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DOI:10.2214/AJR.04.1507
AJR 2006; 186:1697-1702
© American Roentgen Ray Society

Clinical Observations

Pulmonary Lesions Associated With Visceral Larva Migrans Due to Ascaris suum or Toxocara canis: Imaging of Six Cases

Shuji Sakai1, Yoshitaka Shida2, Naoki Takahashi3, Hidetake Yabuuchi3, Hiroyasu Soeda3, Takashi Okafuji3, Masamitsu Hatakenaka3 and Hiroshi Honda3

1 Department of Health Sciences, School of Medicine, Kyushu University, 3-1-1, Maidashi, Higashi-ku, Fukuoka 812-8582, Japan.
2 Department of Radiology, International Medical Center of Japan, Tokyo, Japan.
3 Department of Clincal Radiology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.

Received September 24, 2004; accepted after revision March 22, 2005.

 
Address correspondence to S. Sakai (sakai{at}shs.kyushu-u.ac.jp).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The objective of our study was to evaluate chest radiographic and CT findings of patients with pulmonary lesions associated with visceral larva migrans due to Ascaris suum or Toxocara canis. CT investigation was focused on the location, size, contour, and internal features of the lesions; migration of lesions; mediastinal lymphadenopathy; and pleural effusion.

CONCLUSION. Pulmonary visceral larva migrans appears on CT as multifocal subpleural nodules with halo or ground-glass opacities and ill-defined margins.

Keywords: Ascaris suum • CT • nematodes • parasites • pulmonary diseases • roundworms • Toxocara canis • visceral larva migrans


Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Visceral larva migrans was first described by Beaver et al. in 1952 [1]; it results mainly from the infection of dogs by Toxocara canis. A large percentage of dogs are infected, and the soil of public playgrounds is often contaminated with the eggs of T. canis [2]. Visceral larva migrans due to Ascaris suum has also been reported in humans [3], with several cases of visceral larva migrans due to A. suum seen recently in Kyushu, the southern part of Japan [4, 5]. Eggs of T. canis and A. suum remain capable of infecting a host for a long period of time in the environment because they can withstand dryness and a wide range of temperatures [2, 6]. Therefore, contact between humans and dogs or pigs is not necessary for transmission of the disease. Humans are usually infected by eating fresh vegetables cultivated using pig manure or by eating raw liver from chickens or cattle that are paratenic hosts of these roundworms [7-9]. Infected larvae of these roundworms then migrate to the liver, lung, eye, myocardium, or CNS in humans and nondefinitive hosts and cause various symptoms such as fever, cough, eruption, or chest pain [4, 10-13].

Because these larvae are unable to grow into mature adults in nondefinitive hosts, eggs or worms are not detected in the feces of patients. Therefore, clinical diagnosis of larva migrans has been difficult in the past. In recent years, enzyme-linked immunosorbent assay (ELISA) has been available for the diagnosis of T. canis and A. suum. This method has been reported to have high sensitivity and specificity [2, 4, 14].

The clinical finding of lung lesions associated with larva migrans is usually nonspecific. There are only a few case reports regarding the radiographic findings of lung involvement in pulmonary visceral larva migrans [5, 15, 16]. Lung involvement causes pulmonary infiltration, and the mechanism of the infiltration is believed to be an allergic response to the larva. However, a case was reported in which no abnormalities were detected on chest radiography, but multiple nodules were detected on CT [5]. Thus, chest CT is expected to be a contributory technique for the differential diagnosis in patients with eosinophilia when the determining the final diagnosis is difficult and other clinical findings are poor. The aim of our study was to evaluate the CT features of pulmonary lesions associated with visceral larva migrans due to A. suum or T. canis. To our knowledge, our study is the first that used CT for the evaluation of pulmonary lesions associated with visceral larva migrans due to these roundworms.


Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
We reviewed the medical records of our hospitals over the previous 5 years and identified nine patients diagnosed with visceral larva migrans. Among them, three adult patients did not have pulmonary lesions associated with visceral larva migrans. These three patients included one with myocarditis, one with meningitis due to A. suum, and one with liver involvement due to T. canis. Finally, between February 2000 and March 2003, six patients (three males and three females, one child and five adults) who ranged in age from 3 to 62 years (mean age, 43 years) were diagnosed with visceral larva migrans that presented with lung lesions. All adult patients have a smoking history of 12-20 cigarettes per day for 16-32 years.

