Introduction
Ticks are vectors of a range of viral, bacterial, and protozoan pathogens of economic and public health importance (de la Fuente et al.,
2008). Babesiosis, theileriosis, and anaplasmosis cause major livestock
production losses in Kenya (Franck et al., 2015; Gachohi et al., 2012;
Latib et al., 1995; Norval et al., 1984), while rickettsiosis
constitutes a serious emerging public health threat globally (Brown,
2016; Fournier et al., 2017; Jensenius et al., 2017; Maina et al., 2017;
Ndip et al., 2004; Parola et al., 2013; Rutherford et al., 2004). In
addition to Rickettsia, tick-borne bacteria such as Ehrlichia and Anaplasma, and protozoa such as Babesia have been shown to infect humans in the Americas and
Europe (Doudier et al., 2010). Ticks also transmit nairoviruses, most of
which cause a mild febrile illness in humans, but
some, such as Crimean-Congo haemorrhagic fever (CCHF) and Dugbe viruses,
can cause severe systemic illness and mortality, affirming the
importance of ticks in the transmission of viral haemorrhagic fevers
(Papa et al., 2017). In livestock, Nairobi sheep disease virus, also a Nairovirus, is a constant threat to sheep production in East
Africa and the Horn of Africa (Baron, 2015).
While the vectorial capacity of ticks is established, the role of lice
and fleas in the epidemiology of vector-borne zoonoses is rarely
investigated. Flea-borne rickettsioses, such as murine typhus
(Rickettsia typhi) and flea-borne spotted fever (Rickettsia
felis), both endemic in East Africa, are transmitted by Xenopsylla cheopis and Ctenocephalides felis fleas,
respectively. However, these Rickettsia spp. have been detected
in several other flea species in addition to the chief vectors
(Luce-fedrow et al., 2015). Louse infestations result in severe pruritic
mange in livestock, leading to production losses (Hornok et al., 2010),
and epidemic typhus, caused by Rickettsia prowazekii, in humans,
especially in overcrowded and poor social settings (Raoult & Roux,
1997).
With travel and trade thought to be major drivers of emerging pathogen
spread (Kilpatrick, 2012), the movement of livestock and people among
East African countries could enhance the circulation of emerging
pathogens, especially given that high arboviral activity has been
reported across the region (Mossel et al., 2017; Nyaruaba et al., 2019).
Smallholder livestock production in East Africa is associated with
livestock movement across provincial and national borders to livestock
markets (LMs) in peri-urban areas (Fèvre et al., 2005) in which animals
have been found to be heavily infested by ticks (Sang et al., 2006).
Livestock movement plays a major role in the introduction of infective
foci in naïve areas where they can then be disseminated by capable
vectors (Fèvre et al., 2006). Livestock movements have been implicated in
past and recent Rift Valley fever (RVF) outbreaks in Kenya (Baba et al.
2016; Munyua et al., 2010; WHO, 2018).
Outbreaks of CCHF (Dunster et al., 2002) and RVF (WHO, 2018) have been
reported before in Western Kenya, and there is serological evidence of
circulation of chikungunya, yellow fever, West Nile, and RVF viruses
(Cook et al., 2017; Inziani et al., 2020; Mease et al., 2011; Nyaruaba
et al., 2019). While reports on the occurrence of zoonotic vector-borne
bacteria are scant, the high prevalence of malaria in western Kenya
results in under-investigation of other causes of febrile illnesses.
Ticks, fleas, and lice may be both vectors and reservoirs of most
pathogens they transmit, making them an important component in the
transmission dynamics of vector-borne zoonoses (Raoult & Roux, 1997).
Elsewhere in Kenya and East Africa, the occurrence of bacterial
pathogens of zoonotic and veterinary potential in ticks and fleas has
been reported. Tick and flea-borne spotted fever group (SFG)
rickettsiosis agents (R. africae, Rickettsia conorii, Rickettsia aeschlimanii, R. felis, and Rickettsia
asembonensis sp. nov.) have been detected elsewhere in Kenya (Maina et
al., 2014, 2019; Mwamuye et al., 2017; Macaluso et al., 2003) and East
Africa (Kumsa et al., 2015; Nakao et al., 2013; Nakayima et al., 2014).
A broad spectrum of bacteria and protozoa of veterinary and public
health importance have also been detected, including Theileria
parva, Ehrlichia ruminantium, Ehrlichia chaffeensis, Anaplasma marginale, Anaplasma phagocytophilum, and Anaplasma platys (Oundo et al., 2020; Ringo et al., 2018; Omondi
et al., 2017; Mwamuye et al., 2017; Teshale et al., 2015). Hyalomma, Amblyomma, and Rhipicephalus ticks
sampled from livestock in North-Eastern Kenya were previously shown to
be infected with CCHF, Bunyamwera, Dugbe, Ndumu, Semliki forest,
Thogoto, Ngari, Dhori, and West Nile viruses (Lwande et al., 2013; Sang
et al., 2011, 2006). These viruses are endemic in East Africa (Nyaruaba
et al., 2019) and some, such as Semliki Forest, Wesselsbron, Ngari, and
Bunyamwera viruses, have only been isolated from mosquitoes (Ajamma et
al., 2018; Villinger et al., 2017; Lwande et al., 2013). In most
instances, ticks with arboviruses were collected from cattle at LMs and
abattoirs, confirming the importance of these facilities for
epidemiological investigations of these viruses.
Active surveillance for zoonotic pathogens and their vectors generates
information on their presence and prevalence and can identify novel
vector-pathogen associations. Such information can facilitate early
detection and quantification of pathogen burdens and thus is important
for planning control strategies to reduce spill-over infection from
livestock to humans. Most of the diseases are characterised by
non-specific febrile illness, which can be easily confused with other
fever-causing agents. Awareness of their presence improves clinical
referral and diagnosis.
To investigate the risk posed by the movement of arthropod vector
infested animals via LMs in the Lake Victoria basin of East Africa, we
collected ticks, fleas, and lice from livestock at both LMs and
slaughterhouses (SHs). We employed high-throughput molecular techniques
coupled with Sanger sequencing to rapidly detect pathogens of zoonotic
and veterinary importance in these arthropods.