Modeling sepsis, with a special focus on large animal models of porcine peritonitis and bacteremia

. 2022 ; 13 () : 1094199. [epub] 20230110

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid36703923

Infectious diseases, which often result in deadly sepsis or septic shock, represent a major global health problem. For understanding the pathophysiology of sepsis and developing new treatment strategies, reliable and clinically relevant animal models of the disease are necessary. In this review, two large animal (porcine) models of sepsis induced by either peritonitis or bacteremia are introduced and their strong and weak points are discussed in the context of clinical relevance and other animal models of sepsis, with a special focus on cardiovascular and immune systems, experimental design, and monitoring. Especially for testing new therapeutic strategies, the large animal (porcine) models represent a more clinically relevant alternative to small animal models, and the findings obtained in small animal (transgenic) models should be verified in these clinically relevant large animal models before translation to the clinical level.

Zobrazit více v PubMed

Al-Obeidallah M., Jarkovská D., Valešová L., Horák J., Jedlička J., Nalos L., et al. (2021). SOFA score, hemodynamics and body temperature allow early discrimination between porcine peritonitis-induced sepsis and peritonitis-induced septic shock. J. Pers. Med. 11, 164. 10.3390/jpm11030164 PubMed DOI PMC

Alverdy J. C., Keskey R., Thewissen R. (2020). Can the cecal ligation and puncture model Be repurposed to better inform therapy in human sepsis? Infect. Immun. 88, 009422-19. 10.1128/IAI.00942-19 PubMed DOI PMC

Bailey J. D., Diotallevi M., Nicol T., McNeill E., Shaw A., Chuaiphichai S., et al. (2019). Nitric oxide modulates metabolic remodeling in inflammatory macrophages through TCA cycle regulation and itaconate accumulation. Cell. Rep. 28, 218–230. e7. 10.1016/j.celrep.2019.06.018 PubMed DOI PMC

Balls M. (2022). Alternatives to laboratory animals: Trends in replacement and the three rs. Altern. Lab. Anim. 50, 10–26. 10.1177/02611929221082250 PubMed DOI

Basas J., Palau M., Ratia C., Del Pozo J. L., Martín-Gómez M. T., Gomis X., et al. (2018). High-dose daptomycin is effective as an antibiotic lock therapy in a rabbit model of Staphylococcus epidermidis catheter-related infection. Antimicrob. Agents Chemother. 62, 017777-17. 10.1128/AAC.01777-17 PubMed DOI PMC

Benes J., Chvojka J., Sykora R., Radej J., Krouzecky A., Novak I., et al. (2011). Searching for mechanisms that matter in early septic acute kidney injury: An experimental study. Crit. Care 15, R256. 10.1186/cc10517 PubMed DOI PMC

Bergman E. N. (1990). Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 70, 567–590. 10.1152/physrev.1990.70.2.567 PubMed DOI

Bhavani S. V., Semler M., Qian E. T., Verhoef P. A., Robichaux C., Churpek M. M., et al. (2022). Development and validation of novel sepsis subphenotypes using trajectories of vital signs. Intensive Care Med. 48, 1582–1592. 10.1007/s00134-022-06890-z PubMed DOI PMC

Brook B., Harbeson D., Amenyogbe N., Ben-Othman R., Kollmann T. R., Aniba R. (2019). Robust health-score based survival prediction for a neonatal mouse model of polymicrobial sepsis. PLoS One 14, e0218714. 10.1371/journal.pone.0218714 PubMed DOI PMC

Brooks G. A. (2020). The tortuous path of lactate shuttle discovery: From cinders and boards to the lab and ICU. J. Sport Health Sci. 9, 446–460. 10.1016/j.jshs.2020.02.006 PubMed DOI PMC

Cai S., Paudel S., Jin L., Ghimire L., Taylor C. M., Wakamatsu N., et al. (2021). NLRP6 modulates neutrophil homeostasis in bacterial pneumonia-derived sepsis. Mucosal Immunol. 14, 574–584. 10.1038/s41385-020-00357-4 PubMed DOI PMC

Cavaillon J. M. (2018). Exotoxins and endotoxins: Inducers of inflammatory cytokines. Toxicon 149, 45–53. 10.1016/j.toxicon.2017.10.016 PubMed DOI

Cazorla O., Freiburg A., Helmes M., Centner T., McNabb M., Wu Y., et al. (2000). Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ. Res. 86, 59–67. 10.1161/01.res.86.1.59 PubMed DOI

