339
Views
2
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Common Variables That Influence Sepsis Mortality in Mice

, , , & ORCID Icon
Pages 1121-1134 | Received 03 Dec 2022, Accepted 18 Feb 2023, Published online: 14 Mar 2023

References

  • Editors, Rubin, E. Striving for diversity in research studies. N Engl J Med. 2021;385(15):1429–1430.
  • Liu KA, Mager NAD. Women’s involvement in clinical trials: historical perspective and future implications. Pharm Pract. 2016;14(1):708.
  • Kelty M, Bates A, Pinn VW. National Institutes of Health policy on the inclusion of women and minorities as subjects in clinical research. In: Principles and Practice of Clinical Research. Elsevier; 2007:129–142.
  • Miller LR, Marks C, Becker JB, et al. Considering sex as a biological variable in preclinical research. FASEB J. 2017;31(1):29–34. doi:10.1096/fj.201600781r
  • Jackson SJ, Andrews N, Ball D, et al. Does age matter? The impact of rodent age on study outcomes. Lab Anim. 2017;51(2):160–169. doi:10.1177/0023677216653984
  • Remick DG, Ayala A, Chaudry IH, et al. Premise for standardized sepsis models. Shock. 2019;51(1):4–9. doi:10.1097/SHK.0000000000001164
  • Osuchowski MF, Ayala A, Bahrami S, et al. Minimum quality threshold in pre-clinical sepsis studies (MQTiPSS): an international expert consensus initiative for improvement of animal modeling in sepsis. Intensive Care Med Exp. 2018;6(1):26. doi:10.1186/s40635-018-0189-y
  • Lewis AJ, Seymour CW, Rosengart MR. Current murine models of sepsis. Surg Infect. 2016;17(4):385–393. doi:10.1089/sur.2016.021
  • Goswami DG, Garcia LF, Dodoo C, et al. Evaluating the timeliness and specificity of CD69, CD64 and CD25 as biomarkers of sepsis in MICE. Shock. 2021;55(4):507–518. doi:10.1097/SHK.0000000000001650
  • Goswami DG, Rubio AJ, Mata J, Munoz S, Gallegos A, Walker WE. Large peritoneal macrophages and transitional premonocytes promote survival during abdominal sepsis. ImmunoHorizons. 2021;5(12):994–1007. doi:10.4049/immunohorizons.2100086
  • Heipertz EL, Harper J, Goswami DG, et al. IRF3 signaling within the mouse stroma influences sepsis pathogenesis. J Immunol. 2021;206(2):398–409. doi:10.4049/jimmunol.1900217
  • Heipertz EL, Harper J, Walker WE. STING and TRIF contribute to mouse sepsis, depending on severity of the disease model. Shock. 2017;47(5):621–631. doi:10.1097/SHK.0000000000000771
  • Laitano O, Van Steenbergen D, Mattingly AJ, et al. Xiphoid surface temperature predicts mortality in a murine model of septic shock. Shock. 2018;50(2):226–232. doi:10.1097/SHK.0000000000001007
  • Dwivedi AK. How to write statistical analysis section in medical research. J Investig Med. 2022;2022:jim-2022–002479.
  • Zellweger R, Wichmann MW, Ayala A, Stein S, DeMaso CM, Chaudry IH. Females in proestrus state maintain splenic immune functions and tolerate sepsis better than males. Crit Care Med. 1997;25(1):106–110. doi:10.1097/00003246-199701000-00021
  • Hoogland IC, Houbolt C, van Westerloo DJ, van Gool WA, van de Beek D. Systemic inflammation and microglial activation: systematic review of animal experiments. J Neuroinflammation. 2015;12:114. doi:10.1186/s12974-015-0332-6
  • Zhang M, Montroy J, Sharma R, et al. The effects of biological sex on sepsis treatments in animal models: a systematic review and a narrative elaboration on sex- and gender-dependent differences in sepsis. Crit Care Explorations. 2021;3(6):e0433–e0433. doi:10.1097/CCE.0000000000000433
  • Diodato MD, Knoferl MW, Schwacha MG, Bland KI, Chaudry IH. Gender differences in the inflammatory response and survival following haemorrhage and subsequent sepsis. Cytokine. 2001;14(3):162–169. doi:10.1006/cyto.2001.0861
  • Angele MK, Frantz MC, Chaudry IH. Gender and sex hormones influence the response to trauma and sepsis: potential therapeutic approaches. Clinics. 2006;61(5):479–488. doi:10.1590/S1807-59322006000500017
  • Goswami DG, Walker WE. Aged IRF3-KO mice are protected from sepsis. J Inflamm Res. 2021;14:5757–5767. doi:10.2147/JIR.S335203
  • Kennedy LH, Hwang H, Wolfe AM, Hauptman J, Nemzek-Hamlin JA. Effects of buprenorphine and estrous cycle in a murine model of cecal ligation and puncture. Comp Med. 2014;64(4):270–282.
