Application of network analysis and cluster analysis for better prevention and control of swine diseases in Argentina.

RATIONALE/
BACKGROUND: Though much smaller than the bovine industry, the porcine sector in Argentina involves a large number of farms and represents a significant economic sector. In recent years Argentina has implemented a national registry of swine movements amongst other measures, in an effort to control and eventually eradicate endemic Aujesky's disease. Such information can prove valuable in assessing the risk of transmission between farms for endemic diseases but also for other diseases at risk of emergence.
METHODS: Shipment data from 2011 to 2016 were analyzed in an effort to define strategic locations and times at which control and surveillance efforts should be focused to provide cost-effective interventions. Social network analysis (SNA) was used to characterize the network as a whole and at the individual farm and market level to help identify important nodes. Spatio-temporal trends of pig movements were also analyzed. Finally, in an attempt to classify farms and markets in different groups based on their SNA metrics, we used factor analysis for mixed data (FAMD) and hierarchical clustering.
RESULTS: The network involved approximate 136,000 shipments for a total of 6 million pigs. Over 350 markets and 17,800 production units participated in shipments with another 83,500 not participating. Temporal data of shipments and network metrics showed peaks in shipments in September and October. Most shipments where within provinces, with Buenos Aires, Cordoba and Santa Fe concentrating 61% of shipments. Network analysis showed that markets are involved in relatively few shipments but hold strategic positions with much higher betweenness compared to farms. Hierarchical clustering yielded four groups based on SNA metrics and node characteristics which can be broadly described as: 1. small and backyard farms; 2. industrial farms; 3. markets; and 4. a single outlying market with extreme centrality values.
CONCLUSION: Characterizing the network structure and spatio-temporal characteristics of Argentine swine shipments provides valuable information that can guide targeted and more cost-effective surveillance and control programs. We located key nodes where efforts should be prioritized. Pig network characteristics and patterns can be used to create dynamic disease transmission models, which can both be used in assessing the impact of emerging diseases and guiding efforts to eradicate endemic ones.

1. Introduction

The porcine sector in Argentina is a relatively small industry comparatively to the beef sector, representing only about 2% of the Argentinian livestock population [1]. This is similar to its neighboring countries of Paraguay and Uruguay also covering the great plains of the South-Eastern America. However, Argentinian swine production includes a robust industrial sector as well as numerous backyard farmers whose livelihood depend on the small number of animals they raise. Argentina has established goals to eradicate endemic diseases, with high economic costs, such as Aujesky's disease which has been present in the country since 1979 [2, 3] and to prevent the introduction of others for which the country is free, such as porcine reproductive respiratory syndrome (PRRS), African swine fever (ASF) and classical swine fever (CSF) [3]. In Argentina all movements of domestic livestock must be declared to the state veterinary service (National Service for Agrifood Health and Quality, SENASA). If statutory requirements are met, SENASA allows the movement of identified animals by issuing a permit and data are recorded and stored in a database called the Integrated System of Management in Animal Health (Sistema Integrado de Gestión de Sanidad Animal, Sigsa). Many infectious agents are mainly transmitted between farms through the transport of live animals or via contaminated fomites carried by vehicles such as trucks transporting animals or products [4]. Thus, the analysis of pig movement networks can provide valuable insights to design more cost-effective risk-based surveillance and control programs for diseases for which the country aims to achieve eradication, like Aujesky’s disease. Moreover, with the global re-emergence of diseases such as PRRS or ASF, it may help to better prevent and potentially control any of those transboundary, diseases if they enter the country.

The use of social network analysis (SNA) and graph theory has been used in multiple instances to characterize animal movements within a given livestock sector. This has been used extensively to characterize movement networks for swine in Europe [5-7] and more recently in North America and other regions [8, 9]. In South America, the method has been used to characterize cattle movements in Uruguay [10] and Argentina [11] but to the best of our knowledge has been scarcely used in the swine industry to date. In combination with other methods such as mapping [12], epidemic simulation using the network structure [13] and space-time clustering [14], SNA can define locations in time and space that are strategic for the implementation of surveillance programs by for example, identify major nodes that can act as super-spreaders and super-receivers, or identify communities and other network structures that may be used to prevent disease transmission among regions or maximize the effectiveness of control and vaccination programs.

The objective of this study is to describe and characterize the spatio-temporal swine movement network in Argentina. For such purpose we will use a combination of spatio-temporal analysis methods, network analysis and unsupervised machine learning techniques (cluster analysis). Results of this study would inform the design of more cost-effective prevention and control programs for swine diseases in the country and contribute to swine production improvement and sustainability in South America.

2. Methods

2.1. Data collection and sources

In Argentina, the following data are recorded for each movement event: the province and district of origin, the unique identifier of the source farm or market (RENSPA) and its geolocation (latitude and longitude), the date animals are to be transported, the species involved, the number of individuals by age category, the reason for the movement, the province and district of destination and the RENSPA and geolocation of the destination premise (farm, market or slaughterhouse). These data are recorded and stored in a database called the Sanitary Management System (Sistema de Gestión Sanitaria, Sigsa).

The swine demographics and movement data were provided by SENASA. Two datasets were provided. The first one was the farm census of 2016, which included all registered productive units as defined by SENASA, with at least one pig on site, their geolocation, and the number of pigs (and other livestock species) in the unit. A productive unit is defined as the unit managed by one farmer; a single actual farm can contain multiple units if multiple farmers produce in the same farm. Therefore, the unit of observation in this study is the productive unit. The second dataset included all pig movements in Argentina between units, from/to markets, and to slaughterhouses from January 2011 to December 2016. For this study, shipments from units or markets to slaughterhouses were not included as they are considered dead-end points for disease transmission and we were particularly interested to focus our attention in the potential disease spread between farms.

2.2. Analysis

2.2.1 Descriptive analyses and mapping

Spatio-temporal aspects of pig farming and movements in Argentina were described using tables, graphs, and maps. Bar plots were built on a monthly basis for overall movements, movements to and from markets, overall pigs moved, pigs moved through markets, and average shipment size to observe seasonal patterns.

Euclidean distance between shipping partners was computed using the geolocation of each unit or market from the dataset. Using these geolocations, units and pig movements were geographically mapped using the “maps” package in R [15, 16] which pulls its shapefiles from the open-source Natural Earth database [17].Points are plotted as units or markets involved in movements, and arcs as shipments. Maps of all pig shipments were created for the total 2011–2016 period as well as for each year and month. Similarly, maps with the subset of pig shipments involving markets were created. To improve visualization of areas with high density of swine farming and movements, kernel density maps were created in ArcGIS [18] for unit density, pig density, number of shipments per unit and number of pigs per shipment per unit.

2.2.2 Network construction and visualization

The networks were built using the igraph package in R [19]. Nodes were defined as productive units and markets. Edges were defined as individual shipments and weighted using the number of pigs per shipment. We built directed networks, meaning the edges accounted for the direction of the shipment from one node to another (i.e., Unit A sends pigs to Unit B). Networks were created for the total dataset as well as by year to allow for comparison over time. Comparing networks over time help us to understand if there are stable and predictable movement patterns and relationships. In this manner, we could identify specific nodes or groups of nodes that are likely to be important in future movements, and thus could be targeted as strategic points for surveillance and intervention strategies. Networks were graphed overall as well as on a monthly basis with a force-directed Kamada-Kawai layout [20] for better visualization of individual nodes as well as network structures. Graphing monthly networks allowed us to observe smaller structures where features could be better distinguished. Color-coding was used to define node type (productive unit or market).

2.2.3 Network analyses

From the full, yearly, and monthly networks we were able to determine how many units and markets were involved in pig movements as well as to compute key network metrics: in- and out-degree, betweenness, Eigen centrality, and network density. Closeness centrality could not be properly computed as this was a disconnected network [21, 22]. We examined weak and strong components to evaluate clustering. These measures, which have been previously described and shown relevant for preventive veterinary medicine [23], are briefly described in Table 1. With these metrics, it was possible to evaluate the global structure of the network, compare the roles of markets and units in the movement network, and evaluate the role of subgroups and individual nodes. Both weak and strong components allow the identification of groups of units that have an intensive trade relationship with each other. In terms of disease transmission, these components may help evaluate the extent to which an outbreak might spread, if started in a given location in the network [e.g. 10]. Individual unit and market metrics permit the evaluation of the level of activity and direct movements of an individual node (degree), as well as the position of the node in relation to the network (betweenness and Eigen centrality), which considers both direct and indirect connections. Individual nodes with outstanding values, thus holding strategic positions, could then be suitable for targeted intervention. For instance, in the case of an outbreak, it would be possible to determine which strategic nodes should be targeted first for surveillance and potential vaccination programs in a short period of time.

