Prevalence and factors associated with human Taenia solium taeniosis and cysticercosis in twelve remote villages of Ranomafana rainforest, Madagascar

Abstract

Background

Infections with the tapeworm Taenia solium (taeniosis and cysticercosis) are Neglected Tropical Diseases (NTD) highly endemic in Madagascar. These infections are however underdiagnosed, underreported and their burden at the community level remains unknown especially in rural remote settings. This study aims at assessing the prevalence of T. solium infections and associated risk factors in twelve remote villages surrounding Ranomafana National Park (RNP), Ifanadiana District, Madagascar.

Methodology

A community based cross-sectional survey was conducted in June 2016. Stool and serum samples were collected from participants. Tapeworm carriers were identified by stool examination. Taenia species and T. solium genotypes were characterised by PCR and sequencing of the mitochondrial cytochrome c oxidase subunit 1 ( cox1) gene. Detection of specific anti-cysticercal antibodies (IgG) or circulating cysticercal antigens was performed by ELISA or EITB/Western blot assays.

Principal findings

Of the 459 participants with paired stool and blood samples included ten participants from seven distinct villages harbored Taenia spp. eggs in their stools samples DNA sequencing of the cox1 gene revealed a majority of T. solium Asian genotype (9/10) carriage. The overall seroprevalences of anti-cysticercal IgGs detected by ELISA and EITB were quite similar (27.5% and 29.8% respectively). A prevalence rate of 12.4% of circulating cysticercal antigens was observed reflecting cysticercosis with viable cysts. Open defecation (Odds Ratio, OR = 1.5, 95% CI: 1.0–2.3) and promiscuity with households of more than 4 people (OR = 1.9, 95% CI: 1.1–3.1) seem to be the main risk factors associated with anticysticercal antibodies detection. Being over 15 years of age would be a risk factor associated with an active cysticercosis (OR = 1.6, 95% CI: 1.0–2.7). Females (OR = 0.5, 95% CI: 0.3–0.9) and use of river as house water source (OR = 0.3, 95% CI: 0.1–1.5) were less likely to have cysticercosis with viable cysts.

Conclusions/Significance

This study indicates a high exposure of the investigated population to T. solium infections with a high prevalence of cysticercosis with viable cysts. These data can be useful to strengthen public health interventions in these remote settings.

Author summary

Taenia solium infections in humans (taeniosis and neurocysticercosis) and in pigs (cysticercosis) are endemic in Madagascar presenting a significant public health burden. Neurocysticercosis with localization of the parasite in the Central Nervous System is the most severe and frequent form of parasitic brain diseases in humans and responsible of thousands of worldwide deaths per year. Madagascar is a T. solium endemic country where poor sanitation, free roaming pigs and outdoor defecation are common, and maintain the parasite transmission cycle. Little information is available regarding taeniosis/cysticercosis epidemiology in Madagascar. We carried out a community-based study to investigate the prevalence of human taeniosis/cysticercosis and associated risk factors in 12 rural remote villages of Ranomafana and Kelilalina townships (Ifanadiana district, Madagascar). Our results reveal that in 7/12 villages investigated, a high number of participants had teaniosis. Moreover, a high number of active cysticercosis cases were detected. Open defecation and promiscuity were seemed to be the main risk factors associated to T. solium infections. The results of this study will be useful to guide interventions in these remote settings surrounding the Ranomafana National Park.