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Investigating the role of free-ranging wild boar (Sus scrofa) in the re-emergence of enzootic pneumonia in domestic pig herds: a pathological, prevalence and risk-factor study.

Batista Linhares M, Belloy L, Origgi FC, Lechner I, Segner H, Ryser-Degiorgis MP - PLoS ONE (2015)

Bottom Line: A control program carried out from 1999 to 2003 successfully reduced disease occurrence in domestic pigs in Switzerland, but recurrent outbreaks suggested a potential role of free-ranging wild boar (Sus scrofa) as a source of re-infection.We have concluded that M. hyopneumoniae is widespread in the Swiss wild boar population, that the same risk factors for infection of domestic pigs also act as risk factors for infection of wild boar, and that infected wild boar develop lesions similar to those found in domestic pigs.However, based on our data and the outbreak pattern in domestic pigs, we propose that spillover from domestic pigs to wild boar is more likely than transmission from wild boar to pigs.

View Article: PubMed Central - PubMed

Affiliation: Centre for Fish and Wildlife Health (FIWI), Vetsuisse Faculty, University of Bern, Bern, Switzerland.

ABSTRACT
Enzootic pneumonia (EP) caused by Mycoplasma hyopneumoniae has a significant economic impact on domestic pig production. A control program carried out from 1999 to 2003 successfully reduced disease occurrence in domestic pigs in Switzerland, but recurrent outbreaks suggested a potential role of free-ranging wild boar (Sus scrofa) as a source of re-infection. Since little is known on the epidemiology of EP in wild boar populations, our aims were: (1) to estimate the prevalence of M. hyopneumoniae infections in wild boar in Switzerland; (2) to identify risk factors for infection in wild boar; and (3) to assess whether infection in wild boar is associated with the same gross and microscopic lesions typical of EP in domestic pigs. Nasal swabs, bronchial swabs and lung samples were collected from 978 wild boar from five study areas in Switzerland between October 2011 and May 2013. Swabs were analyzed by qualitative real time PCR and a histopathological study was conducted on lung tissues. Risk factor analysis was performed using multivariable logistic regression modeling. Overall prevalence in nasal swabs was 26.2% (95% CI 23.3-29.3%) but significant geographical differences were observed. Wild boar density, occurrence of EP outbreaks in domestic pigs and young age were identified as risk factors for infection. There was a significant association between infection and lesions consistent with EP in domestic pigs. We have concluded that M. hyopneumoniae is widespread in the Swiss wild boar population, that the same risk factors for infection of domestic pigs also act as risk factors for infection of wild boar, and that infected wild boar develop lesions similar to those found in domestic pigs. However, based on our data and the outbreak pattern in domestic pigs, we propose that spillover from domestic pigs to wild boar is more likely than transmission from wild boar to pigs.

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Histological lesions associated with Mycoplasma hyopneumoniae infection and their distribution in wild boar lungs.A: Lung without macroscopic enzootic pneumonia-like lesions (MaEPL) with moderate multifocal BALT hyperplasia along a bronchiole (measurement bar = 500nm). B: Lung with early type MaEPL and mild to moderate multifocal BALT hyperplasia (black arrow) and diffuse moderate thickening of the interalveolar septa (broncho-interstitial pneumonia). Marginal subpleural atelectasis is considered an artefact (measurement bar = 50mm). C: Lung with early type MaEPL and severe infiltration of mononuclear cells expanding the interlobular septum (thick black arrow) and compressing the regional airways. A discrete hyperplastic lymphoid follicle is also present (thin black arrow, measurement bar = 2mm). D: Lung with late type MaEPL and moderate to severe multifocal BALT hyperplasia (thick arrows), moderate infiltration of the submucosa of the airways (thin black arrow) and mild to moderate multifocal thickening of the interalveolar septa by infiltrating inflammatory cells (measurement bar = 500nm). E: Magnification (20x) of the framed area in D (inset). Intraluminal collection of neutrophils (thin black arrows, measurement bar = 20μm). F: Lung with late type MaEPL and diffuse intraalveolar collection of amorphous eosinophilic material (edema, black arrows) with mild to moderate multifocal lympho-plasmacytic clusters in the interstitium (black circles). Few numbers of mononuclear cells are also observed in the alveolar spaces along with free erythrocytes (hemorrhages, gunshot-related, measurement bar = 20μm).
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pone.0119060.g005: Histological lesions associated with Mycoplasma hyopneumoniae infection and their distribution in wild boar lungs.A: Lung without macroscopic enzootic pneumonia-like lesions (MaEPL) with moderate multifocal BALT hyperplasia along a bronchiole (measurement bar = 500nm). B: Lung with early type MaEPL and mild to moderate multifocal BALT hyperplasia (black arrow) and diffuse moderate thickening of the interalveolar septa (broncho-interstitial pneumonia). Marginal subpleural atelectasis is considered an artefact (measurement bar = 50mm). C: Lung with early type MaEPL and severe infiltration of mononuclear cells expanding the interlobular septum (thick black arrow) and compressing the regional airways. A discrete hyperplastic lymphoid follicle is also present (thin black arrow, measurement bar = 2mm). D: Lung with late type MaEPL and moderate to severe multifocal BALT hyperplasia (thick arrows), moderate infiltration of the submucosa of the airways (thin black arrow) and mild to moderate multifocal thickening of the interalveolar septa by infiltrating inflammatory cells (measurement bar = 500nm). E: Magnification (20x) of the framed area in D (inset). Intraluminal collection of neutrophils (thin black arrows, measurement bar = 20μm). F: Lung with late type MaEPL and diffuse intraalveolar collection of amorphous eosinophilic material (edema, black arrows) with mild to moderate multifocal lympho-plasmacytic clusters in the interstitium (black circles). Few numbers of mononuclear cells are also observed in the alveolar spaces along with free erythrocytes (hemorrhages, gunshot-related, measurement bar = 20μm).

