DOI:10.2214/AJR.05.0213
AJR 2006; 186:1300-1303
© American Roentgen Ray Society
Acute Schistosomiasis in Nonimmune Travelers: Chest CT Findings in 10 Patients
Lam-Quynh Nguyen1,
Jeannelyn Estrella1,
Elizabeth A. Jett1,
Eduardo L. Grunvald2,
Laura Nicholson2 and
David L. Levin1
1 Department of Radiology, University of California, San Diego Medical Center,
Mail Code 8756, 200 W. Arbor Dr., San Diego, CA 92103.
2 Department of Medicine, University of California, San Diego Medical Center,
San Diego, CA 92103.
Received February 8, 2005;
accepted after revision March 22, 2005.
Address correspondence to D. L. Levin
(dlevin{at}ucsd.edu).
Abstract
OBJECTIVE. We describe the findings of unenhanced chest CT in 10
patients with acute schistosomiasis.
CONCLUSION. Despite the absence of pulmonary symptoms in four
individuals, all patients had parenchymal abnormalities. Small pulmonary
nodules were the most common finding, identified in nine patients. These
nodules ranged in size from 2 to 5 mm in five patients, with larger nodules
ranging up to 15 mm seen in four patients. In one patient, the only
parenchymal abnormality was a single 5-mm focus of ground-glass attenuation.
No relationship was seen between either the presence of pulmonary symptoms or
the presence of peripheral eosinophilia and the severity of parenchymal
disease. No additional significant findings were identified.
Keywords: chest • CT • infectious diseases • lung diseases • schistosomiasis
Introduction
Schistosomiasis is a helminthic infection endemic to tropical and
subtropical regions. The infection is common in parts of Africa, South
America, the Middle East, the Caribbean, and Asia and is a leading cause of
morbidity and mortality in these areas
[1]. In individuals within
these regions, chronic complications most often develop from progressive and
recurrent infection. In the lungs, granuloma formation and fibrosis around the
Schistosoma eggs retained in the pulmonary vasculature may result in
an obliterative arteriolitis and pulmonary hypertension
[2]. Acute schistosomiasis is
associated with primary exposure and is more commonly seen in individuals
traveling through endemic regions
[3]. The clinical presentation
of acute schistosomiasis varies widely, but most individuals are asymptomatic
[4]. Katayama fever, an acute
febrile episode, may be seen approximately 3-8 weeks after the initial
infection. In addition to fever and chills, arthralgia, nausea, headache,
diarrhea, hepatosplenomegaly, and marked eosinophilia may be present. The
pulmonary symptoms of coughing and wheezing are variably reported and are more
commonly associated with S. mansoni or S. japonicum
infection [2].
The radiographic findings of patients with confirmed, or probable,
pulmonary involvement from acute schistosomal infection have been documented
previously in case reports
[4-9].
Nearly all these reported cases occurred in patients with acute pulmonary
symptoms. Chest radiographs typically showed ill-defined pulmonary nodules.
Chest CT studies also were obtained for a few of these cases. These studies
typically showed poorly defined nodules, often with a surrounding ground-glass
halo. A primarily peribronchovascular distribution was reported for one
patient [9]. A pattern of
bilateral diffuse ground-glass opacity with ill-defined nodules was reported
for another patient [8]. Patchy
infiltrates involving the left lower lobe and right middle lobe or dense
consolidation involving the right middle lobe was reported for two additional
patients [5]. In two patients,
radiographic abnormalities appeared only after the initiation of therapy with
praziquantel [8].
In this report, we describe the chest CT findings of a cohort of 10
nonimmune patients with documented acute schistosomiasis resulting from a
simultaneous exposure. In contrast to previous studies, four of the patients
in this study had no pulmonary symptoms and four additional patients had only
minor pulmonary symptoms.
