in three-
(21).
CMV
infection
been
reported
scess
in the liver.
Disseminated
is uncommon
to cause
but
has
multifocal
In a patient
ab-
with
AIDS (22), multiple small lesions of low attenuation at CT and increased echogenicity at ultrasound (US) simulated metastases radiographically. However, they were proved pathologically to be collections of intranuclear CMV inclusion bodies surrounded by inflammatory cells, hepatocellular degeneration, and focal fatty infiltration. CMV is ubiquitous among patients who have undergone organ transplantation. In this patient population, it can be associated with manifesta-
5. Figures
6. 5, 6.
(5) CMV
esophagitis.
Air-contrast
barium
esophagograms
demonstrate
isolated ulceration of the midesophagus. The remainder of the esophageal mucosa (6) Actinomycosis esophagitis. Single-contrast barium esophagogram demonstrates tramural tracts filled with barium noted diffusely throughout the esophageal wall.
a large,
is normal. deep in-
tions and radiographic appearances similar to those described in the AIDS population. In addition, CMV has been implicated in severe gastrointestinal bleeding and colonic perforation. The areas of the gut most often associ-
ated with massive gastrointestinal bleeding (often lethal) are the stomach (23,24) and the cecum (25-27). CMV
and
novirus,
other
viruses
Coxsackie can cause
such
as ade-
virus A and a debilitating
B, and
rotavirus and severe, watery, and/or hemorrhagic diarrhea. Such infections can be fatal in severely immunocompromised pa-
tients,
and
patient
this
also
Esophageal culosis has involvement
is especially
has
intestinal
disease
been
due
described
of the
colon
true
7.
herein,
the small intestine. The jejunal folds are thickened, but the ileum is featureless, demonstrating the so-called ribbon bowel. (8) MA! enteritis. Barium examination demonstrates irregular thickening of small bowel folds with some separation of bowel loops. Note also splenomegaly.
may
noted as well (28). Sometimes may be isolated to the ileocecal which will ever, there the colonic
330
the
but
be
disease valve,
appear thickened. Howmay also be thickening wall. This may be re-
stricted to the medial cum, but sometimes volve marked
if the
GVHD. to M tuber-
terminal disease,
#{149} Radiology
wall of the ceit can also in-
ileum. With the circumferential
more
of
Figures
8. 7, 8.
(7) Cryptosporidiosis.
Barium
cecum will be abnormal, and continuous involvement of the ascending colon may be seen. Frequently there is
regional lymphadenopathy, and often these lymph nodes are of decreased attenuation
at contrast-enhanced
CT
examination
demonstrates
(Fig 11). Clusters thy in the right
diffuse
abnormality
of lymphadenopalower quadrant
of
adja-
cent to a thick-walled cecum is typical of M tuberculosis in the abdomen, and
this
finding
diagnosis
helps
from
differentiate
the
CMV colitis. November
1992
with HIV to the development of clinical AIDS has increased to a current mean
of 10 years
peated spread an
(30).
In spite
predictions that of the epidemic
increased
number
ues
to be reported
rus
is transmitted
sexual contact contaminated
of re-
the rate of is declining, of cases
each
year.
largely
by
contin-
The
vi-
intimate
but also by exposure blood or bloody body
secretions.
The
homosexual nous drug previously
or bisexual men, users, and recipients unscreened blood
disease
affects
to
mainly
intraveof or blood
products. In this country, heterosexual contact has had a smaller impact on the epidemic to date, but the rate
of heterosexual creasing
sion
through
care
is rare
The
transmission
(29).
the
(32).
transmis-
delivery
of health
(31).
CD4
lymphocyte
count
as a marker of immune for HIV patients, and
nostic along
is in-
Occupational
serves
competency
it can be progregarding the patient’s status the spectrum of HIV disease
Several
opportunistic
infections
are associated tion of CD4
with the level of deplelymphocytes. For instance, oral candidiasis (thrush) and hairy leukoplakia tend to manifest when CD4 counts fall to 300-400. Pneumocystis carinii pneumonia is uncommon if the CD4 count has not dropped below 300-400, and 85% of the cases occur in patients whose CD4 count
is below
200.
