Intraspinal Paragonimiasis in Children: MRI Findings and Suggestions for Pathogenesis

DISCUSSION

Paragonimus infection can invade various parenchymal organs and tissues, including the lungs, pleura, brain, liver, and subcutaneous tissue.^{3,11⇓⇓⇓⇓⇓–17} The infection involving the CNS is rare and constitutes approximately 0.8%–31.0% of all active paragonimiasis.³ Spinal involvement is even more uncommonly encountered, with the occurrence ranging from 2% to 10% among CNS paragonimiasis.⁵ In our series, only 6 cases of spinal involvement occurred among 83 patients with CNS paragonimiasis (7.2%, 6/83), which is similar to that in previous reports.

The pathogenesis of the formation of spinal paragonimiasis is still uncertain.^{1,5⇓⇓–8,18} Several theories have been proposed in previous reports. The first is that the Paragonimus larvae may directly migrate from the lung and/or pleura to the spinal canal through the paravertebral soft tissue.⁵ A second theory was suggested by Diaconita and Nagy¹⁸ in 1957, which stated that paragonimiasis involvement in the spinal canal could result from hematogenous extension. Another theory was that the infection of the spinal canal was caused by the direct downward movement of cerebral paragonimiasis.⁵ The above theories regarding the spinal involvement of paragonimiasis are conflicting, and none of these notions have been confirmed by any clear imaging or other evidence. In this study, the imaging findings of the 6 extradural spinal paragonimiasis cases provided strong evidence for a mechanism of pathogenesis in which the lung flukes directly invade the spinal canal from the pleural lesions through the intervertebral foramen. First, all the intraspinal granulomatous masses in this series occurred in thoracic segments, also consistent with the report from Moon et al⁵ showing that thoracic spines were involved in all 8 patients with spinal paragonimiasis examined in that study. Second, all the lesions located in the extradural space were connected to the pleural lesions through the intervertebral foramen. This physical connection indicated that the intraspinal extradural lesions were from the adjacent pleural (or pulmonary) lesions. Third, no imaging evidence of either cervical paragonimiasis or cerebral paragonimiasis was found in this group of patients; therefore, the possibility that extradural spinal paragonimiasis was caused by the downward movement of cerebral paragonimiasis could be excluded. In addition, no imaging or laboratory data in our cases supported the theory of hematogenous extension.

On the basis of the mode of invasion of paragonimiasis from the pleura to the spinal canal, the extradural space could be inevitably invaded. This has been confirmed in our cases and in most previously reported cases.^5⇓–7 However, in the previous reports, there were a few cases complicated by intradural or/and spinal cord involvement except for extradural invasion. There has been no reasonable explanation for this phenomenon. We speculate that the intradural or/and spinal cord lesions could be a result of migration from the extradural space. Because the Paragonimus larvae habitually migrate, they can penetrate the intestinal wall, pleura, and meninges. In this mode, they can also penetrate the dura mater and the soft spinal membrane, resulting in intraspinal or/and spinal lesion formation. Whether the intradural or/and spinal cord lesions occur could be determined by the progression of the disease. In our series, the lesions in all cases were limited in the extradural space. This could be attributed to the early detection achieved via the application of modern imaging technology.

As with cerebral paragonimiasis, hemorrhage is also considered a very important imaging feature in the diagnosis of spinal paragonimiasis. In this group of patients, 83.3% (5/6) had hemorrhage, which showed patchy hyperintensity on T1WI and hypointensity on T2WI. The hemorrhagic tendency of paragonimiasis could be attributed to the biologic behavior of the parasite.^19⇓–21 When the worm entered the epidural space through the intervertebral foramen, it formed granulomatous lesions; additionally, the migration of worms can cause hyperemia, vasculitis, and broken capillaries, resulting in hemorrhage.^1,19 In addition, hemorrhage is more likely to occur in children because their blood vessels are more vulnerable than those of adults. In this study, the granuloma of 1 patient did not show hemorrhage with obvious hyperintensity on T1WI, which may be due to the small size of the granulomatous lesion or the different maturity grades of the granuloma.^20,22

