The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs

Karen Elisabeth Sørensen; Kerstin Skovgaard; Peter M. H. Heegaard; Henrik Elvang Jensen; Ole Lerberg Nielsen; Páll S. Leifsson; Helle Gerda Olsen; Bent Aalbæk; Annemarie Thuri Kristensen; Mads Kjelgaard-Hansen; Bo Wiinberg; Tine Moesgaard Iburg

doi:10.1177/0300985812439726

The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs

Karen Elisabeth Sørensen, Kerstin Skovgaard, Peter M. H. Heegaard, Henrik Elvang Jensen, Ole Lerberg Nielsen, Páll S. Leifsson, Helle Gerda Olsen, Bent Aalbæk, Annemarie Thuri Kristensen, Mads Kjelgaard-Hansen, Bo Wiinberg, Tine Moesgaard Iburg

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Abstract

Acute respiratory distress syndrome is a common complication in severe sepsis. In pigs, the lungs play an important role in clearing systemic bacterial infections due to pulmonary intravascular macrophages found specifically in pigs. However, this increases the exposure of the porcine lungs to pathogens and potential injury. The authors propose that increasing the concentration of the inoculum without changing the bacterial dose will lead to severe sepsis with pronounced pulmonary lesions. This could potentially create a risk of cytokine spillover to the circulation, leading to an increased systemic response. Eight Danish Landrace pigs, approximately 10 weeks old, were inoculated twice with a low or once with a high concentration of Staphylococcus aureus. Three pigs were sham-inoculated. The animals were grouped based on macro- and microscopic lung lesions. The mRNA expression of local pulmonary inflammatory markers was compared to protein levels of systemic inflammatory markers. The most severe pulmonary lesions were observed in animals receiving the high S. aureus concentration, indicating that severity of lesions is dependent on inoculum concentration rather than total numbers of bacteria. Furthermore, local mRNA expression of inflammatory cytokines appeared to be dependent on the magnitude and severity of tissue destruction, including the ability to confine the lesions. Increasing mRNA levels of serum amyloid A could be a confident marker of severity of pulmonary lesions. Since no correlation was observed between local and systemic levels of inflammatory cytokines, this finding could indicate an ability of the porcine lung to compartmentalize the local inflammatory response and thus restrict systemic contribution.

Originalsprog	Engelsk
Tidsskrift	Veterinary Pathology
Vol/bind	49
Udgave nummer	6
Sider (fra-til)	950-962
Antal sider	13
ISSN	0300-9858
DOI	https://doi.org/10.1177/0300985812439726
Status	Udgivet - nov. 2012

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10.1177/0300985812439726

Veterinary Pathology 2012 Soerensen 1Indsendt manuskript, 970 KB

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Sørensen, K. E., Skovgaard, K., Heegaard, P. M. H., Jensen, H. E., Nielsen, O. L., Leifsson, P. S., Olsen, H. G., Aalbæk, B., Kristensen, A. T., Kjelgaard-Hansen, M., Wiinberg, B., & Iburg, T. M. (2012). The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs. Veterinary Pathology, 49(6), 950-962. https://doi.org/10.1177/0300985812439726

The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs. / Sørensen, Karen Elisabeth; Skovgaard, Kerstin; Heegaard, Peter M. H. et al.
I: Veterinary Pathology, Bind 49, Nr. 6, 11.2012, s. 950-962.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

Sørensen, KE, Skovgaard, K, Heegaard, PMH, Jensen, HE , Nielsen, OL , Leifsson, PS, Olsen, HG, Aalbæk, B , Kristensen, AT , Kjelgaard-Hansen, M , Wiinberg, B & Iburg, TM 2012, 'The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs', Veterinary Pathology, bind 49, nr. 6, s. 950-962. https://doi.org/10.1177/0300985812439726

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title = "The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs",

abstract = "Acute respiratory distress syndrome is a common complication in severe sepsis. In pigs, the lungs play an important role in clearing systemic bacterial infections due to pulmonary intravascular macrophages found specifically in pigs. However, this increases the exposure of the porcine lungs to pathogens and potential injury. The authors propose that increasing the concentration of the inoculum without changing the bacterial dose will lead to severe sepsis with pronounced pulmonary lesions. This could potentially create a risk of cytokine spillover to the circulation, leading to an increased systemic response. Eight Danish Landrace pigs, approximately 10 weeks old, were inoculated twice with a low or once with a high concentration of Staphylococcus aureus. Three pigs were sham-inoculated. The animals were grouped based on macro- and microscopic lung lesions. The mRNA expression of local pulmonary inflammatory markers was compared to protein levels of systemic inflammatory markers. The most severe pulmonary lesions were observed in animals receiving the high S. aureus concentration, indicating that severity of lesions is dependent on inoculum concentration rather than total numbers of bacteria. Furthermore, local mRNA expression of inflammatory cytokines appeared to be dependent on the magnitude and severity of tissue destruction, including the ability to confine the lesions. Increasing mRNA levels of serum amyloid A could be a confident marker of severity of pulmonary lesions. Since no correlation was observed between local and systemic levels of inflammatory cytokines, this finding could indicate an ability of the porcine lung to compartmentalize the local inflammatory response and thus restrict systemic contribution.",

