Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 https://doi.org/10.1186/s13620-020-00176-w RESEARCH Open Access A cross-sectional survey on respiratory disease in a cohort of Irish pig farms Maria Rodrigues da Costa1,2,3,4*, Rose Mary Fitzgerald5, Edgar Garcia Manzanilla1,3, Helen O’Shea5, John Moriarty6, Máire C. McElroy6 and Finola Catherine Leonard3 Abstract Background: Respiratory disease is one of the most important factors impacting pig production worldwide. There is no available information on the prevalence of key pathogens implicated in Irish pig production. The objective of this study was to describe the prevalence of pleurisy, pneumonia, lung abscesses, pericarditis and liver milk spots in finisher pigs of a cohort of Irish pig farms, and to describe the seroprevalence of: influenza A virus (IAV), porcine reproductive and respiratory syndrome virus (PRRSv), Mycoplasma hyopneumoniae (Mhyo) and Actinobacillus pleuropneumoniae (APP). Results: In brief, 56 farrow-to-finish farms (29% of the Irish breeding herd) were enrolled in the study in 2017. Data on lungs, heart, and liver lesions were assessed for each farm at slaughter. An average of 417 (range 129–1154) plucks per farm were assessed for pleurisy, pneumonia, lung abscesses, pericarditis, and liver milk spots. Blood samples from 32 finisher pigs were collected at slaughter for each farm. The observed prevalence of pleurisy and pneumonia was one of the lowest reported in similar studies in Europe (13 and 11% estimated average within farm, respectively). Pleurisy lesions were mostly moderate and severe. Pneumonia lesions affected a low level of lung surface (5.8%). Prevalence of pericarditis was mid-high (8%) and the prevalence of liver milk spots was high, with an average of 29% of the livers affected. For serology, 78.6% of the farms were positive for IAV, 50% were positive for PRRSv, 71.4% were positive for Mhyo, and 98.2% were positive for APP. Influenza virus was the main pathogen associated with pleurisy (P < 0.001) and Mhyo was the main pathogen associated with pneumonia (P < 0.001) and pericarditis (P = 0.024). Conclusions: Farms affected with pleurisy had moderate to severe lesions. Farms affected with pneumonia had mild lesions, which could be the effect of the generalised use of Mhyo vaccination in piglets. The seroprevalence of IAV, PRRSv, Mhyo and APP in the present study sample is similar to or lower than in other European countries. Further research on the PRRSv and APP strains circulating in Ireland is necessary to support the design of national or regional control plans. Keywords: Actinobacillus pleuropneumoniae, Influenza A virus, Lung scoring, Mycoplasma hyopneumoniae, Pluck lesions, Porcine reproductive and respiratory syndrome virus, Porcine respiratory disease complex, Seroprevalence * Correspondence: costa.mariarodrigues@gmail.com; maria.costa@sruc.ac.uk 1 Pig Development Department, Teagasc - Animal & Grassland Research and Innovation Centre, Moorepark, Fermoy, P61 C996 Co. Cork, Ireland 2 Departament de Ciencia Animal i dels Aliments, Facultat de Veterinaria, Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 2 of 10 Background Republic of Ireland. In 2017, it included 107 pig herds, Respiratory disease is one of the most important factors representing over 77,000 sows or 52% of the national impacting pig production worldwide. Agents contributing commercial sow herd [7]. Participation in the cross- to the porcine respiratory disease complex include viruses sectional study was offered to all the farrow-to-finish pig and bacteria such as Influenza A virus (IAV), Porcine re- farmers providing data to the ePM, and 56 farms partici- productive and respiratory syndrome virus (PRRSv), pated voluntarily (cohort in study). Farms were recruited Mycoplasma hyopneumoniae (Mhyo) and Actinobacillus through the Teagasc advisory service and represented pleuropneumoniae (APP) [1]. The relative importance of 29.2% of the national commercial sow herd. each one of these pathogens varies between countries and At least two batches per farm were assessed with regions due to factors such as structure of farms, hus- blood samples being harvested from the first batch. A bandry practices or climate. In Ireland, there is no baseline batch was defined as all the finisher pigs from a given information available on the prevalence of respiratory farm killed in a slaughterhouse on the same day. Vaccin- pathogens and disease in pig farms. However, the future ation data were obtained via phone calls to farmers and implementation of control and eradication programmes corresponding private veterinary practitioners during the requires the characterisation of the national herd health same period. Additionally, farmers and veterinarians were status [2]. This national characterisation is also important asked if there were any changes in the vaccination scheme for individual farms, given their susceptibility to new out- in the previous year. Farm characteristics for the partici- breaks when the regional disease prevalence is high. pating farms were retrieved from the Teagasc ePM. Veterinary practitioners carry out regular diagnostics All the farmers participating in this study provided in- to monitor the health status of pig farms and the efficacy dividual signed consent to the use of the farm data col- of disease control measures e.g. vaccination [3]. Slaugh- lected, and to the retrieval of their production data from terhouse checks, including lung scoring and the record- the Teagasc ePM, according to Teagasc´s internal data ing of other lesions e.g. pericarditis and liver