The Microbiology of Multiple Organ Failure: The Proximal Gastrointestinal Tract as an Occult Reservoir of Pathogens
Abstract
The microbiology of infection acquired in the intensive care unit (ICU) was studied prospectively in 205 consecutive patients admitted to a surgical intensive care unit. A multiple organ failure (MOF) score was calculated for each admission. Susceptibility to ICU-acquired infection increased with increasing MOF scores. While Escherichia coli, Bacteroides fragilis, and enterococci were the most common isolates from infections present at the time of ICU admission, Staphylococcus epidermidis, Candida, and Pseudomonas dominated infections occurring in patients with high MOF scores. Mortality correlated highly with infection due to S epidermidis or Candida and only poorly with infection due to Pseudomonas or E coli; significant foci of invasive infection were frequently absent at autopsy. Quantitative cultures of proximal gastrointestinal fluid in 16 of these patients showed Candida, S epidermidis, and Pseudomonas to be the most common isolates, and all but one patient colonized with these organisms had invasive infection with the same organism. The proximal gastrointestinal tract appears to be an important occult reservoir of the predominant pathogens in MOF.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In critical illness, the stomach and proximal small intestine become overgrown by a small number of species, such as E coli, P aeruginosa, and Enterococcus spp.
“The stomach and proximal small intestine, which are usually sparsely populated, become overgrown by a small number of species, such as E coli, P aeruginosa, and Enterococcus spp.”
From The microbiome and critical illness (2016) · cites this paper as [67]
The upper gastrointestinal tract becomes a stagnant reservoir of potential pathogens whose presence is predictive of extra-abdominal infections and multiorgan failure.
“The upper gastrointestinal tract becomes a stagnant reservoir of potential pathogens, the presence of which is predictive of extra-abdominal infections and multiorgan failure.”
From The microbiome and critical illness (2016) · cites this paper as [67]
The dynamics of the aerodigestive tract become inverted during critical illness: the overgrown microbial reservoir of the stomach and small intestine becomes the primary source community for the mouth and lungs.
“the overgrown microbial reservoir of the stomach and small intestine becomes the primary source community for the mouth and lungs.”
From The microbiome and critical illness (2016) · cites this paper as [67]
Cites
Baker, S. P., O’Neill, B., Haddon, W. F., & Long, W. B. (1974) · PubMed · Cited by 7,946 · see citing works
APACHE—acute physiology and chronic health evaluation: a physiologically based classification system
Knaus, W. A., Zimmerman, J. E., Wagner, D. P., Draper, E. A., & Lawrence, D. E. (1981) · Critical Care Medicine · doi:10.1097/00003246-198108000-00008 · Cited by 2,190 · see citing works
Cachectin: More Than a Tumor Necrosis Factor
Epstein, F. H., Beutler, B., & Cerami, A. (1987) · New England Journal of Medicine · doi:10.1056/nejm198702123160705 · Cited by 1,423 · see citing works
McCabe, W. R. (1962) · Archives of Internal Medicine · doi:10.1001/archinte.1962.03620240029006 · Cited by 1,378 · see citing works
Fry, D. E. (1980) · Archives of Surgery · doi:10.1001/archsurg.1980.01380020006003 · Cited by 740 · see citing works
Stoutenbeek, C. P., SAENE, H. K. F. V., Miranda, D. R., & Zandstra, D. F. (1984) · Intensive Care Medicine · doi:10.1007/bf00259435 · Cited by 711 · see citing works
Lehmann, V., Freudenberg, M. A., & Galanos, C. (1987) · The Journal of Experimental Medicine · doi:10.1084/jem.165.3.657 · Cited by 547 · see citing works
Multiple Organ Failure in Polytrauma Patients
Faist, E., Baue, A. E., Dittmer, H., & Heberer, G. (1983) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/00005373-198309000-00002 · Cited by 494 · see citing works
Multiple, Progressive, or Sequential Systems Failure
Baue, A. E. (1975) · Archives of Surgery · doi:10.1001/archsurg.1975.01360130011001 · Cited by 481 · see citing works
DUMOULIN, G. (1982) · The Lancet · doi:10.1016/s0140-6736(82)90974-6 · Cited by 468 · see citing works
Patterns Of Septic Shock In Man—a Detailed Study Of 56 Patients
MacLean, L. D., Mulligan, W. G., McLean, A. P. H., & Duff, J. H. (1967) · Annals of Surgery · doi:10.1097/00000658-196710000-00004 · Cited by 384 · see citing works
FUNGÆMIA AND FUNGURIA AFTER ORAL ADMINISTRATION OF CANDIDA ALBICANS
Kŕause, W., Matheis, H., & Wulf, K. (1969) · The Lancet · doi:10.1016/s0140-6736(69)91534-7 · Cited by 354 · see citing works
Respiratory failure, hypotension, sepsis, and jaundice
Skillman, J. J., Bushnell, L. S., Goldman, H., & Silen, W. (1969) · The American Journal of Surgery · doi:10.1016/0002-9610(69)90011-7 · Cited by 284 · see citing works
Determinants of Organ Malfunction or Death in Patients With Intra-abdominal Sepsis
Pine, R. W. (1983) · Archives of Surgery · doi:10.1001/archsurg.1983.01390020084014 · Cited by 214 · see citing works
Remote organ failure: a valid sign of occult intra-abdominal infection.
