Abstract
Foot-and-mouth disease (FMD) is a transboundary animal disease that has
a major impact on livestock production, regional and international trade
and livelihoods of smallholder farmers in endemic settings. Livestock
movement is one of the most important ways of spreading infectious
diseases including FMD. Many livestock diseases are transmitted through
direct contact between animals, and thus between herds and flocks
through animal movements. In this study, we described the pattern of
livestock movements among smallholder farmers within a communal farming
area in South Africa. A cross-sectional survey using a semi-structured
questionnaire was administered to 116 respondents, and 13 focus group
discussions employing participatory mapping and semi-structured
interviews were conducted among smallholder goat farmers. Data from the
study reported 37 nodes and 78 ties with an overall network density of
0.059 (SD 0.235) for goats, and 42 nodes and 90 ties with an overall
network density of 0.052 (SD 0.223) for cattle across the study area.
The study identified several FMD high-risk locations to prioritise
vaccination programmes and targeted disease surveillance. Four locations
within the (former) FMD-free zone of the country were identified to have
connections with movement of goats from the study area. Findings from
this study further demonstrated that goats are moved without official
movement permits to the FMD free zone of the country, with most farmers
being ignorant of the need to obtain official veterinary movement
permits. These animal movements put the country at risk of future FMD
outbreaks within the free zone. We recommend that the relevant
authorities implement risk-based control measures to prevent the spread
of infectious diseases.
1
Introduction
Foot-and-mouth disease (FMD) is a highly infectious transboundary animal
disease that affects cloven-hoofed livestock and wildlife including
cattle, buffalo, pigs, sheep, goats, impala, deer and antelope (OIE,
2018; Poolkhet et al., 2019). The disease is caused by infection with
foot-and-mouth disease virus (FMDV), a single-stranded RNA virus in the
genus Aphthovirus, family Picornaviridae (Han et al.,
2018). Goats are the most common livestock species kept by smallholder
communal farmers in South Africa. However, the clinical signs of FMD in
goats have been described to be inapparent or mild with nasal discharge,
ulcerative lesions of the oral mucosa and fever occurring in a
proportion of animals (Lazarus et al., 2019). Goats affected by FMD also
do not show obvious sickness behaviours (Wolf et al., 2020). Goats can
be considered “silent shedders” of disease because of the lack of
obvious clinical signs of FMD compared to some other cloven-hoofed
animals.
FMDV is primarily transmitted through direct contact via inhalation
(OIE, 2018; Poolkhet et al., 2019) and can be further spread through the
movement of infected and susceptible hosts (Brito et al., 2017;
Tekleghiorghis et al., 2016). Effective movement controls, such as those
implemented during the 2001 FMD epidemic in the United Kingdom, can slow
down the spread of disease (Ferguson et al., 2001; Haydon et al., 2004).
Risk factors for the occurrence and spread of FMD include poor farm
biosecurity practices (Ellis-Iversen et al., 2011; Megersa et al.,
2009), presence of infected animals (Gibbens et al., 2001), presence of
wildlife reservoirs (Molla et al., 2010; Vosloo et al., 1996), exposure
to secretions or products derived from infected animals (Elnekave et
al., 2016), exposure to contaminated fomites (Alexandersen et al.,
2003), poor vaccination coverage (Jori et al., 2009; Nyaguthii et al.,
2019), longer vaccination intervals (Lazarus et al., 2017), poor
livestock inspection (Jori et al., 2009) and unvaccinated animal
populations (Bravo de Rueda et al., 2014).
Livestock movement is one of the most important ways of spreading
infectious diseases between holdings (Nremark et al., 2011). Many
livestock diseases are transmitted through direct contact between
animals, and thus between herds and flocks through animal movements.
This has caused many countries of the developed world to register
livestock movements using national databases (Anonymous, 2014).
Information generated from such databases could be used for surveillance
and planning disease control programmes. The rapid analysis of livestock
movements could also be used to implement effective movement
restrictions.
The application of social network analysis within the livestock industry
has improved our knowledge of livestock movement patterns and has
informed risk-based surveillance systems (Dubé et al., 2008; Poolkhet et
al., 2019). Social network analysis has been used extensively to analyse
livestock movements (Aznar et al., 2011; Green et al., 2008; Kao et al.,
2006; Kiss et al., 2008; Mweu et al., 2013; Nremark et al., 2011;
Robinson et al., 2007; Webb, 2006), and can help identify targets for
surveillance, intervention and control (Bajardi et al., 2012; Christley
et al., 2005; Kiss et al., 2006; Natale et al., 2009). A network
analysis study of the 2001 UK FMD outbreak (Shirley & Rushton, 2005),
identified livestock markets and dealers as the hubs for disease spread.
Certain nodes (units of interests) like some farms, animal markets and
dealers were key players in the early spread of FMD during the outbreak
(Ortiz-Pelaez et al., 2006). All nodes had a high between-ness
centrality, a measure of how frequent a node is located between each
pair of node connections. Auction markets were key players for the
spread of disease during this outbreak (Robinson & Christley, 2007). A
similar study in Denmark also reported that cattle markets influenced
other nodes within the Danish cattle movement network (Mweu et al.,
2013). The transportation of infected cattle is known to be responsible
for disease transmission (Dubé et al., 2008) and the out-degree
centrality, a quantification of the number of outgoing ties (links
between nodes) from the node, is useful for estimating the resulting
size of the outbreak. The control of infectious livestock diseases such
as FMD should focus on livestock movements within the cattle trade
network (Natale et al., 2009).
The aim of this study was to investigate the importance of livestock
movements within the FMD protection zone of South Africa to identify
high-risk locations for implementation of improved surveillance and
strategic vaccination programmes.
2
Materials and methods
2.1
Study area
This study was conducted in the Mnisi Tribal Authority (MTA), a communal
farming area within the FMD protection zone with vaccination in
Bushbuckridge Local Municipality, Mpumalanga Province, South Africa
(Figure 1). The MTA is divided into three animal health wards
(Bushbuckridge East, Animal Health Wards I-III) and totals 16 communal
dip tanks (livestock inspection points). Communal farmers within this
area are involved mostly in livestock rearing. The proximity to the
Kruger National Park (KNP) poses a threat to livestock production due to
infectious diseases and the surrounding areas have poor market access as
they are located within the FMD protection zone with vaccination
(Lazarus et al., 2018).
FMD control measures in South Africa include the separation of wildlife
and livestock using fences, clinical surveillance, routine vaccination
of cattle and movement control of susceptible livestock, wildlife and
their products (DAFF 2014). According to the South African veterinary
legislation, three zones exist for the control of FMD (DAFF 2014). The
three zones classify the country into: a) FMD infected zone b) FMD
protection zone (with or without vaccination and c) formerly FMD free
zone (majority of the country). The FMD protection zone protects the
status of animals in the FMD free zone and movement of livestock into
the free zone is restricted using a permit system after the animal has
been examined and certified to be free from FMD.
Farmers within the protection zones are mostly engaged in communal
farming activities, which are considered to be a cost-effective farming
system (Dovie et al., 2006). However, it is a high-risk husbandry system
due to poor biosecurity practices that might lead to the occurrence and
spread of diseases including FMD. As a control measure for FMD and other
infectious diseases, movement of cattle out of this zone of the country
is only allowed if the animal originates from a herd that has evidence
of previous FMD vaccination and has a movement permit issued by the
official veterinary service. Thus, FMD vaccinated animals can only move
to other vaccination areas or a designated abattoir for direct
slaughter.
Between January and November 2019, two FMD serotype SAT2 outbreaks were
reported in the formerly FMD free zone of Limpopo Province, (DAFF 2019a;
DAFF 2019b). These outbreaks caused South Africa to lose the World
Organisation for Animal Health (OIE) certified free zone status without
vaccination.
2.2
Target population and sample size calculations
The target population was smallholder farmers who kept goats within the
three animal health wards of the MTA. The required sample size was
calculated based on the desire to estimate the proportion of respondents
that reported small ruminant movement (in and out) of their flock at
least once during a one-year period (July 2017 –June 2018). Given the
lack of knowledge of small ruminant movements in the area, the
proportion was assumed to be 50% and calculations were based on a
desired confidence level of 95% and absolute error of ±10%. The sample
size was estimated to be 97 respondents (Thrusfied, 2005) but increased
by 5% to account for non-response and the possibility of data
exclusions. Participants were selected proportional to the total number
of registered livestock owners (stratified by small stock) per communal
dip tank (Supplemental Table 1).
2.3
Ethical considerations
The study was approved by the University of Pretoria, Faculty of
Veterinary Science, Animal Ethics Committee (Project Number V022-17) and
the Faculty of Humanities, Ethics Committee (Project Number
GW20170623HS). Participants were presented with a consent form before
the commencement of interviews or focus group discussions and their
identity was coded to ensure confidentiality. Verbal consent was
obtained from illiterate respondents.
2.4
Data collection