Subjects and Methods
Patient Data
A group of 14 individuals lived and traveled within Tanzania for
approximately 2 months. All the individuals swam in Lake Victoria during their
visit—a region strongly associated with both S. mansoni and
S. haematobium infection
[10]. The first patient came
to medical attention approximately 2 months after his return to the United
States, when he presented with intermittent high fever, chills, diarrhea,
vomiting, anorexia, fatigue, headaches, dry cough, and a 20-lb (9.1-kg) weight
loss. His laboratory results were significant for a WBC of 16,600 with 42%
eosinophils. The findings of an initial, extensive, microbiologic examination
were negative. The patient's initial chest radiographs showed abnormal
findings (Fig. 1A), prompting
further evaluation with CT. A screening enzyme-linked immunosorbent assay done
at the Centers for Disease Control and Prevention was subsequently positive
for antischistosomal antibodies. The diagnosis of S. mansoni
infection was confirmed with a species-specific immunoblot. Given their risk
for schistosomiasis, the remaining members of the group underwent serologic
testing at the Centers for Disease Control and Prevention regardless of
clinical presentation.
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Fig. 1B —19-year-old man with acute schistosomiasis. CT image shows multiple
pulmonary nodules (arrows) with ground-glass halos bilaterally. In
addition, region of geographic ground-glass attenuation (arrowheads)
is present within right lower lobe.
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Our study group consisted of 10 of these 14 individuals. The other four
individuals were unavailable for study for logistic reasons, either because
they lived outside San Diego or because they declined CT evaluation. At the
time of imaging, eight of the patients had peripheral eosinophilia (range,
6-67%). The other two patients had an eosinophil count of 4% (upper limit of
normal, 5%). All patients had S. mansoni infection, which had been
confirmed using enzyme-linked immunosorbent assay antischistosomal antibody
screening and species-specific immunoblot. All patients were negative for
S. haematobium infection. In addition, two patients had serology
findings positive for filariasis, which likely represented a cross reaction
with Schistosoma antigen
[11]. One patient had serology
findings positive for Entamoeba histolytica. The findings of all
other microbiologic studies were negative. Specifically, all patients had
serology findings negative for coccidiomycosis. Eight of the patients were
between 19 and 23 years old (five women and three men). One man and one woman
were 50 and 47 years old, respectively. Three of the patients had significant
pulmonary symptoms, three had mild pulmonary symptoms, and four had no
pulmonary symptoms. For six of the patients, the CT examination preceded the
start of therapy. Patient details are summarized in
Table 1.
Image Acquisition and Analysis
All subjects were imaged using an MDCT scanner (LightSpeed Plus 4i, GE
Healthcare). All studies were performed without IV contrast medium. Images
were obtained from the thoracic inlet through the upper abdomen using a 5-mm
slice thickness. A variable-amperage option was used (Smart mA, GE Healthcare)
to minimize dose (range, 127-390 mAs). The studies were reviewed on a
dedicated PACS workstation by two thoracic radiologists. The character,
extent, and distribution of parenchymal disease were determined by consensus.
The presence or absence of lymphadenopathy and pleural abnormalities was also
recorded.
Statistical Analysis
Given the smallsample size and the abnormal distribution of data,
nonparametric methods were used to test for correlation (Spearman's rank
correlation) or differences between groups (Kruskal-Wallis). For all tests, a
p value of less than 0.05 was considered significant.
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Fig. 2 —Axial CT images of three patients with acute schistosomiasis. Small
pulmonary nodules (arrows) are identified in each patient. From left
to right, images are of 23-year-old man, 20-year-old woman, and 50-year-old
man.