In the serum of the six patients, anti-IgG to A. suum or T. canis was detected using a commercial multiple-dot ELISA kit (SRL, Tokyo) or an original kit at the Department of Parasitology, Miyazaki Medical College, Japan [4, 15]. These kits contain 12 antigens to different parasites including A. suum and T. canis. Five of the cases of visceral larva migrans were due to A. suum and one was due to T. canis on the basis of ELISA results. In all patients, neither the eggs nor the worms of the parasites were detected in the feces of patients. Other parasitic diseases such as Dirofilaria immitis, Anisakis simplex, Gnathostoma doloresi, Strongyloides ratti, Paragonimus westermani, Paragonimus miyazakii, and Toxocara cati were excluded using ELISA. All patients were immunocompetent.

The clinical symptoms of these patients included cough in three, urticaria in two, and chest pain and sputum in one. Only one patient did not show any symptoms. Diagnoses of drug-induced lung disease, hypersensitivity pneumonitis, respiratory bronchiolitis, vasculitis, and hematologic malignancy were clinically denied. Chest radiographs and CT scans of these patients were available for review. The duration from the onset of clinical symptoms and the initial CT examination ranged from 1 to 6 months (mean, 2.3 months). However, the period between the initial CT examination and ELISA was less than 2 weeks.

Eosinophilia (11-33%) was seen in five patients at the time of the initial CT examinations. The patient with T. canis did not show eosinophilia at the time of the initial CT examination, but mild eosinophilia was seen 1 week later. The values of IgE were high (275-2,290 IU/mL) in four of the five examined patients. Transbronchial lung biopsies or bronchoalveolar lavages were not performed in all patients. Two patients who showed multiple liver lesions underwent percutaneous liver biopsy under sonographic guidance. These specimens revealed nonspecific granulomatous tissue with eosinophilic infiltration without evidence of larvae.

Albendazole was administered to all patients after the diagnosis had been confirmed. Thereafter, in all patients, the pulmonary lesions had "disappeared" on follow-up CT, and the percentage of eosinophils, the IgE value, and ELISA results all fell within the normal ranges. Thus, in our study, we could not identify larvae in the lung or sputum. Our diagnosis of pulmonary lesions associated with visceral larva migrans was based on positive antibodies using ELISA; immediate resolution of pulmonary lesions, symptoms, eosinophilia, and ELISA results after the administration of albendazole; and exclusion of other causes.

All patients were examined using chest radiography and conventional CT (10-mm collimation at 10-mm interval), and the interval between the initial CT and chest radiographic examinations was less than 3 days. The reasons for requesting chest CT were as follows: to rule out lung metastasis of gastric cancer or neuroblastoma (n = 2), to assess the extent of the disease from liver lesions (n = 2), and because of suspicion of underlying primary pulmonary malignancy (n = 2). Because the two cases of malignancy were well controlled, the patients were not treated with chemotherapy. Among the six patients, three patients underwent high-resolution CT (2-mm collimation) and three patients underwent two or more CT examinations before oral albendazole was initiated. Three patients did not undergo high-resolution CT because one patient was a child, one patient had only a single lesion, and one patient had multiple liver lesions.

The chest radiographs and CT scans were reviewed retrospectively by two radiologists who arrived at a consensus interpretation. Conventional CT investigation was focused on the location, size, and migration of pulmonary lesions; mediastinal lymphadenopathy; and pleural effusion. In addition, the internal features and contours of the pulmonary lesions were examined in the three patients who underwent high-resolution CT. The internal features were classified into three categories—namely, ground-glass opacities, nodules with halos, and consolidation [17, 18]. Ground-glass opacities were defined as hazy areas of increased attenuation of the lung with the underlying lung vessels not obscured. A nodule with a halo was defined as an area of lung attenuation that was clearly less dense than the central nodule. A consolidation was defined as an area of increased attenuation with the underlying lung vessels obscured. In addition, margin characteristics were classified into two categories, well defined and ill defined.


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
In five patients, chest radiography showed normal findings, although CT depicted definite lesions. Chest radiography showed a solitary nodule only in the child patient. Table 1 shows the conventional CT findings for each patient. In four patients with A. suum, conventional CT showed multiple nodules that were smaller than 3 cm in diameter. In the patient with T. canis, CT showed many nodules ranging from 4 to 40 mm in diameter. All nodules were located in the subpleural area of the lungs, and none was seen in the central area. In all three patients who underwent follow-up CT examinations, CT showed migration of the lesions. Lesions seen on the earlier CT scans had "disappeared," and new lesions appeared at different locations on follow-up CT scans. All of the new lesions that appeared showed features similar to those of the lesions detected at the earlier examination. CT showed no mediastinal lymphadenopathy or pleural effusion in any of the patients.


