The DOI matches its Crossref record; 39 of the 42 references it cites were found in a registry or an index.
Markers of intestinal injury are associated with endotoxemia in successfully resuscitated patients
Abstract
Aims Gut dysfunction is suspected to play a major role in the pathophysiology of post-resuscitation disease through an increase in intestinal permeability and endotoxin release. However this dysfunction often remains occult and is poorly investigated. The aim of this pilot study was to explore intestinal failure biomarkers in post-cardiac arrest patients and to correlate them with endotoxemia.Methods Following resuscitation after cardiac arrest, 21 patients were prospectively studied. Urinary intestinal fatty acid-binding protein (IFABP), which marks intestinal permeability, plasma citrulline, which reflects the functional enterocyte mass, and whole blood endotoxin were measured at admission, days 1-3 and 6. We explored the kinetics of release and the relationship between IFABP, citrulline and endotoxin values.Results IFABP was extremely high at admission and normalized at D3 (6668 pg/mL vs 39 pg/mL, p=0.01). Lowest median of citrulline (N=20-40 μmol/L) was attained at D2 (11 μmol/L at D2 vs 24 μmol/L at admission, p=0.01) and tended to normalize at D6 (21 μmol/L). During ICU stay, 86% of patients presented a detectable endotoxemia. Highest endotoxin level was positively correlated with highest IFABP level (R(2)=0.31, p=0.01) and was inversely correlated with lowest plasma citrulline levels (R(2)=0.55, p<0.001). Endotoxin levels increased between admission and D2 in patients with post-resuscitation shock, whereas it decreases in patients with no shock (median +0.33 EU vs -0.19 EU, p=0.03). Highest endotoxin level was positively correlated with D3 SOFA score (R(2)=0.45, p=0.004).Conclusion Biomarkers of intestinal injury are altered after cardiac arrest and are associated with endotoxemia. This could worsen post-resuscitation shock and organ failure.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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 the citing paper
“and secondary to increased intestinal permeability resulting from extreme physiologic stress,32 ethanol exposure,33 or a “fast-food style” Western diet, high in both carbohydrate and saturated fat.34”
From The Gut Microbiome and the Brain (2014) · cites this paper as [32]
Citations
Cites
Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury
Mehta, R. L., Kellum, J. A., Shah, S. V., Molitoris, B. A., Ronco, C., Warnock, D. G., Levin, A., & the Acute Kidney Injury Network (2007) · Critical Care · doi:10.1186/cc5713 · Cited by 7,046
Cardiac Arrest and Cardiopulmonary Resuscitation Outcome Reports
Jacobs, I. G., Nadkarni, V., the ILCOR Task Force on Cardiac Arrest and Cardiopulmonary Resuscitation Outcomes, PARTICIPANTS, C., Bahr, J., Berg, R. A., Billi, J. E., Bossaert, L. L., Cassan, P., Coovadia, A. H., et al. (2004) · Circulation · doi:10.1161/01.cir.0000147236.85306.15 · Cited by 2,563
TLR4 mutations are associated with endotoxin hyporesponsiveness in humans
Arbour, N. C., Lorenz, E., Schutte, B. C., Zabner, J., Kline, J. N., Jones, M., Frees, K., Watt, J. L., & Schwartz, D. A. (2000) · Nature Genetics · doi:10.1038/76048 · Cited by 2,024
Post-cardiac arrest syndrome: Epidemiology, pathophysiology, treatment, and prognostication
Nolan, J. P., Neumar, R. W., Adrie, C., Aibiki, M., Berg, R. A., Böttiger, B. W., Callaway, C. W., Clark, R. S. B., Geocadin, R. G., Jauch, E. C., et al. (2008) · Resuscitation · doi:10.1016/j.resuscitation.2008.09.017 · Cited by 1,519
Kawai, T., & Akira, S. (2007) · Seminars in Immunology · doi:10.1016/j.smim.2006.12.004 · Cited by 1,461
Zipes, D. P., Camm, A. J., Borggrefe, M., Buxton, A. E., Chaitman, B., Fromer, M., Gregoratos, G., Klein, G., Moss, A. J., Myerburg, R. J., et al. (2006) · Circulation · doi:10.1161/circulationaha.106.178233 · Cited by 1,080
