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Gut Bacterial Translocation via the Portal Vein: A Clinical Perspective with Major Torso Trauma
Abstract
Animal studies implicate gut bacterial translocation via the portal vein as a major factor in the pathogenesis of postinjury multiple organ failure (MOF). We therefore inserted portal vein catheters for sequential blood sampling in the operating room, at 6, 12, 24, and 48 hours, and 5 days postoperatively in 20 injured patients (13 blunt, seven penetrating; mean age, 34 years) requiring emergent laparotomy and who were at known risk for MOF. The mean Revised Trauma Score was 6.4 +/- 0.4, and the Injury Severity Score, 29.3 +/- 2.3. Twelve (60%) patients arrived in shock (SBP less than 90 torr). Eight (2%) of 212 portal blood cultures were positive; seven were presumed contaminants. The only positive systemic culture (total, 212) was a Staphylococcus aureus on day 5 in a patient with a concurrent staphyloccal pneumonia. In the first 48 hours, we could not detect endotoxin in portal or systemic blood. Additionally, simultaneous portal and systemic blood levels of complement fragment C3a, tumor necrosis factor, and interleukin-6 were nearly identical and, specifically, were not different in those patients who developed MOF. In summary, this prospective clinical study has not confirmed portal or systemic bacteremia within the first 5 days postinjury, despite an eventual 30% incidence of MOF.
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“in a study of trauma patients at high risk of multiorgan failure,101 serial blood cultures drawn from indwelling portal vein catheters have shown minimum evidence of bacterial translocation and no association between portal vein bacteraemia and subsequent illness.”
From The microbiome and critical illness (2016) · cites this paper as [101]
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Zhang, Q., Raoof, M., Chen, Y., Sumi, Y., Sursal, T., Junger, W., Brohi, K., Itagaki, K., & Hauser, C. J. (2010) · Nature · doi:10.1038/nature08780 · Cited by 3,812
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Moore, F. A., & Moore, E. E. (1995) · Surgical Clinics of North America · doi:10.1016/s0039-6109(16)46587-4 · Cited by 522
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Self-citationEarly Predictors of Postinjury Multiple Organ Failure
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“While bacterial translocation clearly occurs in some preclinical models of critical illness (10), human data has generally remained inconclusive or not supportive of this as a common phenomenon seen in critically ill patients, although it likely occurs in select pathophysiologic conditions (11;12).”
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BackgroundBacterial Translocation from the Gastrointestinal Tract
Berg, R. D. (1999) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4143-1_2 · Cited by 407
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BackgroundMITOCHONDRIAL DNA IS RELEASED BY SHOCK AND ACTIVATES NEUTROPHILS VIA P38 MAP KINASE
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BackgroundEndotoxemia: Methods of detection and clinical correlates
Hurley, J. C. (1995) · Clinical Microbiology Reviews · doi:10.1128/cmr.8.2.268 · Cited by 318
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Diebel, L. N., Dulchavsky, S. A., & Brown, W. J. (1997) · doi:10.1097/00005373-199711000-00019 · Cited by 289
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Self-citationIntestinal permeability and systemic infections in critically ill patients: Effect of glutamine*
De-Souza, D. A., & Greene, L. J. (2005) · Critical Care Medicine · doi:10.1097/01.ccm.0000162680.52397.97 · Cited by 285
“(48), 20 critically ill patients were analyzed after major torso trauma (13 patients with blunt trauma and seven patients with penetrating trauma), some of them in a state of shock at the time of hospitalization (systolic blood pressure 90 torr in 12 patients, i.”
BackgroundPape, H., Rixen, D., Morley, J. R., Husebye, E. E., Mueller, M. R., Dumont, C., Gruner, A., Oestern, H. J., Bayeff-Filoff, M., Garving, C., et al. (2007) · Annals of Surgery · doi:10.1097/sla.0b013e3181485750 · Cited by 280
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Self-citationPape, H., Grimme, K., van Griensven, M., Sott, A. H., Giannoudis, P. V., Morley, J. R., Røise, O., Ellingsen, E., Hildebrand, F., Wiese, B., et al. (2003) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/01.ta.0000075787.69695.4e · Cited by 265
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“Importantly, the bacterial lineage was constant one year after the dietary intervention for a given body weight, validating the bacterial signature of each individual.”
