- Top of page
- Supporting Information
Purpose: To estimate the lifetime prevalence of neurocysticercosis (NCC)–associated epilepsy and the proportion of NCC among people with epilepsy in three Burkina Faso villages.
Methods: Three villages were selected to represent three types of pig-rearing methods: (1) Batondo, where pigs are left to roam; (2) Pabré, where pigs are mostly tethered or penned; and (3) Nyonyogo, where the majority of residents are Muslim and few pigs are raised. In Batondo and Nyonyogo, all concessions (a group of several households) were included. Half of the concessions in Pabré were randomly chosen. All households of selected concessions were included, and one person per household was randomly selected for epilepsy screening and serologic testing for cysticercosis. Self-reported cases of epilepsy were also examined and confirmed cases included in analyses other than the estimate of NCC-associated epilepsy prevalence. Epilepsy was defined as ever having had more than one episode of unprovoked seizures. Individuals with medically confirmed epilepsy had a computerized tomography (CT) scan of the brain before and after contrast medium injection. The diagnosis of NCC was made using a modification of the criteria of Del Brutto et al.
Key Findings: Thirty-nine (4%) of 888 randomly selected villagers and 33 (94%) of 35 self-reported seizures cases were confirmed to have epilepsy by medical examination. Among the 68 participants with epilepsy who had a CT scan, 20 patients were diagnosed with definitive or probable NCC for a proportion of 46.9% (95% confidence interval [CI] 30.2–64.1) in Batondo and 45.5% (95% CI 19.0–74.1) in Pabré. No cases of NCC were identified in Nyonyogo.
Significance: All the definitive and probable cases of NCC were from the two villages where pig breeding is common. Prevention policies intended to reduce the burden of epilepsy in this country should include measures designed to interrupt the life cycle of Taenia solium.
Many studies have reported a higher prevalence of epilepsy in developing countries than in the developed world (reviewed by Roman et al., 2000; Preux & Druet-Cabanac, 2005). Infections such as malaria, meningitis, viral or bacterial encephalitis, and perinatal factors are mentioned as possible reasons for the higher prevalence (Jallon, 1997; Preux & Druet-Cabanac, 2005). One infection that has received only limited attention in some parts of the world is neurocysticercosis (NCC), although it has been reported as the most frequent parasitic infection of the central nervous system (CNS) (Garg, 1998; Roman et al., 2000).
Neurocysticercosis results from the invasion of the CNS by the larval stage of Taenia solium after ingestion of the parasite eggs. The adult form of the parasite is hosted by humans, causing an intestinal parasitosis (taeniasis), occurring when humans consume poorly cooked pork infected with larvae (metacestode cysticerci) of the parasite. The eggs of the parasite are shed in human feces. Pigs, the intermediate hosts, become infected when consuming human feces or food or water contaminated by human feces. Poor pig management practices, hygiene, and sanitation all contribute to the transmission of T. solium infection (Pal et al., 2000; Preux & Druet-Cabanac, 2005).
Humans may become accidental hosts for the larvae leading to cysticercosis when they ingest the parasite’s eggs in contaminated food or water (oral–fecal contamination) (Palacios et al., 1997; Pittella, 1997; Garg, 1998; Pal et al., 2000). Cysticercosis occurs when the larvae migrate from the intestine to any tissue, but the CNS is believed to be a site of predilection. Once established in the CNS, the larva evolves through four different stages: cystic, where it is a viable vesicle of 10–20 mm full of liquid containing a scolex; colloidal, where the vesicle starts degenerating, causing a thickening of the liquid and often causing an inflammatory reaction in surrounding brain tissue; granular, with deposition of mineral salts; and finally calcified, or nonviable cysts, which appear as hyperdense areas on computerized tomography (CT) (Palacios et al., 1997; Pittella, 1997; Garg, 1998; Nash et al., 2004). The larvae may migrate into any structure of the CNS, including the spinal cord, subarachnoid space, and ventricles, but the most common site is the parenchyma. The CNS symptoms reflect both the location and the inflammation caused by the larvae, with seizures being the most common presentation (Garg, 1998; White & Garcia, 1999; Pal et al., 2000; Riley & White, 2003; Carabin et al., 2011). Other CNS symptoms include severe progressive headache, focal neurologic deficit, hydrocephalus, or symptoms of intracranial hypertension (nausea, dizziness, vomiting, or visual symptoms) (Palacios et al., 1997; Garg, 1998; White & Garcia, 1999; Pal et al., 2000; Prabhakar & Singh, 2002a; Carabin et al., 2011).