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Results
All 10 patients showed some degree of parenchymal abnormality. Small
pulmonary nodules were the most common finding, identified in nine patients
(Fig. 2). These nodules ranged
in size from 2 to 5 mm in five patients and from 7 to 15 mm in size in four
patients. The total number of nodules identified varied greatly (range, 2-102;
median, 15). The nodules were more frequent within the lung bases, and no
central or peripheral predominance was present. In two patients, the
distribution of nodules was primarily peribronchovascular. The smaller nodules
were typically well defined. Ground-glass halos were identified in five
patients, typically surrounding larger nodules
(Fig. 1B). In one patient, the
only parenchymal abnormality was a single 5-mm focus of ground-glass
attenuation. One patient showed geographic regions of consolidation or
ground-glass attenuation in addition to pulmonary nodules
(Fig. 1B). None of the patients
had significant lymphadenopathy or pleural, cardiac, pulmonary arterial, or
extrathoracic findings. Two patients had an incidental finding of a thyroid
nodule.
No relationship was observed between the percentage of peripheral
eosinophilia and the total number of nodules on CT, the size of the largest
nodule, or the presence of ground-glass opacity. No relationship was observed
between the presence of pulmonary symptoms and the total number of nodules,
the size of the largest nodule, or the presence of ground-glass opacity. The
presence of pulmonary symptoms did, however, correlate with the degree of
peripheral eosinophilia (p = 0.02).
Discussion
Schistosomiasis affects more than 200 million people worldwide and is a
major cause of morbidity and mortality, with 20 million people classified as
having severe disease [10].
The spread of infection requires an intermediate host—a freshwater snail
specific to each Schistosoma species—whose geographic
distribution in turn limits the distribution of the parasite. The infection
can be divided into three broad categories: allergic dermatitis, acute
schistosomiasis, and chronic schistosomiasis. Human infection is acquired
through direct contact with freshwater containing the cercariae (larval form
of the parasite), which penetrate the skin and shed their tails to become
schistosomula. Localized dermatitis may develop at the entry site in the
infected individual [8].
Schistosomula then migrate into the dermal veins and continue into the
pulmonary vasculature, where they enter the systemic circulation and
ultimately reside in the portal venous system of the liver. There, they mature
and mate. S. mansoni and S. japonicum schistosomula will
migrate to the mesenteric veins to lay eggs that penetrate the rectum. S.
haematobium will migrate to the vesicular veins to lay eggs that
penetrate the bladder. The eggs are released into the environment to hatch and
continue their life cycle
[3].
Acute schistosomiasis may present as Katayama fever, an immune
complex-mediated illness resembling serum sickness that occurs from 3 to 8
weeks after the primary infection
[3]. This period marks the
schistosome's first egg production in the human host. These eggs are highly
immunogenic, and a hypersensitivity response by the host to the sudden release
of antigens is thought to be responsible for the illness. Marked peripheral
eosinophilia may also be seen at this time. Symptoms and signs can include
fever, malaise, lethargy, cough, arthralgias, myalgias, headache, diarrhea,
abdominal pain, hepatosplenomegaly, and lymphadenopathy. The disease usually
is self-limited, but severe cases can result in death
[1].
Chronic schistosomiasis results from granuloma formation in response to the
schistosome eggs; however, a complex relationship exists between the severity
of clinical disease, the intensity of infection, and the infecting species
[3]. Pulmonary schistosomiasis
can be seen with S. mansoni or S. japonicum. With heavy
infections, these species can cause hepatic fibrosis, leading to the
development of collateral veins and the direct passage of eggs into the lungs.
Embolized ova may obstruct pulmonary arterioles, resulting in obliterative
arteriolitis. Over time, this may lead to pulmonary hypertension and cor
pulmonale [2].
One limitation of this study is the absence of pathologic proof that the CT
findings are related to schistosomiasis. The presence of S. mansoni
infection was confirmed for all patients. However, it is possible that the
radiographic findings were due to another process. As described, we attempted
to exclude other possible processes clinically. Specifically, the most likely
infectious process to lead to these findings would have been coccidiomycosis,
and this was excluded for all patients.