BackgroundWanner, G. A., Keel, M. J. B., Steckholzer, U., Beier, W., Stocker, R. A., & Ertel, W. (2000) · Critical Care Medicine · doi:10.1097/00003246-200004000-00007 · Cited by 263
“Severe trauma represents an insult that causes a wide array of pathophysiologic alterations including hemorrhagic shock, hypoxia, hypotension, or even the invasion of bacterial compounds from the gut into the circulation ("bacterial translocation") (29, 30).”
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Deitch, E. A. (2001) · Current Opinion in Critical Care · doi:10.1097/00075198-200104000-00007 · Cited by 249
Postinjury neutrophil priming and activation: An early vulnerable window*
Botha, A. J., Moore, F. A., Moore, E. E., KIM, F., BANERJEE, A., & Peterson, V. M. (1995) · Surgery · doi:10.1016/s0039-6060(05)80345-9 · Cited by 252
Self-citationTiming of Fixation of Major Fractures in Blunt Polytrauma
Pape, H., Giannoudis, P. V., Krettek, C., & Trentz, O. (2005) · Journal of Orthopaedic Trauma · doi:10.1097/01.bot.0000161712.87129.80 · Cited by 249
“When 3 groups of patients with similar injuries were separated according to the duration of initial surgery, patients with the longest initial surgery (.6 hours) developed a significantly higher complication rate, namely ARDS and MOF.143 These results support the idea that orthopaedic surgeons play a pivotal role in i…”
BackgroundInfluentialGut-origin sepsis in the critically ill patient: pathophysiology and treatment
Assimakopoulos, S. F., Triantos, C., Thomopoulos, K., Fligou, F., Maroulis, I., Marangos, M., & Gogos, C. A. (2018) · Infection · doi:10.1007/s15010-018-1178-5 · Cited by 244
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Deitch, E. A. (2002) · Surgery · doi:10.1067/msy.2002.116408 · Cited by 233
Challenge to the Intestinal Mucosa During Sepsis
Haußner, F., Chakraborty, S., Halbgebauer, R., & Huber-Lang, M. S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00891 · Cited by 233
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“Furthermore, the attachment of commensal bacteria to the intestinal mucosa, and possible invasion across the epithelial barrier, has been hypothesized as a possible additional mechanism by which commensal bacteria may play a role in the development of gut-derived sepsis and multiple organ failure following trauma (6–9…”
ResultInfluentialChanges in blood lymphocyte populations after multiple trauma
Menges, T., Engel, J., Welters, I. D., Rm, W., Little, S., Ruwoldt, R., Wollbrück, M., & Hempelmann, G. (1999) · Critical Care Medicine · doi:10.1097/00003246-199904000-00026 · Cited by 228
Endotoxemia—menace, marker, or mistake?
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“growing bacteria from mesenteric lymph nodes than from portal blood [25, 26].”
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Ciesla, D. J. (2005) · Archives of Surgery · doi:10.1001/archsurg.140.5.432 · Cited by 2
“In 1987, we developed an MOF scale as a descriptive end point for clinical studies.(17) Since 1992, we have prospectively collected clinical data on patients at risk for postinjury MOF for the first 28 postinjury days.”
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“[126] inserted portal vein catheters for sequential blood sampling in 20 injured patients requiring emergency laparotomy and who were at known risk of MOF.”
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Gatt, M., REDDY, B. S., & Macfie, J. M. (2006) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2006.03174.x · Cited by 205
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BackgroundSHANAB, A. A. A., Scully, P., Crosbie, O. M., Buckley, M. J. M., O’Mahony, L., Shanahan, F., Gazareen, S., Murphy, E., & Quigley, E. M. M. (2010) · Digestive Diseases and Sciences · doi:10.1007/s10620-010-1447-3 · Cited by 195
“Endogenous lipopolysaccharide (LPS) is continuously released from the gut after the death of Gram-negative bacteria [29] and is then transported via a toll-like receptor 4 (TLR-4)-dependent process into intestinal capillaries [30–32].”
