1. Introduction
Foot and mouth disease (FMD), a highly contagious infectious disease, has a major economic impact on livestock trade [
1]. At the global level, the costs of production losses and vaccine costs are assumed to be in the range of US
$6.5–21 billion, which directly affects overall food security in endemic countries [
2]. At the local community level, animal morbidity results in the largest amount of financial losses [
3]. Notably, FMD affects mainland Southeast Asia, namely Lao People’s Democratic Republic, Cambodia, Myanmar, Vietnam, Malaysia, and Thailand [
4]. There were 4930 FMD outbreaks in the period 2007 to 2016 [
5]. A variety of livestock production has been commonly practiced in Northern Thailand including dairy and beef cattle. In this area, FMD outbreaks gradually increased. The accumulative number of outbreaks was 140 between 2008 and 2015 [
6]. Nonetheless, the situation was worsened in 2016. In this particular year, 73 outbreaks were reported [
7].
FMD affects cloven-hoofed animals, such as cattle, sheep, goats, pigs, and wild boar. The virus causes noticeable vesicles on feet, mammary glands, and around the oral cavity of infected animals [
8]. It has been established well that the FMD virus (FMDV) is transmitted through direct or indirect contact between infected and susceptible animals, their secretions, and contaminated animal products [
9]. As evidenced by various previous studies, the movement of animals was significantly associated with FMD outbreaks [
10,
11,
12]. The movement of live cattle may result in the introduction of the FMDV onto a farm. For example, contamination may occur via the purchase of new cattle from infected farms and premises [
13] and the movement of live cattle during an outbreak [
14]. Cattle movement is not only a risk in and of itself, but contamination can also occur as a result of indirect or mechanical spread from farm to farm via contaminated vehicles as well as their secretions, urine, and feces (cattle manure) [
15]. As for the risk of indirect transmission, the FMDV can contaminate the environment and be transmitted through fomites on vehicles, equipment, feed, persons [
16,
17], and the unrestricted movements of people or vehicles such as live cattle tradesman [
18].
In Northern Thailand, one of the most common agricultural activities is the trading of cattle manure. Manure tradesmen visit cattle farms to buy cattle manure filled in used concentrate cattle feed bags and then transport manure to final purchasers who use manure as a fertilizer for crops. The spread of FMDV may occur via contaminated vehicles or manure bags because FMDV can survive on such fomites for many days [
15]. Regarding FMD control measures, authorities from the Department of Livestock Development announced that the movement of manure transport vehicles should be restricted during FMD outbreaks as this activity may involve the spreading of disease [
19]. However, there is a knowledge gap, as no studies have examined the movement inside manure trade networks, making it difficult to track such movement.
Social network analysis (SNA) has been applied as an important methodological approach of veterinary epidemiology to document contact patterns among interacting individuals and to characterize animal movement as it relates to the spread of disease [
20,
21,
22]. Studies using SNA have shown that farmers, cattle tradesmen, and animal markets were key players in the spread of FMD among farm animals, and particular attention should be paid to these important nodes when attempting to reduce future FMD outbreaks [
23,
24,
25]. Similar to cattle movement, the trading activity of manure tradesman, cattle farmers, and final purchasers can be considered as a network.
It is beneficial to determine and explore the network of manure trading as the transmission of FMDV can occur through network activities. In addition, understanding the route and frequency of movements is important for livestock authorities and stakeholders to develop effective control strategies, particularly for the endemic FMD area. Therefore, the aim of this study was to determine the characteristics of the manure trade network and movement pathways of manure transport vehicles.
4. Discussion
Previous studies conducted in Thailand, Laos, and Cambodia indicated that cattle tradesmen and their movements were key factors in the spread of infectious diseases within the cattle trade network [
39,
40,
41]. In Thailand, especially in the northern region, manure tradesmen conduct some activities similar to cattle tradesmen. For example, they routinely visit multiple cattle farms on a daily basis and some travel further to other provinces. Therefore, there is an opportunity for the FMDV to spread among cattle farms via the contaminated manure bags and/or vehicles of tradesmen. In this study, we determined the network of manure tradesman–cattle farmers and explored the movement pathways of manure transport.
