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DOI:10.2214/AJR.05.0213
AJR 2006; 186:1300-1303
© American Roentgen Ray Society

Clinical Observations

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
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 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
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
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 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
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
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 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
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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.


Figure 1
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  		Fig. 1A —19-year-old man with acute schistosomiasis. Chest radiograph shows multiple ill-defined, nodular densities bilaterally.

 


Figure 2
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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.

 
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.


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  		TABLE 1: Clinical Data for the 10 Patients

 

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.


Figure 3
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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.

 

Results
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 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
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
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
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
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

  1. World Health Organization. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Geneva, Switzerland: World Health Organization, 2002, WHO Technical Report Series 912
  2. Gopinath R, Nutman TB. Parasitic diseases. In: Murray JF, Nadel JA, eds. Textbook of respiratory medicine, 3rd ed. Philadelphia, PA: Saunders, 2000:1143 -1171
  3. Morris W, Knauer CM. Cardiopulmonary manifestations of schistosomiasis. Semin Respir Infect1997; 12:159 -170[Medline]
  4. 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]
  5. 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]
  6. 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[Free Full Text]
  7. Salanitri J, Stanley P, Hennessy O. Acute pulmonary schistosomiasis. Austral Radiol 2002;46 : 435-437[CrossRef][Medline]
  8. Schwartz E, Rozenman J, Perelman M. Pulmonary manifestations of early schistosome infection among nonimmune travelers. Am J Med 2000; 109:718 -722[CrossRef][Medline]
  9. 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]
  10. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Trop2000; 77:41 -51[CrossRef][Medline]
  11. 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[CrossRef][Medline]
  12. 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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