BackgroundThe intestinal microenvironment in sepsis
Fay, K. T., Ford, M. L., & Coopersmith, C. M. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.03.005 · Cited by 196
“Further, in a classic study of trauma patients – who typically have intestinal hyperpermeability -- catheters placed in the portal venous system demonstrated intact bacteria less than ten percent of the time (13).”
BackgroundEarly Definitive Stabilization of Unstable Pelvis and Acetabulum Fractures Reduces Morbidity
Vallier, H. A., Cureton, B. A., Ekstein, C., et al. (2010) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/ta.0b013e3181e50914 · Cited by 180
Translocation of gut flora and its role in sepsis
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Early Complementopathy After Multiple Injuries in Humans
Burk, A.-M., Martin, M., Flierl, M. A., Rittirsch, D., Helm, M., Lampl, L. A., Brückner, U. B., Stahl, G. L., Blom, A. M., Perl, M., et al. (2012) · Shock · doi:10.1097/shk.0b013e3182471795 · Cited by 173
“However, despite detection of increased serum anaphylatoxin concentrations after trauma, clinical studies failed to confirm C3a or other complement fragments as specific markers for adult respiratory distress syndrome or multiple-organ failure (28, 29).”
BackgroundTrauma alarmins as activators of damage-induced inflammation
Manson, J., Thiemermann, C., & Brohi, K. (2011) · British journal of surgery · doi:10.1002/bjs.7717 · Cited by 188
Review article: intestinal failure
Lal, S., Teubner, A., & Shaffer, J. (2006) · Alimentary Pharmacology and Therapeutics · doi:10.1111/j.1365-2036.2006.02941.x · Cited by 141
Serum Levels of Hsp 72 Measured Early after Trauma Correlate with Survival
Pittet, J., Lee, H., Morabito, D. J., Howard, M., Welch, W. J., & Mackersie, R. C. (2002) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/00005373-200204000-00001 · Cited by 160
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Carsin, H., Assicol, M., Féger, F., et al. (1997) · Burns · doi:10.1016/s0305-4179(96)00124-6 · Cited by 155
Panzer, A. R., Lynch, S. V., Langelier, C., Christie, J. D., McCauley, K. E., Nelson, M. F., Cheung, C. K., Benowitz, N. L., Cohen, M. J. M., & Calfee, C. S. (2017) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201702-0441oc · Cited by 157
Pathophysiology in patients with polytrauma
Pape, H., Moore, E. E., McKinley, T. O., & Sauaia, A. (2022) · Injury · doi:10.1016/j.injury.2022.04.009 · Cited by 163
Self-citationIntestinal Permeability Correlates with Severity of Injury in Trauma Patients
Faries, P. L., Simón, R., Martella, A. T., Lee, M. J., & Machiedo, G. W. (1998) · doi:10.1097/00005373-199806000-00016 · Cited by 148
Deitch, E. A., Adams, C. A., Lu, Q., & Xu, D.-Z. (2001) · Surgery · doi:10.1067/msy.2001.109119 · Cited by 146
VALIDATION OF POSTINJURY MULTIPLE ORGAN FAILURE SCORES
Sauaia, A., Moore, E. E., Johnson, J. L., Ciesla, D. J., Biffl, W. L., & Banerjee, A. M. (2009) · Shock · doi:10.1097/shk.0b013e31818ba4c6 · Cited by 143
“The Denver MOF score was first proposed in 1991 as part of a National Institutes of Health Center Project (34), then modified in 1993 (35) by a panel of expert trauma surgeons and trauma investigators.”
