Multicompartmental traumatic injury and the microbiome: Shift to a pathobiome

Munley, Jennifer A.; Kelly, Lauren; Pons, Erick E; Kannan, Kolenkode B.; Coldwell, Preston S.; Whitley, Elizabeth M.; Gillies, Gwendolyn S.; Efron, Philip A.; Nagpal, Ravinder; Mohr, Alicia M.

doi:10.1097/ta.0000000000003803

Cited by 15 publications

(22 citation statements)

References 52 publications

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“…The gut microbiome will be measured as per our previously described methods (4,12,(23)(24)(25)(26)(27). Briefly, genomic DNA from 200 mg of the fecal specimen was extracted using the QIAmp PowerFecal Pro DNA Kit (Qiagen) according to the manufacturer's instructions.…”

Section: Gut Microbiome Analysismentioning

confidence: 99%

Prebiotic mechanisms of resistant starches from dietary beans and pulses on gut microbiome and metabolic health in a humanized murine model of aging

et al. 2023

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Dietary pulses, being a rich source of fiber and proteins, offer an ideal and inexpensive food choice for older adults to promote gut and metabolic health. However, the prebiotic effects of dietary pulses-derived resistant starches (RS), compared to RS from cereals and tubers, remain relatively underexplored, particularly in context to their gut modulatory potential in old age. We herein investigate the prebiotic effects of pulses-derived RS on the gut microbiome and intestinal health in aged (60-week old) mice colonized with human microbiota. C57B6/J mice were fed for 20 weeks with either a western-style high-fat diet (control; CTL) or CTL diet supplemented (5% w/w) with RS from pinto beans (PTB), black-eyed-peas (BEP), lentils (LEN), chickpeas (CKP), or inulin (INU; reference control). We find that the RS supplementation modulates gut microbiome in a sex-dependent manner. For instance, CKP enriched α-diversity only in females, while β-diversity deviated for both sexes. Further, different RS groups exhibited distinct microbiome differences at bacterial phyla and genera levels. Notably, LEN fostered Firmicutes and depleted Proteobacteria abundance, whereas Bacteroidota was promoted by CKP and INU. Genus Dubosiella increased dominantly in males for all groups except PTB, whilst Faecalibaculum decreased in females by CKP and INU groups. Linear discriminant analysis effect size (LEfSe) and correlational analyzes reveal RS-mediated upregulation of key bacterial genera associated with short-chain fatty acids (butyrate) production and suppression of specific pathobionts. Subsequent machine-learning analysis validate decreased abundance of notorious genera, namely, Enterococcus, Odoribacter, Desulfovibrio, Alistipes and Erysipelatoclostridium among RS groups. CKP and LEN groups partly protected males against post-prandial glycemia. Importantly, RS ameliorated high-fat diet-induced gut hyperpermeability and enhanced expression of tight-junction proteins (claudin-1 and claudin-4), which were more pronounced for LEN. In addition, IL10 upregulation was more prominent for LEN, while TNF-α was downregulated by LEN, CKP, and INU. Together, these findings demonstrate that RS supplementation beneficially modulates the gut microbiome with a reduction in gut leakiness and inflammation, indicating their prebiotic potential for functional food and nutritional applications.

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Section: Gut Microbiome Analysismentioning

confidence: 99%

Prebiotic mechanisms of resistant starches from dietary beans and pulses on gut microbiome and metabolic health in a humanized murine model of aging

et al. 2023

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“…Histological slides of terminal ileum and descending colon were analyzed by a blinded veterinary pathologist and scored for injury similar to previously described; each category was graded from 0 (no injury) to 4 (severe changes) (see Tables in Supplemental Digital Content 3, http://links.lww.com/TA/C899, and 4, http://links.lww.com/TA/C900). 24 …”

Section: Methodsmentioning

confidence: 99%

“…Microbiome profiles were analyzed per our previously described methods 24,30 . Briefly, genomic DNA was extracted from fecal samples and quantified using a nanodrop spectrophotometer (Thermo Fisher Scientific, Waltham, MA).…”

