Evidence of suppression of onchocerciasis transmission in the Venezuelan Amazonian focus

Abstract

Background: The World Health Organization (WHO) has set goals for onchocerciasis elimination in Latin America by 2015. Most of the six previously endemic countries are attaining this goal by implementing twice a year (and in some foci, quarterly) mass ivermectin (Mectizan®) distribution. Elimination of transmission has been verified in Colombia, Ecuador and Mexico. Challenges remain in the Amazonian focus straddling Venezuela and Brazil, where the disease affects the hard-to-reach Yanomami indigenous population. We provide evidence of suppression of Onchocerca volvulus transmission by Simulium guianense s.l. in 16 previously hyperendemic Yanomami communities in southern Venezuela after 15 years of 6-monthly and 5 years of 3-monthly mass ivermectin treatment.

Methods: Baseline and monitoring and evaluation parasitological, ophthalmological, entomological and serological surveys were conducted in selected sentinel and extra-sentinel communities of the focus throughout the implementation of the programme.

Results: From 2010 to 2012-2015, clinico-parasitological surveys indicate a substantial decrease in skin microfilarial prevalence and intensity of infection; accompanied by no evidence (or very low prevalence and intensity) of ocular microfilariae in the examined population. Of a total of 51,341 S. guianense flies tested by PCR none had L3 infection (heads only). Prevalence of infective flies and seasonal transmission potentials in 2012-2013 were, respectively, under 1% and 20 L3/person/transmission season. Serology in children aged 1-10 years demonstrated that although 26 out of 396 (7%) individuals still had Ov-16 antibodies, only 4/218 (2%) seropositives were aged 1-5 years.

Conclusions: We report evidence of recent transmission and morbidity suppression in some communities of the focus representing 75% of the Yanomami population and 70% of all known communities. We conclude that onchocerciasis transmission could be feasibly interrupted in the Venezuelan Amazonian focus.

Fig. 1

Venezuelan part of the Amazonian onchocerciasis focus. The legend lists the 12 geographical areas of the focus coloured by baseline endemicity of Onchocerca volvulus infection, from lowest (light blue) in Ventuari to highest (dark red) in Orinoquito. The numbers indicate the 31 geographical sub-areas described in Table 1

Fig. 2

Temporal trends in therapeutic coverage (%) of ivermectin treatment for the eligible Yanomami population in the Venezuelan part of the Amazonian focus. From 1993 through 1999, treatment was distributed annually by mobile teams. In 2000 treatment frequency was increased to twice per year and in 2009 to four times per year. a Coverage of annual and twice per year treatment. b Coverage of three-monthly treatment since 2009 (black, grey, hatched and dotted bars indicate, respectively, the therapeutic coverage in the first, second, third and fourth quarters of the year). The red horizontal line at 85 % in both (a) and (b) indicates the minimum coverage of eligibles that needs to be reached and sustained to interrupt transmission according to OEPA’s strategy

Fig. 3

Ivermectin rounds by geographical sub-area in the Venezuelan part of the Amazonian focus. The number of treatment rounds achieving ≥85 % coverage for twice per year and quarterly treatment frequency by decreasing order for the 31 geographical sub-areas of the focus. The grey and black sections of the bars indicate, respectively, the number of rounds that achieved the desired ≥85 % coverage at twice per year and quarterly frequency (Table S1 of Additional file 1)

Fig. 4

Temporal trends of Onchocerca volvulus infection in sentinel communities of the Venezuelan part of the Amazonian focus. For each panel, the baseline values of microfilarial prevalence (%) and intensity (arithmetic mean no. mf/mg) were averaged and plotted for 1995. The solid lines and circles represent infection prevalence, and the dotted lines and open circles represent infection intensity. (a) Hasupiwei; (b) Awei; (c) Pashopëka; (d) Koyowë

Fig. 5

Temporal trends of ocular onchocerciasis prevalence in sentinel communities of the Venezuelan part of the Amazonian focus. a Prevalence of microfilariae in the cornea (MFC). b Prevalence of microfilariae in the anterior chamber of the eye (MFAC). Orange triangles: Hasupiwei; red diamonds: Awei; black circles: Pashopëka; green squares: Koyowë; blue triangles: Waharafitha; purple squares: Matoa; brown circles: Kanoshewë