The epidemiology and geographic distribution of relapsing fever borreliosis in West and North Africa, with a review of the Ornithodoros erraticus complex (Acari: Ixodida)

Abstract

Background: Relapsing fever is the most frequent bacterial disease in Africa. Four main vector / pathogen complexes are classically recognized, with the louse Pediculus humanus acting as vector for B. recurrentis and the soft ticks Ornithodoros sonrai, O. erraticus and O. moubata acting as vectors for Borrelia crocidurae, B. hispanica and B. duttonii, respectively. Our aim was to investigate the epidemiology of the disease in West, North and Central Africa.

Methods and findings: From 2002 to 2012, we conducted field surveys in 17 African countries and in Spain. We investigated the occurrence of Ornithodoros ticks in rodent burrows in 282 study sites. We collected 1,629 small mammals that may act as reservoir for Borrelia infections. Using molecular methods we studied genetic diversity among Ornithodoros ticks and Borrelia infections in ticks and small mammals. Of 9,870 burrows investigated, 1,196 (12.1%) were inhabited by Ornithodoros ticks. In West Africa, the southern and eastern limits of the vectors and Borrelia infections in ticks and small mammals were 13°N and 01°E, respectively. Molecular studies revealed the occurrence of nine different Ornithodoros species, including five species new for science, with six of them harboring Borrelia infections. Only B. crocidurae was found in West Africa and three Borrelia species were identified in North Africa: B. crocidurae, B. hispanica, and B. merionesi.

Conclusions: Borrelia Spirochetes responsible for relapsing fever in humans are highly prevalent both in Ornithodoros ticks and small mammals in North and West Africa but Ornithodoros ticks seem absent south of 13°N and small mammals are not infected in these regions. The number of Ornithodoros species acting as vector of relapsing fever is much higher than previously known.

Figure 1. Map of northwestern Africa with the location of study sites positive (red circles) or negative (blue circles) for the occurrence of Ornithodoros ticks in small mammal burrows.

At least 30 burrows were investigated in each negative site.

Figure 2. Phylogenetic relationships among Ornithodoros species using 16S rRNA sequences (820 seq.).

The colored triangles indicate the genetic diversity of the sequences detected for each Ornithodoros species. The colored-spots correspond to the Borrelia species detected in each tick species. The phylogram was constructed using a maximum-likelihood method from partial 16S sequence data (457 nucleotides). Bootstrap values >90 are shown (Scale bar, 0.05 substitutions per site). Ornithodoros moubata (GenBank accession number AB073679), O. porcinus (GenBank acc. no. AB105451), O. turicata (GenBank acc. no. L34327), and O. parkeri (GenBank acc. no. EU009925) were treated as outgroups. Five of these species are newly described: O. occidentalis, O. costalis, O. rupestris, O. kairouanensis, and O. merionesi.

Figure 3. Map of northwestern Africa with the distribution of Ornithodoros species found in small mammal burrows.

Figure 4. Phylogenetic relationships among Borrelia species using partial Intergenic spacer (IGS, 510 nucleotides) and partial FlaB gene (FLA, 269 nucleotides) concatenated sequences

(PhyML 100 bootstraps, available at http://mobyle.pasteur.fr/cgi-bin/portal.py). The colored triangle estimated the Borrelia species diversity. We included in the B. merionesi clade (9 seq.) a Borrelia detected in a rodent captured in El Argoub (Morocco). The colored full circle correspond to the tick species determined by the 16S phylogenetic analysis of this study. The phylogram was constructed using a maximum-likelihood method from concatenated sequence data (220 sequences including GenBank reference sequences, 779 nucleotides). Bootstrap values >70 are shown (Scale bar, 0.01 substitutions per site). Seq. A.: B. crocidurae (GU350723 and NC017808), seq. B.: B. recurrentis (DQ000277 and DQ346814), seq. C.: B. duttonii (DQ000279 and DQ346833), seq. D.: B. merionesi (JX257047 and JX257050), seq. E.: B. hispanica (GU350718 and GU357614) and concatened sequences were used as references.

Figure 5. Map of northwestern Africa with the distribution of Borrelia species found in Ornithodoros ticks and/or rodents.

Figure 6. Projection of individual ticks on the first factorial plane of a Linear Discriminant Analysis.

All ticks collected in the same location project to the same point. The percentages along the axes labels are the proportions of between-species variance explained by the corresponding linear discriminant. Units have no meaning. The labels indicating each species are located at the center of the individual points belonging to that species. Ellipses encompass around 66% of the distribution of each species. Abbreviations: so: O. sonrai, co: O. costalis, ma: O. marocanus, oc: O. occidentalis, me: O. merionesi, ka: O. kairouanensis, er: O. erraticus, no: O. normandi, ru: O. rupestris.

Figure 7. Dorsal view of O. erraticus (A), O. marocanus (B), O. sonrai (C), O. costalis (D), O. merionesi (E), O. occidentalis (F), O. rupestris (G), and O. kairouanensis (H).