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  		TABLE 1: Summary of Six Cases of Visceral Larva Migrans

 

High-resolution CT was performed in three patients as follows: a total of seven lesions were detected two times in case 3, three lesions in case 4, and all of the lesions in case 6. Among the 10 lesions in cases 3 and 4, five were nodules with halos, all of which had ill-defined margins (Fig. 1A, 1B and 1C); three were consolidations, all of which had well-defined margins—what is usually called nodule (Fig. 2A, 2B); and two were ground-glass opacities, one with an ill-defined margin and one with a well-defined margin. All lesions in case 6 were ground-glass opacities with ill-defined margins (Fig. 3A, 3B).


Figure 1
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  		Fig. 1A —Visceral larva migrans due to Ascaris suum in 57-year-old woman (case 3). High-resolution CT scan (2-mm collimation) through right middle lobe shows nodule with halo with ill-defined margin (arrow).

 

Figure 2
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  		Fig. 1B —Visceral larva migrans due to Ascaris suum in 57-year-old woman (case 3). High-resolution CT scan (2-mm collimation) through lingula obtained 8 days after A shows another nodule with halo with ill-defined margin (arrow).

 

Figure 3
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  		Fig. 1C —Visceral larva migrans due to Ascaris suum in 57-year-old woman (case 3). High-resolution CT scan (2-mm collimation) obtained through left upper lobe at follow-up shows ground-glass opacity with ill-defined margin (arrow).

 

Figure 4
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  		Fig. 2A —Visceral larva migrans due to Ascaris suum in 62-year-old man (case 4). High-resolution CT scans (2-mm collimation) show nodules with irregular margins (arrows).

 

Figure 5
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  		Fig. 2B —Visceral larva migrans due to Ascaris suum in 62-year-old man (case 4). High-resolution CT scans (2-mm collimation) show nodules with irregular margins (arrows).

 

Figure 6
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  		Fig. 3A —Visceral larva migrans due to Toxocara canis in 46-year-old man (case 6). High-resolution CT scans (2-mm collimation) through left upper lobe show multiple nodular or wedge-shaped ground-glass opacities (arrows).

 

Figure 7
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  		Fig. 3B —Visceral larva migrans due to Toxocara canis in 46-year-old man (case 6). High-resolution CT scans (2-mm collimation) through left upper lobe show multiple nodular or wedge-shaped ground-glass opacities (arrows).

 

Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Visceral larva migrans is a zoonotic disease in which the human viscera are infected by the migrating larvae of T. canis or, less commonly, by larvae of Toxocara catis and A. suum [2, 4]. T. canis, T. catis, and A. suum are the common intestinal ascarids of the dog, cat, and pig, respectively. Visceral larva migrans due to these roundworms may occasionally cause severe complications including meningitis, encephalopathy, ophthalmopathy, and myocarditis [10-13]. Lung involvement of the visceral larva migrans with T. canis or A. suum has previously been reported [3, 4]. In the lung, the initial inflammatory response is diffuse with eosinophils predominating. Later, histiocytes collect around the degenerating larvae, occasionally forming a widespread granuloma. Larvae within the granuloma are occasionally identified by visualization of two prominent excretory columns [2, 15]. Cases of visceral larva migrans due to A. suum have occurred in Kyushu, Japan [4]. All of the patients in our study also lived in Kyushu. Pulmonary involvement occurs in 20-85% of patients of visceral larva migrans [2, 19].

Clinical manifestations of pulmonary visceral larva migrans include cough, wheezing, acute bronchiolitis, asthma, and acute pneumonia. Eosinophilia is a common laboratory abnormality. In particular, severe eosinophilia has been reported in patients with visceral larva migrans due to A. suum [4]. In our study, all patients with A. suum showed severe eosinophilia, but the patient with T. canis did not show eosinophilia. In addition, the values of IgE are frequently elevated in patients with visceral larva migrans [20]. In our study, four of the five patients examined showed an elevated IgE value.