Generally,
cere-
bral toxoplasmosis
Figure gram
12.
HIV
ulcer.
Barium
esophago-
of a patient with odynophagia and recent HIV seroconversion demonstrates single, large ulcer (arrow) on an otherwise normal mucosal background. Endoscopic biopsy revealed Symptoms and ously.
HIV and ulceration
no other resolved
CD4 (T helper-inducer) where it remains dormant
able Figure 11. demonstrates increased
Ileocecal tuberculosis. CT scan thickening of the cecum and attenuation
adjacent
moderate
of the
to large
central low attenuation. mass displaces anteriorly
bowel losis
in this patient and
HIV
pericecal
lymph
fat.
node
with
ileocecal
curs An
has
The inflammatory the distal small
tubercu-
period
weeks known
of time
to years. stimulus,
with
those
7_1..____
from Un-
destruction
direct network,
T...........I........
nistic the
The
like
gradually
decrease
and
infections
interval
and
from
some
dethere
tumors.
occurs
seroconversion.
seroconversion, and it has not been reported to occur more than 6 months later. Symptoms are similar to those of mononucleosis, and they may involve the gastrointestinal tract with nausea, anorexia, and sometimes diarrhea. Occasionally patients will complain of odynophagia, and this can be severe. Endoscopy or esophagography generally demonstrates discrete ulceration of the esophagus, when present (Fig 12) (33,34). A local cluster of small
de-
infection
after
of
system that to opportu-
initial
soon
This generally
in num-
unrelenting
of the immune the patient
illness
oc-
lymphocytes and infection of The CD4 lymphocytes, which many other cells in the immune
others.
pression predisposes
DISEASE
is caused by a retrovirus as HIV (29). HIV enters 1o
ranging
After an as yet viral replication
subsequent
is a profound
AIDS known
lymphocytes, for a vari-
ber, and they develop qualitative fects in function. Consequently,
disease.
HIV
organism. spontane-
occurs after the count drops below 150, and, in the gastrointestinal tract, CMV and MAI infections are seen when the CD4 count is below 100. Because the CD4 count tends to decline at an approximate rate of 10-15 cells per month, the initial episode of P carinii pneumonia can be predicted to follow the appearance of thrush or hairy leukoplakia within 6-12 months. Radiographic findings suggestive of CMV and MA! are especially reliable when the CD4 count is below 50. Long before the development of clinical AIDS, patients with early HIV disease may demonstrate a brief flu-
within
weeks
of
(0.3-1.5-cm)
ulcers
there may cm) ulcer; near
may
be seen,
trointestinal
or
be an isolated, large (2.0the latter is often located
the
gastroesophageal
ential
trointestinal
junction,
as the
complaint
occurs
within
of the
flu-like
The
Occasionally
biopsy
ulcer has and there umentation infection During
remainder
symptoms
for the
resolve
of the
and
the
to a current
mately 10 years with HIV disease
during
this
to be due few such
at biopsy
generally
(35). In a been re-
gastrointesti-
include often have
helps
are
exclude
tion.
pattern
could
mild
have
progressed
been
noted
focal
abnormalities
dilatation
and
of the
thickening
wall.
stricture ab-
MARROW
TRANSPLANTATION
AND
Bone marrow transplantation, a common procedure in many
system with
ters,
is performed
leukemia,
now cen-
for the treatment
lymphoma,
of
congenital
im-
in-
blood pain,
cell and
function
intrahepatic
of the
Pericholecystic
bile
gallblad-
fluid
As disease
may
progresses,
be
the
extrahepatic bile duct becomes dilated, and thickening of the bile duct wall may be noted. Endoscopic retro-
tation
tients
Figure onstrates
of the
ducts,
intra-
much
and
like
sclerosing
with
HIV
extrahepatic
that
seen
cholangitis.
disease
13.
