Biological scoring system for early prediction of acute bowel ischemia after cardiac surgery: the PALM score
Open accessAbstract
BACKGROUND: Bowel ischemia is a life-threatening emergency defined as an inadequate vascular perfusion leading to bowel inflammation resulting from impaired colonic/small bowel blood supply. Main issue for physicians regarding bowel ischemia diagnosis lies in the absence of informative and specific clinical or biological signs leading to delayed management, resulting in a poorer prognosis, especially after cardiac surgery. The aim of the present series was to propose a simple scoring system based on biological data for the diagnosis of bowel ischemia. METHODS: In a retrospective monocentric study, patients admitted in cardiac ICU, after cardiovascular surgery, were screened for inclusion. According to a 1:2 ratio (case-control), matching between two groups was based on sex, type of cardiovascular surgery, and the operative period (per month). Patients were divided into two groups: "ischemic group" which corresponds to patients with confirmed bowel ischemia and "non-ischemic group" which corresponds to patients without bowel ischemia. Primary objective was the conception of a scoring system for the diagnosis of bowel ischemia. Secondary objectives were to detail the postoperative morbidity and the diagnostic features for the distinction between acute mesenteric ischemia and ischemic colitis. RESULTS: Forty-eight patients (1.3%) had confirmed bowel ischemia ("ischemic group"). According to the 2:1 matching, 96 patients were included in the "non-ischemic group." Aspartate aminotransferase > 449 UI/L, lactate > 4 mmol/L, procalcitonin > 4.7 μg/L, and myoglobin > 1882 μg/L were found to be independently associated with bowel ischemia. Based on their respective odds ratios, points were assigned to each item ranging from 4 to 8. AUROCC [95% confidence interval] of the scoring system to diagnose bowel ischemia was 0.93 [0.91-0.95], p < 0.001. The optimal threshold after bootstrapping was ≥ 14 points; this yielded a sensitivity of 85.4%, a specificity of 94.8%, a positive likelihood ratio of 16.42, a negative likelihood ratio of 0.15, a Youden's index of 0.802, and a diagnostic odds ratio of 106.62. CONCLUSIONS: A biological scoring system based on PCT, ASAT, lactate, and myoglobin measurement allows the diagnosis of bowel ischemia after cardiac surgery with high accuracy. This score could help clinician to propose an early diagnosis and an early treatment in this high mortality disease.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Scores or combinations of biomarkers were assessed in only 5 studies, mainly combining laboratory biomarkers with radiological or clinical markers, and this did not permit meta-analysis.
“Scores/combinations of biomarkers were assessed in only 5 studies [23, 35, 42, 85, 94], mainly combining laboratory biomarkers with radiological or clinical markers and thus not permitting any meta-analysis.”
From Diagnostic accuracy of biomarkers to detect acute mesenteric ischaemia in adult patients: a systematic review and meta-analysis (2023) · cites this paper as [85]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
High serum procalcitonin concentrations in patients with sepsis and infection
Assicot, M., Bohuon, C., Gendrel, D., Raymond, J., Carsin, H., & Guilbaud, J. (1993) · The Lancet · doi:10.1016/0140-6736(93)90277-n · Cited by 2,195 · see citing works
Procalcitonin increase after endotoxin injection in normal subjects
Dandona, P., Nix, D. E., Wilson, M. F., Aljada, A., Love, J., Assicot, M., & Bohuon, C. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.6.7989463 · Cited by 964 · see citing works
