Maes et al. Veterinary Research (2023) 54:8 Veterinary Research https://doi.org/10.1186/s13567-023-01136-2 REVIEW Open Access Review on the methodology to assess respiratory tract lesions in pigs and their production impact Dominiek Maes1* , Marina Sibila2,3,4, Maria Pieters5, Freddy Haesebrouck1, Joaquim Segalés2,4,6 and Luís Guilherme de Oliveira7 Abstract Porcine respiratory disease is one of the most important health problems in pig production worldwide. Cranioventral pulmonary consolidation (CVPC) and pleurisy are the two most common lesions in the respiratory tract of slaugh- tered pigs. The present review paper discusses pathogens involved in the lesions, lesion prevalence, scoring systems, advantages and disadvantages of slaughterhouse examination, and the impact of CVPC and pleurisy on performance, carcass, and meat quality. Cranioventral pulmonary consolidation and pleurisy in slaughter pigs are characteristic for infections with Mycoplasma hyopneumoniae and Actinobacillus pleuropneumoniae, respectively, although other pathogens may cause similar lesions and/or be involved in their development. The overall prevalence of CVPC and pleurisy in slaughter pigs are still high, being the prevalence of CVPC generally higher than that of chronic pleurisy. The advantages and disadvantages of slaughterhouse examination are discussed in relation to practical aspects, the assessment of lesions, the number and representativeness of the examined animals and the interpretation and value of the results for the stakeholders. The main scoring methods for CVPC and pleurisy are shortly reviewed. In gen- eral, scoring methods can be applied rapidly and easily, although significant variation due to abattoir and observer remains. Artificial intelligence-based technologies that automatically score lesions and facilitate processing of data may aid solving these problems. Cranioventral pulmonary consolidation and pleurisy have a major negative impact on pig performance, and the effects increase the extension of the lesions and/or presence of multiple lesions. The performance losses caused by these lesions, however, vary significantly between studies and farms, possibly due to differences in study population and used methodology. Both lesions also have a negative impact on different carcass and meat quality parameters, leading to increased risk for poor processing and storage of the carcasses. Monitoring lung lesions of slaughter pigs should be optimized and implemented routinely; however, it is recommended to com- plement this information with farm data and laboratory results for specific pathogens. Keywords Pigs, lung, lesion, slaughterhouse, cranioventral pulmonary consolidation, pleurisy, impact Table of Contents 1 Introduction Handling editor: Marcelo Gottschalk 2 Characterization of cranioventral pulmonary consoli- *Correspondence: dation and pleurisy Dominiek Maes 2.1 Cranioventral pulmonary consolidation Dominiek.Maes@UGent.be Full list of author information is available at the end of the article 2.2 Pleurisy © The Author(s) 2023. 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://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​ mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Maes et al. Veterinary Research (2023) 54:8 Page 2 of 17 3 Pathogens involved in CVPC and pleurisy Evaluation of the respiratory tract is particularly 4 Prevalence of CVPC and pleurisy lesions important, as the porcine respiratory disease com- 5 Slaughterhouse examination plex (PRDC) is considered the most important health problem in pig production worldwide. This is the case 5.1 Practical aspects in intensive production systems, where large groups 5.2 Assessment of lesions of pigs are housed in confinement [2]. The two most 5.3 Examined animals prevalent pulmonary conditions observed in pigs on 5.4 Interpretation of the results abattoir inspection are suppurative bronchopneumo- 6 Scoring systems for CVPC and pleurisy nia, characterized by cranioventral pulmonary con- solidation (CVPC), and pleuritis or pleurisy, which is 6.1 Scoring of CVPC most frequently seen over the caudal lobes [1, 3–5]. As 6.2 Scoring of pleurisy these lesions are rather easy to examine at the slaughter 6.2.1 System by Madec and Kobisch line, they are often assessed in epidemiological stud- 6.2.2 System by the centre technique de produc- ies and/or monitoring systems [1, 6]. The outcome of tions animales (CTPA) this assessment allows providing information about the 6.2.3 System by Pointon et al. [66] respiratory health status of fattening pigs, to bench- mark farms and to implement possible control meas- 6.2.4 Slaughterhouse pleurisy evaluation system ures against respiratory disease at the farm. The lesions (SPES) are also economically important, as they are associated 6.2.5 System by Christensen et al. [41] with increased time to market [7, 8]. In addition, they 6.2.6 System by Sibila et al. [27] might cause problems in abattoirs because carcasses 6.3 Artificial intelligence to score lesions need to be trimmed due to partial condemnations [9]. 7 Impact of CVPC and pleurisy on performance This requires extra labor and may slow down the speed of the slaughter line. Finally, respiratory disease has sig- 7.1 Cranioventral pulmonary consolidation nificant negative impacts on indicators of pig welfare, 7.1.1 Impact of presence of CVPC as pigs may suffer from coughing, dyspnea, fever, dis- 7.1.2 Impact of severity (extension) of CVPC comfort, and reduced feed intake [10, 11]. 7.2 Pleurisy The present review paper discusses CVPC and pleu- 8 Impact of CVPC and pleurisy on carcass and meat risy lesions in fattening pigs, their characteristics, the most important pathogens involved, their occurrence, quality lesion scoring systems, advantages and disadvantages of 9 Conclusions and areas for further research slaughterhouse examination, and the impact of CVPC References and pleurisy on performance, carcass, and meat quality. 1 Introduction 2 Characterization of cranioventral pulmonary In the slaughterhouse, pig carcasses are evaluated by consolidation and pleurisy means of different parameters to assess their quality 2.1 Cranioventral pulmonary consolidation and suitability for human consumption. In addition to In the present paper, the term cranioventral pulmonary the food safety aspects, the slaughterhouse also rep- consolidation (CVPC) will be used to describe Myco- resents a key check-point to capture more informa- plasma hyopneumoniae (M. hyopneumoniae)-like gross tion about the health status of pig farms. In this sense, lung lesions, which consist of purple to grey areas of slaughterhouse data may complement data collected pulmonary consolidation, mainly located bilaterally in at farm level (e.g. clinical signs observation, necropsy the apical intermediate and accessory lobes, including findings, laboratory results and performance data) and the cranial parts of the diaphragmatic lobes in the most be part of an integrated system for animal health moni- extensive cases [12, 13]. In the literature, also other terms toring. Lesions in many different organ systems such as have been used to describe these lesions such as catarrhal the respiratory, cardiovascular, intestinal and urogeni- pneumonia, bronchopneumonia, Mycoplasma-pneumo- tal tracts, integument and locomotion can be assessed. nia, Mycoplasma-like lesions or enzootic pneumonia-like Such slaughterhouse data may provide unique and val- lesions. uable feedback to the pig producers and their herd vet- Lesions caused by M. hyopneumoniae infections reach erinarians, as well as be an important source of data for the maximum extension at 3–4 weeks post-inoculation epidemiological and efficacy studies [1]. [14–16]. Uncomplicated lesions are characterized by the Maes et al. Veterinary Research (2023) 54:8 Page 3 of 17 presence of a catarrhal-purulent exudate in the airways, often result in tearing of the lungs during removal at nec- a uniform color of the parenchyma of the lung and a ropsy or at the slaughterhouse, leaving portions of the “meaty” consistency. Completely consolidated lung areas lung adhered to the thoracic wall. Necrotic areas tend sink in water, whereas normal aerated lung areas float to resolve by fibrosis and scarring; however, in a number [11]. In incipient cases in which the consolidation does of cases, necrotic foci remain surrounded by scar tissue, not completely affect the entire parenchyma, the lung and they are known as sequestra. Fibrous pleurisy affect- may still float in water due to the presence of air. It takes ing