Epidemiological surveillance and economic impact analysis of different porcine reproductive and respiratory syndrome virus infection statuses in 23 breeding pig farms in Hubei, China

Abstract

Porcine reproductive and respiratory syndrome virus (PRRSV) has emerged as a significant threat to the pig farming industry worldwide, resulting in considerable economic losses. However, few reports detail its economic impact on the pig farming sector. A study was conducted on 23 breeding pig farms in Hubei Province from January 2021 to December 2023, and the PRRSV infection status and associated economic losses were monitored to address this gap. PRRSV antigens and antibodies were identified through enzyme-linked immunosorbent assay (ELISA) and quantitative reverse transcription polymerase chain reaction (qRT-PCR). Additional monthly production data and weaning costs were gathered. The Kruskal-Wallis nonparametric test was used to assess the differences in production efficiency and weaning costs across various PRRSV infection statuses. Dunn’s test was used to compare multiple groups. The parameter distributions of various variables were determined via @RISK (V. 8.5.2) software. Models were developed to evaluate the economic impact of PRRSV infection status on breeding pig farms and assess the losses from a PRRSV outbreak in either provisional PRRSV-negative or PRRSV-positive stable farms. A total of 754 months of monitoring was conducted across 23 breeding pig farms, which included 131 months (17.37%) classified as PRRSV provisional negative, 298 months (39.52%) as PRRSV-positive stable, and 325 months (43.11%) as PRRSV-positive unstable. The production efficiency and weaning costs were similar between provisional PRRSV-negative farms and PRRSV-positive stable farms, revealing no significant differences. However, these metrics varied significantly compared with those of PRRSV-positive unstable farms. With respect to provisional PRRSV-negative farms, PRRSV-positive stable farms and unstable farms faced additional annual losses of ¥3,135.17 and ¥4,898.79 per sow, respectively. Compared with PRRSV-positive stable farms, PRRSV-positive unstable farms incurred an extra annual loss of ¥1,763.62 per sow. Upon a PRRSV outbreak on a swine farm, followed by a return to preoutbreak conditions, the average economic loss per sow on provisional PRRSV-negative farms is approximately ¥3,061.21. Conversely, PRRSV-positive stable farms face an average loss of approximately ¥508.42 per sow. This study provides a systematic evaluation of the economic impact of PRRSV on Chinese pig farms, offering data to support the quantitative assessment of economic losses stemming from PRRSV within the domestic pig farming industry.

Introduction

Porcine reproductive and respiratory syndrome (PRRS) is a highly contagious disease caused by porcine reproductive and respiratory syndrome virus (PRRSV), which naturally infects domestic and wild pigs. In fattening pigs typically aged eight weeks to slaughter, PRRS mainly presents as a respiratory illness, whereas in sows, it is characterized primarily by reproductive disorders (Albina 1997; Rossow 1998). PRRSV replicates in pig macrophages, resulting in prolonged viremia and persistent infection (Kimman et al. 2009). PRRSV was first described in the United States in 1987 (Rossow 1998), isolated in Europe and North America in the 1990s (Collins et al. 1992; Wensvoort et al. 1991), and reported in China in 1995 (Gao and Chen 1996). PRRSV is a single-stranded positive-sense RNA virus that belongs to the order Nidovirales, family Arteriviridae, and genus Betaarterivirus (Adams and Carstens 2012). The particles of PRRSV measure approximately 50‒60 nm in diameter (Lunney et al. 2016). Its genome is approximately 15 kb long, featuring a cap structure at the 5' end and a poly-A tail at the 3' end (Snijder and Meulenberg 1998). Porcine reproductive and respiratory syndrome virus (PRRSV) can be classified into two distinct genotypes on the basis of genetic nucleotide sequence variations: PRRSV-1 (European type) and PRRSV-2 (North American type) (Murtaugh et al. 1995; Nelsen et al. 1999). The Lelystad and VR-2332 virus strains are representative of PRRSV-1 and PRRSV-2, respectively, with nucleotide sequence similarities between the two genotypes ranging from approximately 50% to 70% (Collins et al. 1992; Wensvoort et al. 1991). Genetic evolutionary analysis of the ORF5 gene has revealed that PRRSV-1 can be classified into three subtypes (lineages 1–3), whereas PRRSV-2 can be divided into nine subtypes (lineages 1–9) (Balka et al. 2018; Shi et al. 2010; Stadejek et al. 2013). In China, PRRSV-2 is the predominant genotype, with circulating strains belonging primarily to lineage 8 (JXA-1-like/CH-1a-like strains), lineage 5 (VR2332-like strains), lineage 3 (QYYZ-like strains), and lineage 1 (NADC30-like strains) (Guo et al. 2018; Shi et al. 2010, Ouyang et al. 2024).