milk spots protection regulation. (caused by Ascaris suum) are inexpensive monitoring tools, allowing the collection of data from several farms Blood sampling and pluck examinations at slaughter at one time point [4]. Serology in finisher pigs at slaughter In the slaughterhouse, blood was collected from a total also allows estimation of the prevalence of exposure to of 32 randomly selected pigs per farm at sticking (exsan- pathogens or the efficacy of vaccination on farm [5, 6]. guination). The number of pigs to be sampled was Combining slaughterhouse checks and serology with in- chosen to detect viral or bacterial infections with a mini- formation on vaccination protocols is a useful approach to mum within-herd prevalence of 10% (α = 0.05). Samples study the health status of farms in terms of respiratory were transported for analysis to the Blood Testing La- disease. boratory of the Department of Agriculture, Food and the Thus, the aims of this study were (1) to describe the Marine (Cork, Ireland). Blood was allowed to clot at prevalence of pleurisy, pneumonia, lung abscesses, peri- room temperature, serum was separated, aliquoted and carditis and liver milk spots in finisher pigs of a cohort frozen at -80ºC until required for testing. For analysis, of Irish farrow-to-finish pig farms, (2) to describe the 16 randomly selected samples per farm for PRRSv and seroprevalence of four main pathogens related to re- Mhyo, and all 32 samples per farm for IAV and APP spiratory disease: IAV, PRRSv, Mhyo and APP in those were tested, based on power calculation for detection of farms, and (3) to analyse the associations between the viral and bacterial infections. The number of pig samples average within-farm prevalence of pluck lesions and processed for the detection of IAV and APP (n = 32) farm health status for the pathogens described by allowed a minimum within-herd prevalence of 10% (α = serology. 0.05), while the number of samples processed for the de- tection of PRRSv and Mhyo (n = 16) allowed a minimum Methods within-herd prevalence of 18% (α = 0.05). The processing Data on lung lesions, the presence of pericarditis and of half of the samples for the former two pathogens was liver milk spots, and also blood samples were obtained based on its seroconversion dynamics. Previous studies during visits to eight slaughterhouses (seven in the Re- suggest that, once a farm is infected, the disease preva- public of Ireland and one in Northern Ireland, UK) from lence in finisher pigs tends to 100%, particularly in November 2017 to April 2018, targeting 56 Irish farrow- farrow-to-finish farms [8, 9]. to-finish pig farms. This cohort of farms was part of a Pluck (lungs, heart, and liver) examinations were all larger study selected from the Teagasc e-Profit Monitor carried out by the same trained veterinarian. For each (ePM) clients. The Teagasc ePM is a herd monitoring pig, lung lobes were scored for pneumonia lesions accord- system (production performance and economic data) ing to the method described by Madec and Derrien [10], available on a voluntary basis to all the farmers in the with the overall surface affected averaged accounting for Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 3 of 10 lobe weights [11]. The variables prevalence of pneumonia infectious pathogen: farm status (farms were considered (%) and average surface of pneumonic lungs (%), herein- positive if at least one animal tested positive by ELISA after called (lung) surface with pneumonia (%), were used test) and within farm prevalence (number of pigs posi- for statistical analysis. Pleurisy was scored in the dorsocau- tive divided by the total number of pigs tested per farm). dal lobes using a modified version of the Slaughterhouse Pleurisy Evaluation System (SPES), which was developed Vaccination by Dottori et al., [12] and described by Merialdi et al., [13]. The main vaccination protocols on farm were recorded, The scores were 0 (no pleurisy), 2 (focal lesions in one with special focus on vaccination for IAV, PRRSv, Mhyo lobe), 3 (bilateral adhesions or unilateral lesions affecting and APP in sows and in piglets, as present or absent. more than 1/3 of the diaphragmatic lobe), and 4 (extensive lesions affecting more than 1/3 of both diaphragmatic Data input, management and analysis lobes). The prevalence of pleurisy (lesions with SPES ≥ 2) All data were entered and collated into a Microsoft® and the prevalence of scores 3 and 4 (prevalence of mod- Excel 365 spreadsheet. Descriptive statistical analysis erate or severe dorsocaudal pleurisy) were used for statis- and data visualisation were completed using R version tical analysis. Cranial pleurisy (adhesions between lobes, 3.4.4 [16] and R package ggplot2 version 3.3.0 [17]. on the surface of the apical and cardiac lobe, and/or adhe- Pluck lesions, vaccination, and serology (farm status, sions between the lung and the heart), which corre- within-farm prevalence) were characterised and de- sponded to score 1 of the original SPES, and scars (healing scribed. Herd-level prevalence was calculated as the indicative of pneumonic lesions which developed earlier number of positive herds (farm status positive) divided in the pig’s life) were recorded as absent or present and by the total number of herds (n = 56). Herd-level true used in the analysis. In summary, all pleurisy-related vari- prevalence was estimated from apparent prevalence as ables included pleurisy, moderate and severe pleurisy and described by Rogan & Gladen (1978) [18] and reported cranial pleurisy, while pneumonia-related variables were in Thrusfield (2007) [19]. The results for pluck lesions included pneumonia, lung surface with pneumonia, and are presented as average within-farm prevalence. scars. Additionally, lung abscesses (presence of one or Variables were checked for normality using graphic more abscesses in the lung), pericarditis (defined as ex- examination and Kolmogorov-Smirnov test. Productive pansion of the pericardial cavity with inflammatory exud- performance for the cohort of farm was compared to the ate [14]), and liver milk spots (presence of white spots in general population using ANOVA with an alpha level for the liver indicative of transhepatic migration of the larvae determination of significance of 0.05. The associations be- of Ascaris suum [15]) were also recorded as absent or tween average within-farm prevalence for pluck lesions present. In slower speed lines, every pig in the batch was and farm status was explored using SAS 9.4 (SAS Insti- scored while in the fastest speed line (max. 600 per hour), tute, Carey, US). Univariate analysis of the associations of every other pluck was assessed. The pluck examinations pluck lesions and serology was carried out using Mann- here described were recorded using the Ceva Lung Pro- Whitney U test. Multivariable analysis was carried out gram app (CEVA Santé Animale, Libourne, France). using generalized linear models with manual stepwise se- lection of variables with P = 0.10 and P = 0.05 as inclusion Serology and retention criteria. Seroprevalence of antibodies against IAV, PRRSv, Mhyo and APP were determined using the following IDEXX Results ELISA kits (Hoofddorp, The Netherlands), respectively: Farm performance and herd characteristics Influenza A Ab Test (95.3% sensitivity, 99.6% specificity A total of 56 farrow-to-finish farms participated in this for swine sera), PRRS X3 Ab Test (for the detection of study. A summary of the farm characteristics and their both the European and North American genotypes with performance in comparison to the Teagasc ePM popula- 98.8% sensitivity, and 99.9% specificity), HerdChek tion for the year 2017 is shown in Table 1. No statistical Mycoplasma hyopneumoniae Antibody Test (89.4% sen- differences were found for any parameter between the sitivity, 99.67% specificity), APP-ApxIV Ab Test (97.8% two groups of farms (P > 0.05). The average live weight sensitivity, 100% specificity). Following the manufac- at which pigs were sent to slaughter (111 ± 4.9 kg) turers’ recommendations, each pig was considered posi- depended on the sale target defined by each farmer tive to: IAV if their S/N value (sample to negative ratio which also considered slaughterhouse preferences. value) for IAV was less than 0.6, PRRSv if their S/P value (sample to positive ratio value) was greater or equal to 0.4, Mhyo if their S/P values were greater than 0.4, and Pluck lesions to APP if their S/P values were greater or equal to 0.5. The prevalence of lung lesions, pericarditis and liver milk ELISA results were transcribed into two variables per spots per farm recorded at slaughter is presented in Fig. 1. Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 4 of 10 Table 1 Description of the farm characteristics and production performance of a cohort of 56 Irish farrow-to-finish pig farms (study farms) and 2017 data from all herds in the Teagasc e-Profit Monitor system (population; n = 107) Farm characteristics and Teagasc e-Profit Monitora Study farms performance mean ± SD mean ± SD Median (range) Average herd size (number of sows) 728 ± 487.2 789 ± 564.1 659 (109-2498) No. pigs produced per sow per year 26.4 ± 2.31 26.7 ± 2.23 26.5 (21.8-32.0) Weaner mortality, % 2.8 ± 1.63 2.8 ± 1.61 2.7 (0.5-8.9) Finisher mortality, % 2.2 ± 1.19 2.0 ± 0.76 1.8 (0.9-4.1) Average daily gain, g/day 711 ± 62.8 726 ± 62.6 725 (538-903) Feed conversion ratio 2.37 ± 0.335 2.38 ± 0.105 2.38 (2.21-2.68) Age at sale, day 175 ± 12.9 174 ± 11.8 172 (148-208) a National herd monitoring system for production performance and economic data which is available on a voluntary basis A total of 23,372 plucks were assessed at slaughter. Data is affected of around 5.8%. Each farm had an average of presented as mean ± SD across all farms. On average, each 13 ± 9.4% of scarred lungs. The average within-farm batch had 163 ± 55.5 plucks assessed and 2.6 batches were prevalence of lung abscesses, pericarditis, and liver milk assessed per farm, with a minimum of two batches spots was 1.2 ± 3.38%; 8.1 ± 4.39% and 29.2 ± 28.04%, assessed and a maximum of five batches assessed. An respectively. average of 417 ± 204.1 plucks were assessed per farm (range 129–1154). Vaccination and farm serology results The prevalence of pleurisy was 13 ± 14.7%. Out of A total of 39.3 and 42.9% of the farms were vaccinating these lesions, 73% of these were moderate and severe le- sows for IAV and PRRSv, respectively. Additionally, one sions (SPES scores 3 and 4). The prevalence of pneumo- farm reported also vaccinating piglets for IAV, and five nia on farm was (11 ± 11.2%), with an average surface farms were also vaccinating piglets for PRRSv. A total of Fig. 1 Prevalence (%) of lung lesions, pericarditis and liver milk spots in finisher pigs of a cohort of 56 Irish farrow-to-finish farms from November 2017 to April 2018 (mean ± SE in yellow). A total of 23,372 plucks were assessed, with an average of 417 ± 204.1 plucks assessed per farm (range 129 - 1154). Legend: PL – dorsocaudal pleurisy; ModSev PL – Moderate and severe dorsocaudal pleurisy; CP – Cranial Pleurisy; PN – Pneumonia; Avg area PN – average lung surface affected with pneumonia; ABS – lung abscesses; PC – pericarditis; MS – Liver milk spots. Scars correspond to the healing indicative of pneumonic lesions Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 5 of 10 73.2% of the farms were vaccinating piglets for Mhyo. Of PRRSv, Mhyo; APP could not be included in the analysis the farms vaccinating piglets, 39% administered a double because almost all farms were positive. All variables re- shot. APP vaccination was only used in five farms lated to pleurisy and pneumonia were associated with (8.9%), all of which vaccinated weaner pigs with one the three studied pathogens in the univariate analysis. In farm also vaccinating sows. the multivariable analysis, higher level of dorsocaudal Approximately 94.6% of the farms vaccinated piglets pleurisy, moderate and severe pleurisy and cranial pleur- for PCV2 (Porcine circovirus type 2), 80.4% vaccinated isy were associated with positive status for IAV (P < sows and gilts for Escherichia coli, 17.9% for Clostridium 0.001 in all cases). Pneumonia, surface affected by pneu- spp., and 7.1% reported vaccinating piglets for atrophic monia and scars were higher for farms positive for Mhyo rhinitis. All farms vaccinated their sows for porcine (P ≤ 0.001 in all cases). IAV was also associated with parvovirus and Erysipelothrix rhusiopathiae, and none higher levels of pneumonia (P = 0.023) and scars (P = vaccinated for Glaesserella parasuis. 0.008). Abscesses tended to be associated with IAV (P = The results of the serological survey showed that the ap- 0.061) and pericarditis was associated with Mhyo (P = parent herd-level prevalence in the study sample was 0.024). Liver milk spots were not associated with any of 78.6% for IAV, 50.0% for PRRSv, 71.4% for Mhyo, and the pathogens. 98.2% for APP. True herd-level prevalence was estimated to be 82% [95% CI 71.0–93.7%], 51% [95% CI 37.3– Most of the pathogens co-occurred with other patho- 63.8%], 80% [95% CI 66.6–93.1%] and 100% [95% CI gens as shown in Table 3. The main co-infections de- 96.9–100%] for IAV, PRRSv, Mhyo and APP, respectively. scribed were farms positive to IAV, PRRSv, Mhyo (42.9 In positive farms, the within-farm prevalence for each of farms) and farms positive to IAV and Mhyo (21.4%). pathogen was (mean ± SD): 50.3 ± 28.88% for IAV, 97.2 ± 5.44% for PRRSv, 93.0 ± 11.31% for Mhyo, and 76.0 ± 28.15% for APP. The distribution of within-farm preva- Discussion lence for the different pathogens is presented in Fig. 2. This study presents detailed data on lung, heart and liver lesions in finisher pigs of a cohort of Irish farrow-to- Associations between farm health status and the within finish farms and the first antibody prevalence report of herd average prevalence of pluck lesions IAV, PRRSv, Mhyo and APP across Irish farms (country Table 2 presents the univariate and multivariate analysis level). This study relied on the Teagasc advisory services for all the pluck lesions depending on serology for IAV, for farm selection (convenience sampling), thus, it Fig. 2 Distribution of within-farm prevalence (%) of influenza A virus (IAV), porcine reproductive and respiratory virus (PRRSv), Mycoplasma hyopneumoniae (Mhyo), and Actinobacillus pleuropneumoniae (APP) in finisher pigs of 56 Irish farrow-to-finish farms (mean ± SE in black). Farms were considered positive if one pig was positive Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 6 of 10 Table 2 Univariate and multivariable analysis of average within herd prevalence (%) of pluck lesions and lung surface affected with pneumonia depending on farm serology for influenza A virus (IAV), porcine respiratory and reproductive syndrome virus (PRRSv) and Mycoplasma hyopneumoniae (Mhyo)a,b IAV PRRSv Mhyo Dorsocaudal Pleurisy Pos: 9.8 (0.9, 51.8) Pos: 10.2 (2.8, 51.8) Pos: 8.2 (2.0, 51.8) Neg: 2.4 (0.4, 47.7) Neg: 4.0 (0.4, 49.5) Neg: 2.9 (0.4, 47.7) Univariate P < 0.001 P = 0.008 P = 0.009 Multivariable P < 0.001 - - Mod Sev dorsocaudal pleurisy Pos: 7.5 (0.7, 46.9) Pos: 8.7 (1.8, 46.9) Pos: 6.8 (0.5, 46.9) Neg: 1.7 (0.0, 42.6) Neg: 3.8 (0.0, 42.6) Neg: 2.6 (0.0, 42.6) Univariate P < 0.001 P = 0.006 P = 0.025 Multivariable P < 0.001 - - Cranial pleurisy Pos: 12.4 (1.9, 54.2) Pos: 12.4 (4.2, 54.2) Pos: 10.9 (2.5, 54.2) Neg: 4.8 (1.2, 35.1) Neg: 7.1 (1.2, 51.6) Neg: 5.8 (1.2, 35.1) Univariate P = 0.001 P = 0.007 P = 0.032 Multivariable P < 0.001 - - Pneumonia Pos: 9.5 (0.7, 50.0) Pos: 10.3 (1.3, 34.7) Pos: 11.0 (2.0, 50.0) Neg: 1.5 (0.0, 18.9) Neg: 2.6 (0.0, 50.0) Neg: 1.3 (0.0, 30.7) Univariate P = 0.003 P = 0.035 P < 0.001 Multivariable P = 0.023 - P < 0.001 Avg pneumonia surfacec Pos: 6.0 (1.0, 13.5) Pos: 6.4 (2.2, 13.5) Pos: 6.5 (2.0, 13.5) Neg: 2.7 (0.0, 9.5) Neg: 4.6 (0.0, 10.6) Neg: 2.3 (0.0, 6.6) Univariate P = 0.002 P = 0.014 P < 0.001 Multivariable - - P < 0.001 Scars Pos: 12.5 (1.9, 39.3) Pos: 17.5 (1.4, 39.3) Pos: 15.9 (3.1, 39.3) Neg: 2.3 (0.0, 23.1) Neg: 8.0 (0.0, 24.3) Neg: 2.5 (0.0, 13.2) Univariate P < 0.001 P < 0.001 P < 0.001 Multivariable P = 0.008 - P < 0.001 Abscesses Pos: 0.5 (0.0, 11.1) Pos: 0.3 (0.0, 4.3) Pos: 0.5 (0.0, 11.1) Neg: 0.1 (0.0, 21.5) Neg: 0.3 (0.0, 21.5) Neg: 0.2 (0.0, 21.5) Univariate P = 0.073 P = 0.842 P = 0.194 Multivariable P = 0.061 - - Pericarditis Pos: 8.0 (1.2, 19.1) Pos: 8.0 (2.3, 16.4) Pos.: 8.2 (1.5, 19.1) Neg: 6.1 (1.5, 14.8) Neg: 7.4 (1.2, 19.1) Neg.: 5.5 (1.2, 15.6) Univariate P = 0.251 P = 0.561 P = 0.018 Multivariable - - P = 0.024 Liver milk spots Pos: 27.1 (0.5, 97.3) Pos: 24.4 (0.5, 87.9) Pos.: 15.7 (0.4, 88.8) Neg: 12.4 (0.4, 88.8) Neg: 17.8 (0.4, 97.3) Neg.: 25.3 (0.4, 97.3) Univariate P = 0.374 P = 0.838 P = 0.899 Multivariable - - - a Univariate