Table 1

Definitions of social network centralities used in this study.

Metric	Definition	Reference
In/out-degree centrality	Total number of incoming or outgoing contacts during the period considered for a single node. This is a measure of the absolute connectivity of a given node	[23, 27, 28]
Betweenness centrality	For node A it is the sum of the proportion of shortest paths between pairs of other nodes in the network that go through node A. It’s a measure of the importance node A has in connecting other nodes in the network which don’t have a direct connection.	[23, 27, 29]
Eigen centrality	For a given node, it’s centrality is a proportion of the sum of centralities of its neighbors	[27, 30]
Network density	Proportion of observed edges in the network compared to the total number of theoretical connections between all nodes.	[23, 31]
Strong component	Component considering direct connections only between nodes. Directionality of shipment is considered.	[22, 23, 32, 33]
Weak component	Component considering both direct and indirect connections between nodes. Directionality of shipment is considered.	[22, 23, 32, 33]

The sub-network without markets was also analyzed, given the apparent key role of markets in the network, to see how this would affect the cohesiveness of the network. The same metrics were measured for this sub-network. All analyses were conducted with R 3.3.1. [15] and mapped using ArcGIS 10.6.1 [18].

We also aimed to identify groups of units and markets with similar movement patterns. For such purpose we used FAMD (Factor Analysis for Mixed Data). FAMD is a variant of MFA (Multiple Factor Analysis) which can account for both categorical and continuous variables by combining PCA (Principal Component Analysis) for the continuous variables and MCA (Multiple Correspondence Analysis) for the categorical ones. For FAMD, two categorical variables (province and node type) and thirteen continuous variables were considered (unit area, unit population of pigs, unit population of other livestock, unit population of poultry, indegree, outdegree, betweenness, number of pigs shipped out, number of pigs received, average outgoing shipment size, average incoming shipment size, average distance of outgoing shipment, average distance of incoming shipment). Following the selection of a model, hierarchical clustering was used to define groups of nodes. Analysis was performed only on nodes which participated actively in pig movements at any given point during 2011 and 2016 and was conducted using the FactoMineR package in R [24].

2.2.4 Missing data

Some units and markets present in the shipment data (3.7% of the total nodes) were not present in the 2016 census, and lacked geolocation. In those cases, we used the mean values for longitude and latitude of other units in the same department as their locations. This approach was chosen over the department centroid as it assumed that units aren’t always uniformly distributed within a department. In this case a unit with unknown coordinates is more likely to be closer to where other units might be concentrated or clustered.

3. Results

3.1 General characteristics of the pig industry in Argentina

The 2016 farm census recorded 97,605 productive units containing 4,988,169 pigs for 2016. These units also recorded 15,832,134 other large animals, including cattle, small ruminants and horses and 23,347,128 poultry. The average unit size was 51 pigs and the median was 8, with the largest unit registering 98,230 pigs.

In total, 739,786 movements were recorded between 2011 and 2016 involving 33,927,547 pigs. After taking out movements to slaughterhouses, analysis was performed on the remaining 135,538 movements for a total of 5,934,881 pigs involving farms and markets only. Average shipment size was 44 pigs, with the median being 20 pigs. The 75%, 95% and 99% percentiles were of 40, 141 and 450 pigs in a shipment. A total of 351 markets and 17,809 units were involved in recorded movements, forming 40,931 shipment pairs. The remaining 83,506 units from the census were not involved in shipping pigs between 2011 and 2016. The average number of shipments per pair of nodes was 3.3 and the median 1 (the 75%, 95% and 99% percentiles being of 2, 11 and 37 respectively, with the maximum shipments between a pair reaching 544). The average number of pigs shipped between pairs was 145, with a median of 15 (the 75%, 95% and 99% percentiles being of 56, 393 and 1498 pigs, with the maximum reaching 368,398 pigs shipped between a pair).

3.2 Temporal trends in pig movements

As shipment data collection was first introduced in 2011, seasonal trends could not be observed for that year, with the steady increase in the number of shipments during 2011 reflecting the increase in coverage and improvement in data collection, not an increase in shipments. Movement patterns showed that peak months in number of shipments for the period 2012 to 2016 were the months of September and October (average of 2,430 and 2,439 shipments, respectively) and the lowest months were January and February (average of 1,588 and 1,615) (Fig 1). Average monthly shipments for other months varied from 1,881 to 2,053. These observations were even more pronounced when looking at markets exclusively. When comparing to the average number of monthly shipments going through markets each year, September and October had 1.82 and 1.66 times the amount of shipments whereas January and February had 0.40 and 0.56 times the number of shipments. For other months these values varied between 0.79 and 1.16. However peak month for average shipment size were January and December (54 and 53 pigs per shipment), with the lowest months being September and October (39 and 40 pigs per shipment) with other months varying between 42 and 49 pigs per shipment on average. The average size of shipments increased steadily over the years from 34 pigs in 2011 to 55 in 2016 (median from 15 to 20) (Fig 2). Therefore, even though the number of shipments decreased from 25,655 in 2012 to 22,110 in 2016, the number of pigs shipped increased from 962,006 to 1,219,726. For the years 2012 to 2016, we observed very similar monthly patterns in movements, suggesting a relatively stable and predictable movement network in Argentina.

Fig 1

Number of pig shipments per month between 2011 and 2016 in Argentina.

Fig 2

Average shipment size per month between 2011 and 2016.

3.3 Spatial distribution of the swine industry in Argentina

Mapping swine movements from 2011 to 2016 shows a concentration of movements in the areas west of Buenos Aires, with a number of major actors on the periphery interacting with the core industrial center of swine production (Fig 3). In terms of unit and pig density, we can distinguish three distinct areas concentrated in the provinces of Formosa, Chaco, Corrientes and Misiones (Fig 4A–4B). The first is an area of high unit and high swine density covering parts of the provinces of Buenos Aires, Santa Fe and Cordoba, and to a lesser extent those of Entre Rios and San Luis. This area is on an axis that includes, from West to East, the cities of Buenos Aires, Rosario, Santa Fe, Cordoba and San Luis. Secondly, there is an area of high unit density but low swine density covering the Northeastern provinces of Formosa, Chaco and Misiones and to a lesser extent the provinces of Salta, Santiago del Estero and Corrientes. This area is essentially located along the border with Bolivia and Paraguay. Finally, the rest of the country has both low densities in units and pigs. At the provincial level, we can see that the 3 provinces of Buenos Aires, Cordoba and Santa Fe contain 36.6% of units (35,707) but 62.6% of pigs (3,123,567). The remaining 9 North-East provinces contain 57.0% of units (55,619) and 32.2% of pigs (1,606,938) and the 11 western and southern provinces contain 6.4% of units (6,279) and 5.2% of pigs (257,677) (Table 2). We observe that in all provinces, the mean size is always quite higher than the median, indicating strongly right-skewed distributions in productive unit sizes.

Fig 3

Distribution of pig movements in Argentina from 2011 to 2016.

Red nodes represent markets and blues nodes farms. Red lines are movements coming from markets and blue lines coming from farms.

Fig 4

Kernel density maps: of Argentinian (A), farm distribution in 2016, (B) swine distribution in 2016, (C) outgoing shipments from 2011 to 2016, (D) outgoing traded pigs from 2011 to 2016, (E) incoming shipments from 2011 to 2016 and (F) incoming traded pigs from 2011 to 2016.

Table 2

Farm and pig distribution by province in Argentina in 2016.