PRRS has emerged as one of the most devastating diseases in the global pig farming industry, leading to considerable economic losses. In 2006, an outbreak of highly pathogenic PRRSV (HP-PRRSV) in China resulted in the deaths of more than two million pigs across ten provinces in a short period, with morbidity rates ranging from 50 to 100% and mortality rates ranging from 20 to 100% (Tong et al. 2007; Tian et al. 2007). PRRS leads to approximately $66.4 million in annual economic losses for the U.S. pig farming industry, with losses continuing to rise (Holtkamp et al. 2012; Neumann et al. 2005). European researchers developed a model to simulate the economic impact of the PRRS on various pig farms. Their findings indicate that a 1,000-sow farm experiencing mild PRRSV infection during the nursery and fattening stages incurred a median annual economic loss of €75,724 (90% CI: €78,885‒€122,946). In stark contrast, severe infections across all stages resulted in median annual losses of €650,090 (90% CI: €603,585–€698,379). Moderate infections at all stages lead to annual losses of approximately €46,021 for sows, €422,387 for fattening pigs, and €25,435 for nursery pigs (Nathues et al. 2017). Renken et al. developed a cost simulation tool utilizing production data from 21 PRRS-affected pig farms in Germany to assess the economic impact of the PRRS at the farm level. They reported that PRRS infection leads to a median annual loss of €255 per sow (Renken et al. 2021). In a related study, Kim et al. compared the production efficiency of a provisional PRRSV-negative farrow-to-weaning farm in Korea before and after a PRRSV-1 outbreak. Following the outbreak, they reported a 7.1% decrease in the farrowing rate, a decrease of 1.2 piglets per litter, and a decrease of 2.2 live piglets per litter. Furthermore, the number of weaned piglets decreased by 2.7, and the weaning weight decreased by 0.9 kg per piglet. The average daily gain for fattening pigs declined by 69.8 g. Notably, the abortion rate rose by 3.9%, the return-to-estrus rate increased by 2.9%, the preweaning mortality rate increased by 2.8%, and the feed efficiency improved by 0.26. The average loss per sow was $294.6 (Kim et al. 2022). Danish pig farms infected with a highly virulent PRRSV-1 recombinant strain experienced a significant 10.8% decrease in the farrowing rate, a reduction of 4.8 live piglets per litter, and a decrease of 6.5 weaned piglets per litter (Kristensen et al. 2020).

Despite the significant threat posed by PRRSV to swine health and farm profitability, comprehensive studies that quantify its impact on production efficiency and economic outcomes, particularly in China, remain conspicuous. Therefore, it is urgently necessary to evaluate and analyze the impact of PRRSV on production efficiency and economic performance in Chinese pig farms. This study selected twenty-three pig farms in Hubei Province, China. Monthly samples, including serum, umbilical cord blood, lung lavage fluid, oral fluid, and boar testicular fluid, were collected monthly for PRRSV antigen and antibody testing to assess various PRRSV infection statuses across the farms. Additionally, monthly production and weaning cost data were collected and compared, and a model was used to evaluate the economic impact of PRRSV on these pig farms via a systematic simulation approach.

Results

Location of breeding pig farms and monthly PRRSV infection status

As of December 2023, 23 large-scale pig breeding farms in Hubei Province were selected for analysis (data for farm No. 2 were collected up to November 2023). Among these farms, six were PRRSV provisional negative, 11 were PRRSV positive stable, and six were PRRSV positive unstable (Fig. 1). Among these 23 breeding pig farms, the earliest was established in 1995, whereas the most recent began operations in 2022. The average number of sows on these farms ranges from 631 to 5,630. From January 2021 to December 2023, 17 farms conducted PRRSV antigen and antibody testing for 36 consecutive months, accounting for 65.38% of the total farms. The shortest monitoring period spanned five months, from August 2023 to December 2023. Eleven farms collected 30 umbilical cord blood samples, 30 weaned piglet nasal swabs, one boar testicular fluid sample monthly for PRRSV antigen testing, and 40 sow serum samples monthly for PRRSV antibody testing. The remaining 12 farms randomly collected umbilical cord blood, oral fluid, lung lavage fluid, and serum samples from 3% of the sow population for PRRSV antigen and antibody testing. With respect to PRRSV vaccination, four farms administered inactivated PRRSV vaccines, whereas 19 farms opted not to use any vaccination (Table 1). Across the 23 farms, PRRSV antigen and antibody prevalence was monitored for 754 months. Among these cases, those at 131 months (17.37%) were categorized as PRRSV provisional negative, those at 298 months (39.52%) as PRRSV-positive stable, and those at 325 months (43.11%) as PRRSV-positive unstable (Table 2). The distribution of the monthly PRRSV infection status across the various farms is shown in Fig. 2.

Fig. 1

Geographic location and PRRSV infection status of pig farms in Hubei Province in December 2023. Note: Farm No. 1 (PRRSV-positive stable) is not shown on the map because of its proximity to farm No. 20 (PRRSV provisional negative). Farm No. 2 is monitored until November 2023. PRRSV, porcine reproductive and respiratory syndrome virus

Table 1 Background information and monthly PRRSV monitoring of breeding pig farms

Table 2 Contingency table of PRRSV vaccine use and PRRSV infection status in pig farms

Fig. 2

The monthly counts of different PRRSV infection statuses across various pig breeding farms. PRRSV, porcine reproductive and respiratory syndrome virus