A definitive diagnosis of visceral larva migrans can be made only by identifying larvae in the affected viscera. Larvae are rarely isolated from the sputum in patients with pulmonary visceral larva migrans [3]. Because the larvae of A. suum and T. canis do not mature in humans, eggs of these roundworms are never detected [2, 4]. Thus, the diagnosis of visceral larva migrans is based on visualization of specific serum antibodies to these roundworms by ELISA. This test has a sensitivity of 78% and a specificity of 92% [14].

Previous reports have suggested that the common features of chest radiographs in patients of pulmonary visceral larva migrans were mild bilateral infiltrates, which can be migratory [4, 15]. However, in our study, the chest radiographs were normal except in one patient. Researchers reported that chest radiographs of a patient with visceral larva migrans due to A. suum did not show any abnormalities, but that CT showed multiple nodules [5]. In that report [5], the predominant pulmonary lesions were ground-glass opacities with ill-defined margins and nodules with halos located in the subpleural area. Although there was no description of the high-resolution CT findings in that patient [5], the CT characteristics of our study patients were similar to those of that patient. In our study, CT enabled better detectability and estimation of the distribution characteristics and the extent of the lesions than did chest radiography. Furthermore, CT depicted unexpected features that chest radiography did not depict.

The migration of lesions is generally seen in patients with Löffler's syndrome, cryptogenic organizing pneumonia, eosinophilic pneumonia, or Churg-Strauss syndrome [21]. The depiction of migratory lesions by visceral larva migrans on CT has not, to our knowledge, been reported in the past. In our study, CT showed migration of the lesions in all three patients who underwent follow-up CT. Even with the short follow-up period of 7-8 days in cases 1 and 3, all lesions seen on the first CT examination had "disappeared," and multiple new lesions appeared on the follow-up CT scans. The cause of the migration of pulmonary nodules associated with visceral larva migrans was not verified definitively because repeated histologic confirmation of lesions is impossible. The presumptive mechanism is an allergic response to the larva in the lung with eosinophilic infiltration of the lung [21]. A patient with visceral larva migrans due to T. canis that developed by a pattern of acute eosinophilic pneumonia has been reported in the past [22], although there was no such patient in our study.

The high-resolution CT features of pulmonary lesions associated with visceral larva migrans have not been reported in the past to our knowledge. High-resolution CT scans were available in three patients in our study, and the predominant findings were nodules with halos and pure ground-glass opacities located in the peripheral zone of the lung. However, the nature of the these findings was uncertain because no comparative study with histology was performed. Furthermore, identifying larvae in the areas of these dominant findings with transbronchial biopsy or bronchoalveolar lavage is difficult. Thus, we cannot determine whether the present findings represent direct changes of the lung caused by larvae or indirect changes.

Differential diagnoses of pulmonary lesions associated with visceral larva migrans include viral infection; MALToma; and vasculitis, such as Wegener's granulomatosis and Churg-Strauss syndrome [23-26]. Churg-Strauss syndrome is particularly important because this disease shows migratory opacities, eosinophilia, and a high serum IgE value [26]. Furthermore, differential diagnosis with respect to other parasitic diseases, such as paragonimiasis or dirofilariasis, is not difficult because the predominant pattern of pulmonary paragonimiasis is patchy consolidation with cavities and that of pulmonary dirofilariasis is noncalcified nodules of 3 cm or less in diameter [26-28]. In our study, neither pleural effusion nor mediastinal lymphadenopathy was seen. Pleural effusion has been reported in a patient with visceral larva migrans due to T. canis [29], but none has been reported in a case of visceral larva migrans due to A. suum.

It is unlikely that the CT features in our series represent the full spectrum of CT findings in patients with pulmonary lesions associated with visceral larva migrans because our study was retrospective. In most patients, visceral larva migrans was not suspected in the clinical setting, and a serology test was performed based on CT findings in some patients.

In conclusion, chest radiographs did not show any abnormalities in five of six patients with pulmonary lesions associated with visceral larva migrans; a solitary patchy opacity was seen in the remaining patient, a child. In four patients with A. suum, conventional CT showed multiple nodules that were smaller than 3 cm on the major axis. Only one patient with A. suum showed a single lesion. In another patient, the one with T. canis, CT showed many nodules ranging from 4 mm to 4 cm on the major axis. All nodules were located in the peripheral area of the lungs. In all three patients who underwent follow-up CT examinations, CT showed migration of the lesions. In three patients who underwent high-resolution CT, the predominant pattern involved ground-glass opacities with ill-defined margins and nodules with halos.


References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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