Chalupova M., Horak J., Kramna L., Nalos L., Stengl M., Chudejova K., et al. (2022). Gut microbiome diversity of porcine peritonitis model of sepsis. Sci. Rep. 12, 17430. 10.1038/s41598-022-21079-6 PubMed DOI PMC

Chung C. S., Bogomolovas J., Gasch A., Hidalgo C. G., Labeit S., Granzier H. L. (2011). Titin-actin interaction: PEVK-actin-based viscosity in a large animal. J. Biomed. Biotechnol. 2011, 310791. 10.1155/2011/310791 PubMed DOI PMC

Coutinho M. L., Matsunaga J., Wang L.-C., de la Peña Moctezuma A., Lewis M. S., Babbitt J. T., et al. (2014). Kinetics of leptospira interrogans infection in hamsters after intradermal and subcutaneous challenge. PLoS Negl. Trop. Dis. 8, e3307. 10.1371/journal.pntd.0003307 PubMed DOI PMC

Dawson H. D., Lunney J. K. (2018). Porcine cluster of differentiation (CD) markers 2018 update. Res. Vet. Sci. 118, 199–246. 10.1016/j.rvsc.2018.02.007 PubMed DOI

DeMerle K. M., Angus D. C., Baillie J. K., Brant E., Calfee C. S., Carcillo J., et al. (2021). Sepsis subclasses: A framework for development and interpretation. Crit. Care Med. 49, 748–759. 10.1097/CCM.0000000000004842 PubMed DOI PMC

Durosier L. D., Herry C. L., Cortes M., Cao M., Burns P., Desrochers A., et al. (2015). Does heart rate variability reflect the systemic inflammatory response in a fetal sheep model of lipopolysaccharide-induced sepsis? Physiol. Meas. 36, 2089–2102. 10.1088/0967-3334/36/10/2089 PubMed DOI PMC

Fairbairn L., Kapetanovic R., Sester D. P., Hume D. A. (2011). The mononuclear phagocyte system of the pig as a model for understanding human innate immunity and disease. J. Leukoc. Biol. 89, 855–871. 10.1189/jlb.1110607 PubMed DOI

Fink M. P., Heard S. O. (1990). Laboratory models of sepsis and septic shock. J. Surg. Res. 49, 186–196. 10.1016/0022-4804(90)90260-9 PubMed DOI

Fleischmann C., Scherag A., Adhikari N. K. J., Hartog C. S., Tsaganos T., Schlattmann P., et al. (2016). Assessment of global incidence and mortality of hospital-treated sepsis. Current estimates and limitations. Am. J. Respir. Crit. Care Med. 193, 259–272. 10.1164/rccm.201504-0781OC PubMed DOI

Ghanta S., Kwon M.-Y., Perrella M. A. (2021). Induction of sepsis via fibrin clot implantation. Methods Mol. Biol. 2321, 17–25. 10.1007/978-1-0716-1488-4_3 PubMed DOI

Gibot S. (2012). On the origins of lactate during sepsis. Crit. Care 16, 151. 10.1186/cc11472 PubMed DOI PMC

Granfeldt A., Letson H. L., Dobson G. P., Shi W., Vinten-Johansen J., Tønnesen E. (2014). Adenosine, lidocaine and Mg2+ improves cardiac and pulmonary function, induces reversible hypotension and exerts anti-inflammatory effects in an endotoxemic porcine model. Crit. Care 18, 682. 10.1186/s13054-014-0682-y PubMed DOI PMC

Guillon A., Preau S., Aboab J., Azabou E., Jung B., Silva S., et al. (2019). Preclinical septic shock research: Why we need an animal ICU. Ann. Intensive Care 9, 66. 10.1186/s13613-019-0543-6 PubMed DOI PMC

Haake D. A. (2006). Hamster model of leptospirosis. Curr. Protoc. Microbiol. Chapter 12, Unit 12E.2, Chapter 12, Unit 12E.2. 10.1002/9780471729259.mc12e02s02 PubMed DOI PMC

Hua T., Wu X., Wang W., Li H., Bradley J., Peberdy M. A., et al. (2018). Micro- and macrocirculatory changes during sepsis and septic shock in a rat model. Shock 49, 591–595. 10.1097/SHK.0000000000000954 PubMed DOI