AGA technical review on intestinal ischemia
Brandt, L. J., & Boley, S. J. (2000) · Gastroenterology · doi:10.1016/s0016-5085(00)70183-1 · Cited by 594 · see citing works
Systematic review of survival after acute mesenteric ischaemia according to disease aetiology
Schoots, I. G., Koffeman, G. I., Legemate, D. A., Levi, M., & van Gulik, T. M. (2004) · Journal of British Surgery · doi:10.1002/bjs.4459 · Cited by 502 · see citing works
Contemporary management of acute mesenteric ischemia: Factors associated with survival
Park, W. M., Gloviczki, P., Cherry, K. J., Hallett, J. W., Bower, T. C., Panneton, J. M., Schleck, C., Ilstrup, D., Harmsen, W. S., & Noel, A. A. (2002) · Journal of Vascular Surgery · doi:10.1067/mva.2002.120373 · Cited by 463 · see citing works
ESTES guidelines: acute mesenteric ischaemia
Tilsed, J. V. T., Casamassima, A., Kurihara, H., Mariani, D., Martinez, I., Pereira, J., Ponchietti, L., Shamiyeh, A., al-Ayoubi, F., Barco, L. A. B., et al. (2016) · European Journal of Trauma and Emergency Surgery · doi:10.1007/s00068-016-0634-0 · Cited by 382 · see citing works
Unchanged high mortality rates from acute occlusive intestinal ischemia: six year review
Kassahun, W. T., Schulz, T., Richter, O., & Hauss, J. (2008) · Langenbeck's Archives of Surgery · doi:10.1007/s00423-007-0263-5 · Cited by 262 · see citing works
Diagnostic accuracy of plasma biomarkers for intestinal ischaemia
Block, T., Nilsson, T. K., Björck, M., & Acosta, S. (2008) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365510701646264 · Cited by 172 · see citing works
Leone, M., Bechis, C., Baumstarck, K., Ouattara, A., Collange, O., Augustin, P., Annane, D., Arbelot, C., Asehnoune, K., Baldési, O., et al. (2015) · Intensive Care Medicine · doi:10.1007/s00134-015-3690-8 · Cited by 162 · see citing works
Gastrointestinal Complications in Patients Undergoing Heart Operation
Mangi, A. A., Christison-Lagay, E. R., Torchiana, D. F., Warshaw, A. L., & Berger, D. L. (2005) · Annals of Surgery · doi:10.1097/01.sla.0000164173.05762.32 · Cited by 158 · see citing works
Serological markers for human intestinal ischemia: A systematic review
Derikx, J. P. M., Schellekens, D. H. S. M., & Acosta, S. (2017) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2017.01.004 · Cited by 96 · see citing works
Lethal mesenteric ischaemia after cardiopulmonary bypass: a common complication?
Venkateswaran, R. (2002) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/s1010-7940(02)00373-1 · Cited by 84 · see citing works
Ischemic colitis: The ABCs of diagnosis and surgical management
Moszkowicz, D., Mariani, A., Trésallet, C., & Ménégaux, F. (2013) · Journal of Visceral Surgery · doi:10.1016/j.jviscsurg.2013.01.002 · Cited by 76 · see citing works
Acute Mesenteric Ischemia Among Postcardiac Surgery Patients Presenting with Multiple Organ Failure
Guillaume, A., Pili-Floury, S., Chocron, S., Delabrousse, E., De Parseval, B., Koch, S., Samain, E., Capellier, G., & Piton, G. (2017) · Shock · doi:10.1097/shk.0000000000000720 · Cited by 68 · see citing works
Early bloodstream infection after cardiopulmonary bypass
Ryan, T., Carthy, J. F., Rady, M. Y., Serkey, J. M., Gordon, S. M., Starr, N. J., & Cosgrove, D. M. (1997) · Critical Care Medicine · doi:10.1097/00003246-199712000-00018 · Cited by 64 · see citing works
Procalcitonin and intestinal ischemia: A review of the literature
Cossé, C., Sabbagh, C., Kamel, S., Galmiche, A., & Regimbeau, J. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i47.17773 · Cited by 57 · see citing works
Self-citationPostinfection Irritable Bowel Syndrome
Downs, I. A., Aroniadis, O. C., Kelly, L., & Brandt, L. J. (2017) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000924 · Cited by 52 · see citing works