analysis was carried using Mann-Whitney test and data is presented as median (range) for positive (pos) and negative (neg) farms. Multivariable analysis was carried out using generalized linear models with forward selection with a P for inclusion of 0.10 and a P for retention of 0.05 b Results for APP are not presented as there was only one farm negative to it c Average lung surface affected with pneumonia (%) cannot be assumed to be representative of the whole of farms. The prevalence of pleurisy is difficult to compare Irish pig production. However, it represents approxi- between countries due to the characterisation of these mately 29% of the national herd and the results obtained lesions, which is poorly described in some studies [20]. may provide useful insights into the prevalence of In Spain, Fraile et al. [21] presented an overall preva- respiratory disease in Irish pig farms. lence of 26.8% (cranial and dorsocaudal pleurisy), and The first objective of the study was to describe the 14.2% of dorsocaudal pleurisy, which is comparable to prevalence of pleurisy, pneumonia, lung abscesses, peri- the 12% reported in our study. In Belgium, Meyns et al. carditis and liver milk spots in finisher pigs of those [22] also used the SPES and reported an average pleurisy Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 7 of 10 Table 3 Percentage of farms (n = 56) depending on co-occurrence of pathogens influenza A virus (IAV), porcine respiratory and reproductive syndrome virus (PRRSv) and Mycoplasma hyopneumoniae (Mhyo)a IAv PRRSv Mhyo Number of pathogens Percentage (number) of farms - - - 0 12.5 (7) + - - 1 10.7 (6) - + - 1 1.8 (1) - - + 1 5.4 (3) + + - 2 3.6 (2) - + + 2 1.8 (1) + - + 2 21.4 (12) + + + 3 42.9 (24) a Farm positive (+) or negative (-) to the pathogen by serology of 20.8% for scores > 1, which is comparable to the presence of common respiratory pathogens over time. prevalence of dorsocaudal pleurisy of 13 ± 14.7% re- The prevalence of abscesses was similar to that reported ported in the present study. Additionally, the severity of in the UK [28]. A limitation of the scoring method is its the lesions described is seldom reported. In this study, focus on “enzootic-pneumonia-like” lesions, partly disre- when present, lesions of dorsocaudal pleurisy were usu- garding interstitial pneumonias which have a different ally moderate or severe (SPES scores 3 and 4). This le- presentation and are notoriously difficult to score using sion is commonly considered to be due to infection with the Madec system [10]. In Ireland, given the PRRSv and APP but further aetiological investigation is required to IAV prevalence nation-wide and the proportion of farms support the development and implementation of control vaccinating for these diseases (at least in the study sam- plans on farms. The questionnaire results showed that ple reported here), it would be worthwhile investigating few farmers in this study vaccinated against APP; the the prevalence of viral pneumonias at slaughter. data on prevalence and severity of pleurisy suggest that The prevalence of pericarditis is much higher than that this control measure could be of benefit on many farms. reported in Austria [31] and in Denmark by Nielsen Improving the husbandry, cleaning, and disinfection, and et al. [32]. However, these authors maintain that the applying strict all-in-all-out or all-forward policies for method of inspection, which avoids heart incisions, stock management are likely to prevent or attenuate the probably contributed to a lower rate of detection of this spread of APP throughout the farm [23, 24] and to lesion. Finally, the prevalence of liver milk spots was un- decrease the prevalence of pleurisy [25]. expectedly high, contrasting to the much lower preva- The prevalence of pneumonia was much lower than lence stated in other countries [33–35]. This suggests that reported by other countries [21, 22, 26–28] but that stricter control programmes should be implemented similar to the prevalence reported in Northern Ireland, on-farms. UK [28]. Although this study reports an average preva- The second objective of this study was to describe the lence of 13.4% of pneumonia on farms, the average sur- seroprevalence of four major pathogens: IAV, PRRSv, face affected of pneumonic lungs was low (6.2%). These Mhyo and APP in Irish farrow-to-finish pig farms. To results can be seen from two perspectives: (1) the high the authors’ knowledge, this is the first time this infor- number of farms vaccinating for Mhyo could explain the mation has been generated for Ireland. In our sample, low severity of the lesions at slaughter (only 4 out of 40 herd-level prevalence was 79% for IAV, 50% for PRRSv, farms positive were not vaccinating); and/or (2) the on- 71% for Mhyo, and 98% for APP. These results are com- set of pneumonia caused by Mhyo is typically in the parable to those of four cross-sectional studies on re- weaner stage, and most lesions heal by time of slaughter spiratory disease in Spain, Belgium and France [21, 22, without necessarily leaving scars [27, 29, 30]. Indeed, 26, 36]. The herd-level prevalence of IAV in the study considering that the prevalence of scars was approxi- farms is not high, considering that the ELISA kit used mately 14%, these results suggest that potentially up to does not distinguish between subtypes. Fraile et al. [21] almost 30% of the pigs either had pneumonia or had evi- and Meyns et al. [22], tested for antibodies against IAV dence of pneumonia (scars) over the course of their life- H1N1, H1N2, and H3N2 and concluded that over 