larger areas might be associated with similar lesions approximately 7 to 10 weeks for the lesions to be healed, in the pericardial sac, namely chronic pericarditis [10]. with no evidence of gross lesions anymore [12]. However, The evolution of fibrous pleural lesions is a long process in chronic stages (more frequently seen at the slaughter- with a duration of at least one, more often two to three house), consolidated areas may look purple to grey, and months [10]. usually evolve to scarring and tissue retraction. These interlobular scar retractions of connective tissue are also called fissures [12, 17]. These chronic lesions are, usually, 3 Pathogens involved in CVPC and pleurisy not as well coloured and demarcated as acute ones, and Cranioventral pulmonary consolidation and pleurisy their scoring could be more challenging. lesions in slaughter pigs are typical for infections with Under field conditions, M. hyopneumoniae infections M. hyopneumoniae and A. pleuropneumoniae, respec- are often complicated by other bacterial and/or viral tively. Enøe et al. [19] demonstrated that herds seroposi- pathogens [13]. In case of secondary bacterial pathogens, tive for M. hyopneumoniae or A. pleuropneumoniae had the lesions may occupy a larger surface of the lung and be CVPC and chronic pleurisy in 29% and 51% of the pigs characterized by the presence of mucopurulent exudate at slaughter, respectively. In slaughter-aged pigs, the per- in the airways, a firmer tissue consistency and an incon- centage of lungs with CVPC were significantly higher in sistent greyish color of the parenchyma. In this case, M. hyopneumoniae seropositive farms compared to the the histopathological lesion is diagnosed as suppurative seronegative ones [20]. Mycoplasma hyopneumoniae bronchopneumonia. is the primary etiological agent of enzootic pneumonia In the case of complicating viral infections (PRDC), (EP), a chronic respiratory disease in pigs, and it is one of affected pigs show interstitial pneumonia characterized the main pathogens involved in the PRDC [2, 21]. Actino- by tan-mottled, enlarged and non-collapsed lungs, rub- bacillus pleuropneumoniae is a Gram-negative bacterium bery in consistency, sometimes with interstitial edema. and the etiological agent of porcine pleuropneumonia Frequently, enlargement of tracheobronchial lymph [10]. Infections may lead to inflammation of the lung and nodes does occur as well [13]. In case of complicating the pleura, and may cause either acute or chronic clinical infections with other bacterial and/or viral pathogens, signs and lesions. the healing, repair, and restitution periods are longer Cranioventral pulmonary consolidation and pleu- than in uncomplicated infections, and the probability of risy lesions are however not pathognomonic for these complete resolution is lower. two pathogens, as other pathogens may cause similar lesions and/or also be involved in these lesions as part 2.2 Pleurisy of a polymicrobial disease complex [22]. Cranioventral The serosa of the thoracic cavity, cavum thoracicum, is pulmonary consolidation lesions can also be caused by called pleura. The pleura lining the thorax is called pari- infections with viruses, in particular swine influenza virus etal pleura and originates from the somatopleura. The (IAVs) [2] and other bacterial agents such as Pasteurella pleura covering the lungs is called visceral pleura and multocida (P. multocida) and Bordetella bronchiseptica originates from the splanchnopleura. Pleurisy, an inflam- (B. bronchiseptica). On the other hand, A. pleuropneu- mation of the pleura, is a common pathological condition moniae, M. hyorhinis, Glaesserella parasuis (G. parasuis), observed in slaughter pigs. In the present paper, the term Trueperella pyogenes, streptococci or staphylococci can be pleurisy will be used, although also other terms have detected in CVPC lesions, although these lesions are not been used in literature, such as chronic pleurisy, dorso- primarily caused by these pathogens [2, 23]. caudal pleurisy or pleuritis [10, 18]. Pleurisy has been reported in many different studies Infections with Actinobacillus pleuropneumoniae (A. [24–28] to be strongly associated with A. pleuropneu- pleuropneumoniae) are often involved in pleurisy in pigs. moniae. Mousing et al. [29] had calculated that 44% of In chronic cases, fibrin deposited on serosal surfaces all pleurisy lesions could be attributed to infection with gradually becomes organized, leading to the develop- A. pleuropneumoniae serotype 2. In the study of Jirawat- ment of chronic fibrous adhesions between the visceral tanapong et al. [30], however, such an association was and parietal pleura. These adhesions can be firm and only found in 4 out of 10 farms with pleurisy. The latter Maes et al. Veterinary Research (2023) 54:8 Page 4 of 17 authors and also others [10, 28] reported that a variety of [6], while in another region of the country, in 21 farms infectious agents such as P. multocida, G. parasuis and with different production characteristics, the preva- M. hyorhinis can be involved in pleurisy lesions in pigs. lence was 9% [31], suggesting that it is a widespread The role of Streptococcus suis as causative agent of CVPC challenge. or pleuritis has not been demonstrated convincingly. The results show a large variation between the different In addition, observational studies found an association studies. Part of the variation may be due to differences in between the prevalence of pleurisy and the seropreva- study design (study population, age at slaughter), patho- lence of pathogens that are known not to cause pleurisy, gen prevalence, and scoring of the lesions. The varia- such as M. hyopneumoniae [19, 24, 31], porcine repro- tion between individual farms and/or individual batches ductive and respiratory syndrome virus (PRRSV) [32], of slaughter pigs within each study may even be higher. porcine circovirus 2 [33] and IAVs [29, 34, 35]. These Neumann et al. [38] showed that, based on data from a observations can probably be explained by the multi- large national abattoir-based lesion recording system etiological nature of the clinical respiratory problems in over a 10-year period, farm of origin and not abattoir, most farms, rather than interpreting that these pathogens explained most of the variance in prevalence of CVPC. can cause pleurisy. Also, progressive atrophic rhinitis Interestingly, the overall prevalence of CVPC and pleu- was associated with pleurisy in conventional Danish pig risy in slaughter pigs since 2000 (Table 1) is similar as herds, interacting with A. pleuropneumoniae serotype that reported in older studies (for review, see Maes [42]). 7 [19, 29]. Paisley et al. [36] classified pleurisy lesions This is surprising as some control measures against the according to localization and indicated that pleurisy con- fined to the dorso-caudal lobes is primarily associated with A. pleuropneumoniae infections, whereas cranio- Table 1 Prevalence of cranioventral pulmonary ventral pleuritis is often associated with lesions such as consolidation (CVPC) and pleurisy in slaughter pigsa pericarditis and complicated pneumonia. Country Number of Percentage of References Wallgren et al. [28] reported that, although the preva- pigs with lence of CVPC and pleurisy at slaughter can be quite sim- Farms Pigs CVPC Pleurisy ilar between farms, the pathogens, as well as the infection patterns during the fattening period, can be quite vari- Australia 46 210 –c 15 [89] able. Also, many non-infectious parameters have been Belgium 150 3,750 24 16 [3] identified as risk factors for the prevalence and/or sever- 50 6,335 24 21 [24] ity of CVPC and pleurisy in herds infected by bacterial Brazil 21 908 72 9 [31] 30 900 74 14 [6] pathogens able to cause these lesions [3, 6, 24, 25, 31, 37]. Denmark 259 10 628 –c 27 [18] 321 2064 –c 30 [19] 4 Prevalence of CVPC and pleurisy lesions Finland 46 690 –c 6 [39] Cranioventral pulmonary consolidation and pleurisy are France 1196 110 865 72 14 [90] both commonly observed lesions in slaughter pigs. The 14 6997 58 10 [54] prevalence of slaughter pigs with CVPC and pleurisy 143 4290 69 14 [25] lesions published in peer-reviewed international journals Germany 20 1000 73 -c [46] since 2000 are shown in Table 1. There were no published Ireland 38 5628 58 43 [91] 56 23 372 11 13 [34] studies from North-America, possibly because lung Italy 91 10 041 60 - [85] lesion evaluation in slaughter pigs is less frequently per- 48 4889 46 48 [26] formed in that world region. –b 216 –c 50 [40] The prevalence of CVPC is