In this study, the most common finding was that of small, scattered
pulmonary nodules. Although pulmonary nodules have been reported previously in
acute schistosomiasis
[4-9],
the size range of these nodules was not stated in most of those reports. In
the images presented in those studies, however, the nodules shown are
typically larger than those seen in our study. Lambertucci and colleagues
[5] described micronodules seen
on CT for one patient. Pulmonary micronodules also have been identified with
conventional chest radiography in acute schistosomiasis
[6]. In five patients, many of
the larger nodules were associated with a ground-glass halo. This also has
been reported previously [9].
This ground-glass halo is a nonspecific finding and could relate to immune
complex deposition or eosinophilic infiltration of the lung parenchyma, seen
with acute schistosomiasis [8,
12]. In our study, no clear
relationship was found between the level of peripheral eosinophilia and the
presence of ground glass, however.
Previous studies have imaged almost exclusively patients with pulmonary
symptoms. In our study, four of the 10 patients had no pulmonary symptoms,
whereas two additional patients reported only mild symptoms. All our patients,
however, had parenchymal abnormalities detected using CT, and no significant
relationship was seen between the presence of pulmonary symptoms and the
severity of parenchymal findings. It had been previously suggested that the
broader use of CT would identify a greater pulmonary involvement during acute
schistosomiasis than is suggested by clinical symptoms
[5]. The results of our study
suggest that pulmonary involvement during the acute phase of schistosomal
infection is common, even in the absence of pulmonary symptoms.
References
- World Health Organization. Prevention and control of
schistosomiasis and soil-transmitted helminthiasis. Geneva,
Switzerland: World Health Organization, 2002, WHO Technical
Report Series 912
- Gopinath R, Nutman TB. Parasitic diseases. In: Murray JF, Nadel JA,
eds. Textbook of respiratory medicine, 3rd ed.
Philadelphia, PA: Saunders, 2000:1143
-1171
- Morris W, Knauer CM. Cardiopulmonary manifestations of
schistosomiasis. Semin Respir Infect1997; 12:159
-170[Medline]
- Cooke GS, Lalvani A, Gleeson FV, Conlon CP. Acute pulmonary
schistosomiasis in travelers returning from Lake Malawi sub-Saharan Africa.
Clin Infect Dis 1999;29
: 836-839[Medline]
- Lambertucci JR, Rayes AAM, Barata CH, Teixeira R, Gerspacher-Lara
R. Acute schistosomiasis: report on five singular cases. Mem Inst
Oswaldo Cruz 1997; 92:631
-635[Medline]
- Ritchken J, Gelfand M. Katayama disease, early toxaemic stage of
bilharziasis, with a report on a case showing pulmonary infiltration.
Br Med J 1954; 2:1419
-1420
- Salanitri J, Stanley P, Hennessy O. Acute pulmonary
schistosomiasis. Austral Radiol 2002;46
: 435-437[Medline]
- Schwartz E, Rozenman J, Perelman M. Pulmonary manifestations of
early schistosome infection among nonimmune travelers. Am J
Med 2000; 109:718
-722[CrossRef][Medline]
- Waldman ADB, Day JH, Shaw P, Bryceson ADM. Subacute pulmonary
granulomatous schistosomiasis: high resolution CT appearances—another
cause of the halo sign. Br J Radiol 2001;74
: 1052-1055[Abstract/Free Full Text]
- Chitsulo L, Engels D, Montresor A, Savioli L. The global status of
schistosomiasis and its control. Acta Trop2000; 77:41
-51[CrossRef][Medline]
- Hussain R, Kaushal NA, Ottesen EA. Comparison of immunoblot and
immunoprecipitation methods for analyzing cross-reactive antibodies to
filarial antigens. J Immunol Methods1985; 84:291
-301[Medline]
- Hiatt RA, Sottomayor ZR, Sanchez G, Zambrana M, Knight WD. Factors
in the pathogenesis of acute schistosomiasis mansoni. J Infect
Dis 1979; 139:659
-666[Medline]
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Abstract
Introduction