90% time. Therefore, other methods that assess the impact of of the herds were positive to those subtypes in Spain respiratory disease throughout the lifetime of the pig and in Belgium. Fablet et al. [36] reported a prevalence may be necessary to complement slaughterhouse checks. of 60 and 57.6% for subtypes H1N1 and H1N2 in French Such methods may include monitoring clinical signs herds. Regarding PRRSv, the herd-level prevalence was (cough monitors, activity monitors) and monitoring the similar to that reported by the French study [36], while Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 8 of 10 studies in Spain (100% [26] and 89% [21]), and Belgium IAV in the pneumonia lesions. The importance of this (88% [22]) reported a higher prevalence. The herd-level co-infection in the development of pneumonia should be prevalence of Mhyo was similar to the prevalence re- further studied [41]. Pericarditis also showed an associ- ported by Fraile et al. [21], although lower when com- ation with positive status for Mhyo. This is an interest- pared to the studies from Belgium and France [36, 37]. ing result in light of a 1997 study which reported the The APP herd-level prevalence is similar to that de- microbiological and pathological findings of 46 cases of scribed in other studies for ApxIV detection by ELISA chronic pericarditis in Danish finisher pigs at slaughter [13, 21, 22], and by PCR in 50 herds from Ontario, [42]. In this study, Buttenschon et al. found that Mhyo Canada [38]. Although our results indicate that virtually was involved in 33 out the 46 cases reported. However, all farms contain pigs that are antibody positive to APP, the chronic character of the lesions assessed at slaughter the test does not differentiate antibodies against highly dictates uncertainty when attributing a cause-effect virulent serotypes from antibodies against mild sero- which links pathogens to lesions. Other pathogens like types. Indeed, Chiers et al. [39] stress that this sero- Glaesserella parasuis and Streptococcus suis have been logical assay cannot be used to detect subclinical associated with pericarditis and further studies should infections. Thus, the clinical presentation on-farm and investigate this association. its relationship with pleurisy lesions at slaughter are ne- cessary to recognise a problem [40]. As this study was Conclusions designed to detect disease at farm level, the results pre- Most of the farms affected with pleurisy had moderate sented on the within-farm prevalence for each disease to severe lesions. On the contrary, most of the farms af- are not discussed. Nevertheless, the authors believe that fected with pneumonia had mild lesions, which could be Fig. 2 offers an interesting perspective on the within- the effect of the generalised use of Mhyo vaccination in herd disease prevalence for the four pathogens studied. piglets. At the same time, the prevalence of liver milk Serological tests of herds have some limitations, espe- spots was unexpectedly high which denotes the need for cially in vaccinated herds. These herds will be positive stricter control programmes on-farm. The herd-level by serology whether the vaccine is effective, and whether prevalence of IAV, PRRSv, Mhyo and APP in the present the disease is under control or not. In this study (with study sample is similar to or lower than in other Euro- the exception of APP, whose particularities were dis- pean countries. Pleurisy levels were higher in those cussed before), most of the herds not vaccinating for a herds positive to IAV and pneumonia was associated pathogen were negative in the serology test. Likewise, with positive status for Mhyo and IAV. Further research the interpretation of serological results in herds in which on the PRRSv and APP strains circulating in Ireland are pigs are vaccinated needs to be done carefully; results of necessary to support the design of national or regional other diagnostic tests such as pathogen detection by control plans. PCR, histopathology or immunohistochemistry are re- Abbreviations quired to establish true infection and disease status. APP: Actinobacillus pleuropneumoniae; ePM: e-Profit Monitor; IAV: Influenza A Finally, a third objective was to analyse the associa- virus; Mhyo: Mycoplasma hyopneumoniae; PRRSv: Porcine reproductive and tions between pluck lesions and farm health status de- respiratory syndrome virus scribed by serology. In the univariate approach, most of Acknowledgements the pathogens showed associations with pleurisy and The authors would like to thank Oliver Clear, Jessica Gillespie and Lorna pneumonia lesions. This was probably a consequence of O’Brien for their help with data collection, and the Teagasc advisors for facilitating the contact with farmers. We would also like to thank all the the high level of co-infection in pig farms as shown in farmers and slaughterhouses enrolled in the study. The authors acknowledge Table 3. Multivariable analysis allowed removal of con- CEVA for facilitating the use of their lung scoring app. The authors declare founding effects and IAV was the main pathogen associ- no conflicts of interest. ated with pleurisy lesions. Although APP was probably Authors’ contributions the main etiologic factor for pleurisy [22], no farms were MRC: data collection, curation, statistical analysis and interpretation; negative to APP and its effect on pleurisy lesions could manuscript writing and reviewing. RMF: laboratory analysis, manuscript not be studied. Thus, whether influenza alone was asso- writing and reviewing. EGM: study design, funding acquisition, data collection, statistical