AIDS cholangitis. findings
of acalculous
CT scan demcholecystitis
with thickening of the gallbladder wall and increased attenuation of the pericholecystic fat. Additionally, the adjacent duodenal wall and the gastric antral wall are thickened. Endoscopic biopsy was diagnostic for CMV gastritis and duodenitis, and bile aspirate was positive for CMV.
cholangiography demonstrates of irregular stricturing and dila-
primary
dem-
biliary
of liver
duct
intrahepatic
BONE
AIDS.
typically
results
present.
bile hy-
imaging
abnormal
with Pa-
frequently
findings.
H!V disease
with
is a
thickening,
since clinical
bile
associated
normality.
spp the mid 1980s in AIDS (36-39).
presentation
grade areas
infecthere
extrahepatic
without
stenosis,
tests. Elevation of the serum alkaline phosphatase level can be marked (up to 25 times the normal level). Early abnormalities at CT and US include
der
this
papillary
GVHD
fever, elevated white right upper quadrant
ducts
to associated
Colon
no
Patients
fold
be due
poalbuminemia. onstrates
and
however,
of very
which
normal,
of the
with
mild
diara
an opportunistic
Occasionally,
long
to
of clinical
due to opportunistic infection CMV (Fig 13) or Cryptosporidium
abnormal
marked wasting syndrome. Disease is chronic, and symptoms may be unrelenting or intermittent. Results of radiographic evaluation of the small bowel
first
demonstrate
CHOLANGITIS
Inflammation
cludes count,
it is thought
of the
nal tract. Complaints rhea, and patients
and this combination of findings is the most common pattern seen in AIDS cholangitis (40). Less frequently, radiographic evaluation will demonstrate isolated papillary stenosis or a
should
to be the
AIDS
Clinical
patients enteritis
to the HIV directly patients, HIV has
covered
also
even in patients to be at high
the diagnosis
patients
of approxi-
(30). Many develop
and
radiologist
has been noted
development
mean
period,
differgas-
esophageal
of clinical AIDS, patients are free of documented opportunistic infection or malignancy. This interval has in-
creased
abnormalities
suggest
also.
demonstrated H!V directly, has been an absence of docof other opportunistic or tumor during this illness. the long interval between
seroconversion
the
risk. Because of the gastrointestinal pattern of multifocal abnormalities and the typical findings associated with the opportunistic infections as described above, it is not uncommon
of odynophagia,
weeks.
Hence, of multifocal
include clinical AIDS, not thought previously
much like that seen with CMV esophagitis. The remainder of the esophageal mucosa is normal. Spontaneous resolution of endoscopic and radiographic evidence of ulceration, as well
tract.
diagnosis
who
to clinical
frequently
AIDS
to have
have
multi-
of the
gastrointes65% of are referred for have abnormali-
final tract. Approximately AIDS patients who barium radiography
ties
in three
or more
sites
per or lower gastrointestinal with intervening normal Multiple sites of pathologic
ity can ple
be due
concurrent
enteritis, graphic volvement infection
as CMV stomach,
AIDS
may
MA!
esophagitis,
#{149} Radiology
such
of the esophagus, colon. Some patients
have been opportunistic
frequently
in-
have
CMV colitis. Or radioof multiple sites of in-
ulceration and/or
and AIDS-related Kaposi sarcoma
332
multi-
For
of a single opportunistic may be demonstrated,
with AIDS coexistent
which
with
herpes
and signs
with
organisms.
a patient
up-
tract areas (14). abnormal-
to infection
opportunistic
stance,
of their
a.
noted to have infection(s)
malignancy, or lymphoma, involve
such both the
gas-
as of
b.
Figure 14. GVHD. (a) Barium demonstrates diffuse thickening folds but “ribbon bowel” effect
with some
GVHD
demonstrates
small bowel of jejunal in multiple
prominent
examination folds. heal areas due
irregular
of a child with severe acute GVHD abnormality includes.thickening of some to fold effacement. (b) Image of an adult
fold thickening
of jejunal
and ileal folds
with
nodularity.