Mentions: Histological observations are summarized in Table 4. Six of 14 selected histopathological features were significantly associated with a positive PCR reaction for Mhyop in bronchial swabs; the most frequently observed was BALT hyperplasia together with lymphoid follicle activation (p-value = 0.0136), followed by plasma cell clusters in the interstitium (p-values < 0.0001), neutrophilic infiltration of the bronchi and bronchioles (both the lumen and the airway wall, p-value < 0.0001), intra-alveolar edema (p-value = 0.0124) and neutrophilic infiltration of the alveolar parenchyma and/or the interstitium (p-value = 0.0084). Additionally, scattered interstitial histiocytes and lymphocytes were commonly observed, tending to be more frequent in PCR-positive than PCR-negative lungs (p-value ≥ 0.161). Histological features associated with PCR-positive results were found in animals with MaEPL as well as without, but their frequency and/or severity generally increased with the chronicity of MaEPL (Table 5, Fig. 5).


Investigating the role of free-ranging wild boar (Sus scrofa) in the re-emergence of enzootic pneumonia in domestic pig herds: a pathological, prevalence and risk-factor study.

Batista Linhares M, Belloy L, Origgi FC, Lechner I, Segner H, Ryser-Degiorgis MP - PLoS ONE (2015)

Histological lesions associated with Mycoplasma hyopneumoniae infection and their distribution in wild boar lungs.A: Lung without macroscopic enzootic pneumonia-like lesions (MaEPL) with moderate multifocal BALT hyperplasia along a bronchiole (measurement bar = 500nm). B: Lung with early type MaEPL and mild to moderate multifocal BALT hyperplasia (black arrow) and diffuse moderate thickening of the interalveolar septa (broncho-interstitial pneumonia). Marginal subpleural atelectasis is considered an artefact (measurement bar = 50mm). C: Lung with early type MaEPL and severe infiltration of mononuclear cells expanding the interlobular septum (thick black arrow) and compressing the regional airways. A discrete hyperplastic lymphoid follicle is also present (thin black arrow, measurement bar = 2mm). D: Lung with late type MaEPL and moderate to severe multifocal BALT hyperplasia (thick arrows), moderate infiltration of the submucosa of the airways (thin black arrow) and mild to moderate multifocal thickening of the interalveolar septa by infiltrating inflammatory cells (measurement bar = 500nm). E: Magnification (20x) of the framed area in D (inset). Intraluminal collection of neutrophils (thin black arrows, measurement bar = 20μm). F: Lung with late type MaEPL and diffuse intraalveolar collection of amorphous eosinophilic material (edema, black arrows) with mild to moderate multifocal lympho-plasmacytic clusters in the interstitium (black circles). Few numbers of mononuclear cells are also observed in the alveolar spaces along with free erythrocytes (hemorrhages, gunshot-related, measurement bar = 20μm).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4352045&req=5