Debus, E. S., Müller‐Hülsbeck, S., Kölbel, T., & Larena-Avellaneda, A. A. (2011) · International Journal of Colorectal Disease · doi:10.1007/s00384-011-1196-6 · Cited by 50 · see citing works
Serum value of procalcitonin as a marker of intestinal damages: type, extension, and prognosis
Cossé, C., Sabbagh, C., Browet, F., Mauvais, F., Rebibo, L., Zogheib, E. H., Chatelain, D., Kamel, S., & Regimbeau, J. (2015) · Surgical Endoscopy · doi:10.1007/s00464-014-4038-0 · Cited by 43 · see citing works
Self-citationAcute Mesenteric Ischemia after Cardiac Surgery: An Analysis of 52 Patients
Eriş, C., Yavuz, Ş., Yalçınkaya, S., Gücü, A., Toktaş, F., Yümün, G., Erdolu, B., & Ozyazicioglu, A. F. (2013) · The Scientific World JOURNAL · doi:10.1155/2013/631534 · Cited by 42 · see citing works
The incidence and outcome of ischemic colitis in a population-based setting
Yngvadóttir, Y., Karlsdottir, B. R., Hreinsson, J. P., Ragnarsson, G. B., Mitev, R. M., Jonasson, J. G., Möller, P. H., & Bjornsson, E. S. (2017) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.2017.1291718 · Cited by 38 · see citing works
Intestinal ischemia-reperfusion and plasma enzyme levels
Çağlayan, F., Çağlayan, O., Günel, E., Elcuman, Y., & Çakmak, M. (2002) · Pediatric Surgery International · doi:10.1007/s003830100666 · Cited by 31 · see citing works
Aggressive Management of Nonocclusive Ischemic Colitis Following Aortic Reconstruction
Ménégaux, F. (2006) · Archives of Surgery · doi:10.1001/archsurg.141.7.678 · Cited by 29 · see citing works
L’ischémie mésentérique à l’ère des structures d’urgences vasculaires intestinales
Nuzzo, A., & Corcos, O. (2017) · La Revue de Médecine Interne · doi:10.1016/j.revmed.2017.01.018 · Cited by 29 · see citing works
Nonocclusive mesenteric infarction after cardiac surgery: potential biomarkers
Hong, J., Gilder, E., Blenkiron, C., Jiang, Y., Evennett, N. J., Petrov, M. S., Phillips, A. R. J., Windsor, J. A., & Gillham, M. (2017) · Journal of Surgical Research · doi:10.1016/j.jss.2016.12.001 · Cited by 27 · see citing works
Nagata, J., Kobayashi, M., Nishikimi, N., & Komori, K. (2008) · European Journal of Vascular and Endovascular Surgery · doi:10.1016/j.ejvs.2007.11.014 · Cited by 24 · see citing works
Favier, C., Bonneau, H. P., Minh, V. T., & Dević, J. (1976) · PubMed · Cited by 24 · see citing works
Analysis of serum enzyme levels in a rabbit model of acute mesenteric ischemia
Zhang, F. (2011) · Molecular Medicine Reports · doi:10.3892/mmr.2011.553 · Cited by 16 · see citing works
Cossé, C., Sabbagh, C., Carroni, V., Galmiche, A., Rebibo, L., & Regimbeau, J. (2017) · Journal of Visceral Surgery · doi:10.1016/j.jviscsurg.2017.01.004 · Cited by 14 · see citing works
Self-citationCossé, C., Sabbagh, C., Fuméry, M., Zogheib, E. H., Mauvais, F., Browet, F., Rebibo, L., & Regimbeau, J. (2016) · Digestive and Liver Disease · doi:10.1016/j.dld.2016.12.003 · Cited by 11 · see citing works
Self-citationCherry, K. J. (2007) · Perspectives in Vascular Surgery · doi:10.1177/1531003507301662 · Cited by 5 · see citing works
Nuzzo, A., Ronot, M., Maggiori, L., & Corcos, O. (2017) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000970 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Reintam Blaser, A., Starkopf, J., Björck, M., Forbes, A., Kase, K., Kiisk, E., Laisaar, K.-T., Mihnovits, V., Murruste, M., Mändul, M., et al. (2023) · World Journal of Emergency Surgery · doi:10.1186/s13017-023-00512-9 · Cited by 67 · see citing works
“Scores/combinations of biomarkers were assessed in only 5 studies [23, 35, 42, 85, 94], mainly combining laboratory biomarkers with radiological or clinical markers and thus not permitting any meta-analysis.”