November
1992
munologic defects, aplastic anemia, metabolic disorders of the hematopoietic system, and some metastatic diseases (eg, metastases from breast cancer). Superinfection with opportunistic organisms is one of the common problems associated with bone marrow transplantation (41-44) because the recipient’s immune system first must be destroyed. Infection with bacteria and Candida albicans predominates during the chemotherapy or radiation therapy regimen that occurs prior to the transplantation. However, during the 2-4 weeks following marrow infusion, these infections often are accompanied by herpes virus infection. One to 3 months after transplantation, patients are particularly
susceptible to invasive fungal infections and to CMV infection. Other viruses such as varicella-zoster virus, Epstein-Barr virus, hepatitis viruses, rotavirus, adenovirus and Coxsackie virus also may cause problems. The abnormal immune regulation persists for many months, leaving the patient at risk for infection with varicellazoster virus, P carinii, and encapsulated organisms such as pneumococcus. During the period of re-emerging immune competence, superinfection with opportunistic organisms such as CMV,
Coxsackie
virus
A or B, ade-
novirus, or rotavirus can result in profuse bloody diarrhea with rapid clinical deterioration and high mortality. Although they are difficult to treat, these viruses can be diagnosed by means of enzyme-linked immunosorbent assay (ELISA) of the infected stool. Laboratory diagnosis is important because viral gastritis, enteritis, and colitis may mimic an entirely different gastrointestinal complication that sometimes follows bone marrow transplantation, namely, GVHD. GVHD
occurs
when
the
can
sometimes the major GVHD
(52).
b. 15.
GVHD
and
enterovirus
infec-
tion. (a) A follow-up radiograph taken 24 hours after a small bowel series demonstrates prolonged retention of contrast material in an atonic stomach, as well as abnormal small bowel loops in the right lower quadrant. (Reprinted, with permission, from reference 54.)
(b) CT
scan
obtained
an intraabdominal normal coating
the
of contrast
bowel tracks
lumen in cross in longitudinal 1o
same
day
to exclude
abscess demonstrates abof small bowel loops with
circles
7_1____
acute
is the
or chronic,
forms organs
small
and
occur. One of acute
bowel,
with
of
devel-
opment of severe mucosal inflammation and profuse secretory diarrhea (45-51). Differentiation from viral superinfection is important because treatment of acute GVHD involves use of immunosuppressive agents that would further depress the host defenses and cause exacerbation of an unrecognized opportunistic infection. Furthermore, untreated acute GVHD worsens the host susceptibility to viral gastrointestinal infection because of the impaired intestinal immunity that results from mucosal and submucosal denudation of the intestinal surface
a.
Figure
be
both target
material
T__1___
adherent
section section.
and
to the
parallel
Hence,
their
similar
as well
radiographic
manifestations dictate laboratory evaluation with ELISA of the patient’s stool. The similarities of GVHD and viral superinfection are not limited to the small intestine but also can affect the duodenum and colon (53). For instance, in the duodenum and the small bowel (Fig 14), both processes can produce a shaggy fold thickening or fold effacement with a tubular appearance. In the colon as well, haustral enlargement or effacement can occur. Colonic spasm, ulceration, or a granular mucosal pattern that simu-
as viral
infection,
in four
of 28
patients studied previously (54). This coating resembled a “cast” of the small intestine on follow-up plain radiographs, and it persisted for more than 48 hours in one patient. This appearance was restricted to patients who had undergone bone marrow transplantation. Each patient had Severe mucosal disease with subsequent sloughing of mucosa and pseudomembrane in the stool. The cause of the prolonged coating is speculative. Possibly the barium adheres to the mucosa or the raw surface of the submucosa or to the pseudomembranes, or it is trapped between sheets of sloughed mucosa and the residual lining of the intestine. At CT, the prolonged coating appears as circular collections of contrast material in
cross
section
gitudinal ings
immune-
competent graft reacts against the immune-incompetent host (which was made so by the pretransplantation immune-suppressive conditioning). GVHD
lates ulcerative colitis can be noted in both entities. In addition, an unusual appearance of the small bowel due to a prolonged coating pattern (Fig 15) has been reported with acute GVHD,
or parallel
section
in acute
tracks
(54).