pone.0119060.g005: Histological lesions associated with Mycoplasma hyopneumoniae infection and their distribution in wild boar lungs.A: Lung without macroscopic enzootic pneumonia-like lesions (MaEPL) with moderate multifocal BALT hyperplasia along a bronchiole (measurement bar = 500nm). B: Lung with early type MaEPL and mild to moderate multifocal BALT hyperplasia (black arrow) and diffuse moderate thickening of the interalveolar septa (broncho-interstitial pneumonia). Marginal subpleural atelectasis is considered an artefact (measurement bar = 50mm). C: Lung with early type MaEPL and severe infiltration of mononuclear cells expanding the interlobular septum (thick black arrow) and compressing the regional airways. A discrete hyperplastic lymphoid follicle is also present (thin black arrow, measurement bar = 2mm). D: Lung with late type MaEPL and moderate to severe multifocal BALT hyperplasia (thick arrows), moderate infiltration of the submucosa of the airways (thin black arrow) and mild to moderate multifocal thickening of the interalveolar septa by infiltrating inflammatory cells (measurement bar = 500nm). E: Magnification (20x) of the framed area in D (inset). Intraluminal collection of neutrophils (thin black arrows, measurement bar = 20μm). F: Lung with late type MaEPL and diffuse intraalveolar collection of amorphous eosinophilic material (edema, black arrows) with mild to moderate multifocal lympho-plasmacytic clusters in the interstitium (black circles). Few numbers of mononuclear cells are also observed in the alveolar spaces along with free erythrocytes (hemorrhages, gunshot-related, measurement bar = 20μm).
Mentions: Histological observations are summarized in Table 4. Six of 14 selected histopathological features were significantly associated with a positive PCR reaction for Mhyop in bronchial swabs; the most frequently observed was BALT hyperplasia together with lymphoid follicle activation (p-value = 0.0136), followed by plasma cell clusters in the interstitium (p-values < 0.0001), neutrophilic infiltration of the bronchi and bronchioles (both the lumen and the airway wall, p-value < 0.0001), intra-alveolar edema (p-value = 0.0124) and neutrophilic infiltration of the alveolar parenchyma and/or the interstitium (p-value = 0.0084). Additionally, scattered interstitial histiocytes and lymphocytes were commonly observed, tending to be more frequent in PCR-positive than PCR-negative lungs (p-value ≥ 0.161). Histological features associated with PCR-positive results were found in animals with MaEPL as well as without, but their frequency and/or severity generally increased with the chronicity of MaEPL (Table 5, Fig. 5).

Bottom Line: A control program carried out from 1999 to 2003 successfully reduced disease occurrence in domestic pigs in Switzerland, but recurrent outbreaks suggested a potential role of free-ranging wild boar (Sus scrofa) as a source of re-infection.We have concluded that M. hyopneumoniae is widespread in the Swiss wild boar population, that the same risk factors for infection of domestic pigs also act as risk factors for infection of wild boar, and that infected wild boar develop lesions similar to those found in domestic pigs.However, based on our data and the outbreak pattern in domestic pigs, we propose that spillover from domestic pigs to wild boar is more likely than transmission from wild boar to pigs.

View Article: PubMed Central - PubMed

Affiliation: Centre for Fish and Wildlife Health (FIWI), Vetsuisse Faculty, University of Bern, Bern, Switzerland.

ABSTRACT
Enzootic pneumonia (EP) caused by Mycoplasma hyopneumoniae has a significant economic impact on domestic pig production. A control program carried out from 1999 to 2003 successfully reduced disease occurrence in domestic pigs in Switzerland, but recurrent outbreaks suggested a potential role of free-ranging wild boar (Sus scrofa) as a source of re-infection. Since little is known on the epidemiology of EP in wild boar populations, our aims were: (1) to estimate the prevalence of M. hyopneumoniae infections in wild boar in Switzerland; (2) to identify risk factors for infection in wild boar; and (3) to assess whether infection in wild boar is associated with the same gross and microscopic lesions typical of EP in domestic pigs. Nasal swabs, bronchial swabs and lung samples were collected from 978 wild boar from five study areas in Switzerland between October 2011 and May 2013. Swabs were analyzed by qualitative real time PCR and a histopathological study was conducted on lung tissues. Risk factor analysis was performed using multivariable logistic regression modeling. Overall prevalence in nasal swabs was 26.2% (95% CI 23.3-29.3%) but significant geographical differences were observed. Wild boar density, occurrence of EP outbreaks in domestic pigs and young age were identified as risk factors for infection. There was a significant association between infection and lesions consistent with EP in domestic pigs. We have concluded that M. hyopneumoniae is widespread in the Swiss wild boar population, that the same risk factors for infection of domestic pigs also act as risk factors for infection of wild boar, and that infected wild boar develop lesions similar to those found in domestic pigs. However, based on our data and the outbreak pattern in domestic pigs, we propose that spillover from domestic pigs to wild boar is more likely than transmission from wild boar to pigs.

Show MeSH
Related in: MedlinePlus