MethodSelf-citationThe role of the gut in the development of multiple organ dysfunction in cardiothoracic patients
Baue, A. E. (1993) · The Annals of Thoracic Surgery · doi:10.1016/0003-4975(93)90098-3 · Cited by 147
Current status of bacterial translocation as a cause of surgical sepsis
MacFie, J. (2004) · British Medical Bulletin · doi:10.1093/bmb/ldh029 · Cited by 145
Hauser, C. J., Zhou, X., Joshi, P. C., Cuchens, M. A., Kregor, P. J., Devidas, M., Kennedy, R. J., Poole, G. V., & Hughes, J. L. (1997) · doi:10.1097/00005373-199705000-00021 · Cited by 140
The digestive tract as the origin of systemic inflammation
de Jong, P. R., González-Navajas, J. M., & Jansen, N. J. G. (2016) · Critical Care · doi:10.1186/s13054-016-1458-3 · Cited by 146
“It is important to point out here that, in a classic study, portal vein sampling in trauma patients undergoing laparotomy did not provide evidence for bacterial translocation by blood cultures [43].”
BackgroundMultiple Organ Dysfunction Syndrome
Gourd, N. M., & Nikitas, N. (2019) · Journal of Intensive Care Medicine · doi:10.1177/0885066619871452 · Cited by 137
Bennett‐Guerrero, E. (1997) · JAMA · doi:10.1001/jama.1997.03540320048034 · Cited by 130
Increased gut permeability after multiple trauma
Pape, H., Dwenger, A., Regel, G., et al. (1994) · British journal of surgery · doi:10.1002/bjs.1800810619 · Cited by 129
Baterial Translocation in Humans
Lichtman, S. N. (2001) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200107000-00001 · Cited by 126
“(43) obtained portal venous blood cultures and endotoxin concentrations in 20 patients.”
BackgroundSplanchnic ischaemia/reperfusion and multiple organ failure
Biffl, W. L., & Moore, E. E. (1996) · British Journal of Anaesthesia · doi:10.1093/bja/77.1.59 · Cited by 123
“Although we had not found evidence of bacterial translocation in our severely injured patients who developed MOF [90], we were interested in whether LPS was involved in PMN priming in our I/R model.”
BackgroundMethodInfluentialSelf-citationWickel, D. J., Cheadle, W. G., Mercer-Jones, M. A., & Garrison, R. N. (1997) · Annals of Surgery · doi:10.1097/00000658-199706000-00012 · Cited by 121
Bacterial translocation in multiple organ failure: Cause or epiphenomenon still unproven
Lemaire, L. C. J. M., van Lanschot, J. J. B., Stoutenbeek, C. P., van Deventer, S. J. H., Wells, C. L., & Gouma, D. J. (1997) · British journal of surgery · doi:10.1111/j.1365-2168.1997.00520.x · Cited by 127
Early Cytokine Production Risk Stratifies Trauma Patients for Multiple Organ Failure
Jastrow, K. M., Gonzalez, E. A., McGuire, M. F., Suliburk, J. W., Kozar, R. A., Iyengar, S., Motschall, D., McKinley, B. A., Moore, F. A., & Mercer, D. (2009) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2009.05.002 · Cited by 118
Self-citationThe Horror Autotoxicus and Multiple-Organ Failure
Baue, A. E. (1992) · Archives of Surgery · doi:10.1001/archsurg.1992.01420120085016 · Cited by 116
Clements, T. W., Tolonen, M., Ball, C. G., & Kirkpatrick, A. W. (2021) · Scandinavian Journal of Surgery · doi:10.1177/1457496920984078 · Cited by 115
“Nonetheless, bacterial translocation through the portal system was long been a favored mechanism of systemic insult in abdominal pathology, but this theory now has been superseded by the gut-lymph hypothesis, as systemic sepsis from intra-abdominal sources happens in the absence of clear bacterial translocation (50).”
BackgroundThe role of the lung in postinjury multiple organ failure
Ciesla, D. J., Moore, E. E., Johnson, J. L., Burch, J. M., Cothren, C. C., & Sauaia, A. (2005) · Surgery · doi:10.1016/j.surg.2005.07.020 · Cited by 113
Self-citationDeitch, E. A., Forsythe, R. M., Anjaria, D. J., Livingston, D. H., Lu, Q., Xu, D.-Z., & Redl, H. (2004) · Shock · doi:10.1097/01.shk.0000133592.55400.83 · Cited by 113
“Specifically, this concept that the mesenteric lymphatics rather than the portal blood is the major route by which tissue injurious factors exit the gut after gut injury helps explain how the gut can contribute to distant organ injury and yet the portal vein of trauma patients not contain bacteria or endotoxin (18).”