	Number of Productive units	Number of pigs	Average unit size	Median unit size	Largest unit
Major swine producing provinces	35,707	3,123,567	87
Buenos Aires	17,762	1,226,498	69	10	56,910
Cordoba	12,017	1,117,913	93	12	24,281
Santa Fe	5,928	779,156	131	10	45,739
North East provinces	55,619	1,606,938	29
Capital Federal	-	-	-
Chaco	12,007	253,609	21	9	11,168
Corrientes	6,798	73,685	11	3	9,958
Entre Rios	6,224	345,370	55	6	13,883
Formosa	7,110	172,040	24	8	1,701
La Pampa	3,167	160,835	51	14	19,939
Misiones	3,669	65,591	18	5	2,998
Salta	6,185	220,586	36	17	3,673
San Luis	3,965	216,976	55	6	98,227
Santiago del Estero	6,494	98,246	15	7	2,694
Western and Southern provinces	6,279	257,677	41
Catamarca	1,080	15,732	15	4	943
Chubut	378	24,562	65	12	6,494
Jujuy	581	25,940	45	6	4,676
La Rioja	564	23,610	42	3	12,725
Mendoza	1,137	35,303	31	5	2,687
Neuquen	329	20,593	63	8	9,746
Rio Negro	805	31,205	39	9	5,210
San Juan	258	42,698	165	3	21,489
Santa Cruz	72	3,272	45	13	563
Tierra del Fuego	16	973	61	7	472
Tucuman	1,059	33,789	32	4	4,504
Total	97,605	4,988,182	51	8	98,227

3.4 Spatial and provincial patterns of swine farming and movements

When looking at the density maps of swine movements and comparing them with swine population density, we confirm that there are similar spatial patterns with most movements being conducted around the industrial area of swine farming (Fig 4C–4F), with few major hot-spots concentrating most of the incoming and outgoing shipments. Of 135,538 shipments, 83,077 shipments (61.3%) were internal in the provinces of Buenos Aires, Córdoba and Santa Fe; 19,233 shipments (14.2%) occurred between these 3 provinces; 14,303 shipments (10.6%) were between these 3 provinces and the other 20 provinces; 14,167 shipments (10.5%) were within each of the other 20 provinces and 4,758 shipments (3.5%) were between these 20 provinces (Fig 5 and Table 3).

Fig 5

Allocation of shipments involving the provinces of Buenos Aires, Cordoba and Santa Fe.

Edges thickness is proportional to the number of shipments, with the two most important trade relationships highlighted in red.

Table 3

Provincial distribution of shipments and number of shipped pigs in Argentina from 2011 to 2016.

	Internal shipments (within province)	Incoming shipments	Outgoing shipments	Internally shipped pigs (within province)	incoming pigs	outgoing pigs
Main 3 provinces	83,077	24,371	28,398	3,848,169	828,330	837,858
Buenos Aires	32,740	6,382	8,138	1,243,754	192,302	169,528
Cordoba	30,280	7,177	13,794	1,119,648	160,396	480,045
Santa Fe	20,057	10,812	6,466	1,484,767	475,632	188,285
North East provinces	11,857	6,807	7,132	450,885	521,216	176,315
Capital Federal	-	186	185	-	963	419
Chaco	1,367	490	299	18,426	6,794	6,078
Corrientes	184	386	158	2,910	7,305	6,440
Entre Rios	2,290	1,481	1,263	160,381	24,783	30,966
Formosa	857	217	96	32,906	3,369	3,709
La Pampa	2,298	1,637	2,186	55,716	426,500	56,584
Misiones	2,365	268	69	141,915	6,732	694
Salta	837	435	575	18,795	10,786	18,912
San Luis	1,453	1,082	2,103	13,922	20,132	46,618
Santiago del Estero	206	625	198	5,914	13,852	5,895
Western and Southern provinces	2,310	7,116	2,764	91,088	195,193	530,566
Catamarca	51	535	174	1,042	12,480	6,428
Chubut	119	3	24	2,019	134	722
Jujuy	58	620	20	2,513	16,090	1,120
La Rioja	22	134	347	602	6,528	381,611
Mendoza	767	4,260	113	23,977	110,352	5,457
Neuquen	29	34	11	621	358	522
Rio Negro	759	189	134	45,341	2,870	1,086
San Juan	15	168	1,258	1,600	4,190	109,092
Santa Cruz	18	20	1	129	568	3
Tierra del Fuego	3	3	-	246	148	0
Tucuman	469	1,150	682	12,998	41,475	24,525
Total	97,244	38,294	38,294	4,390,142	1,544,739	1,544,739

Similar patterns could be seen when looking at the number of pigs shipped as opposed to the number of shipments (Table 3). However, when looking at net number of incoming/outgoing shipments between provinces, and disregarding internal provincial movements, there are some interesting relationships (Fig 5). The province with the largest net number of outgoing shipments is La Rioja, and the province with the largest net number of incoming shipments is La Pampa, with 381,598 (99.997% of outgoing pigs) of the pigs leaving La Rioja, going to La Pampa (89.5% of incoming pigs). Of these, 368,398 (96.5%) pigs were from a single movement pair between two units. A similar partnership can be seen between Córdoba and Santa Fe, with 284,005 pigs leaving Córdoba (59.2% of outgoing pigs) going to Santa Fe (59.7% of incoming pigs). Córdoba, La Rioja, Santa Fe, Buenos Aires and San Juan have all sent more than 100,000 pigs to other provinces from 2011 to 2016, making up 86% of between-provinces shipped pigs. Similarly, Santa Fe, La Pampa, Buenos Aires, Cordoba and Mendoza have all introduced more than 100,000 pigs, making up 88% of between-provinces shipped pigs (Fig 6).

Fig 6

Distribution of inter-provincial traded pigs in Argentina between 2011 and 2016.

3.5 Network characteristics

As mentioned above, our unit/market-to-unit/market network had 135,538 edges, 17,809 nodes and 40,931 movement pairs. Of these pairs, 33,973 (83.0% of pairs) shipped between 1 and 99 pigs from 2011 and 2016 for a total of 670,660 pigs (11.3% of pigs), 6,237 (15.2% of pairs) shipped between 100 and 999 pigs for a total of 1,734,453 pigs (29.2% of pigs) and 717 (1.8% of pairs) pairs shipped between 1,000 and 70,000 pigs for a total of 2,602,224 pigs (43.8% of pigs). The remaining 4 movements pairs had shipped more than 160,000 pigs each for a total of 927,544 pigs (15.6% of pigs). Most movements were conducted over small distances with the median equal to 63 km. However, this was highly skewed with a mean of 142 km and a maximum distance of 3,286 km. Over the years both the median and mean distance slightly increased from 59 to 67 km and 136 to 152 km respectively (Table 4).

Table 4

Network centrality values and characteristics for the yearly networks from 2011 to 2016 and the complete network (whole time period).

	2011	2012	2013	2014	2015	2016	Total
Network attributes
Number of farms & markets (nodes)	5,852	8,110	7,603	6,807	6,784	6,323	18,160
Number of shipments (edges)	14,897	25,655	25,826	23,695	23,355	22,110	135,538
Number of pigs shipped	509,965	962,006	1,015,450	1,091,699	1,136,035	1,219,726	5,934,881
Euclidean distance (edge length), km
Median	66.5	59.4	60.6	62.3	65.7	67.9	63.3
Mean	142.8	136.2	135.5	141.8	147.1	152.2	142.3
95th percentile	520.3	527.0	520.6	540.2	544.2	553.1	539.4
Maximum	1,404	2,519	2,872	3,286	1,591	1,278	3,286
Shipment size
Median	15	17	18	20	20	20	20
Mean	34	38	39	46	49	55	44
95th percentile	113	120	125	150	160	200	141
Maximum	7,362	7,819	3,000	10,727	14,443	10,370	14,443
Indegree
Median	1	1	1	1	1	1	1
Mean	2.55	3.16	3.4	3.48	3.44	3.50	7.46
95th percentile	7	8	10	10	11	11	21
Maximum	1,337	1,361	1,423	1,252	1,354	1,239	7,966
Outdegree
Median	1	1	1	1	1	1	1
Mean	2.55	3.16	3.4	3.48	3.44	3.50	7.46
95th percentile	9	12	12	13	13	13	29
Maximum	777	658	730	744	661	708	4,278
Betweenness
Median	0	0	0	0	0	0	0
Mean	771	1,723	3,895	886	1,398	708	20,673
95th percentile	538	1,754	2,571	981	1,259	918	28,143
Maximum	687,196	1,238,883	2,999,446	726,797	1,172,503	601,057	30,558,417
Eigen Centrality	-57.12	41.86	48.45	41.38	45.93	51.93	260.62
Network density (%)	0.0435	0.0390	0.0447	0.0511	0.0508	0.0553	0.0411
Strong components
Number	5,486	7,499	6,911	6,358	6,303	5,882	14,314
Largest component	287	464	564	270	344	285	3,546
Median size	1	1	1	1	1	1	1
Mean size	1.07	1.08	1.10	1.07	1.08	1.08	1.27
Weak components
Number	431	568	533	497	493	485	923
Largest component (% nodes)	4,843 (82.8)	6,684 (82.4)	6,199 (81.5)	5,444 (80.0)	5,468 (80.6)	4,994 (79.0)	16,000 (88.1)
Median size	2	2	2	2	2	2	2
Mean size	13.58	14.28	14.26	13.7	13.76	13.04	19.67