Analysis of production efficiency indicators in breeding pig farms

Table 3 highlights significant differences in sow mortality rates across different PRRSV infection statuses on breeding pig farms. The rates were lowest at 4.61% on provisional PRRSV-negative farms, 7.06% on stable PRRSV-positive farms, and highest at 7.94% on unstable PRRSV-positive farms. Sow repeat breeding rates, average healthy piglets per litter, stillborn counts, and stillbirth rates on provisional PRRSV-negative farms and PRRSV-positive stable farms are similar and lower than those on unstable PRRSV-positive farms. There were significant differences in mummified fetuses and mummification rates among the different PRRSV infection statuses, with the highest rates occurring in PRRSV-positive unstable farms (0.34 and 2.52%). The farrowing rates were similar for the provisional PRRSV-negative (89.87%) and PRRSV-positive stable farms (88.82%), both of which were higher than those for the PRRSV-positive unstable farms (86.15%). The average birth weight of healthy piglets was highest on stable PRRSV-positive farms, at 1.39 kg. Healthy piglet production per sow is greater on provisional PRRSV-negative (27.52) and PRRSV-positive stable farms (27.73) than on PRRSV-positive unstable farms (24.87). Farrowing-house mortality is lower in the first two categories than in PRRSV-positive unstable farms. The average number of weaned piglets per litter was also greater on provisional PRRSV-negative (11.23) and PRRSV-positive stable farms (11.31) than on PRRSV-positive unstable farms (10.68). Preweaning mortality is highest in PRRSV-positive unstable farms, at 15.27%. The average weaning weight was highest on these PRRSV-positive unstable farms, at 6.67 kg. The number of weaned piglets produced per sow per year on provisional PRRSV-negative farms (25.52) and PRRSV-positive stable farms (25.88) was significantly greater than that on PRRSV-positive unstable farms (23.02). The cost of weaning piglets is lowest on provisional PRRSV-negative farms (¥430.11) and PRRSV-positive stable farms (¥438.64) and significantly lower than that on PRRSV-positive unstable farms (¥514.84).

Table 3 Comparison of production efficiency in breeding pig farms with different PRRSV infection statuses

The economic impact of different PRRSV infection statuses on breeding pig farms

Using @Risk for distribution fitting of the collected data, combined with expert and onsite veterinarian opinions, we determined the parameter distributions for variables such as the price of weaned piglets (¥/kg), average annual number of weaned piglets per sow, average weaning weight (kg), total cost per weaned piglet (¥/piglet), and premium for PRRSV provisional negative weaned piglets under different PRRSV infection statuses. The parameter distribution for the price of weaned piglets (¥/kg) was obtained by fitting data from the Ministry of Agriculture and Rural Affairs from January 2021 to December 2023. It follows a triangular distribution (23.25, 23.25 and 96.96) for all three PRRSV infection statuses. The annual number of weaned piglets per sow follows a PERT distribution (5.38, 26.12 and 42.63) on PRRSV provisional negative farms, a PERT distribution (1.13, 27.90 and 40.36) on PRRSV-positive stable farms, and a Kumaraswamy distribution (6.26, 4.97, 13.78 and 38.26) on PRRSV-positive unstable farms. The average weaning weight (kg) follows a PERT distribution (3.00, 6.73 and 6.84) for PRRSV provisional negative farms, a Kumaraswamy distribution (6.48, 22.15, 3.86 and 8.52) for PRRSV-positive stable farms, and a Triangular distribution (4.98, 7 and 7.51) for PRRSV-positive unstable farms. The total cost per weaned piglet (Ұ /piglet) follows a triangular distribution (302.26, 423.03 and 572.96) on PRRSV provisional negative farms, a PERT distribution (246.00, 358.24 and 1056.50) on PRRSV-positive stable farms, and a PERT distribution (271.67, 297.73 and 1811) on PRRSV-positive unstable farms. The premium for PRRSV provisional negative weaned piglets follows a PERT distribution (20, 100 and 300), as shown in Table 4. By conducting systematic simulations on the established model, we obtained frequency distribution histograms of the annual average profit per sow (¥/head) under three PRRSV infection statuses (Fig. 3A-C). The mean annual average profit per sow (¥/head) is −507.64 for PRRSV provisional negative farms, −3,642.81 for PRRSV-positive stable farms, and −5,406.43 for PRRSV-positive unstable farms. Owing to the generally low pork prices from 2021–2023, the annual average profit per sow (¥/head) was mainly in a loss state. The probability of a positive annual average profit per sow (Ұ /head) is 0.41 for PRRSV provisional negative farms, 0.21 for PRRSV-positive stable farms, and 0.16 for PRRSV-positive unstable farms (Table 5). Sensitivity analysis revealed that for provisional PRRSV-negative farms and PRRSV-positive unstable farms, the variable "price of weaned piglet (¥/kg)" had the most significant effect on the average annual revenue of sows. In contrast, for PRRSV-positive stable farms, the variable "Full cost of weaned piglet (¥/head)" was identified as the critical indicator affecting the average annual revenue of sows (data not shown). Further comparative analysis of the annual average profit per sow (¥/head) among PRRSV provisional-negative, PRRSV-positive stable, and PRRSV-positive unstable farms revealed that compared with PRRSV provisional-negative farms, PRRSV-positive stable farms incur an annual loss of 3,135.17 ¥ per sow. In comparison, PRRSV-positive unstable farms incurred annual losses of ¥ 4,898.79 per sow. Additionally, PRRSV-positive unstable farms incur an annual loss of ¥ 1,763.62 more per sow than PRRSV-positive stable farms do (as detailed in Table 5).

