Background
Neurocysticercosis (NCC) constitutes the most frequent parasitic infection of the nervous system [
1]. NCC is the expression of the neurological stage of infestation by
Taenia solium pork tapeworm larvae, when humans become accidental dead-end hosts of the parasitic cycle. Disease results from ingestion of
T. solium eggs shed in the stool of a human tapeworm carrier. The embryos are released from the egg in the intestines after ingestion and cross the intestinal mucosa toward the bloodstream, which carries them to peripheral tissues including the central nervous system (CNS), where they develop into cysticerci [
2]. Lesions are predominantly intracranial although there are other predilection sites like ophthalmic localizations and muscular calcifications [
2]. Most of the neurological infections are asymptomatic, however when symptoms are present, seizures are the most common manifestation of the disease, although headaches, neurological deficits, intracranial hypertension, cerebrovascular complications are also reported [
2].
NCC is endemic in many tropical countries [
3‐
7]. Numerous imported cases have been described in Western Europe and North America [
2]. In France, 67 cases have been reported from 1970 to 2013, most of them thought to be imported from endemic areas [
8]. In Haiti and bordering areas of the Dominican Republic, seroprevalence of cysticercosis has been estimated to be around 3% [
9‐
11]. To our knowledge, only four cases diagnosed in the French West Indies had been reported previously in the literature [
12,
13].
We report on three additional cases of NCC diagnosed over a 2 month period in Guadeloupe, French West Indies, and discuss each particular clinical and radiological presentation.
Discussion
Our three cases illustrate three distinct clinical stages and a variety of radiological presentations of the disease (Table
1). All of them were foreigners, coming from areas of higher endemicity, they all had only intracranial manifestations with variability in the number of cysts, and with seizures in the first two cases and probably in the third case.
Our three patients all fulfilled absolute or major clinical, radiological and/or serological criteria for NCC: histological demonstration of the parasite (Patient 3), evidence of cystic lesions showing the scolex (Patient 1 and 2), positive CSF immunoblot for the detection of anticysticercal antibodies (Patient 2), and resolution of intracranial cystic lesions after therapy with albendazole (Patient 1 and 2) [
14,
15]. Real time PCR (Polymerase chain reaction) for
T. solium in CSF can be helpful when the diagnosis is uncertain (sensitivity 83.3%, specificity 100% [
17]) but we did not have to perform it because our patients all fulfilled criteria for definite NCC.
Their clinical presentation was slightly different from previous case reports from Guadeloupe [
12,
13]. To date, only four other cases have been reported in Guadeloupe in the late nineties. Three of them had intracranial parenchymatous NCC and one had cysticercosis outside CNS, all confirmed by either serology, pathognomonic images on CT scan [
12] or histology [
13] (MRI was not avalaible at that time in Guadeloupe). Three (1 man, 2 woman) had seizures like our cases, among them one woman had subacute meningitis (180 cells/mm3 in CSF and proteins = 0.6 g/L). The last one (child) had a periorbital intramuscular nodule. Two of them were middle-aged women originating from Haiti where they were probably contaminated as for two of our cases. The man, who was born and lived in Guadeloupe, might have been infected abroad as it was reported that he traveled frequently, and the child had probable autochtonous transmission because he had never left Guadeloupe [
12,
13]. More information is missing to better compare them to our cases.
Cerebrovascular and particularly ischemic complications of NCC, are well documented (between 4% and 12% of patients with NCC according to different studies [
18,
19]). Chronic subarachnoid inflammation creates angiitis with progressive stenosis, sometimes leading to the occlusion of one or several cerebral arteries [
20,
21]. However in patient 3, we cannot draw any causal relationship between the stroke and NCC. The stroke was most probably rather due to the dissection of the left internal carotid artery.