Hc, P., & Cl, S. (1977) · PubMed · Cited by 206 · see citing works
The role of Candida in intraperitoneal infections.
Solomkin, J. S., Flohr, A. B., Quie, P. G., & Simmons, R. L. (1980) · PubMed · Cited by 195 · see citing works
McCabe, W. R. (1973) · Disease-a-Month · doi:10.1016/s0011-5029(73)80016-1 · Cited by 190 · see citing works
Enterococcal Bacteremia Clinical Implications and Determinants of Death
Garrison, R. N., FRY, D. E., Berberich, S., & Polk, H. C. (1982) · Annals of Surgery · doi:10.1097/00000658-198207000-00010 · Cited by 166 · see citing works
The Changing Pattern of Life-Threatening Microbial Disease
Rogers, D. E. (1959) · New England Journal of Medicine · doi:10.1056/nejm195910012611401 · Cited by 157 · see citing works
The Bacteriology of Intra-abdominal Infections
Lorber, B., & Swenson, R. M. (1975) · Surgical Clinics of North America · doi:10.1016/s0039-6109(16)40792-9 · Cited by 156 · see citing works
Wiles, J. B., Cerra, F. B., Siegel, J. H., & Border, J. R. (1980) · Critical Care Medicine · doi:10.1097/00003246-198002000-00001 · Cited by 151 · see citing works
Colonization of the gastric contents in critically patients
Hillman, K., Riordan, T., O’Farrell, S., & Tabaqchali, S. (1982) · Critical Care Medicine · doi:10.1097/00003246-198207000-00005 · Cited by 148 · see citing works
Both Inflammatory and Endocrine Mediators Stimulate Host Responses to Sepsis
Watters, J. M. (1986) · Archives of Surgery · doi:10.1001/archsurg.1986.01400020065008 · Cited by 144 · see citing works
Infection Prevention During Profound Granulocytopenia
Schimpff, S. C. (1980) · Annals of Internal Medicine · doi:10.7326/0003-4819-93-2-358 · Cited by 127 · see citing works
Does drainage of intraabdominal pus reverse multiple organ failure?
Norton, L. W. (1985) · The American Journal of Surgery · doi:10.1016/s0002-9610(85)80105-7 · Cited by 118 · see citing works
Intestinal Bacteria Translocate Into Experimental Intra-abdominal Abscesses
Wells, C. L. (1986) · Archives of Surgery · doi:10.1001/archsurg.1986.01400010116016 · Cited by 114 · see citing works
The Surgical Intensive Care Unit: Current Concepts in Infection
Meakins, J. L., Wicklund, B. M., Forse, R. A., & McLean, A. P. H. (1980) · Surgical Clinics of North America · doi:10.1016/s0039-6109(16)42038-4 · Cited by 104 · see citing works
The cause of post-traumatic pulmonary insufficiency in man.
Rl, F., & Ce, J. (1975) · PubMed · Cited by 89 · see citing works
Staphylococcus epidermidis: an important pathogen.
Forse, R. A., Dixon, C., Bernard, K., Martínez, L. F., McLean, A. P., & Jl, M. (1979) · PubMed · Cited by 87 · see citing works
Rotstein, O. D., Pruett, T., & Simmons, R. L. (1986) · PubMed · Cited by 79 · see citing works
The prevention of superinfection in multiple trauma patients
Stoutenbeek, C. P., van Saene, H. K. F., Miranda, D. R., Zandstra, D. F., & Binnendijk, B. (1984) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/14.suppl_b.203 · Cited by 69 · see citing works
Kupffer Cell Modulation of the Systemic Immune Response
Marshall, J. C. (1987) · Archives of Surgery · doi:10.1001/archsurg.1987.01400140073009 · Cited by 59 · see citing works
Prevention of Multiple Systems Failure
Baue, A. E., & Chaudry, I. H. (1980) · Surgical Clinics of North America · doi:10.1016/s0039-6109(16)42240-1 · Cited by 53 · see citing works
Physiology and Metabolism in Isolated Viral Septicemia
Deutschman, C. S. (1987) · Archives of Surgery · doi:10.1001/archsurg.1987.01400130027003 · Cited by 35 · see citing works
Newer Aspects of Septicemia in Surgical Patients
Altemeier, W. A. (1966) · Archives of Surgery · doi:10.1001/archsurg.1966.01320220122020 · Cited by 28 · see citing works
Christou, N. V., Boisvert, G., Broadhead, M., & Meakins, J. L. (1985) · World Journal of Surgery · doi:10.1007/bf01655198 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Bone, R. C., BALK, R. A., Cerra, F. B., Dellinger, R. P., Fein, A. M., Knaus, W. A., Schein, R. M. H., & Sibbald, W. J. (1992) · CHEST Journal · doi:10.1378/chest.101.6.1644 · Cited by 13,192 · see citing works
Multiple Organ Dysfunction Score
Marshall, J. C., Cook, D. J., Christou, N. V., Bernard, G. R., Sprung, C. L., & Sibbald, W. J. (1995) · Critical Care Medicine · doi:10.1097/00003246-199510000-00007 · Cited by 2,531 · see citing works