Jarkovska D., Markova M., Horak J., Nalos L., Benes J., Al-Obeidallah M., et al. (2018). Cellular mechanisms of myocardial depression in porcine septic shock. Front. Physiol. 9, 726. 10.3389/fphys.2018.00726 PubMed DOI PMC

Jarkovska D., Valesova L., Chvojka J., Benes J., Sviglerova J., Florova B., et al. (2016). Heart rate variability in porcine progressive peritonitis-induced sepsis. Front. Physiol. 6, 412. 10.3389/fphys.2015.00412 PubMed DOI PMC

Jin Y., Wei L., Cai W., Lin Z., Wu Z., Peng Y., et al. (2017). Complete characterization of cardiac myosin heavy chain (223 kDa) enabled by size-exclusion chromatography and middle-down mass spectrometry. Anal. Chem. 89, 4922–4930. 10.1021/acs.analchem.7b00113 PubMed DOI PMC

Judges D., Sharkey P., Cheung H., Craig I., Driedger A. A., Sibbald W. J., et al. (1986). Pulmonary microvascular fluid flux in a large animal model of sepsis: Evidence for increased pulmonary endothelial permeability accompanying surgically induced peritonitis in sheep. Surgery 99, 222–234., PubMed

Kapetanovic R., Fairbairn L., Beraldi D., Sester D. P., Archibald A. L., Tuggle C. K., et al. (2012). Pig bone marrow-derived macrophages resemble human macrophages in their response to bacterial lipopolysaccharide. J. Immunol. 188, 3382–3394. 10.4049/jimmunol.1102649 PubMed DOI

Kastello M. D., Spertzel R. O. (1973). The rhesus monkey as a model for the study of infectious disease. Am. J. Phys. Anthropol. 38, 501–504. 10.1002/ajpa.1330380255 PubMed DOI

Kumar V. (2020). Toll-like receptors in sepsis-associated cytokine storm and their endogenous negative regulators as future immunomodulatory targets. Int. Immunopharmacol. 89, 107087. 10.1016/j.intimp.2020.107087 PubMed DOI PMC

Kuypers E., Ophelders D., Jellema R. K., Kunzmann S., Gavilanes A. W., Kramer B. W. (2012). White matter injury following fetal inflammatory response syndrome induced by chorioamnionitis and fetal sepsis: Lessons from experimental ovine models. Early Hum. Dev. 88, 931–936. 10.1016/j.earlhumdev.2012.09.011 PubMed DOI

Lagoa C. E., de Figueiredo L. F. P., Cruz R. J., Silva E., Rocha e Silva M. (2004). Effects of volume resuscitation on splanchnic perfusion in canine model of severe sepsis induced by live Escherichia coli infusion. Crit. Care 8, R221–R228. 10.1186/cc2871 PubMed DOI PMC

Levraut J., Ciebiera J. P., Chave S., Rabary O., Jambou P., Carles M., et al. (1998). Mild hyperlactatemia in stable septic patients is due to impaired lactate clearance rather than overproduction. Am. J. Respir. Crit. Care Med. 157, 1021–1026. 10.1164/ajrccm.157.4.9705037 PubMed DOI

Levy B., Gibot S., Franck P., Cravoisy A., Bollaert P.-E. (2005). Relation between muscle Na+K+ ATPase activity and raised lactate concentrations in septic shock: A prospective study. Lancet 365, 871–875. 10.1016/S0140-6736(05)71045-X PubMed DOI

Levy M. M., Fink M. P., Marshall J. C., Abraham E., Angus D., Cook D., et al. (2003). 2001 SCCM/ESICM/ACCP/ATS/SIS international sepsis definitions conference. Intensive Care Med. 29, 530–538. 10.1007/s00134-003-1662-x PubMed DOI

Li G.-R., Du X.-L., Siow Y. L., O K., Tse H.-F., Lau C.-P. (2003). Calcium-activated transient outward chloride current and phase 1 repolarization of swine ventricular action potential. Cardiovasc. Res. 58, 89–98. 10.1016/s0008-6363(02)00859-3 PubMed DOI

Li J.-L., Li G., Jing X.-Z., Li Y.-F., Ye Q.-Y., Jia H.-H., et al. (2018). Assessment of clinical sepsis-associated biomarkers in a septic mouse model. J. Int. Med. Res. 46, 2410–2422. 10.1177/0300060518764717 PubMed DOI PMC

