Review Article
Prevalence of Rickettsia africae in tick vectors collected from mammalian hosts in sub-Saharan Africa: A systematic review and meta-analysis

https://doi.org/10.1016/j.ttbdis.2022.101960Get rights and content

Abstract

African tick bite fever (ATBF) is one of the most important rickettsial infections in international travellers to sub-Saharan Africa. The heterogeneity of Rickettsia africae infection rates among tick vector species has been studied. However, this information has not been systematised to allow for comparative estimates. Quantifying the trends and heterogeneity in R. africae infection rates among the different tick vector species is paramount in understanding the role in transmission to humans. A systematic search was conducted in PubMed, Web of Knowledge, Google Scholar, and SCOPUS from 2005 to 2020. The selection criteria included all studies in sub-Saharan Africa reporting R. africae infection rates in tick adults, nymphs, and larvae. A quality effects model was used in the meta-analysis due to the observed heterogeneity with an assessment of publication bias using funnel plots. The prevalence estimates were conducted by geographic region and tick genus from 32 studies reporting R. africae infection rates in ticks from sub-Saharan Africa. A total of 12,301 ticks comprising of adults (96.19%, n=11, 832), nymphs (3.6%, n=443) and larvae (0.2%, n=26) and 1214 pooled samples were evaluated for R. africae infection. The overall prevalence of R. africae was higher in Amblyomma spp. (48%, 95% CI: 26-70%) compared to Rhipicephalus spp. (1%, 95% CI: 0-5%), Hyalomma spp. (1%, 95% CI: 0-3%) and other tick genera (1%, 95% CI: 0-4%) throughout all regions. The highest prevalence in Amblyomma spp. was recorded in western Africa (53%, 95% CI: 14-90%) and in Rhipicephalus spp. in southern Africa (2%, 95% CI: 0-5%). Cattle were the most frequently sampled hosts across all tick vectors (62.98%, n=5492), followed by goats (19.07%, n= 1663) and sheep (9.1%, n= 793). To our knowledge, this is the first systematic and quantitative analysis of R. africae infection in tick vectors collected from mammalian hosts in sub-Saharan Africa. The results highlight a marked heterogeneity between species in different regions of sub-Saharan Africa and provide initial estimates of infection rates.

Introduction

Ticks and tick-borne diseases (TTBDs) pose a global threat to the health of humans, domestic animals, and wildlife (Oliveira et al., 2017). The primary threat imposed by ticks lies in their role as vectors in the transmission of pathogenic organisms such as bacteria, viruses, protozoa, and helminths (Baneth, 2014). Some of the major pathogens from the genus Anaplasma, Rickettsia, and Babesia have been recognized as human pathogens with an increasing number of new species and genetic variants (Sahni et al., 2019; Schnittger et al., 2012; Yang et al., 2017). The ongoing geographic expansion of tick species, driven by climatic and environmental changes, has increased awareness on emerging tick-borne pathogens globally (Bouchard et al., 2019; Ogden et al., 2021).

These factors have inspired TTBD surveillance studies in sub-Saharan Africa, where livestock farming is a major source of income (Jongejan and Uilenberg, 2004; Parola et al., 2013). Livestock may act as intermediate or amplifier hosts, from which pathogens can spill over into humans. Additionally, the landscape attracts wild animals into communities where livestock rearing is common; this brings humans and animals into close contact, creating a wildlife–livestock–human interface for disease emergence (Jones et al., 2013). Additionally, this poses a risk to travellers who frequent outdoor activities in endemic areas (Jensenius et al., 2003).

African tick bite fever (ATBF) is one such disease caused by Rickettsia africae, such an obligate intracellular bacterium that has recently emerged with high epidemiological success due to an increase in wildlife-human interactions (Kelly et al., 1996; Parola et al., 2005). Although it is an acute febrile illness, no commercially available diagnostic tests for ATBF exist due to extensive cross-reactivity between spotted fever group rickettsiae (Mazhetese et al., 2021). The lack of surveillance and diagnostics in endemic areas has limited the clinical awareness of ATBF in sub-Saharan Africa (Ndip et al., 2004). The distribution of R. africae through sub-Saharan Africa is dependent on the availability of their tick vectors. It has been detected in ticks from the genus Amblyomma, Hyalomma, and Rhipicephalus (Bitam, 2012). Amblyomma variegatum is considered the principal vector in sub-Saharan Africa and A. hebraeum in southern Africa (Jensenius et al., 2003).

In the last 15 years, several studies have reported prevalence estimates of R. africae in ticks from domestic ruminants and wildlife in sub-Saharan Africa. Despite the expanding geographical distribution of tick-borne R. africae across new regions by transport of livestock with infected vectors (Yssouf et al., 2014), bird migration (Battisti et al., 2020; Wallménius et al., 2014), and human movement, there is limited information summarizing the existing literature on the occurrence and geographical distribution of R. africae and its tick vectors in sub-Saharan Africa.

Therefore, this systematic review aimed to provide a summary on the geographical distribution of R. africae in tick vectors collected from mammalian hosts; quantitatively summarize the proportion of R. africae infection in tick vectors from literature through a meta-analysis; identify research gaps for future studies to understand the important vectors and vertebrate hosts in sub-Saharan Africa and provide a framework for prevention and control. We evaluated literature with prevalence estimates of R. africae according to tick vector species and geographical sampling region in the last 15 years.

Section snippets

Search strategy

A systematic literature search was undertaken following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Google Scholar, SCOPUS, PubMed, and Web of Science Core Collection were searched for peer-reviewed publications using Boolean Operators (AND, OR) and a combination of keywords including R. africae, tick vectors (Amblyomma, Hyalomma, Rhipicephalus), Africa, animal hosts, and epidemiology (Additional Table A.1).

Inclusion and exclusion criteria

The inclusion criteria were: (i) the

Results

The combined search yielded a result of 366 articles (Fig. 1).  After removing 64 duplicates, article titles and abstracts were screened for eligibility. The preliminary review identified 302 articles that warranted a full manuscript review. The exclusion of 258 records in Fig. 1 left 44 articles that met the inclusion criteria. In the final analysis, 32 articles from 19 countries in sub-Saharan Africa were included (Table 1). Thirty-two articles were evaluated as high quality with an index

Discussion

This systematic review assessed 32 articles that included 13,543 ticks from 36 species as potential vectors and reservoirs of R. africae over the past 15 years in sub-Saharan Africa. The meta-analysis on prevalence estimates sheds light on existing and potential vectors of R. africae. Among them, Amblyomma spp. had the highest overall R. africae prevalence (48%, 95% CI: 26-70%), with A. variegatum accounting for the highest prevalence (56%, 95% CI: 25-85%). The epidemiological importance of A.

Conclusion

This systematic review provides initial estimates that reflect the burden and epidemiological traits of R. africae infection in tick vectors throughout sub-Saharan Africa. The frequency of ATBF case reports in travellers to sub-Saharan Africa, and high prevalences of R. africae in endemic tick species are of major concern. In view of this, we recommend that health professionals consider the diagnosis of ATBF in patients with febrile illnesses returning from ATBF endemic countries where exposure

CRediT authorship contribution statement

Alicia Pillay: Conceptualization, Methodology, Writing – original draft. Tawanda Manyangadze: Methodology, Writing – review & editing, Formal analysis. Samson Mukaratirwa: Conceptualization, Validation, Writing – review & editing, Supervision, Funding acquisition.

Declaration of Competing Interest

The authors declare no conflict of interest.

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