Moore, F. A., Feliciano, D. V., Andrassy, R. J., McArdle, A. H., Booth, F. V. M., MORGENSTEIN-WAGNER, T. B., Kellum, J. M., Welling, R. E., & Moore, E. E. (1992) · Annals of Surgery · doi:10.1097/00000658-199208000-00008 · Cited by 1,374 · see citing works
Gastric intramucosal pH as a therapeutic index of tissue oxygenation in critically ill patients
Gutiérrez, G., Pálizas, F., Doglio, G. R., Pusajo, J. F., Wainsztein, N. A., Klein, F., Gallesio, A. O., Román, E. S., Pacin, J., Dorfman, B., et al. (1992) · The Lancet · doi:10.1016/0140-6736(92)90002-k · Cited by 840 · see citing works
Pathological bacterial translocation in liver cirrhosis
Wiest, R., Lawson, M. A., & Geuking, M. B. (2013) · Journal of Hepatology · doi:10.1016/j.jhep.2013.07.044 · Cited by 815 · see citing works
“In addition, proximal gut colonization has been associated with increased BT and septic morbidity in surgical intensive care patients [208,209], indicating that small intestinal bacterial overgrowth has the greatest potential for promoting BT.”
BackgroundThe Logistic Organ Dysfunction System
Gall, J. L. (1996) · JAMA · doi:10.1001/jama.1996.03540100046027 · Cited by 733 · see citing works
The gastrointestinal tract. The “undrained abscess” of multiple organ failure
Marshall, J. C., Christou, N. V., & Meakins, J. L. (1993) · Annals of Surgery · doi:10.1097/00000658-199308000-00001 · Cited by 707 · see citing works
Bacterial translocation (BT) in cirrhosis†
Wiest, R., & Garcia‐Tsao, G. (2005) · Hepatology · doi:10.1002/hep.20632 · Cited by 677 · see citing works
Laboratory models of sepsis and septic shock
Fink, M. P., & Heard, S. O. (1990) · Journal of Surgical Research · doi:10.1016/0022-4804(90)90260-9 · Cited by 541 · see citing works
Multiple Organ Failure Syndrome in the 1990s
Beal, A. L. (1994) · JAMA · doi:10.1001/jama.1994.03510270072043 · Cited by 530 · see citing works
Evolving Concepts in the Pathogenesis of Postinjury Multiple Organ Failure
Moore, F. A., & Moore, E. E. (1995) · Surgical Clinics of North America · doi:10.1016/s0039-6109(16)46587-4 · Cited by 525 · see citing works
Inflammation, coagulopathy, and the pathogenesis of multiple organ dysfunction syndrome
Marshall, J. C. (2001) · Critical Care Medicine · doi:10.1097/00003246-200107001-00032 · Cited by 452 · see citing works
“Characteristic infecting florae include opportunistic organisms of low intrinsic virulence (notably Candida, coagulase-negative Staphylococci, Pseudomonas, and Enterococci) (6), as well as species whose emergence reflects local environmental factors (notably Acinetobacter and Stenotrophomonas) or selective antimicrobi…”
BackgroundThe microbiome and critical illness
Dickson, R. P. (2016) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(15)00427-0 · Cited by 460 · see citing works
Comparison of the Safety of Early Enteral vs Parenteral Nutrition in Mild Acute Pancreatitis
McClave, S. A., Greene, L. M., Snider, H. L., Makk, L., Cheadle, W. G., Owens, N. A., Dukes, L. G., & Goldsmith, L. J. (1997) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/014860719702100114 · Cited by 434 · see citing works
Macfie, J., OBoyle, C., Mitchell, C. J., Buckley, P. M., Johnstone, D. J., & Sudworth, P. (1999) · Gut · doi:10.1136/gut.45.2.223 · Cited by 414 · see citing works
Marik, P. E. (1994) · JAMA · doi:10.1001/jama.1994.03520170064037 · Cited by 398 · see citing works
Uncoupling of biological oscillators
Godin, P. J., & Buchman, T. G. (1996) · Critical Care Medicine · doi:10.1097/00003246-199607000-00008 · Cited by 377 · see citing works
The prevalence of gut translocation in humans
Sedman, P. C., Macfle, J., Sagar, P., Mitchell, C. J., May, J., Mancey-Jones, B., & Johnstone, D. (1994) · Gastroenterology · doi:10.1016/0016-5085(94)90110-4 · Cited by 362 · see citing works
Noninvasive Versus Invasive Microbial Investigation in Ventilator-associated Pneumonia
Ruiz, M., Torres, A., Ewig, S., Marcos, M. Á., Alcón, A., Lledó, R., Asenjo, M. A., & MALDONALDO, A. (2000) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.162.1.9907090 · Cited by 338 · see citing works
“With significant growth in culture 11 (28) 9 (24)”
BackgroundSouba, W. W., Klimberg, V. S., Plumley, D. A., Salloum, R. M., Flynn, T. C., Bland, K. I., & Copeland, E. M. (1990) · Journal of Surgical Research · doi:10.1016/0022-4804(90)90080-l · Cited by 334 · see citing works
Abdominal Compartment Syndrome
Saggi, B. H., Sugerman, H. J., Ivatury, R. R., & Bloomfield, G. L. (1998) · doi:10.1097/00005373-199809000-00033 · Cited by 332 · see citing works