  • Brust V, Schindler PM, Lewejohann L. Lifetime development of behavioural phenotype in the house mouse (Mus musculus). Front Zool. 2015;12(S1):1–14. doi:10.1186/1742-9994-12-S1-S17
  • Dutta S, Sengupta P. Men and mice: relating their ages. Life Sci. 2016;152:244–248. doi:10.1016/j.lfs.2015.10.025
  • Fernández-Sánchez A, Madrigal-Santillán E, Bautista M, et al. Inflammation, oxidative stress, and obesity. Int J Mol Sci. 2011;12(5):3117–3132. doi:10.3390/ijms12053117
  • Vachharajani V, Russell JM, Scott KL, et al. Obesity exacerbates sepsis-induced inflammation and microvascular dysfunction in mouse brain. Microcirculation. 2005;12(2):183–194. doi:10.1080/10739680590904982
  • Singer G, Stokes KY, Terao S, Granger DN. Sepsis-induced intestinal microvascular and inflammatory responses in obese mice. Shock. 2009;31(3):275–279. doi:10.1097/SHK.0b013e3181834ab3
  • Schwab F, Gastmeier P, Hoffmann P, Meyer E. Summer, sun and sepsis-The influence of outside temperature on nosocomial bloodstream infections: a cohort study and review of the literature. PLoS One. 2020;15(6):e0234656–e0234656. doi:10.1371/journal.pone.0234656
  • Wyse C, O’Malley G, Coogan AN, McConkey S, Smith DJ. Seasonal and daytime variation in multiple immune parameters in humans: evidence from 329,261 participants of the UK Biobank cohort. iScience. 2021;24(4):102255. doi:10.1016/j.isci.2021.102255
  • Kiank C, Koerner P, Keler W, et al. Seasonal variations in inflammatory responses to sepsis and stress in mice*. Crit Care Med. 2007;35(10):2352–2358. doi:10.1097/01.CCM.0000282078.80187.7F
  • Lewis A, Zuckerbraun B, Griepentrog J, Zhang X, Rosengart M. Reducing animal use with a biotelemetry-enhanced murine model of sepsis. Sci Rep. 2017;7(1):6622. doi:10.1038/s41598-017-05497-5
  • Helbing DL, Stabenow LK, Bauer R. Mouse sepsis models: don’t forget ambient temperature! Intensive Care Med Exp. 2022;10(1):29. doi:10.1186/s40635-022-00457-4
  • Ganeshan K, Nikkanen J, Man K, et al. Energetic trade-offs and hypometabolic states promote disease tolerance. Cell. 2019;177(2):399–413.e312. doi:10.1016/j.cell.2019.01.050
  • Carpenter KC, Zhou Y, Hakenjos JM, Fry CD, Nemzek JA. Thermoneutral housing temperature improves survival in a murine model of polymicrobial peritonitis. Shock. 2020;54(5):688–696. doi:10.1097/SHK.0000000000001551
  • Appenheimer MM, Evans SS. Chapter 24 - temperature and adaptive immunity. In: Romanovsky AA, editor. Handbook of Clinical Neurology. Vol. 156. Elsevier; 2018:397–415.