analysis and interpretation, manuscript writing, ciated with pleurisy or it acted as a triggering or aggra- reviewing and editing. HOS, JM and MCM: study design, funding acquisition vating factor cannot be elucidated. However, it is known and manuscript reviewing. FCL: funding acquisition, manuscript writing and that viral infections can favour the effects of bacterial reviewing. All authors read and approved the final manuscript. pathogens like APP or Pasteurella multocida in pigs [1]. Funding As expected, Mhyo was the main pathogen associated This study was funded by the Irish Department of Agriculture, Food and the with pneumonia and scars. Mhyo is well known to be Marine under the Research Stimulus Fund (PathSurvPig 14/S/832). The funders had no role in study design, data collection and analysis, decision to the main etiologic agent in pneumonia [8]. However, the publish, or preparation of the manuscript. MRC was supported by the multivariable analysis also showed some association of Teagasc Walsh Fellowship Fund. Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 9 of 10 Availability of data and materials 12. Dottori M, Nigrelli AD, Merialdi G, Gozio S, Bonilauri P, Cominotti F. Proposta The datasets used and/or analysed during the current study are available di un nuovo sistema di punteggiatura delle pleuriti suine in sede di from the corresponding author on reasonable request. macellazione. La griglia S.P.E.S. (Slaughterhouse Pleuritis Evaluation System). Large Animal Review. 2007;13:161–5. Ethics approval and consent to participate 13. Merialdi G, Dottori M, Bonilauri P, Luppi A, Gozio S, Pozzi P, et al. Survey of All the farmers participating in this study gave individual signed consent to pleuritis and pulmonary lesions in pigs at abattoir with a focus on the the use of the data collected on farm, and to the retrieval of their extent of the condition and herd risk factors. Vet J. 2012;193:234–9. characteristics and production performance data from the Teagasc e-Profit 14. Robinson NA, Loynachan AT. Cardiovascular and Hematopoietic Systems. In: Monitor, according to Teagasc´s internal data protection regulation. Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, editors. Diseases of Swine. 11th ed. Hoboken: Wiley-Blackwell; 2019. pp. 223–33. 15. Thomson JR, Friendship RM. Digestive System. In: Zimmerman JJ, Karriker Consent for publication LA, Ramirez A, Schwartz KJ, Stevenson GW, editors. Diseases of Swine. 11th Not applicable. ed. Hoboken: Wiley-Blackwell; 2019. pp. 234–63. 16. R Core Team. R: A language and environment for statistical computing. 3.4. Competing interests 4. (2018-03-15). https://www.R-project.org/. Accessed Mar. 15, 2018. The authors declare that they have no competing interests. 17. Wickham H. ggplot2: Elegant Graphics for Data Analysis. 3.3.3. https:// ggplot2.tidyverse.org. Accessed Accessed May. 15, 2020. Author details 18. Rogan WJ, Gladen B. Estimating prevalence from the results of a screening 1 Pig Development Department, Teagasc - Animal & Grassland Research and test. Am J Epidemiol. 1978;107:71–6. Innovation Centre, Moorepark, Fermoy, P61 C996 Co. Cork, Ireland. 19. Thrusfield M Surveys. Veterinary Epidemiology. 3rd ed. Garsington Road, 2 Departament de Ciencia Animal i dels Aliments, Facultat de Veterinaria, Oxford OX4 2DQ, UK: Wiley-Blackwell; 2007. p. 244. Universitat Autònoma de Barcelona, Bellaterra, 08193 Barcelona, Spain. 20. Andreasen M, Mousing J, Krogsgaard Thomsen L. No simple association 3 School of Veterinary Medicine, University College Dublin, Dublin 4, D04 between time elapsed from seroconversion until slaughter and the extent V1W8 Belfield, Ireland. 4Present address: Epidemiology Research Unit, of lung lesions in Danish swine. Prev Vet Med. 2001;52:147–61. Department of Veterinary and Animal Science, Northern Faculty, Scotland’s 21. Fraile L, Alegre A, Lopez-Jimenez R, Nofrarias M, Segales J. Risk factors Rural College (SRUC), An Lòchran, 10 Inverness Campus, IV2 5NA Inverness, associated with pleuritis and cranio-ventral pulmonary consolidation in Scotland, UK. 5Bio-Explore, Department of Biological Sciences, Cork Institute slaughter-aged pigs. Vet J. 2010;184:326–33. of Technology, Rossa Avenue, Bishopstown, T12 P928 Cork, Ireland. 6Central 22. Meyns T, Van Steelant J, Rolly E, Dewulf J, Haesebrouck F, Maes D. A cross- Veterinary Research laboratory, Department of Agriculture, Food & Marine sectional study of risk factors associated with pulmonary lesions in pigs at Laboratories, Celbridge W23VW2C Co. Kildare, Ireland. slaughter. Vet J. 2011;187:388–92. 23. Gottschalk M, Broes A. Actinobacillosis. Actinobacillus pleuropneumoniae. In: Received: 20 August 2020 Accepted: 3 November 2020 Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, editors. Diseases of Swine. Hoboken: Wiley-Blackwell; 2019. pp. 749–63. 24. Sassu EL, Bossé JT, Tobias TJ, Gottschalk M, Langford PR, Hennig-Pauka I. References Update on Actinobacillus pleuropneumoniae—knowledge, gaps and 1. Brockmeier SL, Halbur PG, Thacker EL. Chapter 13: Porcine respiratory challenges. Transboundary Emerging Diseases. 2018;65:72–90. disease complex. In: Guthmiller KBJ, editor. Polymicrobial diseases. 25. Jäger HC, McKinley TJ, Wood JLN, Pearce GP, Williamson S, Strugnell B, et al. Washington (DC): ASM Press; 2002. Factors associated with pleurisy in pigs: a case-control analysis of slaughter 2. Greiser-Wilke I, Grummer B, Moennig V. Bovine viral diarrhoea eradication pig data for England and Wales. PloS one. 2012;7:e29655–5. and control programmes in Europe. Biologicals. 2003;31:113–8. 