A meta-analysis by Quet et al. (2010) reported an association between epilepsy and seropositivity to cysticercosis from prevalence case–control and cross-sectional studies conducted in sub-Saharan Africa. Yet, when the present study was initiated, no information was available on the prevalence of either human cysticercosis or NCC and their association with epilepsy in Burkina Faso. Such information is key to the development of effective prevention programs and policies for epilepsy in the country. The objective of this study was to estimate the prevalence of NCC-associated epilepsy in three villages of Burkina Faso and the proportion of NCC among people with epilepsy (PWE). We also describe the stage of cyst evolution among people who had CT-identified lesions of NCC.
- Top of page
- Supporting Information
This is the first community-based study of NCC in Burkina Faso. Nearly half of the PWE living in two villages where pigs were raised had NCC, whereas we found no case of NCC among PWE in a village with very few pigs.
Our results are consistent with a recent meta-analysis, which reported that 29% (95% CI 23–36) of PWE have lesions of NCC on imaging of the brain (CT scans or MRI) in endemic areas (Ndimubanzi et al., 2010). Indeed, if we include patients with lesions suggestive of NCC based on the CT scan only (not serology), the proportion of PWE with NCC lesions is 28% (19 of 68) across the three villages.
Our results show a higher prevalence of NCC among PWE than in a clinic-based study from the Mbulu district of Tanzania where NCC was reported in 18% of 212 PWE diagnosed 2–4 years before the study and who were receiving care (Winkler et al., 2009). This difference could be explained by two main reasons. First, the Tanzanian study was limited to patients who were diagnosed at least 2 years before the start of the study, which contrasts with the fact that 25% of our cases had their first seizure in the last 2 years. Moreover, the percentage of active lesions was higher among cases with more recent seizure onset. This resulted in a larger proportion of cases in our study showing active lesions at the CT scan (37% of participants with lesions of NCC), in contrast to only 16% in the Tanzanian study. In other words, our case group represented more recent epilepsy cases, which could explain why NCC lesions were more often observed. The alternative explanation (or additional one) may be that NCC is more common in the villages selected in our study.
In a study of volunteers in Menoua Division, Cameroon, a region where pig breeding is common, Nguekam et al. (2003) found a prevalence of 59% of brain CT lesions suggestive of NCC among those with a positive serologic reaction to T. solium larvae antigen identified with the AgELISA. In our investigation, 9 (90%) of 10 seropositive cases had absolute or highly suggestive lesions of NCC. Furthermore, in the investigation of Nguekam et al., only 22 (65%) of 34 seropositive cases agreed to the CT scan of the brain. The true proportion of subjects with CT-scan lesions suggestive of NCC could be higher or lower if the proportion was different in the participants who declined having the brain scan. In the Eastern Cape Province, South Africa, Foyaca-Sibat et al. (2009) reported a prevalence of 37% (95% CI 27–48) of CT-scan lesions suggestive of NCC in PWE receiving medical care. This high percentage of NCC-associated epilepsy may be due to the low proportion (<0.5%) of self-reported Muslims in the 2001 census in that province (Statistics South Africa, 2004).
No cases of NCC were found among PWE living in Nyonyogo, where most people do not consume pork meat and very few pigs are raised. Hence, it is unlikely that the environment is contaminated with T. solium in that village. Similar results were reported by Secka et al. (2010) in the Gambia in a case–control study that included 210 PWE (cases) and 420 controls matched by gender and age (±5 years), with 95% of the study population being Muslim. In that study, all the participants had a T. solium serologic screening with EITB and AgELISA, and the respondents with positive results (three cases and six controls with AgELISA; none with EITB) had a cranial CT scan. No significant association between epilepsy and cysticercosis was found (odds ratio 0.75, 95% CI 0.13–3.15]). None of the nine participants who had a CT scan had brain lesions suggestive of NCC.
