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Review Article
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The gastrointestinal manifestations of AIDS in children are sons, 2 million of them children, may be infected with HIV [2].
related to opportunistic infections, lymphoproliferative disease, That projection is based on the spread of HIV among women
and cancer. The infections that affect the gastrointestinal tract at of childbearing age who use injectable drugs and become
different sites also occur in patients without AIDS. However, in
infected via contaminated needles or who acquire the virus
children with AIDS, the infections are more severe, often relapse,
from infected sex partners. They then transmit HIV vertically
and are harder to eradicate. Candidiasis is the most common
to the fetus. This mode of transmission and the immaturity of
infection in the esophagus, but infections caused by herpes sim-
plex virus and cytomegalovirus also are common. Radiologic the infant’s immune system alter the natural history of HIV
findings include ulcerations, a cobblestone appearance, and dis- disease and affect medical management [3-6].
ordered motility. Gastritis and enteritis are usually caused by Gastrointestinal symptoms, caused primarily by opportu-
cytomegalovirus. Lesions produced by this virus include ulcer- nistic entenic infections and lymphoproliferative and neoplas-
ations caused by ischemic necrosis as a result of vasculitis. Bar- tic diseases, occur in approximately half of the patients in
ium studies show increased nodularity and effacement of the United States and Europe who have AIDS. In children,
mucosa. Other organisms (typically found in all immunocompro- gastrointestinal dysfunction may be related to HIV replication
mised patients) include Mycobacterium avium-intracellulare,
in cells of the gastrointestinal tract, malabsorption of nutri-
Mycobacterium tuberculosis, Campylobacter, Giardia, and
ents, and intolerance to lactose and other disaccharides [7-
Cryptosporidium. Colitis and proctitis are caused by many of the
9]. Failure to thrive and wasting occur in 16-25% of children
same enteric pathogens. Cytomegalovirus is the most virulent,
causing necrosis, perforation, and often death. Lymphoma, who have AIDS. Possible reasons for this include poor
smooth muscle tumors, and Kaposi’s sarcoma are the most caloric intake, malabsorption, and recurrent gastrointestinal
common neoplasms encountered in children with AIDS. infections, specifically in the small intestine and colon [10].
The most common portal of entry for HIV in adolescents
who abuse drugs and in children born to HIV-infected moth-
The number of patients with AIDS continues to increase ens is direct introduction of the virus into the bloodstream.
annually. In the United States, the disease is now growing This route differs from that in most homosexuals and bisexu-
more rapidly among children than among adults. Between als, in whom the virus enters the host’s rectal mucosa
the beginning of 1988 and the end of 1989, the number of through membrane cells present throughout the intestinal
cases of AIDS in infants and children reported to the Centers tract [11]. These cells then deliver the virus to the lymphatic
for Disease Control and Prevention more than doubled, from lymphoid aggregates [12]. Regardless of the route of trans-
about 800 to nearly 2000 [1]. The World Health Organization mission, the virus ultimately binds to the CD4 molecule on
predicts that by the year 2000 as many as 40 million per- the T cell on to mononuclear cells, which deliver the virus to
Received August 16, 1993: accepted after revision September 29, 1993.
Presented in part at the annual meeting of the Society for Pediatric Radiology, Seattle, May 1993.
1 Both authors: Department of Radiology, State University of New York Health Science Center at Brooklyn (Downstate Medical Center), 450 Clarkson Ave. , Box
1208, Brooklyn, NY 11203. Address correspondence to J. 0. Hatter.