GVHD
Other and/or
in lonCT findviral
in-
fection include wall thickening sometimes associated with pericolic inflammation, a “halo sign” of mural low attenuation suggesting submucosal edema, mesenteric thickening, and small mesenteric lymph nodes. When viral superinfection is present or is coexistent with GVHD, gastric abnormalities may be seen including prolonged coating, dilatation, atony, delayed emptying, and antral deformity. However, gastric abnormalities have not been reported in GVHD alone. The early observations of acute GVHD
reported
effacement
of small
bowel folds (“ribbon bowel”) or fold thickening with predominant involvement of the jejunum. The characteristic featureless or tubular nature of the small bowel seen with fold effacement was thought originally to be pathognomonic
of acute
59). However,
GVHD
(55-
“ribbon bowel” can occur in multiple clinical conditions including infections, effects of irradiation, allergy, ischemia, injury from corrosive
the
ingestion
or medications,
amyloid, mastocytosis, lymphoma, pseudolymphoma, even Crohn disease, and of course celiac disease (54,60). The chronic form of GVHD can de-
velop following
acute
exist coincidentally or it can occur in never had acute velop as early as transplantation.
with acute GVHD, a patient who has GVHD. It can de45-50 days after The target organs
GVHD,
it can
and their responses in chronic are somewhat different from
lion
GVHD those in
acute GVHD. Although the skin is affected in both, a rash predominates in the acute form and in the chronic form the disturbance more closely resembles that seen in patients with scleroderma who have pigmented, dry, tight skin. The major gastrointestinal tract organ affected in chronic GVHD
(10%
of patients)
is the
medical
of fibrotic
strictures.
marrow
transplant
chronic
diarrhea
that
chronic
infection
or malabsorption.
OTHER
recipients
appendix,
and
some-
times
also
terminal
ileum.
The
term
comes
from
the
for “blind
as the “ileocecal
Greek
sac.”
(62) or
kemia
or lymphomatous
anemia,
may
and by leu-
in nine
folds,
produce
folds
simulating
(69-72). edema
tracts
dude
CT is the
preferable
examination. Findings cecal and terminal ileal
thickening, tenuation
Pericolonic
mens
often with decreased atsuggesting edema (64,65). inflammation may be
demonstrated by increased tion of the adjacent fat and of fascial planes. Pericolonic be noted,
continues our use
inwall
as well
and
intravenous
development more effective and mortality
334
Radio1otv
#{149}
fluids
of transmural
prior
and
defects
Also,
the AIDS
transplant
epidemic
can
Recognition
attempting
to differentiate
pathogens, trointestinal
as well as other complications.
Troupin
RH.
Intramural and
is
We
sincerely
di-
AJR 1968;
104:
AJ, Hulnick
EJ, Megibow
in 16 patients.
D, Cho
1987;
149:919-923.
in AIDS. AJR 1985; 144:1201-1204. Wilcox CM, Diehl DL, Cello JP, Marga-
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ME, Robbins
avium-intracellulare
18.
19.
AH. Mycobacterium complex enteritis: pseudisease in AIDS. AJR 1985;
do-Whipple’s 144:921-922. Nyberg DA, Federle MP,Jeffrey RB, Bottles D, Wofsy CB. Abdominal CT findings of disseminated Mycobacterium avium-intracellulare in AIDS. AJR 1985; 145:297-299. Radin DR. Intraabdominal Mycobacterium tuberculosis vs. Mycobacterium avium-intracellulare infections in patients with AIDS: dixtinction based on CT findings. AIR 1991; 156:487-491.