Table 4 Distribution of production efficiency among breeding pig farms with different PRRSV infection statuses

Fig. 3

Simulated sampling distribution histogram of average annual income per sow under different PRRSV infection statuses. A PRRSV provisional negative farm. B PRRSV-positive stable farm. C PRRSV-positive unstable farm. The red line represents the probability density cumulative curve, whereas the red rectangles depict the frequency distribution histogram of the sow's average annual income. PRRSV, porcine reproductive and respiratory syndrome virus

Table 5 Average annual income and economic losses of sows with different PRRSV infection statuses

Simulated economic impact assessment of a PRRSV outbreak on a breeding pig farm

On the basis of the economic impact data of different PRRSV infection statuses from the previous section, we developed a model to simulate the economic losses caused by a PRRSV outbreak in a breeding pig farm with 2,400 sows. Compared with those on provisional PRRSV-negative farms, the annual economic loss per sow on stable PRRSV-positive farms follows a Pearson five distribution (48.88, 1, 464 and 506). In contrast, PRRSV-positive unstable farms followed an extreme value distribution (2, 172.3, 4 and 711.9). Compared with PRRSV-positive stable farms, the annual economic loss per sow on PRRSV-positive unstable farms followed a log-logistic distribution (−40, 375, 41, 580 and 11.195). Additionally, on the basis of the literature review, the distributions of the number of weeks required to produce PRRSV provisional negative pigs at weaning (TTS) and the number of weeks needed to recover to the baseline production level that the herd had before PRRSV detection (TTBP) following a PRRSV outbreak in a breeding pig farm are as follows: trigen distribution (21.6, 26.6, 33, 25 and 75) (a special triangular distribution) and triangular distribution (0, 16.5 and 29) (Linhares et al., 2014), as shown in Table 6. Through sampling simulation, we found that a PRRSV outbreak on a PRRSV-negative farm with 2,400 sows would result in an estimated economic loss of approximately ¥ 7,347,047.87, with an average loss of ¥ 3,061.27 per sow and a median loss of ¥ 2,654.54. In contrast, a PRRSV outbreak in a PRRSV-positive stable farm of the same size would cause an average economic loss of approximately ¥ 1,220,208.13, with an average loss of ¥ 508.42 per sow and a median loss of ¥ 268.84 (Fig. 4A-B and Table 7). Similarly, the sensitivity analysis results indicated that the variable "price of weaned piglet (¥/kg)" significantly impacts the economic losses experienced during PRRSV outbreaks on breeding farms (data not shown).

Table 6 Parameter distribution of economic loss model for an PRRSV outbreak in breeding pig farms

Fig. 4

Simulated sampling distribution histogram of PRRSV outbreak economic losses on a 2,400-sow farm. A An outbreak of PRRSV infection on a provisional PRRSV-negative farm. B An outbreak of PRRSV infection on a stable PRRSV-positive farm. The red line is the cumulative probability density curve. The red rectangle is the frequency distribution histogram of economic losses caused by PRRSV infection. PRRSV, porcine reproductive and respiratory syndrome virus

Table 7 Estimating economic losses due to PRRSV outbreak in a breeding farm with 2,400 sows

Discussion

This study conducted a comprehensive three-year monthly sampling survey across 23 large-scale pig farms in Hubei Province to investigate the prevalence of antibodies and antigens of PRRSV and determine the monthly infection status of these farms. The production data and weaning costs were collected monthly from breeding pig farms, excluding months in which farm capacity utilization fell below 50%. The analysis focused on the differences in production efficiency and economic impact under various PRRSV infection statuses. Throughout the study, the 23 pig farms were monitored for 754 months. The infection states observed included 131 months (17.37%) in a PRRSV provisional negative state, 298 months (39.52%) in a PRRSV-positive stable state, and 325 months (43.11%) in a PRRSV-positive unstable state (as detailed in Table 2). The results revealed no significant differences in production efficiency or costs for weaned piglets between farms in a provisional PRRSV-negative state and those in a stable PRRSV-positive state. However, pronounced differences were noted when these farms were compared with those in a PRRSV-positive unstable state (Table 3). By fitting distributions to the collected production data, we employed Monte Carlo simulation to estimate the average annual profitability of sows under different PRRSV infection statuses. Owing to the continuous decrease in market prices for weaned piglets from January 2021 to December 2023, the annual profitability of sows is anticipated to remain negative. Furthermore, sows from provisional PRRSV-negative farms benefitted from a price advantage when PRRSV-negative weaned piglets were sold, positioning these farms to maintain profitability even in a declining market (with a 41% likelihood of sow profitability). These findings underscore the importance of enhancing overall herd health and expediting disease eradication for the sustainability of pig farms.