AJR 1994;162:387-393 0361-803X/94/1622-0387 © American Roentgen Ray Society
388 HALLER AND COHEN AJR:162, February 1994
the circulation and ultimately back to the lamina propnia of Fig. 1.-Esophageal candidi-
asis in a child with AIDS. An-
the gastrointestinal tract. Several days to weeks later, the
teroposterior radiograph of
patient will experience a mononucleosis type of illness. This barium-filled esophagus on bar-
will include gastrointestinal signs and symptoms: diarrhea, ium examination shows multi-
pie irregularities along entire
nausea, vomiting, and anorexia. As HIV both impairs and
esophagus. Note shaggy or
destroys CD4 and other T cells, the immune response of the cobblestone appearance with
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Esophagus
The most frequent signs and symptoms of esophageal
involvement in children with AIDS are odynophagia and dys-
phagia. The most common causative organism is Candida
albiCans. Next most common, in order, are CMV and herpes
simplex virus [14, 15]. Ten percent of all children currently
being followed up in New York City because of AIDS have
Candida infections. In two independent studies [16, 1 7], Can-
dida esophagitis was associated with survival of less than 1
year. Although double-contrast esophagognams are probably Fig. 2.-Cytomegalovirus in-
better than single-contrast studies for detecting the fine fection of esophagus in a 1-year-
old boy with AIDS. Radiograph
mucosal lesions in Candida esophagitis, these studies are from barium examination shows
not always practical in children [18]. Barium examinations a single ulcer (arrow) on left hat-
show edema of the mucosa, which leads to plaque formation eral aspect of distal part of
esophagus. Remainder of esoph-
and eventually deep ulcerations. On barium examinations, a agus appears normal. Examina-
shaggy or cobblestone appearance is seen as barium fills tion of biopsy specimen obtained
at esophagoscopy showed cy-
the interstices among irregular plaques of monilial colonies
tomegalovirus inclusion bodies.
and necrotic debris (Fig. 1). Pseudodiverticula are also seen
[19]. Nystatin has not been effective in treating children with
Candida esophagitis. Greater success has been achieved
with ketoconazole or with IV ethyltenizine [20]. Candida infec- thickening, a cobblestone appearance, pseudodiverticula, and
tion tends to involve the entire esophagus, whereas CMV strictures.CT of an esophagus with either Candida or CMV
infection tends to involve a focal portion, usually the distal shows thickening of the wail, and mucus and food particles
end[21, 22]. are seen proximally because of the more distal obstruction
CMV infects the endothelial cells of the capillaries of the (Fig. 3).
entenic mucosa. This causes a vasculitis that will lead to Herpes simplex virus usually causes focal involvement in
ischemic necrosis and ulceration of the esophagus. Barium the esophagus, with shallow ulcers. The ulcers are often dia-
studies may show large ulcers in an otherwise normal esoph- mond shaped or stellate [19, 22]. Infection with herpes sim-
agus [19] (Fig. 2). Other findings include linear ulcers, nodular plex virus has less of a propensity for forming linear or
AJR:162, February 1994 GASTROINTESTINAL MANIFESTATIONS OF AIDS IN CHILDREN 389
longitudinal ulceration. Treatment with acyclovin has been caused by Epstein-Barr virus, lymphocytes, mainly CD8
successful in some patients with herpetic lesions [1 9, 20]. cells, are recruited to various organ systems in the body
Mycobacterium tuberculosis often involves the esophagus (e.g., lung, parotid gland, lymph nodes, kidneys, breast, and
by tnansmural inflammation from infected and often necrotic gastrointestinal tract) as a host response to either the
mediastinal lymph nodes, with associated fistulas and for- Epstein-Barr virus on the HIV infection. Invariably the child
mation of sinus tracts [23-25]. expresses the immunophenotype HLA-DR5. It is thought
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Fig. 3.-Esophageal candidiasis. CT scan of Fig. 4.-Aphthous ulcers of stomach caused Fig. 5.-Gut-associated lymphoid tissue in a 4-
mid esophagus at level of carina shows a thick- by cytomegalovirus in a 6-year-old boy with year-old girl with AIDS. Right anterior oblique ma-
walled esophagus. CT was performed because AIDS. Anteroposterior radiograph of barium- diograph of barium-filled stomach on barium cx-
of incidental pulmonary disease. Results of bi- filled stomach on barium examination shows amination shows markedly thickened folds in
opsy showed typical findings of candidiasis. tiny filling defects (arrows) along anterior wall antrum and fundus of stomach. Examination of
of antrum. Results of biopsy were consistent biopsy specimen showed lymphoid infiltration of
with cytomegalovirus infection. stomach and Epstein-Barr virus.