Liu V., Escobar G. J., Greene J. D., Soule J., Whippy A., Angus D. C., et al. (2014). Hospital deaths in patients with sepsis from 2 independent cohorts. JAMA 312, 90–92. 10.1001/jama.2014.5804 PubMed DOI

Locher M. R., Razumova M. V., Stelzer J. E., Norman H. S., Moss R. L. (2011). Effects of low-level α-myosin heavy chain expression on contractile kinetics in porcine myocardium. Am. J. Physiol. Heart Circ. Physiol. 300, H869–H878. 10.1152/ajpheart.00452.2010 PubMed DOI PMC

Lu W.-H., Jin X.-J., Jiang X.-G., Wang Z., Wu J.-Y., Shen G.-G. (2015). Resuscitation with hydroxyethyl starch 130/0.4 attenuates intestinal injury in a rabbit model of sepsis. Indian J. Pharmacol. 47, 49–54. 10.4103/0253-7613.150333 PubMed DOI PMC

Makarenko I., Opitz C. A., Leake M. C., Neagoe C., Kulke M., Gwathmey J. K., et al. (2004). Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circ. Res. 95, 708–716. 10.1161/01.RES.0000143901.37063.2f PubMed DOI

Mazer M., Unsinger J., Drewry A., Walton A., Osborne D., Blood T., et al. (2019). IL-10 has differential effects on the innate and adaptive immune systems of septic patients. J. Immunol. 203, 2088–2099. 10.4049/jimmunol.1900637 PubMed DOI PMC

Mellhammar L., Wullt S., Lindberg Å., Lanbeck P., Christensson B., Linder A. (2016). Sepsis incidence: A population-based study. Open Forum Infect. Dis. 3, ofw207. 10.1093/ofid/ofw207 PubMed DOI PMC

Meurens F., Summerfield A., Nauwynck H., Saif L., Gerdts V. (2012). The pig: A model for human infectious diseases. Trends Microbiol. 20, 50–57. 10.1016/j.tim.2011.11.002 PubMed DOI PMC

Michaeli B., Martinez A., Revelly J.-P., Cayeux M.-C., Chioléro R. L., Tappy L., et al. (2012). Effects of endotoxin on lactate metabolism in humans. Crit. Care 16, R139. 10.1186/cc11444 PubMed DOI PMC

Milani-Nejad N., Janssen P. M. L. (2014). Small and large animal models in cardiac contraction research: Advantages and disadvantages. Pharmacol. Ther. 141, 235–249. 10.1016/j.pharmthera.2013.10.007 PubMed DOI PMC

Minneci P. C., Deans K. J., Hansen B., Parent C., Romines C., Gonzales D. A., et al. (2007). A canine model of septic shock: Balancing animal welfare and scientific relevance. Am. J. Physiol. Heart Circ. Physiol. 293, H2487–H2500. 10.1152/ajpheart.00589.2007 PubMed DOI

Miranda M. L., Balarini M. M., Bouskela E. (2015). Dexmedetomidine attenuates the microcirculatory derangements evoked by experimental sepsis. Anesthesiology 122, 619–630. 10.1097/ALN.0000000000000491 PubMed DOI

Miyata S., Minobe W., Bristow M. R., Leinwand L. A. (2000). Myosin heavy chain isoform expression in the failing and nonfailing human heart. Circ. Res. 86, 386–390. 10.1161/01.res.86.4.386 PubMed DOI

Morimatsu H., Ishikawa K., May C. N., Bailey M., Bellomo R. (2012). The systemic and regional hemodynamic effects of phenylephrine in sheep under normal conditions and during early hyperdynamic sepsis. Anesth. Analg. 115, 330–342. 10.1213/ANE.0b013e31825681ab PubMed DOI

Murakami K., Bjertnaes L. J., Schmalstieg F. C., McGuire R., Cox R. A., Hawkins H. K., et al. (2002). A novel animal model of sepsis after acute lung injury in sheep. Crit. Care Med. 30, 2083–2090. 10.1097/00003246-200209000-00022 PubMed DOI

Murugan R., Karajala-Subramanyam V., Lee M., Yende S., Kong L., Carter M., et al. (2010). Acute kidney injury in non-severe pneumonia is associated with an increased immune response and lower survival. Kidney Int. 77, 527–535. 10.1038/ki.2009.502 PubMed DOI PMC