generally higher than that –b 5902 42 [48] of chronic pleurisy, although that might not be the case New Zealand 279 6 220 664 18 14 [38] in all countries, e.g. Denmark. The lowest CVPC preva- Philippines 471 1887 48 22 [92] lence was found in New Zealand, namely 8% [38], the Serbia 20 625 42 24 [88] highest in Brazil, around 74% [6]. The lowest pleurisy Spain 107 10 404 56 27 [21] Spain and Portugal 221 199 678 31 19 [17] prevalence was found in Finland [39], namely 6%, and Switzerland 10 375 59 –c [46] the highest in Italy, approximately 50% [40]. In a study Thailand 17 646 58 –c [93] conducted before 2000 in Denmark, Christensen and UK 4420 2 261 779 27 12 [1] Enøe [41] showed that pleurisy accounted for approx- a imately 70% of all post-mortem recordings at meat results from peer-reviewed studies published since 2000, and including at least 3 herds or more than 200 pigs inspection. In a Brazilian study conducted in 30 large b not mentioned herds, the lesion was observed in 14% of the animals c not investigated Maes et al. Veterinary Research (2023) 54:8 Page 5 of 17 PRDC have improved during the last two decades, such 5 Slaughterhouse examination as vaccination against respiratory pathogens in fattening Slaughterhouse examination has great potential to assess pigs, e.g. M. hyopneumoniae, PCV-2 and PRRSV. Also, many different aspects of the respiratory health of fat- much emphasis has been placed on the importance of tening pigs such as confirmation and quantification of biosecurity and tools for scoring biosecurity have been respiratory disease in the farm, detection of subclinical developed. The fact that the prevalence of lesions has infections, and it may also serve as an important out- not decreased might be attributed to suboptimal farm come parameter for various types of research studies characteristics and insufficient implementation of proper (e.g. efficacy studies). An overview of the advantages and management and biosecurity practices [39], a potential disadvantages of slaughterhouse examination for assess- decrease in the use of antibiotics, suboptimal vaccines ing respiratory tract lesions is shown in Table 2, which and vaccination practices, possible changes in the viru- are discussed in relation to practical aspects, the assess- lence and/or transmission capacity of pathogens and/or ment of lesions, the number and representativeness of the fact that pig production has become further inten- the examined animals, and the interpretation and value sified, with fattening pigs being raised in larger groups of the results for the stakeholders. and on larger farms. Differences in study design might also play a role. It is not clear whether the severity of the 5.1 Practical aspects lesions has remained the same. Overall, the high preva- Evaluation of respiratory tract lesions at slaughter is a lence values indicate that the respiratory health of fatten- rather easy way to collect information about the respira- ing pigs needs to be improved, and that research focusing tory health of fattening pigs [37]. It is important to make on improving management and biosecurity in pig farms the practical arrangements with the transport company and on developing vaccines that confer better protection and the slaughterhouse on beforehand. Some slaughter- is warranted. In addition to developing better control houses might (temporarily) not allow access to exter- measures, also research focusing on how to increase the nal persons to enter the facilities and/or to evaluate the implementation of these measures is needed. lungs e.g. for biosecurity reasons. Therefore, it is impera- Lower levels of CVPC are found in countries that tive to communicate with the person responsible for are almost free of M. hyopneumoniae such as Switzer- meat inspection and/or monitoring the slaughterhouse land, Finland and Norway. In these countries, official facilities. regional and/or national eradication programs for M. The timing of slaughtering a specific batch of pigs can- hyopneumoniae are in place, and farms infected with M. not always be determined precisely, because of practi- hyopneumoniae are only sporadically detected [43–45]. cal issues at the slaughter line or with the transport of However, and surprisingly, Luehrs et al. [46] examined the pigs. Therefore, the slaughtering of the pigs might the lungs of slaughter pigs from 10 Swiss pig farms that be delayed or else, and even worse, when the expected were free of M. hyopneumoniae and reported an over- arrival of other batches of pigs to the abattoir is delayed, all CVPC prevalence of 59%. The lesions were mild, as the batch of pigs of our interest might be slaughtered their extension was less than 10% of the lung tissue for earlier than the proposed time. In order not to disturb most of the pigs. This finding illustrates that the lesions the process, it is important to understand the slaughter observed in these farms could be caused by other bac- flowchart and to know the specific place where the evalu- terial pathogens different from M. hyopneumoniae. ation will be carried out. The scoring itself can be done The prevalence of pleurisy has traditionally been low fast and, typically, a sufficient number of animals can be in some North-European countries such as Finland and scored in a short time. An accurate assessment of lesions Sweden. However, data from recent studies [28, 39] and might be challenging in case of a fast speed of the slaugh- the Finnish Food Authority [47] showed that the preva- ter line. In some cases, only one side of the lungs can be lence of pleurisy in these countries has increased dur- evaluated. In current industrial slaughter facilities, the ing the last years. The specific reasons are not clear, as speed of slaughtering is often more than 500 pigs per it does not seem to be related to infection with one spe- hour [48]. Therefore, a scoring system that allows quick cific pathogen, like A. pleuropneumoniae. The authors evaluation with ease, in accordance with the speed of the of these studies [28, 39] speculate that it might result slaughter line, is preferred [1]. Else, not all pigs but a sub- from a combination of infections with different patho- set of the population (e.g. every two or three pigs) should gens in combination with suboptimal management and be evaluated. farm conditions. Most probably, the decrease of use of The evaluation is also inexpensive, as it is based on vis- prophylactic antibiotics might have also contributed to ual assessment and palpation of the lungs. In case plucks this scenario. Further research is needed to explore the are taken away from the slaughter line for subsequent reasons for this increase. Maes et al. Veterinary Research (2023) 54:8 Page 6 of 17 more in-depth analysis, payment to the slaughterhouse The presence as well as the severity of different types might be needed. of lung lesions, considering the resolution time of such lesions, can be assessed. Detailed analysis or simultane- ous assessment of many different lesions might be diffi- 5.2 Assessment of lesions cult or impossible in slaughterhouses with high speed of Most scoring methods are based on a visual and subjec- the slaughter process. In this case, one should focus on tive estimation of the proportion of lung affected surface a sample of pigs and/or remove the materials from the and/or volume [49]. Therefore, the scoring should be slaughter line (when allowed) and transfer them to an done by an experienced person or after proper training. appropriate location for more detailed assessment. If this is not the case, it is prone to erroneous assessment. Another disadvantage is that the presence of severe Systems for automatic recording of lesions (pictures or pleurisy may obscure the evaluation of CVPC [49]. This digital data) of the respiratory tract would not have these is especially the case when major parts of the lung stick disadvantages [48]. to the inner chest wall of the carcasses. Slaughter checks are also useful to detect subclinical respiratory infections, i.e. pigs that did not show obvious 5.3 Examined animals clinical signs during the fattening period, although they It is important that the examined pigs are representa- exhibit lung lesions. However, subclinical infections that tive for the situation on the farm. Assessment of the best do not lead to gross lesions of the respiratory tract are or worst performing pigs of a batch will lead to biased not detected [50]. results. This risk is higher in case the pigs of a barn are Table 2 Strengths and limitations of slaughterhouse