With a high value of in- and out-degree, weighted in-degree, and betweenness centralities, tradesman was the most important node in the manure tradesmen–cattle farmers network (
Table 4). These tradesmen connected with many farm owners for manure trading and they also linked with different final purchasers, as illustrated in
Figure 2. This finding was similar to what was observed in previous studies [
27,
42]. This suggested that the nodes found in the cattle movement network influenced how FMDV spread by linking members of the network during an outbreak. Our study also implied that most cattle farm owners sold manure to a specific tradesman. In terms of frequency, dairy farm owners had a higher frequency of manure trading activities than beef farm owners. This finding is explainable by the fact that beef cattle are generally raised in a free-ranging fashion during the daytime. In contrast, dairy cattle are reared within the farms, resulting in a higher amount of accumulated manure.
Within the manure trade network, the subgroup connection has a large weak component that contains 86.4% of nodes. This suggests that some members can be reached by others, but most members were not. The weak component has the advantage that control measures are potentially more efficient than networks with strong components [
43]. Contrarily, the large strong component network has the potential to increase the size of an epidemic; thus, the control measures have to be enhanced as described in previous studies [
11,
42,
44]. Similar to a previous study in Northern Thailand [
45], we found that most of the dyads census were null and most of the triads were empty (
Table 5 and
Table 6). These results indicate that the network possesses unconnected property. The null dyad refers to no manure trading among cattle farm owners. In other words, the movement of the vehicle from one farm to another for manure transportation is not generally observed. Additionally, both network density and clustering coefficient were relatively low, suggesting that the networks were likely to be characterized by a random pattern.
Animal movement restriction is a key FMD control strategy in Thailand [
46]. At the provincial level, the movements of live cattle across provinces are routinely checked based on official movement documents [
47]. However, the vehicle movement of the manure tradesman is not required to be recorded. Although livestock authorities recommend that the movement of dung transport vehicles should be restricted [
19], little is known about the frequency and pathway of trade. Therefore, this information gap could affect the development of effective control measures, as the movement of illegal manure transport vehicles could occur.
This study identified that there is no common movement pathway for manure tradesmen as the traveling schedule depends on an everyday phone call by the cattle owners and the final purchaser. Most traveling occurred within the district and across districts (
Table 3). Interestingly, the tradesmen used the same pathways used by dairy farmers to transport farm bulk tank milk to milk collecting centers. Furthermore, some tradesmen traveled to other districts or neighboring provinces of Chiang Mai (
Figure 2). Several tradesmen traveled back and forth between large dairy farming zones in Chiang Mai and Lamphun. Thus, manure tradesmen may act as a fomite for FMD transmission across a province boundary. As a result, it can be concluded that, with a wide range of tradesmen’s movement pathways and high connectivity between tradesmen and cattle farm owners, manure tradesmen may accommodate the spread of FMD within the network.
Based on the findings from this study, management practices for the prevention of FMDV spread from manure trade activities should be performed in addition to the current FMD control practices. For example, farmers should prepare a disinfecting area for the vehicles of manure tradesman at the farm’s entrance. A logbook should be kept to record the contact information of manure tradesmen and trading activities such as the date and time of the visit and the number of manure bags sold. In addition, an educational campaign on the risk of FMD and biosecurity should be prepared for the manure tradesmen. Importantly, manure bags should not be circulated among cattle farms. In other words, the bags should be discarded after their first use as they can be contaminated with the FMDV and become another source of indirect FMDV transmission.
Approaches used in this study may be useful for researchers in some agricultural producing countries that have manure trading, such as countries in Africa [
48] and Asia [
49]. The SNA technique can be extended to other forms of movement, such as movements of animals, feed vehicles [
17], and cattle traders [
43] corresponding to farm visits. This technique may also be applied to other diseases or health conditions.
To the best of our knowledge, this study is the first report to investigate the characteristics of the cattle manure network and movement pathways of manure tradesmen in Northern Thailand. However, this study has some limitations. Firstly, the relationship between the vehicle movements of manure tradesmen and the occurrence of FMD outbreaks could not be determined because data on the date and time of the manure tradesmen visit to the farm were not recorded. We suggest that the association between manure trading and FMD outbreak should be elaborately investigated for future studies. Secondly, the determination of the static network was based on a cross-sectional design study; therefore, a temporal trend could not be determined. For follow-up studies, the dynamic network accounting for the temporal variations in the trade volume at different times of the year should be determined.