Mutlak H., Jennewein C., Tran N., Mehring M., Latsch K., Habeck K., et al. (2013). Cecum ligation and dissection: A novel modified mouse sepsis model. J. Surg. Res. 183, 321–329. 10.1016/j.jss.2012.11.046 PubMed DOI

Nagy S., Tárnoky K., Tutsek L., Boros M., Karácsony G. (1990). A canine model of hyperdynamic sepsis induced by intestinal ischemia. Acta Physiol. Hung 75, 303–320. PubMed

Napolitano L. M. (2018). Sepsis 2018: Definitions and guideline changes. Surg. Infect. (Larchmt) 19, 117–125. 10.1089/sur.2017.278 PubMed DOI

Natanson C., Danner R. L., Fink M. P., MacVittie T. J., Walker R. I., Conklin J. J., et al. (1988). Cardiovascular performance with E. Coli challenges in a canine model of human sepsis. Am. J. Physiol. 254, H558–H569. 10.1152/ajpheart.1988.254.3.H558 PubMed DOI

Odening K. E., Gomez A.-M., Dobrev D., Fabritz L., Heinzel F. R., Mangoni M. E., et al. (2021). ESC working group on cardiac cellular electrophysiology position paper: Relevance, opportunities, and limitations of experimental models for cardiac electrophysiology research. Europace 23, 1795–1814. 10.1093/europace/euab142 PubMed DOI

Okazaki N., Lankadeva Y. R., Peiris R. M., Birchall I. E., May C. N. (2021). Rapid and persistent decrease in brain tissue oxygenation in ovine gram-negative sepsis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 321, R990–R996. –R996. 10.1152/ajpregu.00184.2021 PubMed DOI

Pabst R. (2020). The pig as a model for immunology research. Cell. Tissue Res. 380, 287–304. 10.1007/s00441-020-03206-9 PubMed DOI PMC

Park I., Lee J. H., Jang D.-H., Kim D., Chang H., Kwon H., et al. (2019). Characterization of fecal peritonitis-induced sepsis in a porcine model. J. Surg. Res. 244, 492–501. 10.1016/j.jss.2019.06.094 PubMed DOI

Raith E. P., Udy A. A., Bailey M., McGloughlin S., MacIsaac C., Bellomo R., et al. (2017). Prognostic accuracy of the SOFA score, SIRS criteria, and qSOFA score for in-hospital mortality among adults with suspected infection admitted to the intensive care unit. JAMA 317, 290–300. 10.1001/jama.2016.20328 PubMed DOI

Reade M. C., Young J. D. (2003). Of mice and men (and rats): Implications of species and stimulus differences for the interpretation of studies of nitric oxide in sepsis. Br. J. Anaesth. 90, 115–118. 10.1093/bja/aeg033 PubMed DOI

Reiser P. J., Portman M. A., Ning X. H., Schomisch Moravec C. (2001). Human cardiac myosin heavy chain isoforms in fetal and failing adult atria and ventricles. Am. J. Physiol. Heart Circ. Physiol. 280, H1814–H1820. 10.1152/ajpheart.2001.280.4.H1814 PubMed DOI

Rothkötter H.-J. (2009). Anatomical particularities of the porcine immune system--a physician’s view. Dev. Comp. Immunol. 33, 267–272. 10.1016/j.dci.2008.06.016 PubMed DOI

Rundell V. L. M., Manaves V., Martin A. F., de Tombe P. P. (2005). Impact of beta-myosin heavy chain isoform expression on cross-bridge cycling kinetics. Am. J. Physiol. Heart Circ. Physiol. 288, H896–H903. 10.1152/ajpheart.00407.2004 PubMed DOI

Santos A. O. M. T., Furtado E. S., Villela N. R., Bouskela E. (2011). Microcirculatory effects of fluid therapy and dopamine, associated or not to fluid therapy, in endotoxemic hamsters. Clin. Hemorheol. Microcirc. 47, 1–13. 10.3233/CH-2010-1358 PubMed DOI

Scheiermann P., Hoegl S., Revermann M., Ahluwalia D., Zander J., Boost K. A., et al. (2009). Cecal ligation and incision: An acute onset model of severe sepsis in rats. J. Surg. Res. 151, 132–137. 10.1016/j.jss.2008.02.032 PubMed DOI