The manner in which pigs are typically raised (e.g., confined, tethered, or roaming) may influence the prevalence of cysticercosis in both pigs and humans (Vázquez-Flores et al., 2001; Morales et al., 2006). The proportion of NCC among PWE was very similar in Pabré and Batondo, which is not surprising, since, even though pigs were raised differently during the rainy season, they were left to roam in both villages during the dry season (Ganaba et al., 2011). Indeed, the seroprevalence of pig infection was very similar in the two villages (Ganaba et al., 2011). What is more surprising, however, is that the seroprevalence to the antigens of T. solium in humans was much lower in Pabré than Batondo (Carabin et al., 2009). In a study in Cameroon, Shey-Njila et al. (2003) did not find any significant difference in the prevalence of cysticercosis between permanently confined and partially confined pigs. Rather, they identified factors associated with infection in pigs as the absence of latrines in the household and the defecation of the household members in the pigpens. A similar situation is likely to exist in the present study, where only 8% of the randomly selected participants reported using a latrine in Batondo, 11% in Nyonyogo, and 37% in Pabré. The NCC-associated epilepsy cases were older in Pabré (median age 57 years) compared to the ones in Batondo (median age 25 years), but the difference was not statistically significant (p = 0.09 with the Mann-Whitney test). It is possible that the seroprevalence in Pabré was lower due to the recent improvements in sanitation, with the NCC being a reflection of past infections, but the proportion of NCC patients with active lesions was similar. The sample size in Pabré was very small, which limits our ability to explore the differences further.
People with NCC and epilepsy were older than PWE without NCC. In addition, the age at onset of seizures was higher among those with NCC-associated epilepsy as compared to those without NCC. This would support the often-mentioned fact that tapeworm infection and cysticercosis are rare in children and affect mostly adults (Prabhakar & Singh, 2002b). Moreover, epilepsy with hereditary or congenital etiology is more likely to manifest early, whereas epilepsy caused by environmental factors may have a later onset.
The present study had some limitations. First, the sample may not be representative of all PWE. Self-identified cases had more generalized seizures, which are easily identifiable by the subject, his or her family, and friends. Moreover, villagers younger than 7 years of age were not included in the study. Even if NCC is rare in young children, some cases have been diagnosed in this age group (Ruiz-García et al., 1997; Salazar & Cornejo, 1997; Ferreira et al., 2001; Scott et al., 2005; Saenz et al., 2006). Other plausible reasons for error in estimating the true prevalence of NCC-associated epilepsy are that PWE may conceal their disease because of fear of stigmatization, and the questionnaire used for screening might have failed to identify some cases with more unusual types of seizure manifestations that were not recognized as epilepsy. If the distribution of NCC varies depending on the type of seizures, it could introduce a bias in our estimate of the proportion of NCC among people with epilepsy. Moreover, imperfect sensitivity and specificity of the AgELISA test used to identify cysticercosis would have influenced the final serology results. The AgELISA serologic test is useful for the diagnosis of current cysticercosis cases, with active cyst antigens circulating in the sera. The AgELISA is not designed to detect past infections (Garcia et al. 2002; Dorny et al., 2004b), and has a poor sensitivity to do so (Praet et al., 2010). This means that the AgELISA will not perform well in older NCC cases (colloidal and calcified lesions) where no circulating antigens are expected to be present. In our study, 4 (40%) of the 10 cases with calcifications and colloidal lesions only with a serologic test had a positive result, whereas 5 (71%) of 7 cases with cystic lesions (with or without scolex) were tested positive. The positive AgELISA results in participants with calcified lesions is mostly likely due to cystic lesions located elsewhere (outside the brain) given the endemic nature of the study villages. Our choice of AgELISA instead of the EITB may have led to an underestimation of the proportion of PWE cases with NCC, or in classifying fewer NCC cases as definite instead of probable. In addition, serologic results for eight epilepsy cases were missing. Finally, magnetic resonance imaging (MRI) might have been more efficient in identifying some types of NCC lesions (White & Garcia, 1999). Indeed, MRI is superior to CT for detecting NCC lesions such as cysts present in the ventricules, whereas CT is more effective for the detection of calcifications. However, no MRI device was available in Burkina Faso at the time of the study. The fact that there were few PWE also limits our ability to run a multivariate analysis of factors associated with NCC. Finally, this was a pilot study including only three villages, which may not represent the true situation in the country as a whole.