The sample collection for assessing PRRSV infection status met the required standards across all farms according to the American Association of Swine Veterinarians (AASV) guidelines (Holtkamp et al. 2011). However, to mitigate testing costs, most large-scale farms utilize pooled samples for PRRSV antigen testing, which limits the ability to obtain results for individual samples. Additionally, some farms (Farms 12–23) collected samples from 3% of the sow inventory, but the exact sample sizes for each farm are still being determined. Furthermore, four farms were vaccinated against PRRSV, influencing antibody and antigen positivity rates. Consequently, each farm's overall PRRSV antibody and antigen positivity rates were not calculated.

This study aimed to determine the PRRSV infection status of each farm through monthly sampling and testing. Therefore, we adjusted the definitions of the various PRRSV infection statuses according to the classification system established by the AASV and the specific circumstances of each farm. From January 2021 to December 2023, we determined each farm's monthly PRRSV infection status through antigen and antibody sampling across 23 pig farms. However, only 17 farms completed 36 months of continuous monitoring because the farms were established at different times. The remaining six farms were monitored for 5, 25, 26, 26, 30 and 35 months (Table 1). The combined proportion of PRRSV-positive statuses (stable and unstable) across all farms was 82.63%. This finding is consistent with epidemiological survey results on PRRSV antibody positivity rates in China (Guo et al. 2018).

There was no difference in production efficiency or the total cost of weaning piglets between provisional PRRSV-negative farms and stable PRRSV-positive farms. However, compared with PRRSV-positive stable farms, PRRSV-positive unstable farms presented a more significant average annual loss per sow of ¥1,763.62, with a median loss of ¥1,094.63, which was slightly greater than the results reported by other researchers. This discrepancy may be because our study assumed that PRRSV-positive unstable farms remained unstable throughout the year, potentially experiencing multiple PRRSV outbreaks and leading to overestimating the losses in our calculations. In contrast, other researchers estimated the economic loss from a single outbreak via partial budgeting methods. Moreover, on the basis of our previous monitoring results, we found that the average monthly proportion of PRRSV instability on farms was only 43.11% (range: 0%−93.54%, data not shown) (Fig. 2 and Table 2). As a result, our computed values may represent an upper limit on the potential sow losses associated with PRRSV instability. Additionally, the cost data for weaned piglets in this study were provided by the financial staff of the relevant breeding pig farms and included all costs incurred during actual production. Factors such as labor costs, vaccination expenses, biosecurity measures, PRRSV strain type, secondary diseases, currency depreciation rates, and market prices also influence the economic losses of breeding pig farms (Ogno et al. 2019; Papatsiros 2012; Thanawongnuwech and Suradhat 2010; Zhao et al. 2021).

Zhendong Zhang assessed the economic impact of PRRSV on China's pig industry by analyzing production data from four pig farms before and after PRRSV outbreaks. Their research indicated an average loss of ¥822.75 per sow per PRRS outbreak, which increased to ¥1,424.37 when factoring in losses from finishing pigs (Zhang et al. 2022). Similarly, Nieuwenhuis examined nine pig farms that underwent an 18-week PRRS outbreak and reported an average loss of €126 per sow (Nieuwenhuis et al. 2012). Our study revealed that the average annual loss per sow was ¥3,135.17 in farms with PRRSV-positive stable conditions and ¥4,898.79 in PRRSV-positive unstable farms, significantly surpassing the losses reported by previous researchers. During our epidemiological surveillance on the farm, we focused solely on collecting samples to monitor the prevalence of PRRSV without sampling or testing for other pathogens. However, no significant outbreaks of diseases other than ASF were detected during the surveillance period. However, the potential circulation of other pathogens within the farm cannot be ruled out, which could lead to an overestimation of the economic losses attributed to PRRSV. On the basis of these findings, we further simulated and assessed the economic losses caused by a PRRSV outbreak in provisional PRRSV-negative farms and stable PRRSV-positive farms. The results revealed that a PRRSV outbreak on a provisional negative PRRSV farm with 2,400 sows would result in an average loss of ¥7.35 million, with an average loss of ¥3,061.27 per sow. In PRRSV-positive stable farms (with 2,400 sows), a PRRSV outbreak led to an economic loss of approximately ¥1.22 million, with an average loss of ¥508.42 per sow. Since PRRSV provisional negative farms cannot sell PRRSV provisional negative weaned piglets during an outbreak, they lose their price advantage, resulting in more significant economic losses. This result is similar to those of other studies but with some differences. The differences may be attributed to this study being the first in China to use a systematic simulation approach to assess the economic impact of PRRSV infection on breeding pig farms. The model variables were dynamically sampled rather than fixed, potentially making the results more reflective of real-world conditions (Dijkhuizen et al. 1995; Spreen et al. 2019). Another critical factor is that this study considered the price advantage of PRRSV provisional negative weaned piglets produced by PRRSV provisional negative farms. Therefore, further research is needed to assess the economic impact of PRRSV accurately.