The monthly network graphs showed similar patterns, thus here we exemplify the 48th month of data, December 2014, which was one of the most legible graphs, to discuss some of the structures of the network (Fig 7). The first pattern we can notice is that a large portion of units and markets are connected, either directly or indirectly forming a major network community (Fig 7, number 1). The rest of the units and markets for smaller communities, are disconnected from the main community (Fig 7, number 2). In the main component, a very large blue node (market) surrounded by a multitude of direct connections can be seen, forming a dense star pattern (Fig 7, number 3). We can also observe some small nodes (usually units) which connect communities that wouldn’t otherwise be connected (Fig 7, number 4). There are pairs of units that ship pigs to one another multiple times (Fig 7, number 5). Though some major nodes exchanged pigs with other major nodes, some also exchanged pigs with a multitude of smaller units and, are only attached to another major node through a minor node (Fig 7, number 6). Finally, we have movement pairs that are completely isolated from the rest of the network (Fig 7, number 7).

Fig 7

Network graph for December 2014.

Node size represents the log value for node betweeness.

Given the limitations of visualizing the network on a graph as it gets bigger (e.g. yearly network or full 6-year network), we also used a number metrics to help quantify some of the structures and network attributes noted above (Table 4). Overall the network is not very cohesive with a density that increased from 0.04% to 0.055% from 2011 to 2016. The majority of units (83,506; 85.6%) in the 2016 census did not send or receive a single shipment during the period 2011–2016. A narrow majority of units that did participate in movements only moved once or twice over the whole period (9,146; 50.4%), with another 5,042 units (27.8%) participating in 3 to 10 shipments. When looking at indegree and outdegree, we observe that over the years the median is 1, with the mean varying between 3 and 3.5. The 95th percentiles are also low, around 7 to 11. However, we can see that the maximums are well above 1,000 for indegree, and around 700 for outdegree each year. Similarly, when looking at betweenness we see a relatively high mean but the median being 0, with some very extreme maximums, between 600,000 and 3,000,000 depending on the year. At the month level, these metrics showed marked seasonal patterns with degree and density peaking in September and October (Fig 8) and betweenness showing even stronger peaks in August, September and October (Fig 9).

Fig 8

Time series of the monthly density values from 2011 to 2016 (A) and boxplot of the density values aggregated by month from 2011 to 2016 (B).

Fig 9

Time series of the monthly mean betweenness value from 2011 to 2016 (A) and boxplot of the betweenness values aggregated by month from 2011 to 2016 (B).

When looking at strong and weak components, we can see a very large number of strong components (between 5,500 and 6,900 depending on the year), and a small number of weak components (between 431 and 568 depending on the year) (Table 4). In the weak components we have one very large component which includes 79 to 83% of all nodes for any given year. All other weak components are much smaller (mean size 2). Strong components are much smaller on average with a mean and median of 1 and yearly maximums ranging from 270 to 564.

3.6 The role of markets

During the total period of study, 11,394 shipments, involving 251,449 pigs arrived from units to markets, 11,812 shipments involving 183,465 pigs went from markets to units and 1,201 shipments and 59,477 pigs going directly from market to slaughter. Thus, markets represent 1.8% of nodes but are involved in 17.4% of shipments and 7.3% of pigs moved. A total of 6,420 movement pairs (15.6% of all pairs) involved markets. Shipments involving markets were much smaller, being on average of 19 pigs, with a median of 8 and a maximum of 487. As mentioned earlier, one particular market stands out, having much higher values for each of the network metrics, compared to any other nodes in the network. This node is mapped with the other 350 markets involved in the network, in Fig 10. We can see that a few markets form star patterns (Fig 10), reflecting that they are connected to multiple units, and so hold strategic positions. The important role of markets is confirmed by the metrics, with markets having higher mean and median in and outdegree (mean of 7.5 and median of 1 for the full network compared to, 18.4 and 6 for market outdegree and 14.5 and 2 for market indegree). The same was observed for betweenness (mean of 318,732 for markets compared to 20,673 for the full network). When building the network without the markets (Table 5), though network density is only slightly different, with markets representing a small proportion of nodes, it is noticeable that eigen centrality for the network is quite lower. Mean yearly betweenness also dramatically decreases from 708 to 3,895 in the full network compared to 22 to 238 in the network without markets. Finally, we can note that largest weak component now only includes 74 to 77% of nodes compared to 79 to 83% to the full network. The new network has 16,145 nodes, 2,015 less compared to the full network. This means, that after accounting for 351 markets, 1,664 units have been excluded as they were moving pigs exclusively with markets.

Fig 10

Map of shipments going to or coming from markets, from 2011 to 2016.

Only market nodes are shown. Red lines represent shipments coming from markets, and blue lines, coming from farms.

Table 5

Network centrality values and characteristics for the yearly sub-networks from 2011 to 2016 and the full sub-network (whole study period) after removing markets.

	2011	2012	2013	2014	2015	2016	Total
Network attributes
Number of farms & markets (nodes)	4,928	7,134	6,737	6,148	6,113	5,662	16,145
Number of shipments (edges)	11,002	21,097	21,443	20,248	19,724	18,820	112,334
Number of pigs shipped	442,382	889,119	939,700	1,022,790	1,063,184	1,142,792	5,499,967
Euclidean distance (edge length), km
Median	80.9	64.8	64.1	65.1	69.3	70.3	67.9
Mean	164.4	146.6	143.6	150.2	157.7	162.2	153.0
95th percentile	549.6	545.1	540.6	551.9	570.2	578.2	554.7
Maximum	1,404	2,519	2,872	3,286	1,591	1,278	3286
Shipment size
Median	20	20	20	22	20	23	20
Mean	40	42	44	51	54	61	49
95th percentile	130	126	140	167	185	200	156
Maximum	7,362	7,819	3,000	10,727	14,443	10,370	14,443
Indegree
Median	1	1	1	1	1	1	1
Mean	2.23	2.96	3.18	3.29	3.23	3.32	6.96
95th percentile	6	7	9	10	10	11	20
Maximum	351	1,293	967	837	733	511	4,547
Outdegree
Median	1	1	1	1	1	1	1
Mean	2.23	2.96	3.18	3.29	3.23	3.32	6.96
95th percentile	8	11	12	12	12	12	27
Maximum	401	388	368	400	417	377	1,955
Betweenness
Median	0	0	0	0	0	0	0
Mean	22	238	109	86	85	66	17,832
95th percentile	20	213	84	56	79	54	18,879
Maximum	8,514	241,007	46,307	40,735	27,899	22,443	17,995,571
Eigen Centrality	17.15	21.91	21.63	23.35	32.37	35.77	90.28
Network density (%)	0.0453	0.0415	0.0473	0.0536	0.0528	0.0587	0.0431
Strong components
Number	4,832	6,918	6,516	5,949	5,919	5,483	13,446
Largest component	8	47	47	51	45	29	2,278
Mean size	1	1	1	1	1	1	1
Median size	1.02	1.03	1.03	1.03	1.03	1.03	1.20
Weak components
Number	483	644	611	539	537	531	1,049
Largest component (% nodes)	3,801 (77.1)	5,484 (76.9)	5,134 (76.2)	4,570 (74.3)	4,693 (76.8)	4,229 (74.7)	13,660 (84.6)
Mean size	2	2	2	2	2	2	2
Median size	10.20	11.08	11.03	11.41	11.38	10.66	15.39

When looking at monthly metrics, monthly density and degree follow similar patterns as previously observed, with slightly lower values. A moderate peak is still visible around October (Fig 11). However, the seasonal patterns observed in the full network for betweenness disappear with no obvious yearly peak in August to October (Fig 12). The seasonality in betweenness was driven by two specific markets mostly operating in August, October and November.