examination for assessing the respiratory health of pigs Strengths Limitations, critical considerations Practical aspects Practical arrangement with slaughterhouse Rather easy Sometimes access to slaughterhouse is not allowed No guarantee of precise time of slaughter- ing Time needed for assessment Short, often less than one hour Speed of slaughter line might be too high to assess all pigs Cost of evaluation Inexpensive (visual assessment, palpation) Payment might be required when removing lung plucks Assessment of lesions Evaluation Easy for experienced person Subjective, training needed; presence of lesion (yes/no) less informative than extension of lesion Subclinical infections Detected in case lesions are present Only for infections leading to gross lesions Severity/extension of lesions Possible Needs more time than detection of presence (yes/ no) of lesion Detailed analysis Possible when plucks are removed from slaugh- Not possible at the slaughter line ter line Simultaneous assessment of different lesions Possible e.g. pneumonia, pleurisy Severe pleurisy may mask evaluation of other lung lesions Examined animals Representative for farm situation Easy in case all pigs of a barn are slaughtered Difficult when pigs are not marketed at once; (all-out principle) evaluation of best or worst pigs might provide biased results Number of animals Large number possible (minimum 30, preferably Representative sample of slaughtered batch can more) be selected Interpretation of results Type of data Prevalence, as lesions are examined only once No incidence data (lesions not monitored over (snapshot) time); lesions are dynamic and can heal over time Relevance for diagnosis Typical lesions may suggest infection (previous No etiologic diagnosis as lesions are not pathog- or active) nomonic Benchmarking Possible, within a farm (time evolution, barn Lesions should be examined in a standardized way effects), against other farms or national average Assessment of intervention strategies Possible e.g. vaccinations Lesions should be examined in a standardized way; association between lesion and carcass char- acteristics at animal level is not always available Maes et al. Veterinary Research (2023) 54:8 Page 7 of 17 not sent to slaughter at once, but in two or three succes- or severity of lesions may be observed at slaughter, sive times over a few weeks. In such scenarios, the first whereas the pigs suffered from the health problem only pigs are usually those with the highest growth and health for a short time, at the end of the fattening period. In status, and therefore, have suffered the least from res- this case, slaughterhouse evaluation results might over- piratory disease. The opposite might be the case for the estimate the problems encountered during the fatten- smallest pigs of a group. These pigs might have had more ing phase. Also, when very small lesions are counted, health problems, and therefore, can result in an overesti- prevalence data might lead to an overestimation of the mation of the prevalence of lung lesions at the farm. importance of the problem. Usually, not all pigs but a subset of representative lungs Apart from the dynamic nature of lung lesions, it is from the farm is examined. Although a minimum of 30 also important to realize that lesions might be typical, randomly selected pigs from the same slaughter batch has but that most lesions are not pathognomonic, that is not been shown to provide reliable information at herd level being specific for a pathogen. Therefore, slaughterhouse [51], it is generally accepted that it is better to evaluate examination does not allow establishing an etiologic more pigs, or to make the sample proportional to the size diagnosis. The results should be regarded to complement of the batch. Statistical criteria to obtain the preferred clinical and performance data from the farm and results accuracy for prevalence and/or severity scoring should be from necropsy and laboratory examinations. used. To this end, the size of the population at risk, the Slaughterhouse data can be used to investigate differ- expected prevalence, and the desired confidence in the ences in the respiratory health of pigs raised in different probability of detecting disease in the sample should be barns within a farm, to assess evolution over time, and to considered. The pigs to be examined can be selected by benchmark the farm against other groups of farms or the different sampling strategies, such as random sampling national average. In this sense, slaughter data important or systematic sampling, in which one pig every e.g. two, in health schemes and for increasing awareness of these three or four pigs is scored. lesions by farmers [1]. Also, the effectiveness of interven- tion strategies can be evaluated. For efficacy trials or for 5.4 Interpretation of the results assessing the impact of lesions on performance, the link Examination of the respiratory tract at the slaughter- between lesion and carcass characteristics is needed at house generates prevalence data, as pigs are not moni- animal level. Depending on the situation in the abattoir, it tored over time, but examined only once. However, might not be possible to obtain this information. lung lesions are dynamic, implying that lesions in young animals may have healed at the time of slaughter. This 6 Scoring systems for CVPC and pleurisy regression of lesions during the fattening period may Different lung scoring systems have been developed over therefore lead to false-negative results [52]. Pessoa et al. the past decades (Figure 1, Table 3). They are based on [53] performed an observational study in which groups visual and manual assessment of the affected propor- of pigs were monitored weekly during the entire fatten- tion of the lung [49]. Most of the scoring systems use a ing period and at slaughter. They found positive asso- two-dimensional approach by assessing the percentage of ciations between the prevalence of CVPC at slaughter lung surface that is affected [27, 55–58]. Other methods and coughing during the last three weeks of the fat- use the percentage of affected lung volume or weight and tening period, but not with coughing earlier during are therefore based on the three-dimensional characteris- the fattening period. They also found positive associa- tics of the lung [59–61]. tions between the prevalence of fissures (attributed to Some slaughter‐check diagrams include more detailed chronic M. hyopneumoniae lesions) and coughing 7 to information about the lung, such as the type of pneumo- 3 weeks prior to slaughter. This suggests that lesions at nia, location, the presence of other lesions on the lung slaughter reflect the respiratory health of the pigs dur- (e.g. pleurisy, adhesions, abscesses) and/or evaluations of ing the last weeks of the fattening period, but that they the liver and heart [60]. In some cases, drawing the lesion are a poor indicator of the respiratory health of the pigs may be of help to better calculate the final scoring. Nev- in the early fattening phase. This corroborates findings ertheless, if this option is not feasible (due to the speed of of Pagot et al. [54] and Baraldi et al. [31]. The healing of the chain), an effective alternative to drawings would be the lesions and the fact that some subclinical infections digital images or photographs of lungs [62]. These images are not detected, may lead to an underestimation of the can/need to be reviewed later, which is time-consuming respiratory problems when relying solely on slaughter- and slaughterhouses may limit the use of a camera in the house examination. On the other hand, some infections premises. Using a voice activated recording device greatly leading to lesions may take place at the end of the fat- simplifies records and allows the hands to manipulate the tening period only. In this case, a high prevalence and/ pluck. Maes et al. Veterinary Research (2023) 54:8 Page 8 of 17 6.1 Scoring of CVPC hyopneumoniae. The score ranges from 0 (no lesions) to An overview of commonly used scoring methods for 35 (all lung tissue affected). The lesions are first sketched CVPC in pigs has been published by Garcia-Morante onto a standard diagram of the lung, followed by analysis et al. [49] (Figure 1). They include the system described of sketches on the diagrams to determine the overall lung by Goodwin et al. [55], Hannan et al. [56], Madec and score. Kobisch [57], Morrison et al. [59], Christensen et al. [60], Sibila et al. [27], Straw et al. [58] and the system recom- 6.2 Scoring of pleurisy mended