Reilly T. Jackson1*, Tamika J.
Lunn1, Isabella K. DeAnglis1, Joseph
G. Ogola2, Paul W. Webala3, Kristian
M. Forbes1
- Department of Biological Sciences, University of Arkansas,
Fayetteville, Arkansas, USA
- Department of Medical Microbiology, University of Nairobi, Nairobi,
Kenya
- Department of Forestry and Wildlife Management, Maasai Mara
University, Narok, Kenya
*Correspondence author: rtj006@uark.edu
ABSTRACT
- Simultaneous use of domestic spaces by humans and wildlife is little
understood, despite global ubiquity, and can create an interface for
human exposure to wildlife pathogens. Bats are associated with several
pathogens that can spillover and cause disease in humans and, due to
loss of natural habitat and urbanization, are increasingly using
anthropogenic structures for roosting. The purpose of this study was
to characterize human interactions with bats in shared buildings to
assess potential for exposure risk to bat pathogens.
- We surveyed 102 people living and working in buildings used as bat
roots in rural Kenya between 2021 and 2023. Based on responses, we
characterized and quantified the timing, intensity, and frequency of
human-bat interactions occurring in this common domestic setting.
- Survey respondents reported living with bats in buildings year-round,
with cohabitation occurring for at least 10 years in 38% of cases.
Human contact with bats occurred through direct and indirect routes,
including exposure to excrement (90% of respondents), and direct
touching of bats (39% of respondents). Indirect contacts most often
occurred daily and direct contacts most often occurred yearly.
Domestic animal consumption of bats was also reported (16%
respondents).
- Synthesis and applications : We demonstrate that shared building
use by bats and humans in rural Kenya leads to prolonged, frequent,
and sometimes intense interactions between bats and humans, consistent
with exposure interfaces that can facilitate pathogen spillover.
Identifying and understanding the settings and practices that may lead
to zoonotic pathogen spillover is of great global importance for
developing countermeasures, and this study establishes bat roosts in
anthropogenic structures as such a setting.
KEYWORDS
Africa, Chiroptera, emerging infectious disease, human-wildlife
interaction, spillover, wildlife conflict, zoonosis
INTRODUCTION
Emerging infectious diseases (EIDs) are a significant threat to global
health and security, as demonstrated by the recent COVID-19 pandemic and
Mpox disease outbreak (Morens and Fauci 2013, Wang et al. 2022, Zumla et
al. 2022). Most EIDs have zoonotic origins and emerge in humans via
spillover of pathogens from animals, often wildlife (Jones et al. 2008).
These risks are exacerbated by growing human populations and conversion
of natural lands to anthropogenic regions, which increase human contacts
with wildlife and exposure to their pathogens (Woolhouse and
Gowtage-Sequeria 2005, Jones et al. 2008, Gottdenker et al. 2014).
Settings and practices that lead to pathogen spillover are little
understood but of great importance for informing outbreak mitigation
strategies. In lieu of direct knowledge on pathogen exposure, which is
extremely difficult to identify from wild animals, characterization of
human-wildlife contact can be used to infer exposure risk. Identifying
exposure settings has primarily focused on direct contact between humans
and wildlife, largely in the form of wildlife hunting and markets for
the sale of live animals (Karesh et al. 2005, Mossoun et al. 2015,
Keatts et al. 2021, Nawtaisong et al. 2022). For example, wildlife
consumption and associated handling and butchering creates human contact
with wildlife viscera and bodily fluids, which can facilitate spillover
of their pathogens (Wolfe et al. 2005). However, contacts between humans
and wildlife occur across numerous settings outside of wildlife trade
and consumption and can result in human exposure to wildlife pathogens
(Plowright et al. 2017). Other settings and practices that promote
contact between wildlife and humans have received far less focus despite
the importance of their characterization to mitigating zoonotic pathogen
spillover.
Wildlife often share spaces with humans and domestic animals, especially
in the Global South, where humans and wildlife coexist closely in
developing landscapes and EID risk is high (Seoraj-Pillai and Pillai
2016, Allen et al. 2017). Studies have reported many communities
struggling to manage small mammal incursion into buildings
(Salmon-Mulanovich et al. 2016, Doty et al. 2017, Balčiauskas and
Balčiauskiene 2020). The presence of mammals in these spaces can create
opportunities for human and domestic animal contact with wildlife and
their excreta, potentially exposing them to wildlife-borne pathogens
(Ogola et al. 2021). Despite the risk, characterization and
quantification of contacts within buildings, where people may spend
significant portions of their lives, is lacking.
Bats can harbor zoonotic pathogens that may be shed in excreta and
bodily fluids (eg., feces, urine,
saliva, blood, etc.; Mildenstein et al. 2016, Waruhiu et al. 2017).