Conclusion

In December 2023, six of the 23 breeding pig farms were PRRSV provisional negative, 11 were PRRSV-positive stable, and six farms were PRRSV-positive unstable. Monitoring the prevalence of PRRSV antibodies and antigens over a cumulative 754 months across these 23 large-scale pig farms revealed that the provisional PRRSV-negative status was present for 131 months (17.37%), the PRRSV-positive stable status was present for 298 months (39.52%), and the PRRSV-positive unstable status was present for 325 months (43.11%). There were no significant differences in production efficiency or weaned piglet costs between provisional PRRSV-negative farms and stable PRRSV-positive farms. However, there were notable differences compared with PRRSV-positive unstable farms. Between 2021 and 2023, the average annual loss per sow was ¥507.64 on provisional PRRSV-negative farms, ¥3,462.81 on PRRSV-positive stable farms, and ¥5,406.43 on PRRSV-positive unstable farms. The probability of positive profitability per sow under the three PRRSV infection statuses was 0.41 for provisional PRRSV-negative farms, 0.21 for PRRSV-positive stable farms, and 0.16 for PRRSV-positive unstable farms. Compared with provisional PRRSV-negative farms, PRRSV-positive stable farms and PRRSV-positive unstable farms presented additional average annual losses per sow of ¥3,135.17 and ¥4,898.79, respectively. Compared with PRRSV-positive stable farms, PRRSV-positive unstable farms presented an additional average annual loss per sow of ¥1,763.62. Simulation estimates indicate that a PRRSV outbreak in a farm with 2,400 sows would result in an approximate loss of ¥7.35 million in PRRSV provisional negative farms, with an average loss of ¥3,061.21 per sow, and a loss of ¥1.22 million in PRRSV-positive stable farms, with an average loss of ¥508.42 per sow. This study systematically evaluated the current economic impact of PRRSV infection on pig farms in China, providing valuable data for accurately estimating the economic losses that PRRSV causes to the country's pig industry. These findings underscore the importance of strengthening PRRSV clinical control as a critical factor influencing the profitability and development of the pig farming sector.

Methods

Sampling methods

In this study, 23 pig farms were selected for monthly sampling to detect PRRSV antibodies and antigens. The 23 breeding farms are all affiliated with a single large-scale corporation group in Hubei Province, China. According to the AASV guidelines for PRRSV infection status monitoring, which assume a PRRSV prevalence of 10% and a 95% confidence interval for an unknown population size, each farm should have at least 30 samples (Holtkamp et al. 2011). Each month, the farm veterinarian created a PRRSV sampling and monitoring plan. The pigs were randomly selected for sample collection to detect PRRSV antigens and antibodies, including serum, umbilical cord blood, nasal swabs, oral fluid, testicular fluid, and bronchoalveolar lavage fluid. Blood samples were collected through the anterior vena cava and allowed to separate at room temperature. For nasal swabs, a long cotton swab was used to collect nasal mucosa samples gently. Oral fluids were collected from ropes soaked in the pigs’ saliva, and bronchoalveolar lavage fluid was obtained post euthanasia via sterile saline. Testicular fluid was expressed manually or with a tool. For PRRSV antigen detection, each sample comprises a mixture of samples from 5 to 10 pigs. For farms 1–12, 61 monthly samples were collected for PRRSV antigen testing, and 40 serum samples were collected for antibody testing (Table 1). Farms 13–23 collected samples on the basis of 3% of their sow inventory, with all farms having more than 1,000 sows. Owing to differences in the establishment and operation times of the breeding farms, the monitoring periods for PRRSV varied among farms, with the overall monitoring timeframe ranging from January 2021 to December 2023. All collected samples were adequately labeled, stored, transported at 4 °C on the same day and transported to the company laboratory for testing by the farm driver.

PRRSV antibody detection

PRRSV antibodies were detected via the PRRS X3 Antibody Test Kit (IDEXX, Switzerland) following the manufacturer's instructions, with a sensitivity of 99.8% and a specificity of 86.4% (Biernacka et al. 2018). Each sample was diluted in duplicate at 1:40, with one PRRS well and one normal host cell (NHC) well. The negative and positive controls were added undiluted, with 100 μL each. One hundred microlitres of controls or diluted samples were transferred to the reaction plate (PRRS or NHC wells) and incubated at 25°C for 30 min. Each well was washed three times with 300 μL of wash solution. Then, 100 μL of enzyme-conjugated antibody was added to each well, and the mixture was incubated at 25°C for 30 min. The washing process was repeated as described above. Then, 100 μL of 3,3’,5,5’-tetramethylbenzidine (TMB) substrate was added to each well, and the mixture was incubated at 25 °C for 15 min. Then, 100 μL of stop solution was added to each well. The optical density (OD) values of the samples and controls were measured at 650 nm via a microplate reader. The sample-to-positive (S/P) ratio was calculated as follows: (Sample PRRS Well OD value-Sample NHC Well OD value)/(Positive Control PRRS Well mean OD value-Positive Control NHC Well mean OD value). An S/P value < 0.40 is considered negative, and an S/P value ≥ 0.40 is considered positive.