26. Martínez J, Peris B, Gómez EA, Corpa JM. The relationship between 3. Ramirez A, Karriker LA. Herd Evaluation. In: Zimmerman JJ, Karriker LA, infectious and non-infectious herd factors with pneumonia at slaughter and Ramirez A, Schwartz KJ, Stevenson GW, editors. Diseases of Swine. 10th ed. productive parameters in fattening pigs. Vet J. 2009;179:240–6. Ames: Wiley-Blackwell; 2012. pp. 5–17. 27. Pagot E, Pommier P, Keïta A. Relationship between growth during the 4. Correia-Gomes C, Smith RP, Eze JI, Henry MK, Gunn GJ, Williamson S, et al. fattening period and lung lesions at slaughter in swine. Rev Méd Vét. 2007; Pig Abattoir Inspection Data: Can It Be Used for Surveillance Purposes? PLos 158:253–9. . One. 2016;11:e0161990. . 28. Eze JI, Correia-Gomes C, Borobia-Belsue J, Tucker AW, Sparrow D, Strachan 5. Elbers ARW, Tielen MJM, Cromwijk WAJ, Hunneman WA. Sero- DW, et al. Comparison of Respiratory Disease Prevalence among Voluntary epidemiological screening of pig sera collected at the slaughterhouse to Monitoring Systems for Pig Health and Welfare in the UK. PLoS One. 2015; detect herds infected with Aujeszky’s disease virus, porcine influenza virus 10:e0128137. and Actinobacillus (Haemophilus) pleuropneumoniae in the framework of 29. VanAlstine WG. Respiratory System. In: Zimmerman JJ, Karriker LA, Ramirez an Integrated Quality Control (IQC) system. Vet Q. 1990;12:221–30. . A, Schwartz KJ, Stevenson GW, editors. Diseases of Swine. 10th ed. Ames: 6. Regula G, Lichtensteiger CA, Mateus-Pinilla NE, Scherba G, Miller GY, Weigel Wiley-Blackwell; 2012. pp. 348–63. RM. Comparison of serologic testing and slaughter evaluation for assessing 30. Straw BE, Shin SJ, Yeager AE. Effect of pneumonia on growth rate and feed the effects of subclinical infection on growth in pigs. J Am Vet Med Assoc. efficiency of minimal disease pigs exposed to Actinobacillus 2000;217:888–95. pleuropneumoniae and Mycoplasma hyopneumoniae. Prev Vet Med. 1990;9: 7. Department of Agriculture Food and the Marine. National Pig Census. 2017. 287–94. 2018. https://www.agriculture.gov.ie/animalhealthwelfare/ 31. Schleicher C, Scheriau S, Kopacka I, Wanda S, Hofrichter J, Kofer J. Analysis animalidentificationmovement/nationalpigcensus/. Accessed Sep. 18, 2020. of the variation in meat inspection of pigs using variance partitioning. Prev 8. Sibila M, Pieters M, Molitor T, Maes D, Haesebrouck F, Segales J. Current Vet Med. 2013;111:278–85. perspectives on the diagnosis and epidemiology of Mycoplasma 32. Nielsen SS, Nielsen GB, Denwood MJ, Haugegaard J, Houe H. Comparison of hyopneumoniae infection. Vet J. 2009;181:221–31. recording of pericarditis and lung disorders at routine meat inspection with 9. Maes D. Descriptive epidemiological aspects of the seroprevalence of five findings at systematic health monitoring in Danish finisher pigs. Acta Vet respiratory disease agents in slaughter pigs from fattening pig herds. Scand. 2015;57:18. Epidémiol Santé Anim. 1997;31–32. 33. Fausto MC, Oliveira IC, Fausto GC, Carvalho LM, Valente FL, Campos AK, 10. Madec F, Derrien H, editors. Fréquence, intensité et localisation des et al. Ascaris suum in pigs of the Zona da Mata, Minas Gerais State, Brazil. lésions pulmonaires chez le porc charcutier: Résultats d’une premiére Rev Brasileira de Parasitol Vet. 2015;24:375–8. . série d’observations en abattoir. Journées de la Recherche Porcine en 34. Ondrejková A, Černek Ľ, Prokeš M, Ondrejka R, Hurníková Z, Takáčová D. France; 1981. Monitoring of Ascaris suum in slaughter pigs during 2000–2009 in Slovakia. 11. Christensen G, Soarensen V, Mousing J. Diseases of the respiratory system. Helminthologia. 2012;49:221–4. In: Straw B, D’Allaire S, Taylor WM DJ, editors. Diseases of Swine. 8th ed. 35. Sanchez-Vazquez MJ, Smith RP, Gunn GJ, Lewis F, Strachan DW, Edwards SA. Ames: Iowa University Press; 1999. pp. 913–40. The identification of risk factors for the presence of enzootic pneumonia- Rodrigues da Costa et al. Irish Veterinary Journal (2020) 73:24 Page 10 of 10 like lesions and pleurisy in slaughtered finishing pigs utilizing existing British pig industry data. Pig J. 2010;63:25–33. . 36. Fablet C, Marois-Créhan C, Simon G, Grasland B, Jestin A, Kobisch M, et al. Infectious agents associated with respiratory diseases in 125 farrow-to-finish pig herds: A cross-sectional study. Vet Microbiol. 2012;157:152–63. 37. Meyns T, Maes D, Dewulf J, Vicca J, Haesebrouck F, Kruif Ad. Quantification of the spread of Mycoplasma hyopneumoniae in nursery pigs using transmission experiments. Prev Vet Med. 2004;66:265–75. 38. MacInnes JI, Gottschalk M, Lone AG, Metcalf DS, Ojha S, Rosendal T, et al. Prevalence of Actinobacillus pleuropneumoniae, Actinobacillus suis, Haemophilus parasuis, Pasteurella multocida, and Streptococcus suis in representative Ontario swine herds. Can J Vet Res. 2008;72:242–8. 39. Chiers K, Donné E, Van Overbeke I, Ducatelle R, Haesebrouck F. Actinobacillus pleuropneumoniae infections in closed swine herds: infection patterns and serological profiles. Vet Microbiol. 2002;85:343–52. 40. Marsteller TA, Fenwick B. Actinobacillus pleuropneumoniae disease and serology. J Swine Health Prod. 1999;7:161–5. 41. Thacker EL, Halbur PG, Ross RF, Thanawongnuwech R, Thacker BJ. Mycoplasma hyopneumoniae Potentiation of Porcine Reproductive and Respiratory Syndrome Virus-Induced Pneumonia. J Clin Microbiol. 1999;37: 620–7. 42. Buttenschon J, Friis NF, Aalbaek B, Jensen TK, Iburg T, Mousing J. Microbiology and pathology of fibrinous pericarditis in Danish slaughter pigs. Zentralbl Veterinarmed A. 1997;44:271–80. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.