20.
Balthazar
ulencia
of
colitis
21.
Jones
EJ, Megibow
JF, Engel in AIDS:
patients.
specific
AIR
Balthazar EJ, Megibow AJ, Hulnick DH. Cytomegalovirus esophagitis and gastritis
143:549-554.
17.
when
E, Dsop-
Cytomegalovirus
radiographic
Radiology B, Fishman
AJ, Fazzini
DI.
findings
a
22.
Vieco
PT, Rochon
sions
Emil
Balthazar, MD, for his gracious contribution of several figures, as well as Francine Martin and Fay R. Cromer for their assistance with manuscript preparation.
23.
simulating
in 11
1985; 155:585-589. EK.
CT of the
gut
immunocompromised host. Radiol North Am 1989; 27:763-771.
gas-
thank
diag-
esophageal
moniliasis.
L, Lisbona
cal cytomegalovirus-associated Acknowledgments:
Candida
Balthazar
persists.
be helpful
I.
11.
rejecdisease.
imagers can expect radiographic abnorherein with in-
frequency. patterns
with regi-
autoimmune
PJ, Laufer
MS. Herpes healthy patients: findings. Radiol-
of pa-
immune
organ
cancer,
these
to the
necrosis in lowering morbidity than is surgical resec-
to treat
tion,
creasing
and
sometimes increased attenuation of the thickened gut wall when intramural hemorrhage is present. Early diagnosis and prompt, aggressive medical support with high doses of antibiotics
continue to for sev-
population
MS. Macones
Radiology
Shortsleeve MJ, Levine esophagitis in otherwise clinical and radiographic ogy 1992; 182:859-861.
16.
to expand, concurrent of immunosuppressive
Hence, abdominal to encounter the malities discussed
attenuathickening fluid may
as pneumotosis
The
acquired
diagnosis.
H, in
613-616.
(73).
hanced
with
Levine
R, Herlinger esophagitis
10.
14.
tients
reasons.
radiographic 165:815-820.
verticulosis
ap-
can progress rapidly to transmural necrosis with subsequent perforation and a high mortality rate. Because of the risk of perforation associated with fluoroscopic contrast material-enstudies,
9.
13.
CONCLUSION
eral
MS, Woldenberg I. Opportunistic
esophagitis: accuracy of radiographic nosis. Radiology 1985; 154:581-587.
12.
of barium thickened
with immunosuppression become more commonplace
10:621-634.
SKC, Beranbaum E. Cytomegalovirus esophagitis in AIDS: radiographic features
In summary, pathologic conditions of the gastrointestinal tract associated
imaging
8.
15.
without process
Levine Laufer AIDS: 1987;
perico-
intramural
1990;
Frager DH, Frager DJD, Brandt U, et a!. Gastrointestinal complications of AIDS: radiologic features. Radiology 1986; 158: 597-603.
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poly-
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6.
folds
minimal
with tracking the markedly
5.
with
eccentric prominent
and
3.
radio-
patients
haustral
wall thickening, wall thickening,
2.
4.
colitis following
of the
pearance, between
infiltrates,
because inflammatory
plain
lonic inflammatory changes Marked fold thickening and
ischemia, focal pseudomembranous colitis, or infection-usually CMV (personal observation). Early diagnosis is important, treatment the
necrosis
Gastrointestinal
immunocompromised host. Clin North Am 1992; 30:555-577.
resection.
colitis can de-
The
findings
haustral
(63). Howto occur
also in patients with aplastic lymphoma, renal transplantation, clinical AIDS. It can be caused
need
vancomycin.
bowel poid
“neutropenic colitis,” it was described initially in children with leukemia and severe neutropenia ever, it is now recognized
air indicating for surgical
the
B, Wall SD.
in the
ef-
(67,68). Findings on contrast-enhanced studies include fold thickening, mucosal edema, and plaquelike lesions. CT findings include diffuse
known
syndrome”
when
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