Selective Decontamination of the Digestive Tract in Surgical Patients
Nathens, A. B. (1999) · Archives of Surgery · doi:10.1001/archsurg.134.2.170 · Cited by 319 · see citing works
Marik, P. E. (1993) · CHEST Journal · doi:10.1378/chest.104.1.225 · Cited by 309 · see citing works
Krueger, W. A., Lenhart, F.-P., Neeser, G., Ruckdeschel, G., Schreckhase, H., Eissner, H. J., Forst, H., Eckart, J., Peter, K., & Unertl, K. E. (2002) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.2105141 · Cited by 299 · see citing works
“The rationale for the use of topical antibiotics is based on the observation that the oropharynges of critically ill patients are colonized by potentially pathogenic bacteria (16, 17), which together with gastrointestinal overgrowth cause nosocomial pneumonia and multiple organ failure (19, 52, 53).”
BackgroundVincent, J., Anaissie, E. J., Bruining, H. A., Demajo, W. A. P., El-Ebiary, M., Haber, J. A., Hiramatsu, Y., Nitenberg, G., Nyström, P. O., Pittet, D., et al. (1998) · Intensive Care Medicine · doi:10.1007/s001340050552 · Cited by 273 · see citing works
“This may not produce systemic infection in otherwise healthy patients, but life-threatening illness may result in the critically ill [18, 19, 5].”
BackgroundThe role of the gastrointestinal tract in postinjury multiple organ failure
Moore, F. A. (1999) · The American Journal of Surgery · doi:10.1016/s0002-9610(99)00231-7 · Cited by 268 · see citing works
Ma, Z., Zuo, T., Frey, N., & Rangrez, A. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01946-6 · Cited by 297 · see citing works
Role of the gut lymphatic system in multiple organ failure
Deitch, E. A. (2001) · Current Opinion in Critical Care · doi:10.1097/00075198-200104000-00007 · Cited by 249 · see citing works
Mortality and causes of death in a burn centre
Bloemsma, G. C., Dokter, J., Boxma, H., & Oen, I. M. M. H. (2008) · Burns · doi:10.1016/j.burns.2008.02.010 · Cited by 235 · see citing works
“[15] Marshall JC, Christou NV, Horn R, Meakins JL.”
BackgroundJain, P. K., McNaught, C. E., Anderson, A. D. G., Macfie, J., & Mitchell, C. J. (2004) · Clinical Nutrition · doi:10.1016/j.clnu.2003.12.002 · Cited by 211 · see citing works
Freestone, P. P. E., Lyte, M., Neal, C. P., Maggs, A. F., Haigh, R., & WILLIAMS, P. H. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.21.6091-6098.2000 · Cited by 210 · see citing works
“In trauma and burn patients, in whom the development of intra-abdominal sepsis due to commensal bacteria is frequently observed, severe tissue damage is associated with massive systemic release of NE, which eventually spills over into the gastrointestinal tract (5, 25, 28, 29, 37).”
BackgroundSelective Decontamination of the Digestive Tract
Heyland, D. K., Cook, D. J., Jaeschke, R., Griffith, L. E., Lee, H. N., & Guyatt, G. H. (1994) · CHEST Journal · doi:10.1378/chest.105.4.1221 · Cited by 210 · see citing works
Bacterial translocation in the gut
Wiest, R., & Rath, H. C. (2003) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/s1521-6918(03)00024-6 · Cited by 204 · see citing works
Hébert, P. C., Drummond, A. J., Singer, J., Bernard, G. R., & Russell, J. A. (1993) · CHEST Journal · doi:10.1378/chest.104.1.230 · Cited by 199 · see citing works
Gianotti, L., Alexander, J. W., Gennari, R., Pyles, T., & Babcock, G. F. (1995) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/014860719501900169 · Cited by 194 · see citing works
Tertiary Peritonitis: Clinical Features of a Complex Nosocomial Infection
Nathens, A. B., Rotstein, O. D., & Marshall, J. C. (1998) · World Journal of Surgery · doi:10.1007/s002689900364 · Cited by 194 · see citing works
Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers
Freestone, P. P. E., Haigh, R. D., Williams, P. H., & Lyte, M. (1999) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1999.tb13449.x · Cited by 199 · see citing works
Intensive care unit management of intra-abdominal infection
Marshall, J. C., & Innes, M. E. (2003) · Critical Care Medicine · doi:10.1097/01.ccm.0000087326.59341.51 · Cited by 183 · see citing works
A prospective randomised trial of probiotics in critically ill patients
MCNAUGHT, C., WOODCOCK, N., ANDERSON, A., & MACFIE, J. (2005) · Clinical Nutrition · doi:10.1016/j.clnu.2004.08.008 · Cited by 179 · see citing works
Increased plasma and ventricular fluid interleukin-6 levels in patients with head injury.