Section: Methodsmentioning

confidence: 99%

“…Microbiome profiles were analyzed per our previously described methods. 24,30 Briefly, genomic DNA was extracted from fecal samples and quantified using a nanodrop spectrophotometer (Thermo Fisher Scientific, Waltham, MA). The V4 hypervariable region of the bacterial 16S rRNA gene was amplified using the barcoded universal primers (515F/806R).…”

Section: Microbiome Analysismentioning

confidence: 99%

“…Rodents were randomly assigned to the following cohorts (n = 8/group): naïve; multicompartmental injury (PT); and multicompartmental injury plus daily restraint stress (PT/CS) similar to previously described. 24 A total of 56 rats were enrolled in the study: 48 assigned to groups (eight males and eight females per cohort) and 8 as donors for pseudofracture. Based on a power analysis, assuming greater than 80% incidence in control rats at baseline, a 30% change would require a minimum of eight rats per group.…”

Section: Experimental Designmentioning

confidence: 99%

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Multicompartmental traumatic injury induces sex-specific alterations in the gut microbiome

Munley

Kelly

Park

et al. 2023

J Trauma Acute Care Surg

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A rat model of multicompartmental traumatic injury and hemorrhagic shock induces bone marrow dysfunction and profound anemia

Kelly,

Munley,

Pons

et al. 2024

Anim Models and Exp Med

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BackgroundSevere trauma is associated with systemic inflammation and organ dysfunction. Preclinical rodent trauma models are the mainstay of postinjury research but have been criticized for not fully replicating severe human trauma. The aim of this study was to create a rat model of multicompartmental injury which recreates profound traumatic injury.MethodsMale Sprague–Dawley rats were subjected to unilateral lung contusion and hemorrhagic shock (LCHS), multicompartmental polytrauma (PT) (unilateral lung contusion, hemorrhagic shock, cecectomy, bifemoral pseudofracture), or naïve controls. Weight, plasma toll‐like receptor 4 (TLR4), hemoglobin, spleen to body weight ratio, bone marrow (BM) erythroid progenitor (CFU‐GEMM, BFU‐E, and CFU‐E) growth, plasma granulocyte colony‐stimulating factor (G‐CSF) and right lung histologic injury were assessed on day 7, with significance defined as p values <0.05 (*).ResultsPolytrauma resulted in markedly more profound inhibition of weight gain compared to LCHS (p = 0.0002) along with elevated plasma TLR4 (p < 0.0001), lower hemoglobin (p < 0.0001), and enlarged spleen to body weight ratios (p = 0.004). Both LCHS and PT demonstrated suppression of CFU‐E and BFU‐E growth compared to naïve (p < 0.03, p < 0.01). Plasma G‐CSF was elevated in PT compared to both naïve and LCHS (p < 0.0001, p = 0.02). LCHS and PT demonstrated significant histologic right lung injury with poor alveolar wall integrity and interstitial edema.ConclusionsMulticompartmental injury as described here establishes a reproducible model of multicompartmental injury with worsened anemia, splenic tissue enlargement, weight loss, and increased inflammatory activity compared to a less severe model. This may serve as a more effective model to recreate profound traumatic injury to replicate the human inflammatory response postinjury.

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Multicompartmental traumatic injury and the microbiome: Shift to a pathobiome

Abstract: Severe trauma in a rodent model shifts the microbiome to a pathobiome characterized by decreased diversity and an overabundance of pathogenic organisms. These findings persist in chronic stress and may influence outcomes after multicompartmental trauma.

Cited by 15 publications

References 52 publications

Prebiotic mechanisms of resistant starches from dietary beans and pulses on gut microbiome and metabolic health in a humanized murine model of aging

Prebiotic mechanisms of resistant starches from dietary beans and pulses on gut microbiome and metabolic health in a humanized murine model of aging

Multicompartmental traumatic injury induces sex-specific alterations in the gut microbiome

A rat model of multicompartmental traumatic injury and hemorrhagic shock induces bone marrow dysfunction and profound anemia

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