author = "S{\o}rensen, {Karen Elisabeth} and Kerstin Skovgaard and Heegaard, {Peter M. H.} and Jensen, {Henrik Elvang} and Nielsen, {Ole Lerberg} and Leifsson, {P{\'a}ll S.} and Olsen, {Helle Gerda} and Bent Aalb{\ae}k and Kristensen, {Annemarie Thuri} and Mads Kjelgaard-Hansen and Bo Wiinberg and Iburg, {Tine Moesgaard}",

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AU - Sørensen, Karen Elisabeth

AU - Skovgaard, Kerstin

AU - Heegaard, Peter M. H.

AU - Jensen, Henrik Elvang

AU - Nielsen, Ole Lerberg

AU - Leifsson, Páll S.

AU - Olsen, Helle Gerda

AU - Aalbæk, Bent

AU - Kristensen, Annemarie Thuri

AU - Kjelgaard-Hansen, Mads

AU - Wiinberg, Bo

AU - Iburg, Tine Moesgaard

PY - 2012/11

Y1 - 2012/11

N2 - Acute respiratory distress syndrome is a common complication in severe sepsis. In pigs, the lungs play an important role in clearing systemic bacterial infections due to pulmonary intravascular macrophages found specifically in pigs. However, this increases the exposure of the porcine lungs to pathogens and potential injury. The authors propose that increasing the concentration of the inoculum without changing the bacterial dose will lead to severe sepsis with pronounced pulmonary lesions. This could potentially create a risk of cytokine spillover to the circulation, leading to an increased systemic response. Eight Danish Landrace pigs, approximately 10 weeks old, were inoculated twice with a low or once with a high concentration of Staphylococcus aureus. Three pigs were sham-inoculated. The animals were grouped based on macro- and microscopic lung lesions. The mRNA expression of local pulmonary inflammatory markers was compared to protein levels of systemic inflammatory markers. The most severe pulmonary lesions were observed in animals receiving the high S. aureus concentration, indicating that severity of lesions is dependent on inoculum concentration rather than total numbers of bacteria. Furthermore, local mRNA expression of inflammatory cytokines appeared to be dependent on the magnitude and severity of tissue destruction, including the ability to confine the lesions. Increasing mRNA levels of serum amyloid A could be a confident marker of severity of pulmonary lesions. Since no correlation was observed between local and systemic levels of inflammatory cytokines, this finding could indicate an ability of the porcine lung to compartmentalize the local inflammatory response and thus restrict systemic contribution.

AB - Acute respiratory distress syndrome is a common complication in severe sepsis. In pigs, the lungs play an important role in clearing systemic bacterial infections due to pulmonary intravascular macrophages found specifically in pigs. However, this increases the exposure of the porcine lungs to pathogens and potential injury. The authors propose that increasing the concentration of the inoculum without changing the bacterial dose will lead to severe sepsis with pronounced pulmonary lesions. This could potentially create a risk of cytokine spillover to the circulation, leading to an increased systemic response. Eight Danish Landrace pigs, approximately 10 weeks old, were inoculated twice with a low or once with a high concentration of Staphylococcus aureus. Three pigs were sham-inoculated. The animals were grouped based on macro- and microscopic lung lesions. The mRNA expression of local pulmonary inflammatory markers was compared to protein levels of systemic inflammatory markers. The most severe pulmonary lesions were observed in animals receiving the high S. aureus concentration, indicating that severity of lesions is dependent on inoculum concentration rather than total numbers of bacteria. Furthermore, local mRNA expression of inflammatory cytokines appeared to be dependent on the magnitude and severity of tissue destruction, including the ability to confine the lesions. Increasing mRNA levels of serum amyloid A could be a confident marker of severity of pulmonary lesions. Since no correlation was observed between local and systemic levels of inflammatory cytokines, this finding could indicate an ability of the porcine lung to compartmentalize the local inflammatory response and thus restrict systemic contribution.

U2 - 10.1177/0300985812439726

DO - 10.1177/0300985812439726

M3 - Journal article

C2 - 22461225

SN - 0300-9858

VL - 49

SP - 950

EP - 962

JO - Veterinary Pathology

JF - Veterinary Pathology

IS - 6

ER -

The impact of Staphylococcus aureus concentration on the development of pulmonary lesions and cytokine expression after intravenous inoculation of pigs

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