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-

retten W, Jacobson MA. Cytomegalovirus esophagitis in patients with AIDS. Ann Intern Med 1990; 113:589-593. Wall SD, Ominsky 5, Altman DF, et al. Multifocal abnormalities of the gastrointestinal tract in AIDS. AJR 1986; 146:1-5. de Silva R, Stoopack PM, Raufman JP. Esophageal fistulas associated with mycobacterial infection in patients at risk for AIDS. Radiology 1990; 175:449-453. Berk RN, Wall SD, McArdle CB, et a!. Cryptosporidiosis of the stomach and small intestine in patients with AIDS. AJR 1984; Vincent

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.

7.

poly-

an “accordionlike”

disease Radiol

Wall SD. Abdominal radiology of acquired immunodeficiency syndrome. Contemp Diagn Radiol 1986; 9:1-b. Jeffrey RB Jr, Nyberg DA, Bottles K, et al. Abdominal CT in acquired immunodeficiency syndrome. AJR 1986; 146:7-13. Federle MP. A radiologist looks at AIDS: imaging evaluation based on symptom complexes. Radiology 1988; 166:553-562. Kuhlman JE, Fishman EK. Acute abdomen in AIDS: CT diagnosis and triage. RadioGraphics

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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