390 HALLER AND COHEN AJR:162, February 1994
Radiologic features of Cryptosporidium in the small intes- intracellulare infections. This distinction is not a reliable mdi-
tine include thick folds (Figs. 6 and 7), fragmentation of bar- cator in M. tuberculosis infections in children [47].
ium, intestinal spasm, and dilatation. The proximal part of Danin et al. [48] stressed that although infectious complica-
the small intestine is involved most frequently [42-45]. tions occur frequently in patients with AIDS, bowel obstruction
Mucosal atrophy, causing a “toothpaste” appearance of the due directly to an AIDS-related disease is rare. Intussuscep-
barium similar to that described in graft-vs-host reaction tion can be manifested as obstruction caused by a lym-
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(Fig. 8), can also occur [45]. Nodes are rarely involved. Gian- phomatous mass as the lead point [48, 49]. The plain film,
diasis, strongyloidiasis, candidiasis, and gut-associated lym- sonographic, and CT findings of intussusception are well rec-
phoid tissue must also be considered. ognized, and a lead point should be sought, especially in chil-
CMV also causes entenitis; however, the radiologic find- dren who test seropositive for HIV [50-53].
ings are usually more severe than those described thus far.
CMV causes a vasculitis by invading the endotheliai cells of
Colon and Rectum
the small blood vessels in the bowel wall. Examination of
biopsy specimens will show inclusion bodies in vessel walls. Although Shigella and Salmonella are pathogens that fre-
The vasculitis leads to ischemic necrosis and perforation. quently involve the colon, CMV infection appears to be the
Radiographically, this is evidenced by pneumatosis intesti- most devastating infection of the colon in children with AIDS.
nalis and even free air in the penitoneum [25, 41]. CMV infection causes numerous bowel movements (up to
When M. avium-intracellulare is present it can cause a 30 per day) that are often associated with incontinence,
pseudo-Whipple-like condition, with fine nodulanity and cramps, fever, weight loss, and debilitation [39]. CMV has
thickening of folds that are readily recognized on CT scans also been blamed for most of the colonic complications
and upper gastrointestinal series. These lesions usually described in children with AIDS (e.g., typhlitis, pneumatosis,
involve the middle and distal parts of the small intestine, pseudomembranous colitis, strictures, and frank perforation)
whereas in cryptosponidiosis, the lesions usually involve the [1 9, 26, 27, 42]. CMV infections involve the colon much
proximal part of the small bowel. M. avium-intracellulare more often than the small intestine [1 9]. In cases of mild
infection is often associated with lesions in the liver and infection, nadiologic findings include thick folds, mucosal
spleen, and mesentenic and retropenitoneal lymph nodes granularity, spasm (especially of the cecum), and ulcerations
may be enlarged [26, 46]. These large lymph nodes are a (superficial, deep, linear, and aphthous) (Fig. 10). In severe
hallmark of M. avium-intracellulare infection (as a differenti- infections, findings include large ulcers, strictures, nodular
ating feature from CMV infection) (Fig. 9). Examination of filling defects (pseudomembranes), and submucosal hemor-
biopsy specimens shows the mycobactenia in the lamina rhage [24-26]. The abnormalities may involve the entire
propnia of the small intestine. When lymph nodes are colon or a segment. The cecum alone may be the only area
involved, a central area of low attenuation in the nodes may affected. CT scans show thickening of the bowel wall, or a
be seen, representing necrosis. This finding is frequently target sign on double ring sign representing mucosal edema
noted in adults with M. tuberculosis as opposed to M. avium- (Fig. 11). Severe cases of CMV colitis can result in toxic
Fig. 6.-Cryptosporidium infection of duodenum Fig. 7.-Cryptosporidium infection of the small Fig. 8.-Cryptosporidium infection
in a 4-year-old boy with AIDS. Anteroposterior radio- bowel in a child with AIDS. Anteroposterior radio- of small intestine in a child with AIDS.