MethodDiagnostic accuracy of hematological parameters in Acute mesenteric ischemia-A systematic review
Khan, S. M., Emile, S. H., Wang, Z., & Agha, M. A. (2019) · International Journal of Surgery · doi:10.1016/j.ijsu.2019.04.005 · Cited by 51 · see citing works
Gastrointestinal complications following cardiac surgery
Chor, C. Y. T., Mahmood, S., Khan, I. H., Shirke, M., & Harky, A. (2020) · Asian Cardiovascular and Thoracic Annals · doi:10.1177/0218492320949084 · Cited by 37 · see citing works
Acute mesenteric ischaemia in refractory shock on veno-arterial extracorporeal membrane oxygenation
Renaudier, M., de Roux, Q., Bougouin, W., Boccara, J., Dubost, B., Attias, A., Fiore, A., de’Angelis, N., Folliguet, T., Mulé, S., et al. (2021) · European Heart Journal. Acute Cardiovascular Care · doi:10.1177/2048872620915655 · Cited by 34 · see citing works
Gastrointestinal complications after cardiac surgery
Schwarzova, K., Damle, S., Sellke, F. W., & Robich, M. P. (2024) · Trauma Surgery & Acute Care Open · doi:10.1136/tsaco-2023-001324 · Cited by 29 · see citing works
Li, Q., Zheng, S., Zhou, P. Y., Xiao, Z., Wang, R., & Li, J. (2020) · Journal of Cardiovascular Medicine · doi:10.2459/jcm.0000000000001017 · Cited by 20 · see citing works
Anatomic risk factors for the occurrence of medial talar osteochondral lesions: a case–control study
Sonnow, L., Pacha, T. O., Richter, M., Yapar, D., Çetin, M., Celik, O. F., & Köse, Ö. (2022) · Skeletal Radiology · doi:10.1007/s00256-022-04024-6 · Cited by 18 · see citing works
Tang, W., Jin, B., Kuang, L.-Q., Zhang, J., Li, C.-X., & Wang, Y. H. (2020) · British Journal of Radiology · doi:10.1259/bjr.20190605 · Cited by 8 · see citing works
Tu, B., Zhu, Z., Lu, P., Fang, R., Peng, C., Tong, J., & Ning, R. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2024.159513 · Cited by 7 · see citing works
Predicting outcomes of mesenteric ischemia postcardiac surgery: A systematic review
Kayali, F., Sarodaya, V., Shah, H. I., Hayat, M. Y., Leung, M. S. T., & Harky, A. (2022) · Journal of Cardiac Surgery · doi:10.1111/jocs.16516 · Cited by 6 · see citing works
An engineered poly(A) tail attenuates gut ischemia/reperfusion-induced acute lung injury
Murao, A., Jha, A., Aziz, M., & Wang, P. (2024) · Surgery · doi:10.1016/j.surg.2024.01.002 · Cited by 6 · see citing works
Yang, J., Xu, Z., Chen, F.-X., Wang, M., Cong, R., Fan, X., He, B.-S., & Xing, W. (2022) · World Journal of Clinical Cases · doi:10.12998/wjcc.v10.i13.4020 · Cited by 3 · see citing works
Deen, R., & Sia, Z. K. (2022) · Emergency Medicine Australasia · doi:10.1111/1742-6723.14145 · Cited by 3 · see citing works
Novotný, T., Staffa, R., Tomandl, J., Křivka, T., Kružliak, P., Tomandlová, M., Slabý, O., Sponiar, J., Čaprnda, M., Gašpar, Ľ., et al. (2022) · Vascular · doi:10.1177/17085381221102812 · Cited by 2 · see citing works
Miyagawa, Y., Yamamoto, Y., Kitazawa, M., Tokumaru, S., Nakamura, S., Koyama, M., Ehara, T., Hondo, N., Iijima, Y., & Soejima, Y. (2022) · Surgery Research and Practice · doi:10.1155/2022/1737161 · Cited by 1 · see citing works
Ağababaoğlu, İ., Yıldız, Ö. Ö., Yapar, D., Ersöz, H., Hazer, S., Helvacı, Ö., Gülhan, S. Ş. E., & Karaoǧlanoǧlu, N. (2022) · Journal of Health Sciences and Medicine · doi:10.32322/jhsm.1061755 · Cited by 1 · see citing works
Ohashi, N., Ichimura, H., Kikuchi, N., Tanaka, Y., Mikoshiba, T., Wada, Y., Okada, K., & Seto, T. (2025) · Journal of Artificial Organs · doi:10.1007/s10047-025-01521-y · Cited by 1 · see citing works
Preparing cardiovascular patients for the operative theatre
Loriaux, D. B., McCartney, S. L., Rampersad, P. P., Bryner, B. S., & Katz, J. N. (2023) · European Heart Journal Acute Cardiovascular Care · doi:10.1093/ehjacc/zuad005 · Cited by 1 · see citing works