PRRSV antigen detection

DNA and RNA were extracted from samples via a commercial nucleic acid extraction kit (HaiTai Bio, Shenzhen) and a KingFisher Flex automated nucleic acid extractor (Thermo Fisher Scientific, USA) based on magnetic bead technology. Under the influence of the lysis buffer, nucleic acids are liberated from the samples and specifically bind to the hydroxyl groups on the surface of the magnetic beads. Magnetic rods facilitate the adsorption, transfer, and release of these beads, allowing for the elution of nucleic acids via elution buffer (Carvalho et al. 2015; Huang and Ketting 2014). Two hundred microlitres of sample containing lysis buffer was added to each well. The deep-well plate and magnetic rod sleeve were placed into the designated positions in the automated extraction instrument, and the extraction program was initiated. After the automated program was completed, the elution buffer containing the nucleic acid was transferred to a clean centrifuge tube for storage. PRRSV pathogens (North American and European strains) were detected via the PRRSV Real-Time Fluorescent RT‒PCR Detection Kit (Guanmu Bio, Hunan), which has a sensitivity of 95% and a specificity of 99% (data provided by the supplier). The PCR mixture was prepared by combining 19 μL of reaction mixture, 1 μL of enzyme mixture, and 0.5 μL of internal control mixture per reaction. Mix well and centrifuge briefly. A total of 20 μL of the PCR mixture was added to each reaction tube and centrifuged briefly. Five microlitres of extracted sample RNA, negative, and positive controls were added to the tubes. The reactions were performed via an Applied Biosystems 7500 Real-Time PCR System (Thermo Fisher Scientific, USA) with a 25 μL reaction volume. The 6-carboxyfluorescein (FAM) channel (reporter: FAM, quencher: none) is designed for detecting the PRRSV North American strain. The hexachloro-fluorescein (HEX) channel (reporter: HEX, quencher: none) was used for internal control detection. The carboxy-x-rhodamine (ROX) channel (reporter: ROX, quencher: none) detects the PRRSV European strain. The cycling conditions were as follows: reverse transcription at 50°C for 15 min; Taq enzyme activation at 95°C for 2 min; 40 cycles of 95°C for 15 s and 60°C for 30 s; and a final cooling step at 25°C for 10 s. If the cycle threshold (Ct) values for both the FAM and HEX channels are ≤ 35 and the ROX channel has no Ct value, the sample is classified as positive for the North American PRRSV strain. If the FAM channel has no Ct value but the Ct values for both the ROX and HEX channels are ≤ 35, the sample is deemed positive for the European strain of PRRSV. If the Ct values for the FAM, ROX, and HEX channels were all ≤ 35, the sample was considered positive for both the North American and European strains of PRRSV. If the Ct value for the HEX channel is ≤ 35, whereas the Ct values for the FAM and ROX channels fall within 35 < Ct ≤ 40, the result is classified as inconclusive. In such cases, resampling and retesting are recommended. The PRRSV sample was considered positive if the retest yielded a Ct value ≤ 35 or if it remained inconclusive. If the HEX channel shows a Ct value ≤ 35 and no Ct values are detected for the FAM and ROX channels, the sample is considered negative for PRRSV.

Classification of PRRSV infection status at pig farms

The AASV has developed a classification system for PRRSV infection status on pig farms on the basis of viral shedding and exposure. This system categorizes breeding pig farms into four types: PRRSV-positive unstable, PRRSV-positive stable, PRRSV provisional negative, and PRRSV negative (Holtkamp et al. 2011). On the basis of the AASV classification method for different PRRSV infection statuses in pig farms and considering the specifics of our study, we adopted a more stringent classification scheme to redefine the PRRSV infection status of the farms involved in this research (shown in Table 8).

Table 8 The modified classification system of different PRRSV infection status in pig farms

Production data collection and processing

Monthly sampling was conducted to monitor PRRSV infection status across the 23 breeding farms. Concurrently, production data and weaning cost estimates calculated by the company for each corresponding month were also collected. The data included the full production rate (%) (the percentage of sows actively producing at the pig farm to the total designed production capacity), the sow mortality rate (%), the sow repeat breeding rate (%) (the percentage of sows subjected to multiple matings within the same estrus cycle), the average number of healthy piglets per litter, the average number of stillborn piglets per litter, the stillbirth rate (%), the average number of mummified fetuses per litter, the mummification rate (%), the average weight of healthy piglets (kg), the average number of litters per sow per year, the average number of healthy piglets per sow per year, the nursery pig mortality rate (%), the average number of weaned piglets per litter, the batch weaning piglet mortality rate (%), the average weaning weight (kg), the annual number of weaned piglets per sow, and the cost per weaned piglet (¥/piglet). The financial departments of each farm provided the cost per weaned piglet, covering expenses such as labor, feed, equipment depreciation, veterinary care, vaccines, transportation, and disinfection. Since the outbreak of African swine fever (ASFV) in China in 2018 (Wang et al. 2018), some farms have experienced reduced production rates due to the epidemic during the study period. To minimize the impact of ASFV infection on the economic loss assessment, we excluded data from months with a full production rate below 50%, which resulted in the removal of 44 months of data, leaving 710 months for analysis. In discussions with farm veterinarians, we learned that biosecurity measures on pig farms have been significantly enhanced since the introduction of ASFV in China. As a result, large-scale outbreaks of diseases other than ASF have become quite rare.