Fig 11

Time series of the monthly density value from 2011 to 2016 in the network without markets (A) and boxplot of the betweenness values aggregated by month from 2011 to 2016 in the network without markets (B). These graph are on the same scale as Fig 8.

Fig 12

Time series of the monthly mean betweenness value from 2011 to 2016 in the network without markets (A) and boxplot of the betweenness values aggregated by month from 2011 to 2016 in the network without markets (B).

3.7 Factor analysis for mixed data

Due to a number of observations having some missing data in the variables of interest, analysis was conducted on 14,099 complete observations out of the 18,160 nodes which participated in the network. A first model was constructed using FAMD which included all the variables originally selected. FAMD plots variables in a multi-dimensional space based on how they interact, with coordinate values ranging from -1 to 1 in each dimension. The number of dimensions is dependent on the number of variables, and the number of categories within categorical variables [24]. Typically, results are interpreted in the first 2 or 3 dimensions as these explain most of the data variation. Values close to 0 reflect variables with low discriminatory power, thus variables which do not divide observations in distinct groups. Coordinate values closer to -1 or 1 have high discriminatory power. For this study, variables which did not reach coordinate values of 0.2 in either dimension 1 or 2 were excluded as active variables and only included as passive supplementary variables, meaning that these variables were not discriminatory enough to help divide nodes into groups. These non-discriminatory variables included unit area, non-swine livestock population, poultry population and distance covered by incoming and outgoing shipments. Province was also excluded from the model as the large number of categories created a large number of dimensions which explained very little of the variance and made it impossible to define clear groupings. The final model was studied in the first two dimensions, which accounted for 27.5% and 23.6% of the total variance respectively. As these accounted for more than half of the variance, and dimension 3 dropped to 14.1% of variance, results were interpreted using graphical representations in the first two dimensions (Fig 13). The three continuous variables with the highest contribution (i.e., the most discriminatory power) were indegree, outdegree and betweenness in both dimension 1 and 2 (Table 6). The active variables all had positive coordinates in both dimensions, thus trending towards discriminating nodes with a combination of higher values. This means that high values of one variable tends to combine with high values of the other variables as well within observations. These variables are plotted in Fig 13.

Fig 13

Correlation circle for continuous variables included in the final factor analysis for mixed data model (FAMD) along dimension 1 and 2.

Variables in green are active and in purple are supplementary. All active variables have positive coordinate values in both dimension 1 and 2. The variable names relate to: indegree, outdegree, betweenness, Pig.in = total number of incoming pigs in a given unit, Pig.out = total number of outgoing pigs, Pig.pop = pig population, Av.pig.out = average size of outgoing shipment Av.pig.in = average size of incoming shipment, Polutry = poultry population, Livestock = livestock population, Distance.out = mean distance of outgoing shipment, Distance.in = mean distance of incoming shipment, Area = area of unit.

Table 6

Results of factor analysis for mixed data (FAMD).

Coordinates represent the mean location of a variable along the 2 dimensions under study, and contribution represents the discriminatory power of the given variable in dimension 1 or 2. (Supplementary categorical variable of province not shown for clarity, due to the large number of provinces).

	Dimension 1		Dimension 2
	Coordinates	Contribution	Coordinates	Contribution
Active Continuous Variables
Betweenness	0.636	13.71	0.497	9.73
Indegree	0.598	12.11	0.556	12.21
Outdegree	0.585	11.61	0.490	9.45
Number of incoming pigs	0.417	5.90	0.478	9.00
Number of outgoing pigs	0.324	3.56	0.388	5.92
Pig population	0.149	0.76	0.278	3.04
Average incoming shipment size	0.109	0.40	0.195	1.50
Average outgoing shipment size	0.107	0.39	0.230	2.09
Active Categorical Variable categories
Node type: Market	5.927	50.70	-4.865	46.26
Node type: Farm	-0.101	0.87	0.083	0.79
Supplementary Continuous Variables
Area	-0.016	NA	0.001	NA
Non-pig livestock population	-0.046	NA	0.013	NA
Poultry population	0.007	NA	0.018	NA
Average distance of incoming shipments	0.082	NA	-0.017	NA
Average distance of outgoing shipments	0.102	NA	0.017	NA

Hierarchical clustering suggested the optimal number of four clusters (Fig 14). These could be defined as cluster 1 comprised of small units (low pig population) with a combination of low network metrics (betweeness and in- and out-degree), low shipment sizes; cluster 2 comprised of large units with a combination of low betweeness but high in- and out-degree and large shipment sizes; cluster 3 comprised of markets (no pig population) with a combination of high betweeness but low in- and ou-degree and small shipment size; and cluster 4 comprised of a single node, the major outlying market mentioned previously with extremely high values for betweenes and in- and ou out-degree but low shipment sizes. Detailed results of the values within each cluster are presented in Table 7.

Fig 14

Location of nodes in dimensions 1 and 2 following coordinates obtained from factor analysis of mixed data (FAMD) with color coding from hierarchical clustering.

Cluster 1 represents small and backyard productive units (low degree, betweenness, pig population and shipment size), cluster 2 represents large and industrial farms (high degree, pig population and shipment size but low betweenness), Cluster 3 represents markets (high betweenness but low degree and shipment size, and no pig population) and cluster 4 is a single outlying market with extremely high values for betweenness, degree but small shipment size and no pig population.

Table 7

Characteristics of the four clusters defined by hierarchical clustering based on the active variables selected from factor analysis for mixed data (FAMD).

Variables	Cluster 1	Cluster 2	Cluster 3	Cluster 4
	Farms with lower trade metrics	Farms with high trade metrics	Markets with lower trade metrics	Market with high trade metrics
Number of nodes in cluster	13,845	17	236	1
Mean Betweenness	19,617	12,754	190,598	30,558,417
Mean Indegree	7.8	117.5	14.5	7,966
Mean Ourdegree	8.1	132.7	31.9	4,278
Mean Number of incoming pigs	299	62,160	214	200,857
Mean Number of outgoing pigs	298	64,078	144	149,550
Mean Pig population	226	22,246	0	0
Average incoming shipment size	14	1,630	12	25
Average outgoing shipment size	19	1,458	5	35

4. Discussion

Swine farming in Argentina may not represent the bulk of meat production compared to cattle or poultry in the country. However, it is still an important sector both at the industrial and community level and has a substantial potential to grow and expand, particularly now that other traditional pig producing regions such as China or Europe have been affected by ASF. Swine farming in Argentina is divided into two main groups, an industrial production sector, and small-scale and backyard farming. Thus, every value relating to pig numbers or movements are highly skewed with a large majority of small holdings and a few very large holdings that ship large numbers of animals. The presence of other livestock species was also indicative of the difference between large and small swine units, with large swine units having little to no other livestock on the premise, and most other livestock being on units with small or medium sized swine herds. The industrial-backyard dichotomy was evident when mapping the units, with swine density not fully matching unit density. The open plains west of Buenos Aires contain the so-called industrial swine belt of Argentina with high densities of both pig units and number of pigs. The more densely forested Northeast is home to a large amount of backyard farmers, which explains the very high density of units with a low density of pigs. Both these areas are also where human population density is the highest [25]. Finally, the less densely populated mountainous regions in the West, bordering Chile, and desert regions in the South is home to fewer small backyard holdings. However large holdings still exist in limited numbers across the country, as noted by the skewness in unit size for each province.