  • Giles DA, Moreno-Fernandez ME, Stankiewicz TE, et al. Thermoneutral housing exacerbates nonalcoholic fatty liver disease in mice and allows for sex-independent disease modeling. Nat Med. 2017;23(7):829–838. doi:10.1038/nm.4346
  • Ferrer R, Martin-Loeches I, Phillips G, et al. Empiric antibiotic treatment reduces mortality in severe sepsis and septic shock from the first hour: results from a guideline-based performance improvement program. Crit Care Med. 2014;42(8):1749–1755. doi:10.1097/CCM.0000000000000330
  • Gaieski DF, Mikkelsen ME, Band RA, et al. Impact of time to antibiotics on survival in patients with severe sepsis or septic shock in whom early goal-directed therapy was initiated in the emergency department. Crit Care Med. 2010;38(4):1045–1053. doi:10.1097/CCM.0b013e3181cc4824
  • Sterling SA, Miller WR, Pryor J, Puskarich MA, Jones AE. The impact of timing of antibiotics on outcomes in severe sepsis and septic shock: a systematic review and meta-analysis. Crit Care Med. 2015;43(9):1907–1915. doi:10.1097/CCM.0000000000001142
  • Vyas D, Javadi P, DiPasco PJ, Buchman TG, Hotchkiss RS, Coopersmith CM. Early antibiotic administration but not antibody therapy directed against IL-6 improves survival in septic mice predicted to die on basis of high IL-6 levels. Am J Physiol. 2005;289(4):R1048–R1053. doi:10.1152/ajpregu.00312.2005
  • Singleton K, Wischmeyer P. Distance of cecum ligated influences mortality, tumor necrosis factor-alpha and interleukin-6 expression following cecal ligation and puncture in the rat. Eur Surg Res. 2003;35(6):486–491. doi:10.1159/000073387
  • Ruiz S, Vardon-Bounes F, Merlet-Dupuy V, et al. Sepsis modeling in mice: ligation length is a major severity factor in cecal ligation and puncture. Intensive Care Med Exp. 2016;4(1):22. doi:10.1186/s40635-016-0096-z
  • Ebong S, Call D, Nemzek J, Bolgos G, Newcomb D, Remick D. Immunopathologic alterations in murine models of sepsis of increasing severity. Infect Immun. 1999;67(12):6603–6610. doi:10.1128/IAI.67.12.6603-6610.1999
  • Wichterman KA, Baue AE, Chaudry IH. Sepsis and septic shock—a review of laboratory models and a proposal. J Surg Res. 1980;29(2):189–201. doi:10.1016/0022-4804(80)90037-2
  • Newcomb D, Bolgos G, Green L, Remick DG. Antibiotic treatment influences outcome in murine sepsis: mediators of increased morbidity. Shock. 1998;10(2):110–117. doi:10.1097/00024382-199808000-00005
  • Zanotti-Cavazzoni SL, Goldfarb RD. Animal models of sepsis. Crit Care Clin. 2009;25(4):703–719. doi:10.1016/j.ccc.2009.08.005
  • Iskander KN, Vaickus M, Duffy ER, Remick DG. Shorter duration of post-operative antibiotics for cecal ligation and puncture does not increase inflammation or mortality. PLoS One. 2016;11(9):e0163005. doi:10.1371/journal.pone.0163005
  • Imai T, Takahashi K, Masuo F, Goto F. Anaesthesia affects outcome of sepsis in mice. Can J Anaesth. 1998;45(4):360–366. doi:10.1007/BF03012029
  • Doi K, Leelahavanichkul A, Yuen PST, Star RA. Animal models of sepsis and sepsis-induced kidney injury. J Clin Invest. 2009;119(10):2868–2878. doi:10.1172/JCI39421
  • Zhang J, Liu ZG, Luo YW, et al. C57BL/6小鼠与 BALB/c 小鼠对脓毒症反应的差异 [Differences in the response to sepsis between C57BL/6 and BALB/c mice]. Nan Fang Yi Ke Da Xue Xue Bao. 2010;30(5):973–975. Chinese.
  • Fay KT, Klingensmith NJ, Chen CW, et al. The gut microbiome alters immunophenotype and survival from sepsis. FASEB J. 2019;33(10):11258–11269. doi:10.1096/fj.201802188R
  • Cotroneo TM, Hugunin KM, Shuster KA, Hwang HJ, Kakaraparthi BN, Nemzek-Hamlin JA. Effects of buprenorphine on a cecal ligation and puncture model in C57BL/6 mice. J Am Assoc Lab Anim Sci. 2012;51(3):357–365.
  • Silver AC, Arjona A, Walker WE, Fikrig E. The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity. 2012;36(2):251–261. doi:10.1016/j.immuni.2011.12.017
  • Heipertz EL, Harper J, Lopez CA, Fikrig E, Hughes ME, Walker WE. Circadian rhythms influence the severity of sepsis in mice via a TLR2-dependent, leukocyte-intrinsic mechanism. J Immunol. 2018;201:193–201. doi:10.4049/jimmunol.1701677
  • Dwivedi AK. How to write statistical analysis section in medical research. J Investig Med. 2022;70:1759–1770. doi:10.1136/jim-2022-002479
  • Dwivedi AK, Shukla R. Evidence‐based statistical analysis and methods in biomedical research (SAMBR) checklists according to design features. Cancer Rep. 2020;3(4):e1211. doi:10.1002/cnr2.1211
  • Flórez-Vargas O, Brass A, Karystianis G, et al. Bias in the reporting of sex and age in biomedical research on mouse models. eLife. 2016;5:e13615. doi:10.7554/eLife.13615
  • Percie du Sert N, Hurst V, Ahluwalia A, et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. J Cereb Blood Flow Metab. 2020;40(9):1769–1777. doi:10.1177/0271678X20943823