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