McClain, C. J., Cohen, D. A., Phillips, R. J., Ott, L. G., & Young, B. A. (1991) · PubMed · Cited by 171 · see citing works
Neuroendocrine–Bacterial Interactions in a Neurotoxin-Induced Model of Trauma
Lyte, M., & Bailey, M. T. (1997) · Journal of Surgical Research · doi:10.1006/jsre.1997.5130 · Cited by 168 · see citing works
“system has often followed traumatic injury in cases Background: The destruction of noradrenergic where direct injury to the gastrointestinal system has nerve cell innervation and resultant release of norepi- not occurred [1–3].”
BackgroundThe Logistic Organ Dysfunction System
Gall, J. R. L., Klar, J. M., & Lemeshow, S. A. (1997) · Yearbook of intensive care and emergency medicine · doi:10.1007/978-3-662-13450-4_18 · Cited by 161 · see citing works
Cytokine expression in severe pneumonia: A bronchoalveolar lavage study
Montón, C., Torres, A., El-Ebiary, M., Filella, X., Xaubet, A., & de la Bellacasa, J. P. (1999) · Critical Care Medicine · doi:10.1097/00003246-199909000-00008 · Cited by 160 · see citing works
Prognosis and Treatment of Peritonitis
Koperna, T. (1996) · Archives of Surgery · doi:10.1001/archsurg.1996.01430140070019 · Cited by 160 · see citing works
Microbial Infection and the Septic Response in Critical Surgical Illness
Marshall, J. C. (1990) · Archives of Surgery · doi:10.1001/archsurg.1990.01410130019002 · Cited by 157 · see citing works
BALK, R. A. (2000) · Critical Care Clinics · doi:10.1016/s0749-0704(05)70113-5 · Cited by 152 · see citing works
Early Risk Factors for Postinjury Multiple Organ Failure
Sauaia, A., Moore, F. A., Moore, E. E., & Lezotte, D. C. (1996) · World Journal of Surgery · doi:10.1007/s002689900062 · Cited by 152 · see citing works
“Other MOF scores that have been developed for trauma [3, 12, 16] and mixed ICU populations [2, 4, 7, 19, 23, 24] are predictably similar.”
MethodResultClinical implications of positive blood cultures
Bryan, C. S. (1989) · Clinical Microbiology Reviews · doi:10.1128/cmr.2.4.329 · Cited by 149 · see citing works
SEVERE SEPSIS AND SEPTIC SHOCK: The Role of Gram-Negative Bacteremia
Munford, R. S. (2006) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev.pathol.1.110304.100200 · Cited by 148 · see citing works
Schein, M. (1991) · World Journal of Surgery · doi:10.1007/bf01675658 · Cited by 144 · see citing works
Gut barrier function and the surgeon
Saadia, R., Schein, M., Macfarlane, C., & Boffard, K. D. (1990) · British journal of surgery · doi:10.1002/bjs.1800770505 · Cited by 138 · see citing works
Nyström, P. O., Bax, R. P., Dellinger, E. P., Dominioni, L., Knaus, W. A., Meakins, J. L., Ohmann, C., Solomkin, J. S., Wacha, H., Wittmann, D. H., et al. (1990) · World Journal of Surgery · doi:10.1007/bf01664867 · Cited by 126 · see citing works
Splanchnic 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 · see citing works
“Continuing with the theme of infection as the aetiological agent of MOF, Marshall and colleagues [76] analysed nosocomial infections bacteriologically and concluded that the proximal gastrointestinal tract was the occult source of infection.”
BackgroundSurgical management of severe secondary peritonitis
Bosscha, K. P., van Vroonhoven, T. J. M. V., & van der Werken, C. (1999) · British journal of surgery · doi:10.1046/j.1365-2168.1999.01258.x · Cited by 117 · see citing works
Persistent Early Organ Failure
Lytras, D., Manes, K., Triantopoulou, C., Paraskeva, C., Delis, S., Avgerinos, C., & Dervenis, C. (2008) · Pancreas · doi:10.1097/mpa.0b013e31815acb2c · Cited by 115 · see citing works
Mucosa or skin as source of coagulase-negative staphylococcal bacteraemia?