The density of recorded shipments, ingoing or outgoing, was also very focalized around certain specific points in the industrial swine belt and this is in part because a few very large holdings and markets were involved in very large portion of shipments. Some of these holdings have near exclusive partnerships with other large holding, repeatedly sending large shipments in one direction. Though the data did not have enough information to confirm this, we suspect that this represents large breading farms sending many young pigs to large fattening or finishing farms, as is relatively common in industrial swine farming worldwide [5,8].

Seasonal trends were less clear to interpret. It is likely that to a certain extent movements reflect seasonal patterns in swine farming as has been shown in the cattle industry [11, 26]. During the summer, pig fattening is less efficient and animals are relatively small when they are shipped out in December-January to make way for new incoming piglets that will start the fattening process. Given the smaller size of shipped animal, more animals are shipped on fewer trucks explaining that there are fewer shipments during those months but with a larger average number of pigs per shipment. However, the increase in the number of shipments in October-November, might also reflect the industry getting ready for increased meat consumption that always occurs during the spring and summer. Movements to and from markets showed a major increase in September and October which might also reflect the period of activity of certain markets, thus affecting the overall picture as well. This is confirmed by the important peaks in mean betweenness during those same months which were mainly driven by markets indirectly connecting multiple units that otherwise would not have been in contact. The fact that shipments through markets drive the peaks in the number of shipments in September and October might also be an explanation as to why these months had on average the smallest shipment sizes, as shipment through markets were smaller than shipments between units only. The repeating patterns over the years 2011 to 2016 showed that shipments follow a stable network that can be predicted with some reliability over future years. The observed trend of decreasing shipments over the years whilst the number of shipped pigs increased might reflects financial strain due to the economic crisis, with farmers aiming to cut cost on shipments by shipping more pigs in a shipment.

Network graphs can provide valuable insights about network structure and can help to identify key nodes where surveillance and outreach should be focused. For example, in the December 2014 graph (Fig 7) we noticed an important market located just west of Buenos Aires which consistently plays on central role between a large number of units, connecting with both major and minor nodes in the network. This same market drives the seasonal variation in betweenness with peaks from August to October, whilst remaining active the rest of the year also. As noted, we distinguished several patterns in this graph which help to illustrate the fact that the number of animals and shipments a node ships is not directly associated with the importance of a node in the network in terms of connecting units and markets and potentially contributing to a high potential of disease spread. Small nodes which only connect between two other nodes and only have 2 shipments, might not appear important in terms of number of shipments and pigs shipped, without visualizing the network and network metrics, but can be located in strategic positions in the network and serve as a bridge by indirectly connecting other groups of nodes or two highly connected communities that otherwise will be not connected. Conversely nodes that send repeated number of shipments to a single other node might not necessarily have an important role in the network in terms of disease spread, despite the large number of shipped animals, as they only contact one or a few partners and can be in an isolated circuit. The repeated nature of shipments between two nodes was also exemplified above with only 4 movement pairs exchanging nearly 16% of swine shipped. Repeated exchanges often occur when there is a specific partnership between a large breading unit and a large fattening unit, with the piglets going from one to the other at regular intervals, without going further into the farm network. Thus, a large portion of shipments could be considered to have relatively low importance for surveillance and control needs. Though some major nodes followed this repeated pair patterns with other major nodes, some send shipments to multiple smaller nodes, and were only attached indirectly to another major node. Here we have much higher spreading risks as these units hold more central role in the various communities. Finally, we noted some isolated pairs outside of the main network which are likely to be backyard farmers that might exchange a few pigs or a boar, with a neighbor without ever contributing to the network as whole. These units can also be seen on the periphery of the communities and a large number of them only participated in pig movements once in the whole 6 years of our time period. However, there were two major limitation in assessing indirect connections between nodes. Firstly, the networks presented in this paper were all static, even if observed at different time-scales. This creates an issue, where, for example: in a monthly network, two farms A and C are connected via two separate shipments through farm B. These two shipments might be distant in time by one day or by as much as thirty, and this time-lapse might make the indirect connection note-worthy or irrelevant in terms of disease transmission from A to C. This problem would be exacerbated with larger time steps. It would thus be useful to use a dynamic network structure to better capture the risk of transmission through indirect connections, considering the incubation period, latent period and other temporal characteristics of any specific disease under study. Secondly, the lack of direct animal tracing meant it wasn’t possible to assess which shipments continued directly from a node A to C via B. This is especially true with markets where numerous shipments come in and exit at any given time, with no resident population. Thus, if farm A, sends a shipment to market B, and shortly after, farm C receives a shipment from market B, there is no way to know if this shipment contains the same pigs sent by farm A, or other pigs that were at the market at the same time, and which might or might not have been in close contact to pigs from farm A. This is certainly something that could be added if individual pig identification expands in Argentina and that information becomes available for analysis in the future.

It is also interesting to discuss and compare the metrics we obtained with those described in previous studies. Overall, monthly network density values varying between 1.5*10−7 and 2.5*10−7 (Fig 8A) reflected a very loose and disjointed network. These values are much lower than that seen in countries with a much larger swine industrial sector but little backyard swine production such as the United States of America, Canada and Germany, [5, 6, 8], with values ranging 3*10−3 and 8*10−3. This can be explained by the very large number of nodes that never engaged in shipping or receiving pigs. It is likely that restricting the network to large industrial farm we would reach density values similar to that shown in the examples above.

Centrality metrics reflected generally the patterns observed in the graph. The very low mean yearly indegree and outdegree confirmed the fact that the vast majority of units participated very little in pig movements over the 6 years under study. However, the very large maximum indegree and outdegree, between 650 and 1,450, each year all relate to the market mentioned above, with the next most important nodes being a few units with several dozens to hundreds of shipments, with yearly maximums ranging from 350 to 1,300. We see here the highly skewed nature of shipments with a few nodes concentrating a large portion of shipments. This pattern was also noted in the Argentinian bovine industry [11, 26]. The mean and median betweenness of 0 each year relates to the fact that most units are peripheral to the network contributing one shipment in one direction or the other without ever connecting indirectly two or more nodes. Once again, the extreme values are from the major market near Buenos Aires. Interestingly, some units with high degree values did not also have high betweenness values. Nodes with high degree values and low betweenness are linked to the pairing partnership discussed above, between a specific breading unit sending multiple shipments to a specific fattening unit, without connecting much with other nodes. In the context of infectious disease, though in and outdegree give useful information in regards to the intensity of movements, betweenness is most interesting in terms of finding nodes with strategic locations in the network and where surveillance would be the most useful. In this sense we can see that markets have a role in the swine movement network in Argentina disproportionate to the number of shipments and pigs that actually go through them. Not only were degree values on average higher for markets than for productive units but taking markets out of the network dramatically reduced the monthly betweenness of the network, presumably breaking up the network into smaller less connected components. Moreover, removing markets from the network also drastically reduced the overall eigen centrality, indicating the role of markets in indirectly connecting multiple communities of nodes together. Thus, markets play key roles in indirectly connecting units that would not have been connected otherwise. Once again, we have to take into account the limitations of static monthly networks and the lack of continued shipment tracing in trying to assess the value of an indirect connection for disease transmission. The fact that monthly centrality values followed repeated patterns over the years, particularly betweenness, is interesting in terms of being able to predict periods of strategic importance with the months of August, September and October being of crucial importance. Thus, by combining information about time and place, we can select specific nodes, productive units and markets, that would be of crucial importance for a control campaign or outbreak management at specific times of the year. Eigen centrality is another way we can distinguish nodes with high connectivity, with strategic roles in the network.

Community algorithms also reflected what we observed in the graph with one large community containing most nodes in any given month, which included multiple strong components connected indirectly by a few nodes, and a multiplicity of small independent communities on the periphery. However, the largest community still contained a smaller proportion of nodes compared to examples in more industrial production systems in the US and Germany [5, 8] where more than 90% of nodes were contained in the largest community. This could be explained by the fairly large proportion of backyard producers that do not exchange pigs with more industrial facilities. However, the proportion of units involved in the large community in Argentina remained much larger compared to examples in Canada, France, Italy and Spain, which also have industrial swine production systems [6, 7]. Given that multiple factors might divide a single country’s sector in multiple communities, such as type of farming, but also presence of industrial groupings or partnerships, geography and natural barriers or the role of markets, it is difficult to draw direct comparison between systems without looking more closely into a more detailed layout of the communities. Looking at geographical clustering of communities [7], would be a next step in characterizing the Network structure in Argentina. Seeing that most shipments remain within a given province does provide some evidence of potential clustering of communities within provinces. The large amount of small strong components reflect that most shipping partnerships are in pairs, with a few nodes branching out into star patterns, connecting directly with multiple other nodes. This community structure was repeated across years and months.