BackgroundMicrobial Translocation in Neonates and Infants Receiving Long-term Parenteral Nutrition
Pierro, A. (1996) · Archives of Surgery · doi:10.1001/archsurg.1996.01430140066018 · Cited by 112
Alterations in intestinal microbial flora and human disease
Othman, M. O., Agüero, R., & Lin, H. C. (2008) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3282f2b0d7 · Cited by 112
“Although it was demonstrated in animal models that bacteria translocate to mesenteric lymph nodes and enter the circulation through portal blood [70], a prospective human trial failed to detect a significant level of bacteria, bacterial endotoxin or inflammatory markers in the portal circulation of patients with major…”
BackgroundAmornphimoltham, P., Yuen, P. S. T., Star, R. A., & Leelahavanichkul, A. (2019) · Digestive Diseases and Sciences · doi:10.1007/s10620-019-05581-y · Cited by 109
Posthemorrhagic Shock Mesenteric Lymph Primes Circulating Neutrophils and Provokes Lung Injury
Zallen, G. S., Moore, E. E., Johnson, J. L., Tamura, D. Y., Ciesla, D. J., & Silliman, C. C. (1999) · Journal of Surgical Research · doi:10.1006/jsre.1999.5569 · Cited by 107
Self-citationSenthil, M., Brown, M., Xu, D.-Z., Lu, Q., Feketeova, E., & Deitch, E. A. (2006) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/01.ta.0000215500.00018.47 · Cited by 104
Endothelial cell activity varies in patients at risk for the adult respiratory distress syndrome
Moss, M. M., Gillespie, M. K., Ackerson, L., et al. (1996) · Critical Care Medicine · doi:10.1097/00003246-199611000-00004 · Cited by 103
Self-citationShenkar, R., Coulson, W. F., & Abraham, E. (1994) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.10.3.8117448 · Cited by 102
Intestinal permeability is increased after major vascular surgery
Roumen, R. M. H., van der Vliet, J. A., Wevers, R. A., et al. (1993) · Journal of Vascular Surgery · doi:10.1016/0741-5214(93)90118-6 · Cited by 98
Metadata
- Authors
- MOORE, F. A., MOORE, E. E., POGGETTI, R., McANENA, O. J., PETERSON, V. M., ABERNATHY, C. M., & PARSONS, P. E.
- Affiliations
- Denver Health Medical Center (US)
- ORCID
- MOORE, ERNEST E.
- Venue
- The Journal of Trauma: Injury, Infection, and Critical Care
- Published
- 1991-05
- Volume
- 31
- Issue
- 5
- Pages
- 629-638
- ISSN
- 0022-5282 (ISSN-L)
- OpenAlex
- W2053522978
- Cited by
- 491
- References
- 0
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 6 · 2023: 8 · 2022: 5 · 2021: 3 · 2020: 12 · 2019: 8 · 2018: 14 · 2017: 18 · 2016: 22 · 2015: 13 · 2014: 9 · 2013: 11 · 2012: 10
- FWCI
- 16.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Trauma: Injury, Infection, and Critical Care (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5p50hl040784-10)
- National Heart, Lung, and Blood Institute (P50 HL-40784-01, K08 HLO-1849-04)
- Topics
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Sepsis Diagnosis and Treatment
- Health Sciences › Medicine › Surgery › Abdominal Trauma and Injuries
- Health Sciences › Medicine › Surgery › Abdominal Surgery and Complications
- Keywords
- gut bacterial translocation, portal vein, multiple organ failure, bacteremia, trauma (physical injury), endotoxin, complement C3a, TNF-α, interleukin-6, traumatic shock
- MeSH terms
- Abdominal Injuries, Adult, Bacteria, Endotoxins, Humans, Intestines, Multiple Organ Failure, Multiple Trauma, Portal Vein, Prospective Studies, Wounds, Nonpenetrating, Trauma Severity Indices, Interleukin-6, Fractures, Bone
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