Successful Cardiopulmonary Resuscitation After Cardiac Arrest as a “Sepsis-Like” Syndrome
Adrie, C., Adib‐Conquy, M., Laurent, I., Monchi, M., Vinsonneau, C., Fitting, C., Fraisse, F., Dinh‐Xuan, A. T., Carli, P. A., Spaulding, C. M., et al. (2002) · Circulation · doi:10.1161/01.cir.0000023891.80661.ad · Cited by 1,009
Jacobs, I. G., Nadkarni, V., Bahr, J., Berg, R. A., Billi, J. E., Bossaert, L. L., Cassan, P., Coovadia, A. H., D’Este, K., Finn, J., et al. (2004) · Resuscitation · doi:10.1016/j.resuscitation.2004.09.008 · Cited by 916
Citrulline as a biomarker of intestinal failure due to enterocyte mass reduction
Crenn, P. P., Messing, B., & Cynober, L. (2008) · Clinical Nutrition · doi:10.1016/j.clnu.2008.02.005 · Cited by 583
Self-citationJEUKENDRUP, A. E., VET-JOOP, K., STURK, A., STEGEN, J. H. J. C., SENDEN, J., SARIS, W. H. M., & WAGENMAKERS, A. J. M. (2000) · Clinical Science · doi:10.1042/cs0980047 · Cited by 371
Marshall, J. C., Foster, D., Vincent, J., Cook, D. J., Cohen, J., Dellinger, R. P., Opal, S. M., Abraham, E. H., Brett, S. J., Smith, T. S., et al. (2004) · The Journal of Infectious Diseases · doi:10.1086/422254 · Cited by 363
Is Hypothermia After Cardiac Arrest Effective in Both Shockable and Nonshockable Patients?
Dumas, F., Grimaldi, D., Zuber, B., Fichet, J., Charpentier, J., Pène, F., Vivien, B., Varenne, O., Carli, P. A., Jouven, X., et al. (2011) · Circulation · doi:10.1161/circulationaha.110.987347 · Cited by 293
Self-citationPostcardiac arrest syndrome: from immediate resuscitation to long-term outcome
Mongardon, N., Dumas, F., Ricôme, S., Grimaldi, D., Hissem, T., Pène, F., & Cariou, A. (2011) · Annals of Intensive Care · doi:10.1186/2110-5820-1-45 · Cited by 236
Self-citationEarly Diagnosis of Intestinal Ischemia Using Urinary and Plasma Fatty Acid Binding Proteins
Thuijls, G., Wijck, K. V., Grootjans, J., Derikx, J. P. M., van Bijnen, A. A., Heineman, E., Dejong, C. H. C., Buurman, W. A., & Poeze, M. (2011) · Annals of Surgery · doi:10.1097/sla.0b013e318207a767 · Cited by 217
Coagulopathy After Successful Cardiopulmonary Resuscitation Following Cardiac Arrest
Adrie, C., Monchi, M., Laurent, I., Um, S., Yan, S.-C. B., Thuong, M., Cariou, A., Charpentier, J., & Dhainaut, J. F. (2005) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2005.03.046 · Cited by 210
Self-citationvan Deventer, S. J. H., ten Cate, J. W., & Tytgat, G. N. J. (1988) · Gastroenterology · doi:10.1016/0016-5085(88)90261-2 · Cited by 194
Mongardon, N., Perbet, S., Lemiale, V., Dumas, F., Poupet, H., Charpentier, J., Pène, F., Chiche, J., Mira, J. P., & Cariou, A. (2011) · Critical Care Medicine · doi:10.1097/ccm.0b013e3182120b56 · Cited by 193
Self-citationHuman Intestinal Ischemia-Reperfusion–Induced Inflammation Characterized
Grootjans, J., Lenaerts, K., Derikx, J. P. M., Matthijsen, R. A., de Bruïne, A. P., van Bijnen, A. A., van Dam, R. M., Dejong, C. H. C., & Buurman, W. A. (2010) · The American Journal of Pathology · doi:10.2353/ajpath.2010.091069 · Cited by 186
A rapid assay of endotoxin in whole blood using autologous neutrophil dependent chemiluminescence
Romaschin, A. D., Harris, D. M., Ribeiro, M. B., PAICE, J. C., Foster, D., Walker, P. M., & Marshall, J. C. (1998) · Journal of Immunological Methods · doi:10.1016/s0022-1759(98)00003-9 · Cited by 165
Intestinal Hypoperfusion Contributes to Gut Barrier Failure in Severe Acute Pancreatitis
Rahman, S. H., Ammori, B. J., Holmfield, J. H. M., Larvin, M., & McMahon, M. J. (2003) · Journal of Gastrointestinal Surgery · doi:10.1016/s1091-255x(02)00090-2 · Cited by 158
Endotoxemia contributes to the immune paralysis in patients with cirrhosis
Lin, C.-Y., Tsai, I.-F., Ho, Y.-P., Huang, C.-T., Lin, Y.-C., Lin, C.-J., Tseng, S.-C., Lin, W.-P., Chen, W.-T., & Sheen, I.-S. (2007) · Journal of Hepatology · doi:10.1016/j.jhep.2006.12.018 · Cited by 145
Acute intestinal failure in critically ill patients: is plasma citrulline the right marker?
