Detection of infectious agents in lungs of slaughtered pigs in association with cranioventral pulmonary consolidation

Respiratory diseases significantly impact swine production worldwide, contributing to economic losses due to reduced growth performance, increased treatment costs and higher mortality rates (22, 23). The aetiology of these diseases is often multifactorial, involving complex interactions between bacterial and viral pathogens, environmental conditions and host immunity (28, 37). One of the most prevalent respiratory syndromes affecting pigs is porcine respiratory disease complex (PRDC), characterised by polymicrobial infections leading to chronic lung lesions and decreased growth (31, 35).

Abattoir evaluation of lung lesions is essential for assessing respiratory disease prevalence and severity in swine herds. It aids in detecting subclinical conditions, evaluating risk factors and assessing vaccine efficacy (4, 9, 15). The methods applied to abattoir porcine lung samples are non-invasive and cost-effective, and enable the evaluation of a representative sample of animals within a relatively short time frame (21, 25, 34). Cranioventral pulmonary consolidation (CVPC) is among the most common gross lung lesions observed in slaughtered pigs, and is often associated with infections caused by bacterial and viral agents (10, 25). The presence and severity of CVPC lesions can serve as indicators of herd health status, and signal both past and ongoing respiratory infections (21). Lung lesion scoring at slaughter also proves valuable in the evaluation of the effectiveness of respiratory disease control programmes, as well as productivity and economic efficiency in commercial swine herds, which explains its frequent implementation (30, 33). However, establishing a clear association between the activity of individual pathogens or their combinations and the prevalence and severity of lung lesions remains challenging. Research has been conducted, and several publications are available on this topic (2, 5, 12, 18, 35). However, because of the diversity of pathogens causing PRDC, knowledge in this area remains insufficient.

The objectives of this study were to evaluate the prevalence of CVPC lesions in slaughtered pigs from commercial farms in western Poland and to investigate the association between these lesions and the presence of selected respiratory pathogens. Molecular diagnostic techniques were used to identify key bacterial and viral agents involved in lung pathology, and the identifications made enhance the understanding of the epidemiology of respiratory infections in swine and support the development of effective control measures.

Cranioventral pulmonary consolidations are among the most commonly observed lung lesions in pigs post slaughter (22). Their occurrence is associated with significant economic losses in pig farms (23). Moreover, CVPC lesions alone cause about 50% of lung rejections after slaughter, significantly impacting processing efficiency (33).

The results of this study confirm that CVPC lesions are highly prevalent on commercial pig farms. In our study, such lesions were observed in pigs from all investigated herds with a prevalence of 79.3%, and their prevalence corresponded well with that of 85.16% in lungs previously observed by Przyborowska et al. (33) in Wielkopolskie voivodeship. However, on a national scale, the occurrence of such changes was lower and ranged between 24 and 58% (33, 34). The difference may be a consequence of the higher density of pig production in the Wielkopolskie voivodeship. It was reported that the greater the concentration of production, the greater the risk for respiratory disease in pigs (38). The CVPC results may also be influenced by the sample size, i.e., the number of herds from which the pigs were sourced, as well as by the cross-sectional rather than longitudinal nature of the study, which may be relevant given the seasonal occurrence of lung lesions (45). The prevalence of CVPC lesions varied significantly across different countries worldwide. The lowest percentage of affected pigs was reported in New Zealand (27), while the highest was observed in Brazil (9). There are European countries where CVPC lesions are only sporadically noted. These are the countries where MHP has been practically eradicated (21). In other European countries, the percentage of lungs with CVPC lesions ranged from 24% in Belgium and 27% in the UK to 72% in France and 73% in Germany (4, 17, 19, 25).

Naturally, CVPC is associated with MHP infections in pigs and these lung changes are sometimes referred to as Mycoplasma-like lesions or enzootic pneumonia-like lesions (10, 30). On the other hand, it has been demonstrated that such lung lesions are not pathognomonic for MHP infection (22). Similar changes are also observed in the course of other bacterial and viral diseases, such as infections with swIAV (32). The possibility that such lesions may be caused by bacterial pathogens other than MHP is further supported by studies showing that 59% of lungs from slaughtered pigs originating from MHP-free farms exhibited mild CVPC lesions affecting less than 10% of lung tissue (19). The development of mild CVPC lesions may also be related to the action of non-infectious factors such as inhalation of ammonia or dust (11).

Whether at the herd level or the individual animal level, MHP was the most commonly occurring pathogen. Similar results were obtained in previous studies conducted in France, Germany and Belgium (5, 19, 26). As noted by Maes et al. (22), the prevalence of CVPC lesions has remained unchanged over the years despite advancements in control methods, including new vaccines and improved biosecurity measures. The present investigation’s high prevalence of MHP observed in lung samples from fattening pigs, despite the widespread implementation of immunoprophylactic programmes targeting this pathogen in the studied herds, suggested that vaccination had not eliminated the pathogen nor prevented its transmission between animals. This conclusion is supported by previous studies which found that vaccination against MHP reduced but did not completely eliminate pathogen circulation and transmission at the farm level (21). Vaccination was shown to alleviate clinical symptoms, decrease the severity of lung lesions and reduce macrophage infiltration in the bronchus-associated lymphoid tissue region (46).