Costa, S. F., Miceli, M. H., & Anaissie, E. J. (2004) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(04)01003-5 · Cited by 113 · see citing works
Schirmer, W. J. (1989) · Archives of Surgery · doi:10.1001/archsurg.1989.01410040055012 · Cited by 113 · see citing works
Gut-derived immune cells and the gut-lung axis in ARDS
Ziaka, M., & Exadaktylos, A. K. (2024) · Critical Care · doi:10.1186/s13054-024-05006-x · Cited by 111 · see citing works
“The upper GI tract, typically characterized by sparse microbial populations, becomes dominated by a limited number of species, such as Escherichia coli ( E. coli ), Enterococcus spp ., and Pseudomonas aeruginosa ( Ps. aeruginosa ) [59, 60].”
BackgroundEffects of High-Dose IgG on Survival of Surgical Patients With Sepsis Scores of 20 or Greater
Dominioni, L. (1991) · Archives of Surgery · doi:10.1001/archsurg.1991.01410260126018 · Cited by 109 · see citing works
Hoerauf, A. M., Hammer, S., Müller‐Myhsok, B., & Rupprecht, H. (1998) · Critical Care Medicine · doi:10.1097/00003246-199812000-00031 · Cited by 108 · see citing works
Pileggi, C., Bianco, A., Flotta, D., Nobile, C. G. A., & Pavía, M. (2011) · Critical Care · doi:10.1186/cc10285 · Cited by 105 · see citing works
“Several studies strongly support the hypothesis that colonization of the aerodigestive tract is primarily involved in VAP and other ICU-acquired infections’ pathogenesis, since micro-organisms move into the lower respiratory tract or, through the gut, into the blood or regional lymphatics [16-22].”
Qin, H.-L., Zheng, J.-J., Tong, D.-N., Chen, W.-X., Fan, X.-B., Hang, X., & Jiang, Y.-Q. (2007) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1602792 · Cited by 106 · see citing works
“the proximal gastrointestinal tract is common in critically ill patients (Marshall et al., 1988).”
Ciocan, D. M., Rebours, V., Voican, C. S., Wrzosek, L., Puchois, V., Cassard, A., & Perlemuter, G. (2018) · Scientific Reports · doi:10.1038/s41598-018-23146-3 · Cited by 104 · see citing works
Splanchnic blood flow is greater in septic shock treated with norepinephrine than in severe sepsis
Meier‐Hellmann, A., Specht, M., Hannemann, L., Hassel, H., Bredle, D. L., & Reinhart, K. (1996) · Intensive Care Medicine · doi:10.1007/bf01709551 · Cited by 104 · see citing works
Kirton, O. C., Windsor, J., Wedderburn, R. V., Hudson-Civetta, J. A., Shatz, D. V., Mataragas, N. R., & Civetta, J. M. (1998) · CHEST Journal · doi:10.1378/chest.113.4.1064 · Cited by 103 · see citing works
Baue, A. E. (2006) · Shock · doi:10.1097/01.shk.0000228172.32587.7a · Cited by 101 · see citing works
“(61) Dobb [(62) Royal Perth Hospital ICU Staff”
BackgroundLiver Dysfunction in Critical Illness
Hawker, F. (1991) · Anaesthesia and Intensive Care · doi:10.1177/0310057x9101900203 · Cited by 99 · see citing works
Multiple Organ Dysfunction Syndrome in Humans and Animals
Osterbur, K., Mann, F. A., Kuroki, K., & DeClue, A. E. (2014) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.12364 · Cited by 97 · see citing works
A comparison of risks and outcomes for patients with organ system failure
Zimmerman, J. E., Knaus, W. A., Wagner, D. P., Sun, X., Hakim, R. B., & Nyström, P.-O. (1996) · Critical Care Medicine · doi:10.1097/00003246-199610000-00006 · Cited by 98 · see citing works
Glutamine Nutrition: Theoretical Considerations and Therapeutic Impact
Souba, W. W., Herskowitz, K., Austgen, T. R., Chen, M. K., & Salloum, R. M. (1990) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/014860719001400516 · Cited by 97 · see citing works
Microbial dysbiosis and mortality during mechanical ventilation: a prospective observational study
for the PROSPECT Investigators, Lamarche, D., Canadian Critical Care Trials Group, Canadian Critical Care Translational Biology Group, Johnstone, J., Zytaruk, N. L., Clarke, F. J., Hand, L. E., Loukov, D., Szamosi, J. C., et al. (2018) · Respiratory Research · doi:10.1186/s12931-018-0950-5 · Cited by 95 · see citing works
“While the proximal gastrointestinal tract is established as an important reservoir of ICU-associated pathogens [44], the role of the stomach as a source of tracheal colonization is controversial, and is not always considered to be a substantial contributor to the Fig.”