The laboratory tests, including the eosinophil counts, the dot-immunogold filtration assay, and enzyme-linked immunosorbent assay, have high specificity and sensitivity to detect paragonimiasis.^1,23 These methods, however, are unable to locate or characterize the lesions. Although myelography was also used for the detection of spinal paragonimiasis lesions by Moon et al,⁵ it is an invasive method and the imaging results are nonspecific, with a low positive rate; thus, this technique is now rarely used. Compared with myelography, MR imaging has the advantage of multiplane imaging and excellent contrast of the soft tissue, which is especially suitable for displaying spinal lesions. In this study, MR imaging not only clearly revealed the location, range, and size of lesions but also found the signal features of the hemorrhage in spinal paragonimiasis, as well as its relationship with the spinal cord, thus providing useful information for the early diagnosis of spinal paragonimiasis and surgical treatment.

Because of some similarities in their imaging manifestations, extradural spinal paragonimiasis needs to be differentiated from the following diseases:

1) Neurogenic tumors: because the intraspinal soft-tissue masses of spinal paragonimiasis are connected to the paravertebral and pleural lesions through the intervertebral foramen, the lesions appear to be distributed along the spinal nerves, similar to the dumbbell-like sign, and they are easily misdiagnosed as neurogenic tumors.²⁴ However, they can be differentiated on the basis of the following features: First, in most cases, the dumbbell-like mass formed by neurogenic tumors has a well-defined boundary, with an enlarged intervertebral foramen and even bone absorption and destruction, while spinal paragonimiasis presents with the exact opposite features. Second, the mass of spinal paragonimiasis is closely related to the pleura with thickening, pleural nodularity, and enhancement. However, in neurogenic tumors, only a few cases showed adjacent slightly pleural responses. Third, paragonimiasis has a tendency to produce hemorrhage, while neurogenic tumors have no such tendency.

2) Tuberculoma or bacterial abscess: tuberculoma is often encountered in the intraspinal extradural space. It shares a similar lesion location and enhancement patterns with paragonimiasis and is also frequently accompanied by pleural and intrapulmonary lesions. However, hemorrhage with hyperintensity on T1WI is seldom observed in intraspinal extradural tuberculoma. In addition, intraspinal tuberculomas are usually accompanied by vertebral or intracranial invasion.⁹ Bacterial abscess is another infectious disease that can form a mass in the intraspinal extradural space. For this disease, enhanced MR imaging usually shows a ring-shaped enhancement, which is different from the substantial enhancement pattern of paragonimiasis granuloma.

3) Intraspinal hematoma: because hemorrhage in granulomas is common in spinal paragonimiasis, it must be differentiated from intraspinal hematoma. In the early stages, intraspinal hematoma usually presents with uniform hyperintensity on T1WI and does not extend to the subpleural space through the intervertebral foramen. Moreover, intraspinal hematoma could change the signal features on follow-up MR imaging.²⁵

4) Lymphomas: most extradural lymphomas usually present with uniform signals on plain and enhanced scans²⁶; however, intraspinal paragonimiasis granulomas often present with heterogeneous signals because of internal hemorrhage.

5) Angiomyolipomas: this tumor occasionally occurs in the epidural space and needs to be considered in the differential diagnosi.²⁷ The fat composition in angiomyolipomas can be easily detected by MR imaging; this feature could be helpful in differentiating it from paragonimiasis. In addition to the differences in imaging features, the Paragonimus endemic areas (especially in East Asia), the increased eosinophil counts in laboratory examinations, and the antibody test by enzyme-linked immunosorbent assay are also strong evidence for the diagnosis of spinal paragonimiasis and the exclusion of all the aforementioned diseases.