The high percentage of lungs in which MHP was detected in our study closely corresponds with the percentage of lungs showing CVPC lesions. We found that the presence of MHP in the lungs of the examined pigs was associated with a higher frequency of CVPC lesions and a higher lesion score. Our findings aligned with previous studies that clearly suggested a link between the presence of MHP in pig lungs and the occurrence of anatomopathological lesions (7, 31). However, respiratory disease in pigs was often polymicrobial and multifactorial in nature (28). The presence of multiple pathogens or co-infections could prolong disease duration and exacerbate its severity (37). The interactions between respiratory pathogens in swine infections were described as highly complex, with mechanisms of action that may be additive or synergistic (41). For instance, prior infection with swIVA could have promoted MHP colonisation in the respiratory tract (31). Additionally, co-infection with MHP and PRRSV could have aggravated clinical severity by compromising immune responses and facilitating secondary bacterial infections, such as those caused by APP or Pasteurella multocida (35).

In our study, the simultaneous presence of multiple pathogens was frequently detected at both the herd and individual animal levels. Notably, only about 12% of lung samples contained a single pathogen, reinforcing the widely accepted notion that co-infections are a key factor contributing to lung lesions in pigs. These findings are consistent with previous research (2, 35). Our results demonstrated that the presence of multiple pathogenic microorganisms at both the herd and individual levels correlated with increased severity of lung lesions. The observed correlation between pathogen detection and CVPC supported the findings of other studies, which demonstrated that increased pathogen load was often associated with more extensive lung damage (44). Studies in Belgium and Italy similarly demonstrated that pigs harbouring three or more respiratory pathogens exhibited significantly more severe lesions than those infected with only one or two agents (21, 25).

Additionally, we confirmed that PRRSV1 and MHR played a significant role in the development of CVPC lesions in pigs. Porcine reproductive and respiratory virus 1, in particular, facilitated secondary bacterial infections, such as those caused by Pasteurella multocida and STREP (35). Although CVPC lesions have been sporadically reported as a consequence of PRRSV1 infection, they are not considered a characteristic feature of this virus (36). The precise role of MHR in CVPC development remains unclear. In several studies it was found that lung lesions typical for MHP infections could also be provoked by infection with MHR without involvement of MHP (1). Contrastingly, Luehrs et al. (19) suggested that MHR alone did not induce lung lesions resembling those observed in MHP infections in fattening pigs. Other studies also indicated that MHR did not act as a primary causative agent but instead exacerbated disease progression initiated by MHP (6). In our study, MHR was detected exclusively in co-infections with other pathogens. In the vast majority of cases, this included co-infection with MHP. Only in one case, in a lung where no lesions were found, was MHR detected together with GLAS without the involvement of MHP.

Our findings also revealed that co-infection with GLAS, MHP, PRRSV1 and PCV3 was associated with more severe lesions in the lungs than infections with MHP alone. This is consistent with previous reports highlighting the role of bacterial-viral co-infections, particularly those involving MHP and PRRSV, in the progression of respiratory disease in pigs (37). Furthermore, PCV3, a relatively recently discovered virus, was implicated in the exacerbation of PRDC (14).

Importantly, our study found that the mere presence of circovirus in lung tissue was insufficient to induce CVPC lesions. Pigs infected solely with PCV2 or coinfected with PCV2, PCV3 and/or GLAS exhibited less pronounced lung lesions than those infected with MHP alone. This aligns with recent insights into PCV2 infections, which demoted "PCV2 lung disease" from being a distinct diagnostic entity and considered it a component of PCV2 systemic disease or PRDC (39). Additionally, PCV2 was recognised as a contributing factor in PRDC, particularly in the context of co-infections with PRRSV (3). However, experimental coinoculation of PCV2 and MHP did not lead to a synergistic exacerbation of the clinical symptoms or lung lesions associated with either pathogen (40).

In this study, we focused on the relationship between the occurrence of CVPC lesions and the presence of selected respiratory pathogens in the lungs of slaughtered pigs. We acknowledge that our chosen method, based on detecting the genetic material of pathogenic microorganisms in lung samples, may not provide a complete picture. The lungs were previously considered sterile; however, current research indicated that their microbiota closely resembled the oral microbiota (18). Sphingobium was among the genera in heaviest presence in both healthy and lesioned lungs, but Methylotenera, Prevotella and Lactobacillus were the other predominant genera in the microbiota of healthy lungs, whereas Mycoplasma, Ureaplasma, Haemophilus and Phyllobacterium joined Sphingobium as the predominant microbial communities in lungs exhibiting severe lesions (12). A limitation of this study is its reliance on PCR detection of pathogen DNA/RNA, which does not distinguish between active infection and residual genetic material. However, detecting antibodies instead and linking their presence to lung lesions in pigs would have been much more challenging because of the potential detection of vaccine-induced antibodies or antibodies from past infections that no longer result in visible lung lesions. Future research should incorporate histopathological analysis and bacterial culture to confirm infection status.

This study reinforced the complexity of respiratory infections in pigs, emphasising the need for comprehensive disease control strategies that address both primary and secondary pathogens. At the same time, these findings confirm the primary role of MHP in the development of CVPC lesions in pigs. Further investigations into co-infection dynamics and intervention efficacy will be essential for improving swine health and productivity.