Ongoing Transmission of Onchocerca volvulus after 25 Years of Annual Ivermectin Mass Treatments in the Vina du Nord River Valley, in North Cameroon.

BACKGROUND:Recent reports of transmission interruption of Onchocerca volvulus, the causing agent of river blindness, in former endemic foci in the Americas, and more recently in West and East Africa, raise the question whether elimination of this debilitating disease is underway after long-term treatment of the population at risk with ivermectin. The situation in Central Africa has not yet been clearly assessed. METHODS AND FINDINGS:Entomologic data from two former endemic river basins in North Cameroon were generated over a period of 43 and 48 months to follow-up transmission levels in areas under prolonged ivermectin control. Moreover, epidemiologic parameters of animal-borne Onchocerca spp. transmitted by the same local black fly vectors of the Simulium damnosum complex were recorded and their impact on O. volvulus transmission success evaluated. With mitochondrial DNA markers we unambiguously confirmed the presence of infective O. volvulus larvae in vectors from the Sudan savannah region (mean Annual Transmission Potential 2009-2012: 98, range 47-221), but not from the Adamawa highland region. Transmission rates of O. ochengi, a parasite of Zebu cattle, were high in both foci. CONCLUSIONS/SIGNIFICANCE:The high cattle livestock density in conjunction with the high transmission rates of the bovine filaria O. ochengi prevents the transmission of O. volvulus on the Adamawa plateau, whereas transmission in a former hyperendemic focus was markedly reduced, but not completely interrupted after 25 years of ivermectin control. This study may be helpful to gauge the impact of the presence of animal-filariae for O. volvulus transmission in terms of the growing human and livestock populations in sub-Saharan countries

Onchocerca ochengi transmission dynamics and the correlation of O. ochengi microfilaria density in cattle with the transmission potential

The intensity of natural transmission of Onchocerca ochengi and Onchocerca volvulus by anthropo-boophilic Simulium damnosum s.l. was studied longitudinally in two cattle watering sites of a cattle ranch within a predominantly cattle populated area of the Guinea savanna of Cameroon and related to cattle O. ochengi skin microfilaria abundance. During the 12 months study period, a total of 4 696 flies was individually dissected to examine the monthly transmission potential (MTP) of O. ochengi and O. volvulus. The estimated Simulium damnosum s.l. annual biting rates (ABR) on human baits were 47 529 flies at the bank of the Vina "du sud"river. The ABR at the lake, which was situated at about 2 km upland from the perennial river, was 8 579. The monthly parous rate was highly correlated with monthly biting rate. The annual transmission potentials (ATP) of O. ochengi were calculated to be 7 732 and 1 669 at the riverbank and the lake, respectively. Transmission occurred mainly in the dry season, peaking in the months of January to mid-March when dermal microfilaria density in the animals was also the highest. The O. ochengi microfilaria uptake by the fly vectors was host microfilaria density-dependent. The MTP of O. ochengi was positively correlated with dermal microfilaria density. The mean number of microfilariae per fly taken up during a blood meal was high during the dry season as was the mean number of infective larvae per fly but declined significantly with the onset of the early rains. A similar seasonality of transmission was also observed for O. volvulus that was concurrently transmitted by the same vector flies, but its ATP was comparatively much lower: 1 332 infective larvae per man per year at the riverbank and 107 around the lake. The population dynamics of cattle microfilariae therefore plays an important role in the regulation of O. ochengi transmission.Dynamique de la transmission de Onchocerca ochengi et corrélation entre la densité de leurs microfilaires chez les bovins et le potentiel de transmission. L'intensité de la transmission naturelle de Onchocerca ochengi et Onchocerca volvulus par l'anthropo-boophile Simulium damnosum s.I. a été étudiée longitudinalement à deux points d'eau d'un élevage de bovins, situé dans une région de savane guinéenne du Cameroun comportant une population principalement bovine, et a été corrélée à l'abondance en microfilaires de O. ochengi dans la peau des bovins. Au cours des 12 mois de l'étude, un total de 4 696 mouches a été disséqué individuellement, afin d'examiner le potentiel de transmission mensuel (PTM) de O. ochengi et O. volvulus. Les taux annuels de morsures (TAM) estimés de Simulium damnosum s.I. sur des proies humaines étaient de 47 529 mouches sur les berges de la rivière Vina du Sud. Les TAM autour du lac, situé à environ 2 km sur les plateaux dominant la rivière permanente, était de 8 579. Le taux de parité mensuelle était fortement corrélé au taux mensuel de morsures. Les potentiels de transmission annuels (PTA) de O. ochengi ont été de 7 732 et 1 669 au niveau de la rivière et du lac, respectivement. La transmission s'est produite principalement pendant la saison sèche, avec un pic pendant les mois de janvier à mi-mars, lorsque la densité de microfilaires dans le derme des animaux était également la plus forte. Le captage des microfilaires de O. ochengi par les mouches vecteurs était dépendant de la densité en microfilaires dans le derme de l'hôte. Le PTM de O. ochengi était positivement corrélé à la densité en microfilaires du derme. Le nombre moyen de microfilaires capté par mouche durant un repas sanguin était élevé durant la saison sèche, comme l'était le nombre moyen de larves infestantes par mouche, mais déclinait significativement avec le début des premières pluies. Un phénomène saisonnier similaire a été également observé pour la transmission de O. volvulus, qui était simultanément transmis par les mêmes mouches vecteurs, mais son PTA était comparativement beaucoup plus faible : 1 332 larves infestantes par humain et par an au bord de la rivière, et 107 autour du lac. La dynamique de population des microfilaires des bovins joue donc un rôle important dans la régulation de la transmission de O. ochengi