by the European Pharmacopoeia (Ph. Eur., mon- An overview of commonly used scoring systems for pleu- ograph number 04/2013:2448) [61] for the evaluation of risy in slaughter pigs is summarized in Table 3. porcine enzootic pneumonia as reference system. Other systems have also been described, e.g. Steinmann et al. 6.2.1 System by Madec and Kobisch [63], but they are not further discussed as frequently The first scoring system for pleurisy was developed they derive from one (e.g. [58]) of the eight systems of by Madec and Kobisch [57]. This scoring system has Figure 1. The affected lung tissue score can be expressed the advantage of defining a score 4 for advanced stages as a number [55–57], or as a percentage [59–61]. Garcia- likely having a major effect on performance and/or lead- Morante et al. [49] reported high correlations between ing to carcass condemnations. Nevertheless, it should the different scoring systems. Also, Sitjar et al. [64] had be ensured that non-evisceration is due to pleural adhe- found two measurement techniques based on either sions and not to incorrect carcass preparation. Interlobar superficial or volumetric pneumonia to provide essen- pleurisy, score 1, is easily identified by handling the lungs. tially identical information. However, localized pleurisy with a diameter smaller than Some scoring systems have been developed to assess 2 cm, score 2, requires good attention and may only be CVPC in pigs under experimental conditions when there visible in good light. Sensitivity of scoring mild pleurisy is more time for the assessment [56], whereas others are cases may vary more between assessors [65] and empha- more suitable for a rather fast assessment of the lesions sizes the need for training. Extensive pleurisy, score 3, under field conditions [59]. The scoring system described and partial or total ribcage condemnations, score 4, are by Hannan et al. [56] is appropriate to carefully quantify obvious and in most cases do not need palpation, but lung lesions caused by experimental infection with M. require carcass inspection. Goodwin et al. [55] Hannan et al. [56] Madec and Kobisch [57] Morrison et al. [59] Two-dimensional Two-dimensional Two-dimensional Three-dimensional Score: 0-55 Score: 0-35 Score: 0-28 Score: 0-100 Straw et al. [58] Christensen et al. [60] Reference method [61] Sibila et al. [27] Two-dimensional Three-dimensional Three-dimensional Two-dimensional Score: 0-100 Score: 0-100 Score: 0-100 Score: 0-100 Figure 1 Commonly used methods to score cranioventral pulmonary consolidation in slaughter pigs (adapted from [49]). Maes et al. Veterinary Research (2023) 54:8 Page 9 of 17 Table 3 Overview of pleurisy scoring systems in slaughter pigsa Score Scoring system Madec and Kobisch [57] CTPA b Pointon et al. [66] SPES c 0 No pleurisy 1 Interlobular pleurisy (visceral Fibrinous pleurisy Interlobular pleu- 1 N: pleurisy with normal Cranioventral lesion: interlobar pleurisy) risy (adhesions lungs pleurisy or at ventral border of between lung 1P: pleurisy with pneumonic caudal lobes lobes) lungs 2 Localized pleurisy < 2 cm Extended pleurisy: lungs Pleurisy (adhe- 2 N: pleurisy with normal Dorsocaudal monolateral focal diameter cannot be removed from the sions of lungs to lungs lesion carcass chest wall) 2P: pleurisy with pneumonic lungs 3 Extensive pleurisy > 2 cm – – Bilateral lesion of type 2 or diameter with adhesions to extended monolateral lesion ribcage (at least one third of one diaphragmatic lobe) 4 Partial or total ribcage con- – – Severely extended bilateral demnation lesion (at least one third of both diaphragmatic lobes) a The Danish system [41] is explained in the text but not listed in the table, as it differs significantly from the other systems b CTPA System by the Centre Technique de Productions Animales[54] c SPES Slaughterhouse Pleurisy Evaluation System[67] 6.2.2 System by the centre technique de productions 6.2.4 Slaughterhouse pleurisy evaluation system (SPES) animales (CTPA) The Zootechnical Institute of Lombardy and Emilia- The Centre Technique des Productions Animales (CTPA) Romagna (Italy) devised a new scoring system entitled in France uses a simplified scoring system from 0 to 2 for SPES (Slaughterhouse Pleuritis Evaluation System) [67]. on-farm trials [54]. It is a simple system for clinical trials The system aims to determine the extension and locali- with score 0 for absence of pleurisy, score 1 for fibrinous zation of the lesions by focusing on the diaphragmatic pleurisy and score 2 for extended pleurisy with adhesions lobes. It has also been used in other studies [21, 24, 27]. to the ribcage. However, as stated in the original paper, Di Provvido et al. [40] investigated an alternative method score 1 would apply exclusively to acute forms of pleurisy for pleurisy scoring, namely the PEPP (pleurisy evalua- (presence of fibrin) and does not apparently include the tion of the parietal pleura). The method is easy to con- possibility of mild chronic forms with minimal adhesions duct and involves the evaluation of the parietal pleura to the thoracic cavity. In contrast, score 2 indicates that i.e. the serous membrane lining the chest wall. Very high lungs cannot be easily removed from the carcass, which correlations were found with the SPES method. indicates exclusively chronic lesions with marked adher- ences. Therefore, a significant number of lungs found at 6.2.5 System by Christensen et al. [41] abattoir might have lesions that should be considered in The Danish system of Christensen et al. [60], which is not between those scoring values and, in consequence, cer- listed in the table due to its dissimilarity with the other tain classification difficulties may arise. systems, involves careful examination of the lungs and sketching of the lesions in a record form [60]. It is much 6.2.3 System by Pointon et al. [66] more precise than other systems, but it is not suitable for In North America and Australia, a system is used that use at the slaughter line. The score is proportional to the specifically differentiates pleurisies with adhesions damaged surface area on each lobe and for each side of between lobe lungs (score 1) or between lungs and the lungs (cranioventral and dorsocaudal). wall chest (score 2) [66]. Moreover, the scores take into account whether or not the pleurisy is associated with pneumonia (N: pleurisy without pneumonia; P: pleu- 6.2.6 System by Sibila et al. [27] risy with pneumonia). The scoring system is used in the This system, developed in Spain, is based on the quantifi- American (PigMON) and Australian (PHMS, Pig Health cation of damaged lung surface by delimitating, in a pic- Monitoring Schemes) monitoring schemes. ture and using an image software, the area of the affected lung tissue [27]. This system requires to take pictures Maes et al. Veterinary Research (2023) 54:8 Page 10 of 17 from both sides of the lung (if presence of lesions at the association was found. Pagot et al. [54] reported that ventral side is confirmed) and the analyses of the images the ADG during the fattening period was approximately through a software, indicating the percentage of affected three percent lower for pigs showing CVPC at slaughter. area. Therefore, this system is difficult to be performed at They detected large differences between farms; in some the slaughterhouse. It has been used to analyze the out- farms, the ADG decrease in pigs with CVPC reached up come of experimental infections with A. pleuropneumo- to 7%. Also, Paisley et al. [36] showed substantial varia- niae [27] as well as M. hyopneumoniae [49]. tion between herds. The presence of CVPC in two farms was associated with a decreased ADG during the fatten- ing period of 31 and 137 g respectively. In a recent study 6.3 Artificial intelligence to score lesions in one farm, Paz-Sánchez et al. [8] found that the pres- The mentioned scoring systems are generally simple ence of CVPC reduced ADG by 9%. and easy to standardize. However, they are rather time- Martínez et al. [69] did not find a negative effect of consuming, and abattoir-related and inter-observer CVPC lesions on ADG and feed efficiency. In that study, variations cannot be fully ruled out. Artificial intelli- performance data were analysed at farm level, whereas gence-based technologies are under development to lung lesions were assessed at slaughter from one sub- automatically score pictures of pleurisy in slaughtered group (35 pigs) per farm only. The subgroup might not pigs [48]. The automation of such a process would be have been fully representative for the farm and the num- extremely helpful to enable a systematic examination of ber of farms might have been too small to observe statis- all slaughtered livestock [68]. In the study of Trachtman tical differences. et al. [48], artificial intelligence was able to differentiate pleural surfaces affected with pleurisy from healthy ones, 7.1.2 Impact of severity (extension) of CVPC with an overall accuracy of 86%. The system was better Several studies also examined the effect of severity of able to make distinction between severely and moder- CVPC on performance (Table 4). The term severity is ately affected pleural surfaces as compared to evaluation used here to refer to the extension of the pneumonic by experienced veterinarians. Further research is needed lesion. Straw et al. [51] calculated, based on the results to train the neural networks to identify and score pneu- of five studies, that ADG is decreased by 37.4 g for every monia, and to implement the system in large capacity 10% of the pig’s lung surface affected by CVPC. They also slaughterhouses. The technology could provide the data demonstrated that, on average, CVPC caused 17% and in a suitable form for statistical analysis, thereby facili- 14% decreases in ADG and in feed efficiency, respectively. tating data processing and the supply of summaries and The same authors further reported that the percentage recommendations to industry stakeholders. Neverthe- increase in feed conversion ratio (FCR) was highly cor- less, these systems will depend, among other factors, on related with the percentage decrease in ADG, meaning the quality and precision of the pictures. The latter issue that when there is a negative effect on ADG, one can also is not easy to be solved in a non-static hanged pluck of expect a negative effect on FCR, and vice versa. lungs. Hill et al. [7] indicated that a 10% increase in the vol- ume of pneumonic tissue (within the range of 1 to 70% 7 Impact of CVPC and pleurisy on performance affected lung volume) was associated with a decrease Various approaches have been used to estimate produc- in ADG by 41.1 g, and a 16.7-day increase in number tivity losses and economic impact of respiratory disease of days to reach 104.5 kg. Very similar results (−31.5 g under field conditions. A commonly used strategy is ADG decrease for each 10% of affected lung volume) to compare the performance of pigs showing lesions of were obtained in a follow-up study two years later [70]. the respiratory tract at slaughter with the performance Regula et al. [50] found a decrease in ADG of 6.8 g for of pigs not showing lesions, or else to compare the per- each percent of affected lung tissue. A recent study [71], formance of batches of pigs with different prevalence obtained results that were in between the two previous of CVPC or pleurisy. Studies that have investigated the studies, namely 1.8 g decrease in ADG during the fat- impact of CVPC and pleurisy in slaughter pigs are dis- tening period for one percent increase in area lung con- cussed below. solidation, corresponding with 18 g decrease in ADG for 10 percent affected lung tissue. Similar results were 7.1 Cranioventral pulmonary consolidation obtained by Christensen [72], who showed that each 1% 7.1.1 Impact of presence of CVPC of lung volume affected by CVPC lesions reduced DWG Morrison et al. [59] studied 23 publications to examine by 2.2 g, and increased the number of days to reach the possible negative effect of CVPC at slaughter on aver- slaughter weight by 0.61 days. He further calculated that age daily gain (ADG). In 10 studies, no negative effect the growth-depressing effects of M. hyopneumoniae of CVPC was identified; in the other studies, a negative Maes et al. Veterinary Research (2023) 54:8 Page 11 of 17 Table 4 Studies assessing the impact of cranioventral pulmonary consolidation (CVPC) on average daily gain (ADG) in pigs. References Study population Impact on ADG Comment Presence of CVPC [59] 23 studies 10 publications: no effect 13 publications: decrease [51] 9 studies −17% Feed conversion ratio +14% High correlation between decreased ADG and feed conversion ratio [36] 2 farms (578 pigs) Farm A: −26 g Farm B: −26 g [54] 14 farms (6,997 pigs) −38 g (−4.9%) Large differences between farms (range: −7% to +2.6% [69] 39 farms No effect No effect on feed conversion ratio Performance data were analysed at farm level; lung lesions were assessed on one subgroup (35 pigs per farm) at slaughter [8] 1 farm (108 pigs) −9% Severity of CVPC [51] 5 studies 37.4 g per 10% of affected lung tissue Five studies [52] 21 pigs 20% CVPC throughout lifetime: 25 kg lower weight at Radiographic monitoring of the lungs from 21 to slaughter 180 days of age 25 days extra to reach slaughter weight [7] 2 farms (41 lungs) 41.1 g/day for 10% affected lung volume 10% affected lung leads to 16.7 days more to reach 104.5 kg [70] 2 farms (58 lungs) 31.4 g/day for 10% affected lung volume 10% affected lung leads to 13·2-days more to reach 104.2 kg Only significant association between lung lesion and ADG in one farm [72] 1 farm (333 pigs) 2.2 g/day for each 1% of affected lung volume 1% affected lung leads to 0.61 days more to reach slaughter weight; early infections cause more perfor- mance loss [50] 7 farms (18 cohorts 6.8 g/day for 1% of affected lung Serologic testing was more effective than slaughter with 30–35 pigs / evaluation in assessing the impact of subclinical infec- cohort) tion on ADG [73] 1 farm (138 pigs) Score 2: −45 g/day (−6%) Lung consolidation: score 1: 0–5%; score 2: 6–40%; score Score 3: −90 g/day (−11%) 3: > 40% Score 2: 3.13 kg less at slaughter Score 2: 10.85 kg less at slaughter [54] 14 farms (6,997 pigs) −7.0 g/day (0.7%) for 1 point increase in severity score More ADG decrease in pigs with severe lesions: score (1–28) 0: 775 g; scores 1–4: 750 g; scores 5–8: 735 g; score > 8: 695 g [71] 1 farm (500 pigs) 1.8 g/day for each 1% of affected lung surface Financial loss of §6.55 in pigs with more than 15% affected lung tissue compared to animals without lesions [8] 1 farm (108 pigs) −66.4 g/day in pigs with > 10% of affected lung Days to slaughter: + 8 days; carcass weight: −3.6 kg surface versus pigs with no lesions: infections are, on a relative scale, more pronounced in Other studies emphasized the importance of the pigs with severe CVPC. Donkó et al. [73] used the scor- dynamic nature of lesions and/or time of infection when ing method of Straw et al. [58] and showed a reduction assessing the impact on performance. Noyes et al. [52] in ADG during the fattening period of 5.5% and 11% and Wallgren et al. [74] indicated that CVPC lesions pre- for pigs with CVPC score 2 (5–40% of lung tissue con- sent at slaughter are a poor indicator of lifetime pneu- solidated) and score 3 (>40% of lung tissue consolidated), monia, as lesions can progress and regress throughout respectively. the life of pigs. They indicated that the approximate time Pagot et al. [54] reported that the CVPC score at of infection should be included to obtain a useful inter- slaughter explained 19% of the ADG variation. One sup- pretation of the severity and impact of CVPC lesions at plementary point in the CVPC Madec score (0–28) cor- slaughter. Morris et al. [75] and Sitjar et al. [64] showed responded with approximately 0.7% of lost growth. that weight losses due to M. hyopneumoniae infections Maes et al. Veterinary Research (2023) 54:8 Page 12 of 17 are more substantial when pigs are infected early in life, based on their serological status against M. hyopneumo- as they have suffered from the respiratory problems for a niae and CVPC at slaughter. Pigs with M. hyopneumo- longer time. niae serum antibodies and CVPC at slaughter, grew from Paisley et al. [36] showed that the presence of interlob- 75 to 176 g/day slower (10.2% to 17.5% reduction) than ular fissures or scars at slaughter, which are considered pigs without antibodies and CVPC. They also showed to be old or healed CVPC lesions [12], was associated that pigs that became seropositive for M. hyopneumoniae with a reduced ADG early in the fattening period, while late during the fattening period without or with only very CVPC (recent Mycoplasma-like lesions) at slaughter was mild CVPC had a reduced ADG (60 g/day) compared to associated with a reduced ADG in the period close to seronegative pigs without CVPC [43]. Similarly, Regula the time of slaughter. Noyes et al. [52] calculated that a et al. [50] reported that M. hyopneumoniae seroposi- pig with 20% affected lung tissue throughout its lifetime, tive pigs had lower ADG (38 g/day) compared to those measured by radiographic examinations throughout the that were seronegative. The latter authors suggested that fattening period, weighs 25 kg less or reaches slaughter regular monitoring for antibodies against respiratory weight about 25 days later than a pig without CVPC. In pathogens during the fattening phase was more effective a later study, Sitjar et al. [64] did not find an overall sig- in assessing the impact of subclinical infection on perfor- nificant association between lifetime pneumonia and mance than monitoring lung lesions at slaughter. reduced ADG. They indicated that the discrepancy with the study of Noyes et al. [52] might be due to the fact 7.2 Pleurisy that the farm studied had a less severe respiratory prob- Pagot et al. [54] reported that pleurisy at slaughter was lem than the one studied previously. Even so, Sitjar et al. associated with an ADG decrease of 39 g (5.2%), and a [64] did find a strong correlation between average life- 6-day increase in the length of the fattening period time pneumonia and decreased ADG in lightweight pigs, (Table 5). They also found that CVPC and pleurisy had which generally had more severe CVPC than heavier a synergistic effect. Hence, animals showing CVPC and weight animals. pleurisy suffered from 15% lower growth than non- Other studies did not only focus on the presence or affected pigs. severity of the lesions, but also emphasized the impor- Straw et al. [51] demonstrated that, on average, pleurisy tance of lesions being the result of either a single infec- decreased ADG and FCR by 34% and 26%, respectively. tion or mixed infection, and therefore included different Paz-Sánchez et al. [8] found an ADG decrease of 11% in disease parameters to assess the impact on performance. pigs with pleurisy. Mousing et al. [29] showed that pigs The effect of a single M. hyopneumoniae infection on with pleurisy had a lower carcass weight at slaughter, and ADG and FCR can only be assessed under experimen- Hartley et al. [79] showed that pleurisy was associated tal conditions, since almost all field infections are com- with increased time (up to 8 days) to slaughter. plicated by other infectious agents. The effects of single On the contrary, Paisley et al. [36] showed that pleurisy M. hyopneumoniae infections on ADG are variable, with without the presence of other lesions was not associated some studies [76, 77] showing pronounced negative with decreased performance. Also, Martínez et al. [69] effects on ADG (−117 g/d and −10–20%, respectively), could not observe a negative effect of pleurisy on per- whereas other studies did not find a negative effect [49, formance. As mentioned before, some limitations of the 78]. The different results might be explained by differ- latter study might have resulted in lack of identifying a ences in the challenge model or other aspects of the study potential relationship. design. Experimental challenge involves a limited num- Jäger et al. [80] estimated the cost of pleurisy in British ber of animals, implying that the statistical power is often pig herds to be £5 (approximately €6) per pig produced. (extremely) low to show significant differences in param- Their calculations were based on industry standard costs eters with a large variation such as ADG. Also, a small associated with 6% increase in mortality during the proportion of dead pigs might have a large impact on the grower-finisher period, 20% prevalence of pleurisy, 50 g outcome. Furthermore, challenge models in which high reduction in ADG and 0.1 reduction of FCR. Ferraz et al. doses of M. hyopneumoniae organisms are inoculated [71] estimated a cost of US$6.6 (approximately €6.4) per once or twice and in which pigs are monitored for a short pig produced considering a reduction in ADG of 27 g period (after infection), are not reliable to mirror the field associated with lesions (CVPC and pleurisy) in ≥ 15% of situation of a chronic respiratory disease. Therefore, chal- the lungs compared with pigs without lesions. Calderón lenge studies are not very suited to assess the impact on Díaz et al. [81] showed, using a bio-economic simula- performance. tion study, that from six recorded pluck lesions, pleurisy Rautiainen et al. [43] compared the performance of and lung scars were the main lesions associated with individual pigs during the fattening period of two farms Maes et al. Veterinary Research (2023) 54:8 Page 13 of 17 Table 5 Studies assessing the impact of the presence of pleurisy on average daily gain (ADG) in pigs. Reference Study population Impact on ADG Comment [79] 9592 pigs from 78 farms; Fattening period + 8 days examined in 4 slaughter- houses [51] 4 studies −34% Feed conversion ratio + 26% [29] 4800 pigs, selected on spe- Lower carcass weight Effect was shown in multivariable logistic model with carcass weight being nega- cific days in one slaughter- tively associated with pleurisy lesions house [36] 2 farms (578 pigs) Farm A: no effect Effects in farm B were depending on localization of pleurisy: dorsocaudal pleurisy: Farm B: -28 g /−42 g no effect; parietal pleurisy: −28 g; antero-ventral pleurisy: −42 g [54] 14 farms (6997 pigs) −39 g (−5.2%) Large differences between farms (range: -19.9% to +4.6%) Severity of pleurisy: score 1: −54 g; score 2: −37 g Fattening duration +6 days Pleurisy and CVPC: ADG −15% (synergistic effect) [69] 39 farms (one batch per farm) No effect No effect on feed conversion ratio Performance data were analysed at farm level; lung lesions were assessed on one subgroup (35 pigs) at slaughter [8] 1 farm (108 pigs) −11% decreases in ADG during the grow-finisher period and a average carcass weight of 77.7 kg at 200.8 days, whereas lower economic return. the carcass weight of pigs with lung disease was 75.5 kg at Apart from a decrease in average performance, there 206 days old. In a first study, Escobar et al. [78] reported is a considerable cost associated with unequal rates of that a single experimental M. hyopneumoniae infection growth of pigs within a herd. Slow growing pigs must did not affect whole-body fat or protein accretion of be held back and marketed later, or the producer must nursery pigs during a four-week experiment. In a later accept a deduction for lightweight pigs at slaughter. study using experimental infection with M. hyopneumo- These hidden costs must be considered when calculating niae and PRRSV [84], they reported that the magnitude the costs and benefits of intervention strategies. of increases in inflammatory cytokines is predictive for In some cases, pigs may have more than one type of decreases in protein accretion and growth. The authors lesion in the respiratory tract or in other organs, e.g. the further suggested that during infection, growth of skele- liver [1]. In that case, such lesions may also influence the tal muscle is limited in part by increased levels of myosta- performance of the animals. This can lead to compari- tin, a circulating factor that may act as a muscle chalone. son of growth rates in groups of pigs with different dis- Ostanello et al. [85] investigated 109 batches of Ital- eases or combinations of diseases, rather than comparing ian pigs of approximately 160 kg (9–10 months of age). diseased and non-diseased groups. This might result in They found a significant negative association between over- or under-estimation of the importance of some the mean CVPC score of a batch of slaughter pigs and lesions. the carcass quality, based on the EUROP evaluation grid. In addition to the performance losses for the farmer, That system uses percentage of lean meat content of the pleurisy also incurs losses for the abattoirs because pleu- carcasses, batch homogeny and carcass attitude for the risy requires trimming of the carcass causing disruption, production of raw ham as carcass quality parameters. reducing line speed, and increasing labor and wastage The authors speculated that the negative effects on car- costs. Some processors might no longer want to bear cass quality might be due to hypoxia due to the pulmo- these costs, implying that producers that keep submitting nary lesions. consignments with high pleurisy prevalence might be Lung lesions may also cause changes in pH, water hold- penalized in the future. ing capacity, color, flavor, and cooking quality loss of the meat [86]. Permentier et al. [87] showed that the pH val- 8 Impact of CVPC and pleurisy on carcass ues measured at the end of the slaughter line in the loin and meat quality of pigs with more than 25% and less than 5% lung lesions, Pigs affected with lung lesions eat less, and therefore, were 6.01 and 6.20, respectively. This indicates pigs with they do not fully use their genetic potential for muscle lung lesions lead to a higher risk for pale, soft and exu- synthesis and fat accumulation [82, 83]. Paz-Sánchez dative (PSE) traits and quality losses in cooked or dry- et al. [8] observed that pigs without lung lesions had an cured ham. The other meat quality parameters were not Maes et al. Veterinary Research (2023) 54:8 Page 14 of 17 significantly different between pigs with and without lung farmer, the herd veterinarian and other stakeholders. More lesions. research is needed to test and optimize this technology, to Čobanović et al. [88] investigated 625 pigs originating develop it for different (lung) lesions in slaughter pigs and to from 20 small-scale farms and assessed the influence of investigate the feasibility of its reliable implementation in dif- different lung lesions on carcass and meat quality param- ferent slaughterhouse conditions. eters. Pigs with CVPC and pleurisy had the lowest live Cranioventral pulmonary consolidation and pleurisy in weight, hot and cold carcass weight and meatiness. Addi- batches of slaughter pigs have a negative impact on per- tionally, pigs with multiple lesions had lower live and car- formance of the pigs, and the negative effects are more cass weights than pigs affected by a single pathological pronounced with the prevalence and the severity of the condition. Likely, this is due to repartitioning of nutrients lesions. The results however vary between studies and from muscle deposition and bone growth towards tis- farms. This is likely due to differences in study design sues where repair processes are needed (e.g. lung tissue (type of pathogens involved, infection levels, infection affected by pneumonia). patterns, farm characteristics and management, age of In a study of Karabasil et al. [83], pigs with CVPC (pH slaughtering) and methods used to assess the lesions. 6.23) and pleurisy (pH 6.23) had higher average pH in The major economic losses due to these lesions suggest the carcasses at the end of the slaughter line compared that research in developing better control measures is to pigs without lesions (pH 6.14). The percentages of car- warranted and will pay off for the farmer and the entire casses with PSE as well as with DFD (dry, firm and dark) pig sector. In addition to the losses for the farmer, CVPC meat were significantly higher in pigs with CVPC (PSE and pleurisy also decrease carcass and meat quality. 9.7%; DFD 12.6%) or pleurisy (PSE 8.0%; DFD 16.0%) The economic losses in this part of the pork production compared to pigs without lesions (PSE 3.9%; DFD 5.1%). chain have largely been neglected so far, but they can This results in meat with a higher risk for poor processing be tremendous as there is an influence on food quality characteristics, bacterial growth and a reduced shelf life. and safety, and the shelf life of the carcasses. Research Similar findings had been obtained in an earlier small- in quantifying these economic losses and the impact for scale (79 pigs) study [83]. food safety and public health is needed. Given the high prevalence and impact of CVPC and 9 Conclusions and areas for further research pleurisy lesions for the farmer, the slaughterhouse and all Cranioventral pulmonary consolidation and pleurisy stakeholders of the pig sector, monitoring lung lesions of lesions in slaughter pigs are typical for infections with slaughter pigs should be optimized and be implemented M. hyopneumoniae and A. pleuropneumoniae, respec- routinely for as many farms as possible. It is recom- tively, but the lesions are not pathognomonic, and other mended to complement this information with other farm pathogens may cause similar lesions and/or also contrib- data such as clinical scores, antimicrobial use, animal ute to these lesions. To have a better view of the patho- behavior and welfare scores and performance data to gens involved, additional diagnostic testing for infectious obtain a more holistic view of the respiratory health sta- agents and their infection patterns should therefore be tus of the farm. conducted. Attention should be paid to the possible pol- ymicrobial nature of the lesions, the effects of possible Abbreviations immunosuppressive pathogens and the environmental A. pleuropneumoniae  Actinobacillus pleuropneumoniae conditions on the farm. ADG average daily gain The overall prevalence of CVPC and pleurisy in slaughter B. bronchiseptica  Bordetella bronchiseptica CTPA centre technique des productions animales pigs is high and similar to values reported two to four dec- CVPC cranioventral pulmonary consolidation ades ago. Possibly, the extension of the lesions has decreased DFD dry, firm and dark in the last decades. There is also a large variation between the EP enzootic pneumonia FCR feed conversion ratio different studies, and among individual farms. This implies G. parasuis  Glaesserella parasuis that future research should be directed towards the develop- M. hyopneumoniae  Mycoplasma hyopneumoniae ment and implementation of better control measures such M. hyorhinis  Mycoplasma hyorhinis PCV2 porcine circovirus 2 as vaccination strategies, management practices, biosecurity, PEPP pleurisy evaluation of the parietal pleura and biocontainment. PRDC porcine respiratory disease complex Evaluation of CVPC and pleurisy at slaughter is simple, PRRSV porcine reproductive and respiratory syndrome virus PSE pale, soft and exudative fast, and rather easy to conduct, but variation due to abat- SPES slaughterhouse pleurisy evaluation system toir, observer and method might be an issue. Artificial intelligence-based technologies hold great promise to auto- Authors’ contributions DM wrote the paper. All coauthors have critically revised the entire manu- matically score lesions and facilitate useful feedback to the script, each with emphasis on specific parts namely, characterization of Maes et al. Veterinary Research (2023) 54:8 Page 15 of 17 lesions and pathogens involved (MS, MP, FH, JS), prevalence (MS, MP, FH, LG, 9. European Union. 2004. Regulation No. 854/2004. Section II. URL: http://. JS), slaughterhouse examination (MS, MP, LG, JS), scoring systems (MS, JS) and eurlex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2004:139:0206:0320: impact of lesions (MS, MP, FH, LG). The authors have collaborated on the topic EN:PDF, Accessed 6 September 2022 when writing the book Mycoplasmas in Swine (ISBN 978–94-6379–796-2, 10. Gottschalk M, Broes A (2019) Actinobacillosis. In: Zimmerman LA, Karriker Acco Publishers, Leuven Belgium), and/or are collaborating on a joint research AR, Schwartz KJ, Stevenson GW, Jianqiang Z, Jeffrey J (eds) Diseases of project related to porcine respiratory disease. All authors read and approved Swine. John Wiley & Sons Inc, New York, pp 749–766 the final manuscript. 11. Carr J, Sibila M, Segalés J (2020) Mycoplasma hyopneumoniae clinical signs and gross lung lesions, including monitoring. In: Dominiek M, Marina S, Maria P (eds) Book Mycoplasmas in Swine. Acco Publishers, Leuven Declarations Belgium, pp 97–107 12. Kobisch M, Blanchard B, Le Potier MF (1993) Mycoplasma hyopneumoniae Competing interests infection in pigs: Duration of the disease and resistance to reinfection. Vet The authors declare that they have no competing interests. Res 24:67–77 13. Pieters M, Maes D (2019) Mycoplasmosis. Diseases of swine, Chapter 56. Author details In: Diseases of Swine, Eleventh Edition. Edited by Jeffrey J. 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Escobar J, Van Alstine WG, Baker DH, Johnson RW (2004) Decreased • rapid publication on acceptance protein accretion in pigs with viral and bacterial pneumonia is associated • support for research data, including large and complex data types with increased myostatin expression in muscle. J Nutr 134:3047–3053. https://​doi.​org/​10.​1093/​jn/​134.​11.​3047 • gold Open Access which fosters wider collaboration and increased citations 85. Ostanello F, Dottori M, Gusmara C, Leotti G, Sala V (2007) Pneumonia • maximum visibility for your research: over 100M website views per year disease assessment using a slaughterhouse lung-scoring method. J Vet Med A 54:70–75 At BMC, research is always in progress. 86. Dailidavičiene J, Januškevičiene G, Milius J, Mieželiene A, Alenčikiene G (2009) Influence of lung pathology on pig carcasses’ microbiological qual- Learn more biomedcentral.com/submissions ity and sensory parameters. Bull Vet Inst Pulawy 53:433–438