Seok J., Warren H. S., Cuenca A. G., Mindrinos M. N., Baker H. V., Xu W., et al. (2013). Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. U. S. A. 110, 3507–3512. 10.1073/pnas.1222878110 PubMed DOI PMC

Seymour C. W., Kennedy J. N., Wang S., Chang C. H., Elliott C. F., Xu Z., et al. (2019). Derivation, validation, and potential treatment implications of novel clinical phenotypes for sepsis. JAMA 321, 2003–2017. –17. 10.1001/jama.2019.5791 PubMed DOI PMC

Siddiqui A. Z., Bhatti U. F., Deng Q., Biesterveld B. E., Tian Y., Wu Z., et al. (2021). Cl-amidine improves survival and attenuates kidney injury in a rabbit model of endotoxic shock. Surg. Infect. (Larchmt) 22, 421–426. 10.1089/sur.2020.189 PubMed DOI

Singer M., Deutschman C. S., Seymour C. W., Shankar-Hari M., Annane D., Bauer M., et al. (2016). The Third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA 315, 801–810. 10.1001/jama.2016.0287 PubMed DOI PMC

Solomon M. A., Correa R., Alexander H. R., Koev L. A., Cobb J. P., Kim D. K., et al. (1994). Myocardial energy metabolism and morphology in a canine model of sepsis. Am. J. Physiol. 266, H757–H768. 10.1152/ajpheart.1994.266.2.H757 PubMed DOI

Stanski N. L., Wong H. R. (2020). Prognostic and predictive enrichment in sepsis. Nat. Rev. Nephrol. 16, 20–31. 10.1038/s41581-019-0199-3 PubMed DOI PMC

Stelzer J. E., Norman H. S., Chen P. P., Patel J. R., Moss R. L. (2008). Transmural variation in myosin heavy chain isoform expression modulates the timing of myocardial force generation in porcine left ventricle. J. Physiol. 586, 5203–5214. 10.1113/jphysiol.2008.160390 PubMed DOI PMC

Stengl M., Bartak F., Sykora R., Chvojka J., Benes J., Krouzecky A., et al. (2010a). Reduced L-type calcium current in ventricular myocytes from pigs with hyperdynamic septic shock. Crit. Care Med. 38, 579–587. 10.1097/CCM.0b013e3181cb0f61 PubMed DOI

Stengl M., Sykora R., Chvojka J., Krouzecky A., Novak I., Varnerova V., et al. (2010b). Differential effects of hemofiltration and of coupled plasma filtration adsorption on cardiac repolarization in pigs with hyperdynamic septic shock. Shock 33, 101–105. 10.1097/SHK.0b013e3181ab6359 PubMed DOI

Stengl M., Sykora R., Krouzecky A., Chvojka J., Novak I., Varnerova V., et al. (2008). Continuous hemofiltration in pigs with hyperdynamic septic shock affects cardiac repolarization. Crit. Care Med. 36, 3198–3204. 10.1097/CCM.0b013e31818f9eda PubMed DOI

Stortz J. A., Raymond S. L., Mira J. C., Moldawer L. L., Mohr A. M., Efron P. A. (2017). Murine models of sepsis and trauma: Can we bridge the gap? ILAR J. 58, 90–105. 10.1093/ilar/ilx007 PubMed DOI PMC

Swindle M. M., Makin A., Herron A. J., Clubb F. J., Frazier K. S. (2012). Swine as models in biomedical research and toxicology testing. Vet. Pathol. 49, 344–356. 10.1177/0300985811402846 PubMed DOI

Tao W., Deyo D. J., Traber D. L., Johnston W. E., Sherwood E. R. (2004). Hemodynamic and cardiac contractile function during sepsis caused by cecal ligation and puncture in mice. Shock 21, 31–37. 10.1097/01.shk.0000101673.49265.5d PubMed DOI

Tarkowski A., Collins L. V., Gjertsson I., Hultgren O. H., Jonsson I. M., Sakiniene E., et al. (2001). Model systems: Modeling human staphylococcal arthritis and sepsis in the mouse. Trends Microbiol. 9, 321–326. 10.1016/s0966-842x(01)02078-9 PubMed DOI

Torio C. M., Moore B. J. (2006). “National inpatient hospital costs: The most expensive conditions by payer, 2013,” in Healthcare Cost and utilization project (HCUP) statistical briefs (rockville (MD): Agency for healthcare research and quality (US)). Available at: http://www.ncbi.nlm.nih.gov/books/NBK368492/(Accessed August 5, 2022). PubMed