BackgroundDynamic Alteration of the Colonic Microbiota in Intestinal Ischemia-Reperfusion Injury
Wang, F., Li, Q., Wang, C., Tang, C. X., & Li, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042027 · Cited by 92 · see citing works
“Intestinal microbial community changes have been investigated in critical ill patients and animal models using conventional bacteriological analysis techniques [21,22,23], while few study applies culture-independent methods [24].”
MethodDeterminants of intestinal barrier failure in critical illness
Aranow, J. S., & Fink, M. P. (1996) · British Journal of Anaesthesia · doi:10.1093/bja/77.1.71 · Cited by 91 · see citing works
“critically ill patients, possibly because of the administration of broad-spectrum antibiotics, the gut commonly becomes colonized by potentially pathogenic faculative Gram-negative bacilli, Gram-positive cocci and fungi [92, 93].”
BackgroundStoutenbeek, C. P., van Saene, H. K. F., Little, R., Whitehead, A., & for the Working Group on Selective Decontamination of the Digestive Tract (2006) · Intensive Care Medicine · doi:10.1007/s00134-006-0455-4 · Cited by 88 · see citing works
Immediate enteral nutrition following multisystem trauma: a decade perspective.
Moore, E. E., & Moore, F. A. (1991) · Journal of the American College of Nutrition · doi:10.1080/07315724.1991.10718183 · Cited by 84 · see citing works
Escherichia, Klebsiella, Enterobacter, Serratia, Citrobacter, and Proteus
Guentzel, M. N. (1996) · Europe PMC (PubMed Central) · Cited by 83 · see citing works
Secondary Organ Dysfunction: From Clinical Perspectives to Molecular Mediators
Cipolle, M. D., Pasquale, M. D., & Cerra, F. B. (1993) · Critical Care Clinics · doi:10.1016/s0749-0704(18)30196-9 · Cited by 79 · see citing works
Silvestri, L., van Saene, H. K. F., Zandstra, D. F., Marshall, J. C., Gregori, D., & Gullo, A. (2010) · Critical Care Medicine · doi:10.1097/ccm.0b013e3181d9db8c · Cited by 78 · see citing works
“018) Lingnau et al (27) 180 177 45 86 22 17 — — Goris et al (33) The difference between time to onset of MODS (Goris score 4 after day 4) was not significant Stoutenbeek et al (28) 49 42 0 6 2 8 0 3 Marshall et al (10); 2 consecutive days with a MOF score 6 There was a significantly higher number of days with a MODS s…”
BackgroundMethodInfluentialSelf-citationYu, S., Xiong, Y., Xu, J., Liang, X., Fu, Y., Liu, D., Yu, X., & Wu, D. (2020) · Digestive Diseases and Sciences · doi:10.1007/s10620-020-06061-4 · Cited by 83 · see citing works
Opioid-induced respiratory depression is associated with increased tidal volume variability
Bouillon, T. W., Bruhn, J., Roepcke, H., & Hoeft, A. (2003) · European Journal of Anaesthesiology · doi:10.1017/s0265021503000243 · Cited by 87 · see citing works
Diagnostic and therapeutic challenges of intraabdominal infections
Rotstein, O. D., & Meakins, J. L. (1990) · World Journal of Surgery · doi:10.1007/bf01664868 · Cited by 75 · see citing works
Diagnosis of intra-abdominal infection in the critically ill patient
Evans, H. L., Raymond, D. P., Pelletier, S. J., Crabtree, T. D., Pruett, T. L., & Sawyer, R. G. (2001) · Current Opinion in Critical Care · doi:10.1097/00075198-200104000-00010 · Cited by 72 · see citing works
The gut: the ‘motor’ of multiple organ dysfunction syndrome?
Nieuwenhuijzen, G. A. P., & Goris, R. J. A. (1999) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-199909000-00008 · Cited by 71 · see citing works
Border, J. R. (1988) · Archives of Surgery · doi:10.1001/archsurg.1988.01400270019001 · Cited by 71 · see citing works
Hirthler, M. A., Simoni, J. M., & Dickson, M. (1992) · Journal of Pediatric Surgery · doi:10.1016/0022-3468(92)90787-8 · Cited by 68 · see citing works
Postinjury Shock and Early Bacteremia
Moore, F. A. (1992) · Archives of Surgery · doi:10.1001/archsurg.1992.01420080027004 · Cited by 68 · see citing works
The gastropulmonary route of infection—Fact or fiction?