Furthermore, factor analysis re-enforced the notion that a small group of large industrial farms play a disproportionate role in sending and receiving swine shipments in terms of volume and could help identify the most crucial of these. The vast majority of farms being small scale enterprises that do not participate much in pig movements, if at all. However, in it is interesting to note that when comparing values between clusters 1 and 2, though cluster 2 had on average values much superior to cluster 1 in almost every variable included in the model, this was not the case for an important exception, betweenness. In this regard small units in cluster 1 had an average betweenness slightly higher than cluster 2 and much lower than the market clusters. This relates to the point mentioned above about smaller nodes with low degree and high betweenness which are likely small holdings moving pigs at “random” as opposed to large holdings sending a large number of repeated shipments to a select few other units, and thus not being necessarily as important in the network as the large number of shipments suggests. It is also notable when looking at Fig 14, that though cluster 3 and 4 are distinctly different from each other and cluster 1 and 2, there seem to be some level of overlap between cluster 1 and 2, despite the large differences in mean values. This suggests, that though we can divide units into two broad types, there is no clear limit between these, and a number of units have more intermediate values. Here again, markets appear to have a much more important role in pig movements even when removing the one major outlier which formed its own spate cluster.

5. Conclusion

The characterization of the network structure of swine movements in Argentina provides useful information to build targeted and cost-effective surveillance and control system in an area of the world where the swine industry has been little studied to date. Such network structures can be adapted to create dynamic disease transmission models for multiple agents to test the impact of risk-based surveillance and intervention to help eradicate endemic diseases such Aujesky’s disease and to predict the impact of the potential introduction of new pathogens such as the PRRS, ASF and CSF viruses. However, to fully assess the risk and impact of introduction of pathogens for which Argentina is currently free, data about pig imports would be crucial. This would allow the localization of startegic points for surveillance and control such as units and markets that are the primary importers and ports of entry. Unfortunately the dataset available to us did not contain such information, thus limiting the scope of our study to national level movements. This should be considered for any future and expanded study of swine movements in Argentina.

Argentina has a broadly two system swine sectors with a very connected centralized industrial core conducting most movements and a very decentralized small-scale sector. Both sectors do have contacts between each other and the presence of small, but highly connected markets provides key locations to be chosen as strategic points for surveillance and control, as well as ideal places to conduct outreach to farmers about biosecurity measures and best management practices for risk-mitigation strategies.

14 Jan 2020

PONE-D-19-34431

Application of network analysis and cluster analysis for better prevention and control of swine diseases in Argentina

PLOS ONE

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Additional Editor Comments (if provided):

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The paper presents very important data regarding to Argentina pigs industry - number of herds, size of herds and all possible connection between them even sesonal data. The statistical data idicate the future solution in preventing the spread of pig diseases such as African swine fever.

Line 60-63 - the sentence is to long and unclear, you should use two separete sentences.

In line 67-68, Porcine Reproductive Respiratory Syndrome, African Swine Fever and Classical Swine Fever should be written with lowercase letters

Line 77-80 you are using twice the word "re-emerging".

Line 386 - you skip comma in the number.

Line 469 - "an" not "a".

When you one use full name of the disease (African swine fever line 68) in the rest part of manuscript use shortcut (see line 471).

In reference you should use one form of ending in order to numer of pages: „p.1-2”, pp.1-2” „p. 1-2”.

In reagarding to point 3 "Have the authors made all data underlying the findings in their manuscript fully available?" - the data presented in paper are clear and available in the manuscript however the authors made declaration that the data are partly confidence:

"Data cannot be shared publicly due to confidentiality issue as this is government individual census data"

so I am not sure if the manusrcipt could be publish.

Reviewer #2: Major issues:

This is a well-written study providing insights for of swine movements networks in Argentina in order to define the most strategic points for infectious diseases prevention and control. This detailed analysis was based on comprehensive and reliable dataset, obtained from national registry of pig movements. The methods selected by the authors (social network analysis – SNA and graph theory) were previously applied by others to characterize swine movement networks in other countries, but this report was the first work regarding this issue in Argentina, thus it seems to be important and necessary in regards to the control of swine pathogens spreading.

I believe this manuscript has a great potential for publication. The manuscript is well organized and the methods are sound. The study cites current literature, which is properly placed in the context. The methods used in the study are clearly stated, the details of the methodology are sufficient to reproduce the study by other authors. The study generated a lot of data, which is presented in the tables and figures, properly placed in the manuscript. The interpretation of results is fully supported by the data, followed by comprehensive discussion with regards to similar studies performed by other authors. Moreover, also limitations of the analysis are well discussed, highlighting the need for collecting of more data regarding individual pig movement to improve the resolution of the study (lines558-559). The use of sample farms A, B, C in discussion significantly improved understanding of the limitations of the study. Discussion section is well written, nevertheless the context of infectious diseases spreading in the context of obtained data is slightly insufficient and should be expanded to reinforce the meaning of the obtained results. The study is performed on the country level, but in the context of exotic diseases, also the issue of pig import into Argentina should be at least mentioned in the introduction, and need minor discussion on the background of obtained data. Any information of pig of foreign origin on the market might indicate the potential sources of disease introduction into Argentina. Nevertheless, this minor missing issues did not affect overall high quality and informativeness of the study.

Minor issues:

1. If is is possible, the tables 2-7 should be moved into supplementary information.

2. White background in the figures 1 and 2 will improve graphical presentation of the data.

3. Figure 10 is not necessary, depicted node is easy to observe at figure 11.

4. Lines 73-75: reference is missing.

5. Lines 77-80: “[…]transboundary, re-emerging diseases if they enter the country” – remove unnecessary comma and change “should” to “if”.

6. Lines 87-88: comma should stand instead of full stop after reference no 13.

7. Line 469: an important

8. 67-68, 471-472: diseases names should be written lowercase, except “African swine fever”.

9. Line 479-480: I would change “[…]we have what is known as the[…]” into “there is so-called”

10. Lines 483-486: too many words of “small”, try to use synonymous words

11. Line 584: “[…]would be the most useful”

**********

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Reviewer #1: No

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

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7 May 2020

Dear editors

We thank you for your comments. Please find attached our response to the reviewers’ comments to our manuscript entitled “Application of network analysis and cluster analysis for better prevention and control of swine diseases in Argentina” by Dr. Jerome Baron, Dr. Maria Aznar, Dr. Mariela Monterubbianesi and Dr. Beatriz Martinez Lopez, as well as an edited copy taking into account these comments. We hope we have addressed the comments as to make this manuscript suitable for publication.

Thank you in advance for your consideration,

Best Regards,

Jerome Baron, DVM, MSc

Center for Animal Disease Modeling and Surveillance (CADMS)

Department of Medicine & Epidemiology

School of Veterinary Medicine

University of California

Davis, CA 95616 USA

jnbaron@ucdavis.edu

APRIL 28 2020 REVIEW

1. Please amend the manuscript submission data (via Edit Submission) to include author Mariela Monterubbianesi.

Author has been added

2. Thank you for taking careful note of Google Map’s policies--their license on map images indeed does not comply with the license PLOS uses, CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/). To confirm that the sources of your new map images do comply with our policy, we still require some additional information. Please indicate what “source and package” you used to create the images and the “open sources shape files.”

The R package used for map sourcing (package “map”) was already referenced (reference 16). The data source (Natural Earth data) for the Argentina shapefile has been added (reference 17), and is indeed open-sourced as is specified in their terms of use (https://www.naturalearthdata.com/about/terms-of-use/)

3. We note our Data Availability Statement reads: “No - some restrictions will apply. Data cannot be shared publicly as this data is owned by a third-party and has confidentiality issue as this is individual census data. Data accessibility and restriction information can be obtained from the National Institute of Agricultural Technology (INTA) and the National Service of Agri-Food health and Quality (SENASA). For more information about data accessibility please contact infopublica@senasa.gob.ar.”