graph of barium-filled duodenum and proximal part graph of barium-filled stomach, duodenum, and je- Radiograph from upper gastrointestinal
of jejunum on barium study shows thickened folds junum on barium study shows jejunum and proximal series with small-bowel follow-through
throughout. Results of biopsy confirmed diagnosis part of ileum have typical stacked coin appearance shows fragmentation of barium, with a
of cryptosporidiosis. with thickened folds. Results of biopsy confirmed di- toothpaste appearance of barium in mid
agnosis of cryptosporidiosis. ileum. Results of biopsy were consis-
tent with cryptosporidiosis.
AJR:162, February 1994 GASTROINTESTINAL MANIFESTATIONS OF AIDS IN CHILDREN 391
Fig. 9.-Mycobacterium avium-intracellulare in a 3-year-old boy with Lymph Nodes and Abdominal Cavity
AIDS. CT scan of abdomen shows a large midabdominal mass with areas
of low attenuation consistent with lymph nodes. At biopsy, lymph nodes In adults with malignant tumors of the gastrointestinal
contained M. avium-intracellulare. tract, Kaposi’s sarcoma is the most common cause. Lym-
phoma is usually second, and smooth muscle tumors are
third [55]. In children, however, cases of lymphoma outnum-
megacolon, perforation, and even peritonitis and death. Pen- ben cases of Kaposi’s sarcoma. Lymphoma is usually the B-
tonitis is rare in children as compared with adults [36, 42]. cell non-Hodgkin’s type. It is intraabdominal in about two
The typhlitislike picture noted in CMV infection (i.e., thirds of patients, and about half of these cases involve the
inflammation of the cecum and ileum) (Fig. 12) appears as gastrointestinal tract [55]. Other sites of involvement, in
thickening of the ileal and cecal walls, edema, penicolonic decreasing frequency, include the liven, adrenal glands,
inflammation, and, rarely, pneumatosis. Penicolonic fluid and lower genitouninary tract, spleen, peritoneum, omentum, and
hemorrhage also are found. Infection with M. avium-intracel- pancreas [55, 56].
lulare and M. tuberculosis can also involve the cecum; how- Imaging studies in lymphoma show enlarged lymph nodes.
ever, clusters of penicecal nodes are typical with these These nodes can involve the entire abdominal cavity (dia-
organisms [19, 36, 49]. phragm to aortic bifurcation), the pelvis alone, or individual
The definitive diagnosis of CMV infection is made by visu- organs (Fig. 13). These nodes can have central areas of low
alization of characteristic inclusion bodies in tissue obtained density, suggesting necrosis. The liver and spleen show focal
by biopsy of the colonic or rectal mucosa. Treatment has lesions that are usually low density and more than 2 cm in
been attempted with ganciciovir with only spotty success. diameter. The degree of hepatosplenomegaly is variable.
Fig. 10.-Cytomegalovirus colitis in an infant Fig. 11.-Cytomegalovirus colitis in an 8- Fig. 12.-Typhhitis in a 6-year-old boy with
boy with AIDS. Anteroposterior radiograph year-old girl with AIDS. CT scan of lower part of AIDS. CT scan of lower part of abdomen shows
from a barium enema shows marked narrowing abdomen shows thick-walled rectum and sig- thickening in region of cecum and terminal ile-
and irregularity in sigmoid colon. Child had ob- mold colon. Results of biopsy were consistent um. Note absence of enlarged lymph nodes. Ex-
struction; cytomegalovirus colitis was noted at with cytomegalovirus colitis. amination of a specimen obtained during
surgery. surgery showed cytomegalovirus infection of
cecum.
392 HALLER AND COHEN AJR:162, February 1994
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