Piton, G., Manzon, C., Cypriani, B., Carbonnel, F., & Capellier, G. (2011) · Intensive Care Medicine · doi:10.1007/s00134-011-2172-x · Cited by 134
Cynober, L., Moinard, C., & Bandt, J. P. D. (2010) · Clinical Nutrition · doi:10.1016/j.clnu.2010.07.006 · Cited by 128
Self-citationMetabolic & Therapeutic Aspects of Amino Acids in Clinical Nutrition
Cynober, L. (2003) · CRC Press eBooks · doi:10.1201/9780203010266 · Cited by 119
Self-citationPlasma citrulline kinetics and prognostic value in critically ill patients
Piton, G., Manzon, C., Monnet, É., Cypriani, B., Barbot, O., Navellou, J.-C., Carbonnel, F., & Capellier, G. (2010) · Intensive Care Medicine · doi:10.1007/s00134-010-1751-6 · Cited by 105
Bacteremia following cardiac arrest and cardiopulmonary resuscitation
Gaussorgues, P., Gueugniaud, P., Vedrinne, J. M., Salord, F., Mercatello, A., & Robert, D. (1988) · Intensive Care Medicine · doi:10.1007/bf00263532 · Cited by 99
Endogenous endotoxemia of intestinal origin during cardiopulmonary bypass
Martínez-Pellús, A., Bru, M., Seller, G., Fuentes, T., Merino, P., Canovas, J., Sapiña, J., & Moro, J. (1997) · Intensive Care Medicine · doi:10.1007/s001340050494 · Cited by 95
de Haan, J. J., Lubbers, T., Derikx, J. P. M., Relja, B., Henrich, D. M., Greve, J.-W. M., Marzi, İ., & Buurman, W. A. (2009) · Critical Care · doi:10.1186/cc7910 · Cited by 84
Korth, U., Krieter, H., Denz, C., Janke, C., Ellinger, K., Bertsch, T., Henn, C., & Klein, J. (2003) · Resuscitation · doi:10.1016/s0300-9572(03)00119-9 · Cited by 79
Unexpected Findings and Complications at Autopsy After Cardiopulmonary Resuscitation (CPR)
Bedell, S. E. (1986) · Archives of Internal Medicine · doi:10.1001/archinte.1986.00360210099015 · Cited by 71
Intestinal Injury and Endotoxemia in Children Undergoing Surgery for Congenital Heart Disease
Pathan, N., Burmester, M., Adamovic, T., Berk, M., Ng, K. W., Betts, H., Macrae, D. J., Waddell, S. J., Paul‐Clark, M. J., Nuamah, R., et al. (2011) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201104-0715oc · Cited by 68
Jakob, S. M., Takala, J. A., & Martínez-Pellús, A. (1998) · Intensive Care Medicine · doi:10.1007/s001340050658 · Cited by 66
Kats, S., Schönberger, J. P. A. M., Brands, R., Seinen, W., & van Oeveren, W. (2010) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/j.ejcts.2010.06.011 · Cited by 54
The Human Response to Endotoxin
Lin, E., & Lowry, S. F. (1998) · Sepsis · doi:10.1023/a:1009890031293 · Cited by 54
Gut mucosal cell damage in meningococcal sepsis in children: Relation with clinical outcome*
Derikx, J. P. M., Bijker, E. M., Vos, G. D., van Bijnen, A. A. J. H. M., Heineman, E., Buurman, W. A., & van Waardenburg, D. A. (2009) · Critical Care Medicine · doi:10.1097/ccm.0b013e3181b4a5ed · Cited by 42
A New Model to Study Intestinal Ischemia-Reperfusion Damage in Man
Derikx, J. P. M., Matthijsen, R. A., de Bruı̈ne, A. P., van Dam, R. M., Buurman, W. A., & Dejong, C. H. C. (2009) · Journal of Surgical Research · doi:10.1016/j.jss.2009.09.046 · Cited by 35
Gut dysfunction and endoscopic lesions after out-of-hospital cardiac arrest.