Before we proceed with the review process, we’ll require some additional information to ensure your submission adheres to the PLOS ONE policy regarding acceptable third-party data restrictions: https://journals.plos.org/plosone/s/data-availability#loc-acceptable-data-access-restrictions.

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I do confirm

2.) Please confirm whether access requests for both the INTA and SENASA data can be sent to infopublica@senasa.gob.ar. If not, please provide non-author contact information (preferably email) to which INTA data access requests can be sent.

I do confirm that data requests can be made at this email. However, I made a mistake in the original statement, data belongs to SENASA only and not INTA. I have modified the statement in the online submission page to correct this and address the 2 requests.

JANUARY 13 2020 REVIEW

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at http://www.journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and http://www.journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

We have made sure that all template requirements have been to the extant of our observations.

2. We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For more information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions.

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We will update your Data Availability statement on your behalf to reflect the information you provide.

Data are owned by a third-party organization, the Argentine National Service of Agri-Food Health (SENASA), a department of the Ministry of Agriculture, which doesn’t not allow us to share the data directly. These data are collected for SENASA’s surveillance operations.They contain sensitive and identifiable information regarding this country’s production system and individual farmers. Moreover, given the analysis completed in this paper, fully de-indentifying the data would involve removing spatial coordinates, which would not make our findings reproducible, as they involved spatial methods that used the detailed individual locations of farms. Researchers may ask about data availability and restrictions to SENASA directly, here is the contact info:

infopublica@senasa.gob.ar

3. We note that Figure(s) 3 and 11 in your submission contain [map/satellite] images which may be copyrighted. All PLOS content is published under the Creative Commons Attribution License (CC BY 4.0), which means that the manuscript, images, and Supporting Information files will be freely available online, and any third party is permitted to access, download, copy, distribute, and use these materials in any way, even commercially, with proper attribution. For these reasons, we cannot publish previously copyrighted maps or satellite images created using proprietary data, such as Google software (Google Maps, Street View, and Earth). For more information, see our copyright guidelines: http://journals.plos.org/plosone/s/licenses-and-copyright.

We require you to either (1) present written permission from the copyright holder to publish these figures specifically under the CC BY 4.0 license, or (2) remove the figures from your submission:

In searching for the possibility of obtaining copyright access from Google maps to use their background, we found a statement from them stipulating that they not grant explicit written permission for use of their content, though use of their maps is still permitted. This is stated in the link below:

https://www.google.com/permissions/geoguidelines/

Thus to remove doubt, we remade the maps using a new source and package with no copyright issues as the figure now uses open-sourced shapefiles. References and legends have been updated accordingly

Reviewer #1: The paper presents very important data regarding to Argentina pigs industry - number of herds, size of herds and all possible connection between them even sesonal data. The statistical data idicate the future solution in preventing the spread of pig diseases such as African swine fever.

Line 60-63 - the sentence is to long and unclear, you should use two separete sentences.

Changed as suggested (line 60-65)

In line 67-68, Porcine Reproductive Respiratory Syndrome, African Swine Fever and Classical Swine Fever should be written with lowercase letters

Changed as suggested (line 69-70)

Line 77-80 you are using twice the word "re-emerging".

Changed as suggested (line 81)

Line 386 - you skip comma in the number.

Changed as suggested (line 388)

Line 469 - "an" not "a".

Changed as suggested (line 472)

When you one use full name of the disease (African swine fever line 68) in the rest part of manuscript use shortcut (see line 471).

Changed as suggested (line 474, 475)

In reference you should use one form of ending in order to numer of pages: „p.1-2”, pp.1-2” „p. 1-2”.

Changed to p.1-2 format (ref 1, 2, 5, 8, 10, 11)

In reagarding to point 3 "Have the authors made all data underlying the findings in their manuscript fully available?" - the data presented in paper are clear and available in the manuscript however the authors made declaration that the data are partly confidence:

"Data cannot be shared publicly due to confidentiality issue as this is government individual census data"

so I am not sure if the manusrcipt could be publish.

We meant that the detailed dataset with individual observations, location and identification numbers was confidential due to the need to protect individual swine operations and the fact that this data is proprietary to SENASA. The summarized data as presented in the manuscript has been approved for publication by our collaborators.

Reviewer #2: Major issues:

This is a well-written study providing insights for of swine movements networks in Argentina in order to define the most strategic points for infectious diseases prevention and control. This detailed analysis was based on comprehensive and reliable dataset, obtained from national registry of pig movements. The methods selected by the authors (social network analysis – SNA and graph theory) were previously applied by others to characterize swine movement networks in other countries, but this report was the first work regarding this issue in Argentina, thus it seems to be important and necessary in regards to the control of swine pathogens spreading.

I believe this manuscript has a great potential for publication. The manuscript is well organized and the methods are sound. The study cites current literature, which is properly placed in the context. The methods used in the study are clearly stated, the details of the methodology are sufficient to reproduce the study by other authors. The study generated a lot of data, which is presented in the tables and figures, properly placed in the manuscript. The interpretation of results is fully supported by the data, followed by comprehensive discussion with regards to similar studies performed by other authors. Moreover, also limitations of the analysis are well discussed, highlighting the need for collecting of more data regarding individual pig movement to improve the resolution of the study (lines558-559). The use of sample farms A, B, C in discussion significantly improved understanding of the limitations of the study. Discussion section is well written, nevertheless the context of infectious diseases spreading in the context of obtained data is slightly insufficient and should be expanded to reinforce the meaning of the obtained results. The study is performed on the country level, but in the context of exotic diseases, also the issue of pig import into Argentina should be at least mentioned in the introduction, and need minor discussion on the background of obtained data. Any information of pig of foreign origin on the market might indicate the potential sources of disease introduction into Argentina. Nevertheless, this minor missing issues did not affect overall high quality and informativeness of the study.

As import/export data was not made available to us, we had to limit the scope of our study at the national level. We are aware that imports of foreign pigs are a potential source for introduction of new diseases. This was addressed in a new paragraph in the conclusion (line 652-658).

Minor issues:

1. If is is possible, the tables 2-7 should be moved into supplementary information.

We think tables 2-7 are key for the understanding and reference of the paper results and, therefore should be kept in the main text, not as supplementary information.

2. White background in the figures 1 and 2 will improve graphical presentation of the data.

Changed as suggested

3. Figure 10 is not necessary, depicted node is easy to observe at figure 11.

Figure removed and figure references adjusted accordingly (lines 378-380, 394-395, 401, 402, 405, 408, 432, 438, 441, 450, 460, 637)

4. Lines 73-75: reference is missing.

Added a reference as suggested (lines 76-77, ref 4)

5. Lines 77-80: “[…]transboundary, re-emerging diseases if they enter the country” – remove

unnecessary comma and change “should” to “if”.

Changed based on reviewer 1’s comment

6. Lines 87-88: comma should stand instead of full stop after reference no 13.

Changed as suggested (line 90)

7. Line 469: an important

Changed as suggested (line 472)

8. 67-68, 471-472: diseases names should be written lowercase, except “African swine fever”.

Changed as suggested (line 69-70)

9. Line 479-480: I would change “[…]we have what is known as the[…]” into “there is so-called”

Sentence modified to fit suggestion (line 482-484)

10. Lines 483-486: too many words of “small”, try to use synonymous words

Sentence changed with new worthing (line 488-489)

11. Line 584: “[…]would be the most useful”

Changed as suggested (line 588)

28 May 2020

Application of network analysis and cluster analysis for better prevention and control of swine diseases in Argentina

PONE-D-19-34431R1

Dear Dr. Baron,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication.

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If your institution or institutions have a press office, please notify them about your upcoming paper to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

With kind regards,

Grzegorz Woźniakowski, PhD ScD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: (No Response)

Reviewer #2: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

3 Jun 2020

PONE-D-19-34431R1

Application of network analysis and cluster analysis for better prevention and control of swine diseases in Argentina

Dear Dr. Baron:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

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on behalf of

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PLOS ONE