Several bat-borne viruses have emerged in humans after transmission from
bats via indirect contact with bat excreta or direct contact with bat
bodily fluids (Belotto et al. 2005, Epstein et al. 2006, Towner et al.
2009, Eby et al. 2023). Domestic animals can also be exposed to these
pathogens after contact with bats excreta and fluids (Marsh and Wang
2004). In developing settings, anthropogenic structures, like family
homes, places of worship, and schools, can be highly permeable to bats,
and with ongoing habitat loss bats are increasingly using these
buildings as roosts (Russo and Ancillotto 2015, Voigt et al. 2016). Few
options exist for people to safely manage bat use of their buildings,
and this provides numerous opportunities for human-bat contact and
conflict. However, detailed characterization of how humans contact bats
and their excreta in relation to pathogen exposure risk in shared spaces
is lacking and requires attention.
We investigated human-bat interactions in anthropogenic structures in
rural south-eastern Kenya to characterize and quantify forms of contact
that could lead to human exposure to bat pathogens. Bats are known to
roost frequently in buildings simultaneously used by humans in this
region (Musila et al. 2018, Jackson et al. 2023, Lunn et al. 2023) and
this area has been forecasted as a hotspot for zoonotic pathogen
emergence where surveillance and mitigation efforts are needed (Allen et
al. 2017). By understanding these contacts and their potential to
facilitate pathogen exposure, we can better identify human health risks
in this interface and provide data necessary to mitigate risks.
METHODS
This study was conducted in Taita-Taveta County, Kenya. The most recent
2019 population estimate of Taita-Taveta County was 340,671 people in
2019 (Kenya National Bureau of Statistics), with a 1.8% annual increase
in population over the preceding 10 years. Almost three-quarters of the
population is considered rural, although urbanization and deforestation
are increasing substantially in the region (Platts et al. 2011, Nyongesa
et al. 2022). This area is characterized by remnant patches of
high-elevation cloud forest surrounded by low-elevation grasslands,
woodlands, and agriculture (Abera et al. 2022).
We surveyed people in Taita-Taveta County during 2021 (August –
October), 2022 (January – April), and 2023 (May – June) to understand
and characterize human and domestic animal interactions with bats living
in buildings. Participants were identified via word-of-mouth
conversations with community members throughout the study area. We
sought out adults who had bats in their homes (permanent and rental
properties) or workplaces at the time of the survey, or who had evidence
of recent sustained bat use (i.e., urine staining, fecal deposits, dead
bats, etc.). Surveys were directed to one individual per property,
however additional family members were sometimes present during
questioning. Participants were informed about the study and verbal
consent was obtained prior to conducting surveys. This research was
approved by the National Commission for Science, Technology and
Innovation (#NACOSTI/P/21/9267) and University of Arkansas
Institutional Review Board (Protocol #2103320918).
Surveys were conducted in the local Taita language, Swahili, or English
by local Taita assistants and at least one of the authors. Questions
were read to respondents by the research team and answers were
transcribed by the team. Our survey consisted of short-answer,
dichotomous, and categorical questions to characterize resident human
and domestic animal demographics of the property, the duration of bat
use of the property and its buildings, and human and domestic animal
interactions with bats and their excreta (see Supplementary Materials
for detailed information on survey questions). Surveys from 2021
(n = 23) included 23 multi-part questions. After this initial
data collection, we added one additional question to characterize human
and domestic animal contact with dead bats on the property. Therefore,
surveys conducted in 2022 and 2023 (n = 79) included 24
multi-part questions.
To explore the effect of the number of residents on the property, length
of bat building use, and respondent demographics (gender, education, and
age) on direct (e.g., touching, scratches, bites, etc.) and indirect
(e.g., contact with bat excrement) interactions with bats, we used
univariate generalized linear models with a binomial error distribution
and logit link function. We used chi-square tests to compare the
frequencies of bat interactions, length of time of bat occupation of
buildings, exclusion methods, and reasons for exclusion. All analyses
were conducted in R (Version 2023.06.2+561) using the stats package
(v4.1.3).
RESULTS
We surveyed 102 people who lived or worked in buildings used by bats
(Table S1). Over 70% of people reported bat use of their buildings for
>5 years (n = 72), with bat presence for 5-10 years most
commonly reported (χ 2 = 36.52, P< 0.01, Fig. 1). Most properties (88%) had bat presence
year-round (n = 90). Survey participants described frequent
exposure to bats that would support pathogen transmission through two
main routes: direct and indirect (fecal/oral) contact, with indirect
contact between bats and people reported more frequently than direct
contacts (χ 2 = 24.77, P <
0.01, Fig. 2A).