Tryba, M. (1991) · The American Journal of Medicine · doi:10.1016/0002-9343(91)90466-b · Cited by 66 · see citing works
Polymorphonuclear leukocyte dysregulation during the systemic inflammatory response syndrome
Simms, H. H., & DʼAmico, R. (1994) · Blood · doi:10.1182/blood.v83.5.1398.1398 · Cited by 64 · see citing works
Quality of life after cardiac surgery complicated by multiple organ failure
Nielsen, D. V., Sellgren, J., & Ricksten, S. (1997) · Critical Care Medicine · doi:10.1097/00003246-199701000-00012 · Cited by 59 · see citing works
Gastric tonometry and direct intraabdominal pressure monitoring in abdominal compartment syndrome
Engum, S. A., Kogon, B. E., Jensen, E., Isch, J. A., Balanoff, C., & Grosfeld, J. L. (2002) · Journal of Pediatric Surgery · doi:10.1053/jpsu.2002.30257 · Cited by 57 · see citing works
Multiple Organ Dysfunction Syndrome in Critical Surgical Illness
Barie, P. S., Hydo, L. J., Pieracci, F. M., Shou, J., & Eachempati, S. R. (2009) · Surgical Infections · doi:10.1089/sur.2009.9935 · Cited by 55 · see citing works
“When infection does complicate critical illness, it sometimes follows rather than precedes MODS [10].”
Gastric intramucosal acidosis in mechanically ventilated patients
Elizalde, J. I., Hernández, C., Llach, J., Montón, C., Bordas, J. M., Piqué, J. M., & Torres, A. (1998) · Critical Care Medicine · doi:10.1097/00003246-199805000-00011 · Cited by 55 · see citing works
Wong, Y. N., Rossignol, D. P., Rose, J., Kao, R., Carter, A. R., & Lynn, M. (2003) · The Journal of Clinical Pharmacology · doi:10.1177/0091270003254804 · Cited by 54 · see citing works
Multiple Organ System Failure in Critically Ill Cirrhotic Patients
Tsai, M.-H., Peng, Y.-S., Lien, J., Weng, H., Ho, Y., Yang, C., Chu, Y., Chen, Y., Fang, J., Chiu, C., et al. (2004) · Digestion · doi:10.1159/000078789 · Cited by 53 · see citing works
Liu, C.-Y., Lai, Y.-C., Huang, L.-J., Yang, Y.-W., Chen, T.-L., Hsiao, L. T., Liu, H., Gau, J.-P., Chen, P.-M., Tzeng, C. H., et al. (2010) · Bone Marrow Transplantation · doi:10.1038/bmt.2010.286 · Cited by 53 · see citing works
Multiple-organ dysfunction in the surgical patient: Pathophysiology, prevention, and treatment
Demling, R. H., Lalonde, C., Saldinger, P. F., & Knox, J. B. (1993) · Current Problems in Surgery · doi:10.1016/0011-3840(93)90054-k · Cited by 51 · see citing works
FACTORS INFLUENCING OUTCOME IN PATIENTS WITH GASTROINTESTINAL FISTULA
Campos, A. C. L., Meguid, M. M., & Coelho, J. C. U. (1996) · Surgical Clinics of North America · doi:10.1016/s0039-6109(05)70507-7 · Cited by 50 · see citing works
The Effect of Endotoxin on Intestinal Mucosal Permeability to Bacteria In Vitro
Go, L. L. (1995) · Archives of Surgery · doi:10.1001/archsurg.1995.01430010055011 · Cited by 50 · see citing works
Kale, T., Kuzu, M. A., Tekelı, A., Tanık, A., Aksoy, M., & Cete, M. (1998) · Diseases of the Colon & Rectum · doi:10.1007/bf02235274 · Cited by 49 · see citing works
Temporal Variations of the Ileal Microbiota in Intestinal Ischemia and Reperfusion
Wang, F., Li, Q., He, Q., Geng, Y., Tang, C., Wang, C., & Li, J. (2012) · Shock · doi:10.1097/shk.0b013e318279265f · Cited by 48 · see citing works
- Authors
- Marshall, J. C.
- Affiliations
- Royal Victoria Hospital (CA)
- Corresponding author
- Marshall, John C.
- Venue
- Archives of Surgery
- Publisher
- American Medical Association (AMA)
- Published
- 1988-03-01
- Volume
- 123
- Issue
- 3
- Pages
- 309
- ISSN
- 0004-0010 (ISSN-L)
- OpenAlex
- W1964088213
- Cited by
- 328
- References
- 36
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 3 · 2022: 1 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 4 · 2017: 3 · 2016: 3 · 2015: 2 · 2014: 4 · 2013: 3 · 2012: 6
- FWCI
- 16.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Archives of Surgery (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Nosocomial Infections in ICU
- Health Sciences › Medicine › Epidemiology › Sepsis Diagnosis and Treatment
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- multiple organ failure, intensive care unit-acquired infections, surgical intensive care unit, Escherichia coli, Bacteroides fragilis, Enterococcus, Staphylococcus epidermidis, Candida, Pseudomonas, mortality, intestinal colonization, autopsy findings
- MeSH terms
- Bacteroides fragilis, Candida, Cross Infection, Digestive System, Duodenum, Gastric Juice, Humans, Infections, Intensive Care Units, Middle Aged, Multiple Organ Failure, Prospective Studies, Pseudomonas, Staphylococcus epidermidis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