L'her, E., Cassaz, C., le Gal, G., Cholet, F., Renault, A., & Boles, J. (2005) · Resuscitation · doi:10.1016/j.resuscitation.2005.03.016 · Cited by 31
Acute Ischemic Pancreatitis Following Cardiac Arrest: A Case Report
Piton, G., Barbot, O., Manzon, C., Moronval, F., Patry, C., Navellou, J. C., Belle, E., & Capellier, G. (2015) · PubMed · doi:10.6092/1590-8577/3434 · Cited by 22
Albrecht, M., Gruenewald, M., Zitta, K., Zacharowski, K. D., Scholz, J., Bein, B., & Meybohm, P. (2011) · Resuscitation · doi:10.1016/j.resuscitation.2011.06.038 · Cited by 17
Research works printed but not linked: 1
- Fragkos KC, Forbes A. Is citrulline a marker of small intestinal absorption? A systematic review and meta-analysis. ESPEN congress; 2011. Abstract no. 11-1075.
Cited by
Sorted by citations
Nolan, J. P., Soar, J., Cariou, A., Cronberg, T., Moulaert, V. R. M., Deakin, C. D., Böttiger, B. W., Friberg, H., Sunde, K., & Sandroni, C. (2015) · Resuscitation · doi:10.1016/j.resuscitation.2015.07.018 · Cited by 1,139
Self-citationNolan, J. P., Sandroni, C., Böttiger, B. W., Cariou, A., Cronberg, T., Friberg, H., Genbrugge, C., Haywood, K. L., Lilja, G., Moulaert, V. R. M., et al. (2021) · Intensive Care Medicine · doi:10.1007/s00134-021-06368-4 · Cited by 1,132
Self-citationNolan, J. P., Soar, J., Cariou, A., Cronberg, T., Moulaert, V. R. M., Deakin, C. D., Böttiger, B. W., Friberg, H., Sunde, K., & Sandroni, C. (2015) · Intensive Care Medicine · doi:10.1007/s00134-015-4051-3 · Cited by 950
Self-citationNolan, J. P., Sandroni, C., Böttiger, B. W., Cariou, A., Cronberg, T., Friberg, H., Genbrugge, C., Haywood, K. L., Lilja, G., Moulaert, V. R. M., et al. (2021) · Resuscitation · doi:10.1016/j.resuscitation.2021.02.012 · Cited by 751
Self-citationThe Gut Microbiome and the Brain
Galland, L. (2014) · Journal of Medicinal Food · doi:10.1089/jmf.2014.7000 · Cited by 648
Metadata
- Authors
- Grimaldi, D., Guivarch, E., Neveux, N., Fichet, J., Pène, F., Marx, J.-S., Chiche, J.-D., Cynober, L., Mira, J.-P., & Cariou, A.
- Affiliations
- Hôpital Cochin (FR)
- Sorbonne Paris Cité (FR)
- Inserm (FR)
- Venue
- Resuscitation
- Publisher
- Elsevier BV
- Published
- 2013-01
- Volume
- 84
- Issue
- 1
- Pages
- 60-65
- ISSN
- 0300-9572 (ISSN-L)
- OpenAlex
- W2119467481
- Cited by
- 130
- References
- 42
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 7 · 2023: 11 · 2022: 13 · 2021: 8 · 2020: 9 · 2019: 13 · 2018: 7 · 2017: 10 · 2016: 10 · 2015: 10 · 2014: 8 · 2013: 9
- FWCI
- 6.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Resuscitation (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Sepsis Diagnosis and Treatment
- Health Sciences › Medicine › Emergency Medicine › Cardiac Arrest and Resuscitation
- Health Sciences › Medicine › Surgery › Abdominal Surgery and Complications
- Keywords
- endotoxemia, intestinal injury, cardiac arrest, intestinal fatty acid binding protein, citrulline, intestinal permeability, gastrointestinal dysfunction, endotoxin, SOFA score, organ failure, biomarkers
- MeSH terms
- Chromatography, High Pressure Liquid, Citrulline, Endotoxins, Enzyme-Linked Immunosorbent Assay, Female, Humans, Intestinal Mucosa, Intestines, Male, Middle Aged, Prospective Studies, Biomarkers, Cardiopulmonary Resuscitation, Statistics, Nonparametric, Endotoxemia, Luminescence, Fatty Acid-Binding Proteins, Out-of-Hospital Cardiac Arrest
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