Tolunay, T., Arıkan, M., Öztürk, R., & Tolunay, H. (2021) · Joint Diseases and Related Surgery · doi:10.52312/jdrs.2021.392 · Cited by 1 · see citing works
BORIONI, R., GAROFALO, M., TURANI, F., WELTERT, L. P., PACIOTTI, C., BELLISARIO, A., & PAULIS, R. D. (2021) · The Journal of Cardiovascular Surgery · doi:10.23736/s0021-9509.21.11924-x
Perioperative management of the high-risk surgical patient: cardiac surgery
Ranucci, M., Castelvecchio, S., & Ballotta, A. (2021) · Oxford University Press eBooks · doi:10.1093/med/9780198849346.003.0076
Cardiothoracic Surgery and Nutrition
Patel, R., & Nixon, A. (2023) · doi:10.1002/9781119809128.ch10
Zhang, W., Liu, Z., Wang, K., Zhang, L., Liu, S., He, K., Wang, H., Wang, J., Wang, Y., Yang, Y., et al. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.138444
RetractedÇelik, Ö., Doğan, U., Elli̇dağ, H. Y., Etli, Ö., Çakır, R. C., Yıldız, T. C., Aydemir, E., & Eyvaz, K. (2025) · European Journal of Trauma and Emergency Surgery · doi:10.1007/s00068-025-02782-1
The utility of thymus and spleen ultrasound in the early prediction of neonatal sepsis
Öztürk, F., Filiz, S., Çetiner, İ., Yağcı, B., Gürses, C., & Yapar, D. (2025) · Journal of Neonatal-Perinatal Medicine · doi:10.1177/19345798251378077
Reintam Blaser, A., Starkopf, J., Björck, M., Forbes, A., Kase, K., Kiisk, E., Laisaar, K.-T., Mihnovitš, V., Murruste, M., Mändul, M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26614438
Reintam Blaser, A., Starkopf, J., Björck, M., Forbes, A., Kase, K., Kiisk, E., Laisaar, K.-T., Mihnovitš, V., Murruste, M., Mändul, M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26614441
Reintam Blaser, A., Starkopf, J., Björck, M., Forbes, A., Kase, K., Kiisk, E., Laisaar, K.-T., Mihnovitš, V., Murruste, M., Mändul, M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26614435
Lin, H., Huang, Z., Liu, M., Li, X., & Guo, Y. (2026) · Frontiers in Surgery · doi:10.3389/fsurg.2026.1780015
Berikkhanov, Z. G. M., Akulov, Z. A., Ekaterina, K., Pogosyan, D., Tarabrin, E. А., Shestakov, A., Kotelnikov, A., Nikolaev, A., Razumovsky, V. S., Ivanova, M. Y., et al. (2026) · Diagnostics · doi:10.3390/diagnostics16203360
- Authors
- Zogheib, E., Cosse, C., Sabbagh, C., Marx, S., Caus, T., Henry, M., Nader, J., Fumery, M., Bernasinski, M., Besserve, P., Trojette, F., Renard, C., Duhaut, P., Kamel, S., Regimbeau, J.-M., & Dupont, H.
- Affiliations
- Inserm (FR)
- Centre Hospitalier Universitaire Amiens-Picardie (FR)
- Corresponding author
- Zogheib, Elie
- ORCID
- Venue
- Annals of Intensive Care
- Publisher
- Elsevier BV
- Published
- 2018
- Volume
- 8
- Issue
- 1
- Pages
- 46
- ISSN
- 2110-5820 (ISSN-L)
- PMC
- PMC5906418
- OpenAlex
- W2802697942
- Cited by
- 30
- References
- 32
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 7 · 2023: 3 · 2022: 7 · 2021: 3 · 2020: 4 · 2019: 1
- FWCI
- 2.08
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Annals of Intensive Care (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- LillOA (Université de Lille (University Of Lille)) (submittedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Abdominal vascular conditions and treatments
- Health Sciences › Medicine › Epidemiology › Sepsis Diagnosis and Treatment
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Abdominal Surgery and Complications
- Keywords
- intestinal ischemia, cardiac surgery, acute mesenteric ischemia, ischemic colitis, procalcitonin, aspartate aminotransferase, lactate, myoglobin, early diagnosis, postoperative morbidity, cardiac intensive care unit, prognostic factors, diagnostic accuracy, case-control matching
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