Data analysis

The collected data on the production efficiency, weaning costs, and monthly PRRSV infection status of the breeding pig farms were entered into Excel 2019 (Microsoft, USA)(Winston 2019). The Shapiro–Wilk normality test revealed that the collected data on pig production efficiency and weaning costs were not normally distributed and constituted repeated measures (Hanusz, Tarasinska, and Zielinski 2016, Omar et al. 1999). Therefore, we used the Kruskal‒Wallis nonparametric test to determine whether there were significant differences in production efficiency and weaning costs under different PRRSV infection statuses (McKight and Najab 2010). If significant differences were found, Dunn's test was used for multiple comparisons between groups (Dunn and Clark 2009). We downloaded the national average piglet price data from January 2021 to December 2023 from the Ministry of Agriculture and Rural Affairs of China's website.

Additionally, we selected data on the weaning piglet costs (¥/piglet), average weaning weight (kg), and annual number of weaned piglets per sow from monthly efficiency data (consistent with the indicators in Table 3) under different PRRSV infection statuses. We then used @RISK (V. 8.5.2) software for distribution fitting of the data via the parameter estimation method (with unknown upper and lower bounds), selecting the distribution with the minor Akaike information criterion value as the parameter distribution for subsequent PRRSV economic impact simulations (Akaike 1987, Raol, Girija, and Singh 2004). Additionally, given that temporarily provisional PRRSV-negative farms can produce PRRSV-negative weaned piglets, we conducted telephone interviews with experts and farm veterinarians to gather information on the price differential between PRRSV-negative and PRRSV-positive weaned piglets. The collected data were then used to fit the PERT distribution of the price advantage of each PRRSV-negative piglet. We subsequently constructed an annual revenue model for each sow under different PRRSV infection statuses (PRRSV-positive stable, PRRSV-positive unstable, and PRRSV provisional negative) via the following formula. We then compared the average annual revenue differences per sow to evaluate the economic impact of PRRSV on breeding pig farms.

Stable PRRSV-positive farms and unstable PRRSV-positive farms:

$$\begin{aligned}Profit/\;(mated&\ female)\;/year(\yen)\\ &=\left(Price\ of\ weaned\ piglet\left(\frac{\yen}{kg}\right)\times Average\ weaned\ weight\left(kg\right)\right.\\ &\left.-Full\ cost\ of\ wean\ piglet\right)\\ &\times(Weaned\ piglets)/(mated\ female)/year\end{aligned}$$

PRRSV provisional negative farm:

$$\begin{aligned} Profit/(mated&\ female)/year(\yen)\\ &=(Price\ of\ weaned\ piglet\left(\frac {\yen}{kg}\right)\times Average\ weaned\ weight\left(kg\right)\\ &-Full\ cost\ of\ weaned\ piglet + Higher\ price\left(\frac{\yen}{head}\right))\\ &\times(Weaned\ piglets)/(mated\ female)/year\end{aligned}$$

In this context, Profit/(mated female)/year (¥) represents the total annual profit per sow (¥). The price of weaned piglets (¥/kg) is the average price per kilogram of a weaned piglet. The average weaned weight (kg) is the average weight of a weaned piglet. The full cost of the weaned piglet is the total cost per weaned piglet (¥/piglet). (Weaned piglets)/(mated female)/year indicates the annual number of weaned piglets each sow provides. After modeling the average annual profit per sow under different PRRSV infection statuses, we further simulated the economic losses for a breeding pig farm with 2,400 sows following a PRRSV outbreak. We developed the following two models.

Economic losses from a PRRSV outbreak at a PRRSV provisional negative breeding pig farm:

$$\begin{aligned}Loss\ of\ a&\ PRRSV\ infection \\ &=(Economic\ loss\ of\ \frac{PNP-PUP}{52}\times TTBP\\ &+Economic\ loss\ of\ \frac{PNP-PSP}{52}\times TTS)\times 2400\end{aligned}$$

Economic losses from a PRRSV outbreak in a PRRSV-positive stable breeding pig farm:

$$\begin{array}{c}Loss\;of\;a\;PRRSV\;infection \\ =Economic\;loss\;of\frac{PSP-PUP}{52}\times TTBP\times 2400\end{array}$$

Here, PNP represents the annual total profit per sow on a PRRSV provisional negative farm (¥), PSP represents the annual total profit per sow on a PRRSV-positive stable farm (¥), and PUP represents the annual total profit per sow on a PRRSV-positive unstable farm (¥). TTBP refers to the number of weeks required for a farm's production efficiency to return to preoutbreak levels. TTS indicates the number of weeks needed for the farm to resume the production of PRRSV provisional negative weaned piglets after an outbreak. After a PRRSV outbreak, a provisional PRRSV-negative farm will progress through four stages: PRRSV provisional-negative, PRRSV-positive unstable, PRRSV-positive stable, and PRRSV provisional-negative. A stable PRRSV-positive farm will go through three stages: PRRSV-positive stable, PRRSV-positive unstable, and PRRSV-positive stable. The economic impact models were subjected to Monte Carlo simulation via @RISK (V. 8.5.2). Each simulation employed Latin hypercube sampling with 50,000 iterations (Mun 2006; Stein 1987; Zhao et al. 2023). Data analysis for this study was conducted via R V. 4.3.3 (R Core Team 2013) and XLSTAT 2022 software. Graphs were created via ggplot2 V. 3.5.0 and ArcGIS 10.7 (ESRI, USA) (Fesseha and Asefa 2022; Villanueva and Chen 2019).