All patients with NCC should receive symptomatic treatment, which consists of antiepileptic medication for patients with seizures, analgetics for patients with pain and corticosteroids for patients with increased intracranial pressure or encephalitis [
2]. Antiparasitic treatment should be adapted based on findings from neuroimaging [
2,
16], including the localization, number and stage of cysts, and the presence of intracranial hypertension. Different options exist including no antiparasitic treatment, albendazole, praziquantel or both in combination with corticosteroids, and surgical treatment.
In patients with only calcified lesions, antiparasitic treatment has not shown any benefit [
16]. For patient 3, despite the presence of only calcified lesions on CT scan, we decided to treat with albendazole, because of the presence of living larvae at pathological examination. In patients with active cysts, albendazole in combination with corticosteroids offers a reduction in the number of generalized seizures in the years following initiation of treatment and the duration of seizure risk compared with placebo [
22,
23].
The association of both albendazole and praziquantel has recently shown to increase the parasiticidal effect in patients with multiple viable intraparenchymal cysts [
24]. This is why it was used on patient 2.
Patients 1 and 2 experienced several relapses, with partial seizures shortly after treatment initiation despite significant resolution of the cysts as shown on repeat MRI (Fig.
1b, c, e, Fig.
2b and d). The rate of seizure recurrence in the first 12 month after treatment with albendazole is approximately 40% [
22,
25]. Inflammation after cyst degeneration with albendazole [
2] can be responsible for seizures but is an indicator of efficient cure [
26]. Drug-drug interactions between some antiepileptics and albendazole or praziquantel might be a source of antiparasitic treatment failure and a source of persisting seizures [
27]. Seizures prior to therapy, persistence of active or calcified lesions on radiological follow-up [
22], family history of seizures, serial seizures and electroencephalographic abnormalities [
28] have all been described as risk factors for seizure recurrence. There is no clear recommendation in the length of treatment with steroids, but patient 1 and 2 could have benefitted from a longer course on the seizure recurrences.
All three patients had multiple lesions, in common with most cases in adults from endemic areas and particularly in South America; a single enhancing lesion is the most frequent finding in children and in India, where the parasitic load is lower [
2,
29].
The three cases described here were probably imported. Patient 1 had most likely the most recently acquired the infection, as indicated by her young age, the CT findings [
15,
30,
31], and the fact that she lived in an area of NCC endemicity until 1 year before her first symptoms. Patient 2 suffered from a later stage of the disease and had probably contracted it in Haiti more than 10 years before. Patient 3 is a vivid illustration of a disseminated NCC that had remained clinically dormant for a long time.
In endemic areas clusters of swine cysticercosis have been described around human carriers and justify interventions for control and elimination in humans [
32]. In high-income countries transmission from pig-to-human is unlikely due to better human hygiene and veterinary standards of the pigs [
33].
T. solium eggs have never been found in water or soil [
8,
9], however NCC has frequently been imported by tapeworm carriers into non-endemic countries [
5]. This confirms that humans can be a reservoir of the disease and that cysticercosis transmission does not require the presence of infected pigs [
34]. One case of autochthonous acquisition has already been described in Guadeloupe, in a child who had never left the island and presented with a extracerebral form of the disease (periorbital intramuscular nodule) [
13]. Clusters of humans with positive
T. solium serology have been described around tapeworm carriers, but no cluster of cases of NCCs was seen [
35]. As epilepsy due to NCC appear late in the history of the infection, it is not routinely diagnosed around tapeworm carriers [
2]. Concurrent intestinal taeniasis is reported in around 5% of the patients with cysticercosis [
2,
36,
37]. These patients usually present with a more severe cerebral infection due to repeated auto-infection [
2].
We failed to identify tapeworm carriage in our neurocyticerosis patients or those in their households, probably because we used direct examination of stool, which is suboptimally sensitive. Specific coproantigen detection by ELISA assays [
38] is more sensitive and could more efficiently detect carriers who would be eligible for treatment with niclosamide to prevent transmission [
2,
38].