Annual biting rates.

<p>Annual biting rates of <i>Onchocerca</i> spp. from two onchocerciasis foci in North Cameroon. Each data point starts at the beginning of the rainy season (April) till the end of the dry season (March of the following year). Years with no data are left blank. <b>A</b> Soramboum, Vina du Nord. Epidemiological data prior to 1998 was published before and modified to fit this graph. Data from 1976 was taken from Touboro, 30 km further downstream. <b>B</b> Galim, Vina du Sud. Epidemiological data prior to 1997 was published before and modified to fit this graph.</p

Entomologic parameters and proportion of filarial stages from <i>Simulium damnosum s</i>.<i>l</i>. at two different sites in Northern Cameroon.

<p>Entomologic parameters and proportion of filarial stages from <i>Simulium damnosum s</i>.<i>l</i>. at two different sites in Northern Cameroon.</p

L3 species proportion.

<p>Species composition of infective third-stage larvae from <i>S</i>. <i>damnosum s</i>.<i>l</i>. at two foci in North Cameroon. White: <i>O</i>. <i>volvulus</i>; light grey: <i>O</i>. <i>ochengi</i> 'Siisa' type; medium grey: <i>O</i>. <i>ochengi</i>; dark grey: <i>O</i>. <i>ramachandrini</i>. <b>A-B</b> Soramboum, Vina du Nord. <b>C-D</b> Galim, Vina du Sud. Left side (A, C): morphological identification. Right side (B, D): PCR-based identification.</p

Annual transmission potentials.

<p>Annual transmission potentials of <i>Onchocerca</i> spp. from two onchocerciasis foci in North Cameroon. Data is given at the beginning of the rainy season (April) till the end of the dry season (March of the following year). Dark grey: <i>O</i>. <i>ramachandrini</i>; light grey: <i>O</i>. <i>ochengi</i>; white: <i>O</i>. <i>volvulus</i>. Insufficient fly dissection data from 1986, 1989–1992 in Soramboum, and from 1985–1987, 1990 and 1997 in Galim have been extrapolated. In 1976 (color transition of white, light grey to dark grey) no species discrimination was done. ATP with available MTP data ≥ 80% have borders in bold; those with data 80% > x ≥ 30% have normal borders, and those with data < 30% have borders with a dotted line. The dotted line marks the beginning of ivermectin mass treatments. The asterisk indicates the introduction of PCR-based methods for species discrimination in the vector. Prior to 1990, the L3 species was determined according to the following body length criteria: <i>O</i>. <i>volvulus</i> ≤ 750 μm; 750 μm < <i>O</i>. <i>ochengi</i> < 900 μm; <i>O</i>. <i>ramachandrini</i> ≥ 900 μm. <b>A</b> Soramboum, Vina du Nord. Epidemiological data prior to 1998 was published before and modified to fit this graph. Data from 1976 was taken from Touboro, 30 km further downstream. <b>B</b> Galim, Vina du Sud. Epidemiological data prior to 1997 was published before and modified to fit this graph.</p

L3 body lengths.

<p>Violin plot of the L3 body lengths of identified <i>Onchocerca</i> spp. in <i>S</i>. <i>damnosum s</i>.<i>l</i>. from North Cameroon. Species identification is based on morphological (light grey) and molecular-genetic (dark grey) characteristics. Two genotypes of <i>O</i>. <i>ochengi</i>, <i>O</i>. <i>ochengi s</i>. <i>str</i>. and <i>O</i>. <i>ochengi</i> 'Siisa', are shown based on their mitochondrial clades. ***<i>P</i> < 0.001; **0.01 > <i>P</i> > 0.001; *<i>P</i> < 0.05.</p