Traeger T., Koerner P., Kessler W., Cziupka K., Diedrich S., Busemann A., et al. (2010). Colon ascendens stent peritonitis (CASP)--a standardized model for polymicrobial abdominal sepsis. J. Vis. Exp. 2299, 2299. 10.3791/2299 PubMed DOI PMC

Través P. G., de Atauri P., Marín S., Pimentel-Santillana M., Rodríguez-Prados J.-C., Marín de Mas I., et al. (2012). Relevance of the MEK/ERK signaling pathway in the metabolism of activated macrophages: A metabolomic approach. J. Immunol. 188, 1402–1410. 10.4049/jimmunol.1101781 PubMed DOI

Uranga-Murillo I., Tapia E., Garzón-Tituaña M., Ramirez-Labrada A., Santiago L., Pesini C., et al. (2021). Biological relevance of granzymes A and K during E. Coli sepsis. Theranostics 11, 9873–9883. 10.7150/thno.59418 PubMed DOI PMC

Utiger J. M., Glas M., Levis A., Prazak J., Haenggi M. (2021). Description of a rat model of polymicrobial abdominal sepsis mimicking human colon perforation. BMC Res. Notes 14, 14. 10.1186/s13104-020-05438-y PubMed DOI PMC

Vaure C., Liu Y. (2014). A comparative review of toll-like receptor 4 expression and functionality in different animal species. Front. Immunol. 5, 316. 10.3389/fimmu.2014.00316 PubMed DOI PMC

Vogel M., Cheung M. M. H., Li J., Kristiansen S. B., Schmidt M. R., White P. A., et al. (2003). Noninvasive assessment of left ventricular force-frequency relationships using tissue Doppler-derived isovolumic acceleration: Validation in an animal model. Circulation 107, 1647–1652. 10.1161/01.CIR.0000058171.62847.90 PubMed DOI

Wang J., Liu X., Ren B., Rupp H., Takeda N., Dhalla N. S. (2002). Modification of myosin gene expression by imidapril in failing heart due to myocardial infarction. J. Mol. Cell. Cardiol. 34, 847–857. 10.1006/jmcc.2002.2023 PubMed DOI

Wang N., Lu Y., Zheng J., Liu X. (2022). Of mice and men: Laboratory murine models for recapitulating the immunosuppression of human sepsis. Front. Immunol. 13, 956448. 10.3389/fimmu.2022.956448 PubMed DOI PMC

Warren H. S., Fitting C., Hoff E., Adib-Conquy M., Beasley-Topliffe L., Tesini B., et al. (2010). Resilience to bacterial infection: Difference between species could be due to proteins in serum. J. Infect. Dis. 201, 223–232. 10.1086/649557 PubMed DOI PMC

Whang K. T., Vath S. D., Becker K. L., Snider R. H., Nylen E. S., Muller B., et al. (2000). Procalcitonin and proinflammatory cytokine interactions in sepsis. Shock 14, 73–78. 10.1097/00024382-200014010-00013 PubMed DOI

Wolffram S., Eggenberger E., Scharrer E. (1986). Kinetics of D-glucose and L-leucine transport into sheep and pig intestinal brush border membrane vesicles. Comp. Biochem. Physiol. A Comp. Physiol. 84, 589–593. 10.1016/0300-9629(86)90370-1 PubMed DOI

Yaghouby F., Daluwatte C., Fukuda S., Nelson C., Salsbury J., Kinsky M., et al. (2017). Progression and variability of physiologic deterioration in an ovine model of lung infection sepsis. J. Appl. Physiol. 123, 172–181. 10.1152/japplphysiol.00122.2017 PubMed DOI

Zanetti G., Heumann D., Gérain J., Kohler J., Abbet P., Barras C., et al. (1992). Cytokine production after intravenous or peritoneal gram-negative bacterial challenge in mice. Comparative protective efficacy of antibodies to tumor necrosis factor-alpha and to lipopolysaccharide. J. Immunol. 148, 1890–1897. PubMed

Zhang H., Li L., Wu J., Qu H.-P., Tang Y.-Q., Chen D.-C. (2020). Time of dissociation between microcirculation, macrocirculation, and lactate levels in a rabbit model of early endotoxemic shock. Chin. Med. J. Engl. 133, 2153–2160. 10.1097/CM9.0000000000000887 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace