Predictive value of transabdominal intestinal sonography in critically ill patients: a prospective observational study

Tao Gao, Min-Hua Cheng, Feng-Chan Xi, Yan Chen, Chun Cao, Ting Su, Wei-Qin Li, Wen-Kui Yu, Tao Gao, Min-Hua Cheng, Feng-Chan Xi, Yan Chen, Chun Cao, Ting Su, Wei-Qin Li, Wen-Kui Yu

Abstract

Background: This study examined the feasibility of transabdominal intestinal ultrasonography in evaluating acute gastrointestinal injury (AGI).

Methods: A total of 116 patients were included. Intestinal ultrasonography was conducted daily within 1 week after admission to the intensive care unit. Ultrasonography indicators including intestinal diameter, changes in the intestinal folds, thickness of the intestinal wall, stratification of the intestinal wall, and intestinal peristalsis (movement of the intestinal contents) were observed to determine the acute gastrointestinal injury ultrasonography (AGIUS) score. The gastrointestinal and urinary tract sonography ultrasound (GUTS) protocol score was also calculated. During the first week of the study, the gastrointestinal failure (GIF) score was determined daily. The correlations between transabdominal intestinal scores (AGIUS and GUTS) and the GIF score were analyzed to clarify the feasibility of evaluating AGI through observation of the intestine. The utility of intestinal ultrasonography indicators in predicting feeding intolerance was investigated to improve the ability of clinicians to manage AGI.

Results: A total of 751 ultrasonic examinations were performed with 511 images (68%) considered to be of "good quality." AGIUS and GUTS scores differed significantly between AGI patients (GIF score 0-2) and non-AGI patients (GIF score 3-4) (p < 0.001). Both scores correlated positively with GIF score (r = 0.54, p < 0.001; r = 0.66, p < 0.001). These ultrasonography indicators could predict feeding intolerance, with an area under the receiver operating characteristic curve of 0.60 (0.48-0.71; intestinal diameter), 0.76 (0.67-0.85; intestinal folds), 0.71 (0.62-0.80; wall thickness), 0.77 (0.69-0.86; wall stratification), and 0.78 (0.68-0.88; intestinal peristalsis). Compared to patients with a normal rate of peristalsis (5-10/min), patients with abnormal peristalsis rates (< 5/min or > 10/min) have increased risk for feeding intolerance (16/83 vs. 25/33, p < 0.001).

Conclusions: The transabdominal intestinal ultrasonography represents an effective means for assessing gastrointestinal injury in critically ill patients. Intestinal ultrasonography indicators, especially the degree of intestinal peristalsis, may be used to predict feeding intolerance.

Trial registration: ClinicalTrial.gov, NCT03589248. Registered 04 July 2018-retrospectively registered.

Keywords: Abdominal hypertension; Abdominal pressure; Acute gastrointestinal injury; GUTS protocol; POCUS; Ultrasound.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Examples of intestinal US images showing increased intestinal diameter, shortened intestinal folds, thickened intestinal walls, and stratified intestinal walls. a Increased intestinal diameter. b Shortened intestinal folds (solid arrow) and thickened intestinal walls (dotted arrow). c Stratified intestinal wall (solid arrow)
Fig. 2
Fig. 2
Enrollment flowchart
Fig. 3
Fig. 3
The evolution of SOFA with increasing AGIUS scores
Fig. 4
Fig. 4
The evolution of SOFA with increasing GUTS scores
Fig. 5
Fig. 5
ROC curve analysis for use of AGIUS, GIF, or GUTS score to predict 28-day mortality. Variables included in analyses were the maximum value within the first week
Fig. 6
Fig. 6
Normal transabdominal intestinal ultrasonography. This is a 36-year-old male. The intestine was screened with a curvilinear probe (5 MHz). The image shows normal intestinal diameter (

References

    1. Mutlu GM, Mutlu EA, Factor P. GI complications in patients receiving mechanical ventilation. Chest. 2001;119:1222–1241. doi: 10.1378/chest.119.4.1222.
    1. Reintam Blaser A, Parm P, Kitus R, Kern H, Starkopf J. Gastrointestinal symptoms in intensive care patients. Acta Anaesthesiol Scand. 2009;53:318–324. doi: 10.1111/j.1399-6576.2008.01860.x.
    1. Reintam Blaser A, Parm P, Kitus R, Starkopf J, Kern H. Gastrointestinal failure score in critically ill patients: a prospective observational study. Crit Care. 2008;12:R90. doi: 10.1186/cc6958.
    1. Reintam Blaser A, Parm P, Redlich U, Tooding LM, Starkopf J, Kohler F, et al. Gastrointestinal failure in intensive care: a retrospective clinical study in three different intensive care units in Germany and Estonia. BMC Gastroenterol. 2006;6:19. doi: 10.1186/1471-230X-6-19.
    1. Reintam Blaser A, Poeze M, Malbrain ML, Bjorck M, Oudemans-van Straaten HM, Starkopf J, et al. Gastrointestinal symptoms during the first week of intensive care are associated with poor outcome: a prospective multicentre study. Intensive Care Med. 2013;39:899–909. doi: 10.1007/s00134-013-2831-1.
    1. Reintam Blaser A, Malbrain ML, Starkopf J, Fruhwald S, Jakob SM, De Waele J, et al. Gastrointestinal function in intensive care patients: terminology, definitions and management. Recommendations of the ESICM Working Group on Abdominal Problems. Intensive Care Med. 2012;38:384–394. doi: 10.1007/s00134-011-2459-y.
    1. Malbrain ML, Peeters Y, Wise R. The neglected role of abdominal compliance in organ-organ interactions. Crit Care. 2016;20:67. doi: 10.1186/s13054-016-1220-x.
    1. Malbrain ML, De Laet I, De Waele JJ, Sugrue M, Schachtrupp A, Duchesne J, et al. The role of abdominal compliance, the neglected parameter in critically ill patients - a consensus review of 16. Part 2: measurement techniques and management recommendations. Anaesthesiol Intensive Ther. 2014;46:406–432. doi: 10.5603/AIT.2014.0063.
    1. Malbrain ML, Roberts DJ, De Laet I, De Waele JJ, Sugrue M, Schachtrupp A, et al. The role of abdominal compliance, the neglected parameter in critically ill patients - a consensus review of 16. Part 1: definitions and pathophysiology. Anaesthesiol Intensive Ther. 2014;46:392–405. doi: 10.5603/AIT.2014.0062.
    1. Cai Z, Malbrain ML, Sun J, Pan R, Ma J, Feng B, et al. Does elevated intra-abdominal pressure during laparoscopic colorectal surgery cause acute gastrointestinal injury? Videosurgery Miniinv. 2015;10:161–169. doi: 10.5114/wiitm.2015.52210.
    1. Moonen PJ, Reintam Blaser A, Starkopf J, Oudemans-van Straaten HM, Van der Mullen J, Vermeulen G, et al. The black box revelation: monitoring gastrointestinal function. Anaesthesiol Intensive Ther. 2018;50:72–81.
    1. Reintam Blaser A, Starkopf J, Moonen PJ, Malbrain ML, Oudemans-van Straaten HM. Perioperative gastrointestinal problems in the ICU. Anaesthesiol Intensive Ther. 2018;50:59–71.
    1. Kirkpatrick AW, Roberts DJ, De Waele J, Jaeschke R, Malbrain ML, De Keulenaer B, et al. Intra-abdominal hypertension and the abdominal compartment syndrome: updated consensus definitions and clinical practice guidelines from the World Society of the Abdominal Compartment Syndrome. Intensive Care Med. 2013;39:1190–1206. doi: 10.1007/s00134-013-2906-z.
    1. Cheatham ML, Malbrain ML, Kirkpatrick A, Sugrue M, Parr M, De Waele J, et al. Results from the International Conference of Experts on Intra-abdominal Hypertension and Abdominal Compartment Syndrome. II. Recommendations. Intensive Care Med. 2007;33:951–962. doi: 10.1007/s00134-007-0592-4.
    1. Malbrain ML, Cheatham ML, Kirkpatrick A, Sugrue M, Parr M, De Waele J, et al. Results from the international conference of experts on intra-abdominal hypertension and abdominal compartment syndrome. I Definitions Intensive Care Med. 2006;32:1722–1732. doi: 10.1007/s00134-006-0349-5.
    1. Lichtenstein D, Malbrain ML. Critical care ultrasound in cardiac arrest. Technological requirements for performing the SESAME-protocol--a holistic approach. Anaesthesiol Intensive Ther. 2015;47:471–481. doi: 10.5603/AIT.a2015.0072.
    1. Lichtenstein D, van Hooland S, Elbers P, Malbrain ML. Ten good reasons to practice ultrasound in critical care. Anaesthesiol Intensive Ther. 2014;46:323–335. doi: 10.5603/AIT.2014.0056.
    1. Sugrue G, Malbrain ML, Pereira B, Wise R, Sugrue M. Modern imaging techniques in intra-abdominal hypertension and abdominal compartment syndrome: a bench to bedside overview. Anaesthesiol Intensive Ther. 2018;50:234–242. doi: 10.5603/AIT.a2017.0076.
    1. Pereira BM, Pereira RG, Wise R, Sugrue G, Zakrison TL, Dorigatti AE, et al. The role of point-of-care ultrasound in intra-abdominal hypertension management. Anaesthesiol Intensive Ther. 2017;49:373–381. doi: 10.5603/AIT.a2017.0074.
    1. Hamada SR, Garcon P, Ronot M, Kerever S, Paugam-Burtz C, Mantz J. Ultrasound assessment of gastric volume in critically ill patients. Intensive Care Med. 2014;40:965–972. doi: 10.1007/s00134-014-3320-x.
    1. Haruma K, Kusunoki H, Manabe N, Kamada T, Sato M, Ishii M, et al. Real-time assessment of gastroduodenal motility by ultrasonography. Digestion. 2008;77(Suppl 1):48–51. doi: 10.1159/000111488.
    1. Hernandez-Socorro CR, Marin J, Ruiz-Santana S, Santana L, Manzano JL. Bedside sonographic-guided versus blind nasoenteric feeding tube placement in critically ill patients. Crit Care Med. 1996;24:1690–1694. doi: 10.1097/00003246-199610000-00015.
    1. Tsujimoto H, Tsujimoto Y, Nakata Y, Akazawa M, Kataoka Y. Ultrasonography for confirmation of gastric tube placement. Cochrane Database Syst Rev. 2017;4:CD012083.
    1. Perez-Calatayud AA, Carrillo-Esper R, Anica-Malagon ED, Briones-Garduno JC, Arch-Tirado E, Wise R, et al. Point-of-care gastrointestinal and urinary tract sonography in daily evaluation of gastrointestinal dysfunction in critically ill patients (GUTS protocol) Anaesthesiol Intensive Ther. 2018;50:40–48. doi: 10.5603/AIT.a2017.0073.
    1. Rice TW, Mogan S, Hays MA, Bernard GR, Jensen GL, Wheeler AP. Randomized trial of initial trophic versus full-energy enteral nutrition in mechanically ventilated patients with acute respiratory failure. Crit Care Med. 2011;39:967–974. doi: 10.1097/CCM.0b013e31820a905a.
    1. Gungabissoon U, Hacquoil K, Bains C, Irizarry M, Dukes G, Williamson R, et al. Prevalence, risk factors, clinical consequences, and treatment of enteral feed intolerance during critical illness. JPEN J Parenter Enteral Nutr. 2015;39:441–448. doi: 10.1177/0148607114526450.
    1. Malbrain ML. Different techniques to measure intra-abdominal pressure (IAP): time for a critical re-appraisal. Intensive Care Med. 2004;30:357–371. doi: 10.1007/s00134-003-2107-2.
    1. Cheatham ML, White MW, Sagraves SG, Johnson JL, Block EF. Abdominal perfusion pressure: a superior parameter in the assessment of intra-abdominal hypertension. J Trauma. 2000;49:621–626. doi: 10.1097/00005373-200010000-00008.
    1. Malbrain ML, Van Regenmortel N, Saugel B, De Tavernier B, Van Gaal PJ, Joannes-Boyau O, et al. Principles of fluid management and stewardship in septic shock: it is time to consider the four D’s and the four phases of fluid therapy. Ann Intensive Care. 2018;8:66. doi: 10.1186/s13613-018-0402-x.
    1. Sharma V, Gudivada D, Gueret R, Bailitz J. Ultrasound-assessed gastric antral area correlates with aspirated tube feed volume in enterally fed critically ill patients. Nutr Clin Pract. 2017;32:206–211. doi: 10.1177/0884533616681530.
    1. Liu Y, Gao YK, Yao L, Li L. Modified B-ultrasound method for measurement of antral section only to assess gastric function and guide enteral nutrition in critically ill patients. World J Gastroenterol. 2017;23:5229–5236. doi: 10.3748/wjg.v23.i28.5229.
    1. Chatelon J, Bourillon C, Darmon H, Carbonne H, Chhor V, Follin A, et al. Feasibility and predictive value of ultrasound assessment of the gastric residual volume in surgical critically ill patients: a pilot study. Crit Care Med. 2016;44:e1255–e1257. doi: 10.1097/CCM.0000000000002040.
    1. Gultekin Y, Oz G, Yorganci K. Comment on Hamada et al. Ultrasound assessment of gastric volume in critically ill patients. Intensive Care Med. 2015;41:958. doi: 10.1007/s00134-015-3747-8.
    1. Kar P, Jones KL, Horowitz M, Chapman MJ, Deane AM. Measurement of gastric emptying in the critically ill. Clin Nutr. 2015;34:557–564. doi: 10.1016/j.clnu.2014.11.003.
    1. Reintam Blaser A, Starkopf J, Kirsimagi U, Deane AM. Definition, prevalence, and outcome of feeding intolerance in intensive care: a systematic review and meta-analysis. Acta Anaesthesiol Scand. 2014;58:914–922. doi: 10.1111/aas.12302.
    1. Reintam Blaser A, Malbrain ML, Regli A. Abdominal pressure and gastrointestinal function: an inseparable couple? Anaesthesiol Intensive Ther. 2017;49:146–158. doi: 10.5603/AIT.a2017.0026.
    1. Reintam Blaser A, Parm P, Kitus R, Starkopf J. Intra-abdominal hypertension and gastrointestinal symptoms in mechanically ventilated patients. Crit Care Res Pract. 2011;2011:982507.
    1. McClave SA, Taylor BE, Martindale RG, Warren MM, Johnson DR, Braunschweig C, et al. Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill patient: Society of Critical Care Medicine (SCCM) and American Society for Parenteral and Enteral Nutrition (A.S.P.E.N.) JPEN J Parenter Enteral Nutr. 2016;40:159–211. doi: 10.1177/0148607115621863.
    1. Kreymann KG, Berger MM, Deutz NE, Hiesmayr M, Jolliet P, Kazandjiev G, et al. ESPEN guidelines on enteral nutrition: intensive care. Clin Nutr. 2006;25:210–223. doi: 10.1016/j.clnu.2006.01.021.
    1. Montejo JC. Enteral nutrition-related gastrointestinal complications in critically ill patients: a multicenter study. The Nutritional and Metabolic Working Group of the Spanish Society of Intensive Care Medicine and Coronary Units. Crit Care Med. 1999;27:1447–1453. doi: 10.1097/00003246-199908000-00006.
    1. Adam S, Batson S. A study of problems associated with the delivery of enteral feed in critically ill patients in five ICUs in the UK. Intensive Care Med. 1997;23:261–266. doi: 10.1007/s001340050326.
    1. Peng YZ, Yuan ZQ, Xiao GX. Effects of early enteral feeding on the prevention of enterogenic infection in severely burned patients. Burns. 2001;27:145–149. doi: 10.1016/S0305-4179(00)00078-4.
    1. Chang JC. Disseminated intravascular coagulation: is it fact or fancy? Blood Coagul Fibrinolysis. 2018;29:330–337. doi: 10.1097/MBC.0000000000000727.
    1. Silva CFA, de Vasconcelos SG, da Silva TA, Silva FM. Permissive or trophic enteral nutrition and full enteral nutrition had similar effects on clinical outcomes in intensive care: a systematic review of randomized clinical trials. Nutr Clin Pract. 2018;33:388–396. doi: 10.1002/ncp.10001.
    1. Holodinsky JK, Roberts DJ, Ball CG, Reintam Blaser A, Starkopf J, Zygun DA, et al. Risk factors for intra-abdominal hypertension and abdominal compartment syndrome among adult intensive care unit patients: a systematic review and meta-analysis. Crit Care. 2013;17:R249. doi: 10.1186/cc13075.
    1. Kralik R, Trnovsky P, Kopacova M. Transabdominal ultrasonography of the small bowel. Gastroenterol Res Pract. 2013;2013:896704. doi: 10.1155/2013/896704.
    1. Wale A, Pilcher J. Current role of ultrasound in small bowel imaging. Semin Ultrasound CT MR. 2016;37:301–312. doi: 10.1053/j.sult.2016.03.001.
    1. Danse EM, Jamart J, Hoang P, Laterre PF, Kartheuser A, Van Beers BE. Focal bowel wall changes detected with colour Doppler ultrasound: diagnostic value in acute non-diverticular diseases of the colon. Br J Radiol. 2004;77:917–921. doi: 10.1259/bjr/18038687.
    1. Malik A, Saxena NC. Ultrasound in abdominal tuberculosis. Abdom Imaging. 2003;28:574–579. doi: 10.1007/s00261-002-0061-z.
    1. Marik PE, Malbrain ML. The SEP-1 quality mandate may be harmful: how to drown a patient with 30 mL per kg fluid! Anaesthesiol Intensive Ther. 2017;49:323–328. doi: 10.5603/AIT.a2017.0056.
    1. Malbrain ML, Marik PE, Witters I, Cordemans C, Kirkpatrick AW, Roberts DJ, et al. Fluid overload, de-resuscitation, and outcomes in critically ill or injured patients: a systematic review with suggestions for clinical practice. Anaesthesiol Intensive Ther. 2014;46:361–380. doi: 10.5603/AIT.2014.0060.
    1. Lewis K, Alqahtani Z, McIntyre L, Almenawer S, Alshamsi F, Rhodes A, et al. The efficacy and safety of prokinetic agents in critically ill patients receiving enteral nutrition: a systematic review and meta-analysis of randomized trials. Crit Care. 2016;20:259. doi: 10.1186/s13054-016-1441-z.
    1. Haq AI, Cook LJ. MRSA enteritis causing a high stoma output in the early postoperative phase after bowel surgery. Ann R Coll Surg Engl. 2007;89:303–308. doi: 10.1308/003588407X179143.
    1. Dell'Aquila P, Pietrini L, Barone M, Cela EM, Valle ND, Amoruso A, et al. Small intestinal contrast ultrasonography-based scoring system: a promising approach for the diagnosis and follow-up of celiac disease. J Clin Gastroenterol. 2005;39:591–595. doi: 10.1097/01.mcg.0000170766.74943.23.
    1. Nylund K, Hausken T, Folvik G, Lied GA, Viola I, Hauser H, et al. Sonography of the small intestine. World J Gastroenterol. 2009;15:11. doi: 10.3748/wjg.15.1319.
    1. Rombeau JL, Takala J. Summary of round table conference: gut dysfunction in critical illness. Intensive Care Med. 1997;23:476–479. doi: 10.1007/s001340050361.
    1. Reintam Blaser A, Starkopf J, Alhazzani W, Berger MM, Casaer MP, Deane AM, et al. Early enteral nutrition in critically ill patients: ESICM clinical practice guidelines. Intensive Care Med. 2017;43:380–398. doi: 10.1007/s00134-016-4665-0.
    1. Ridley EJ, Davies AR, Parke R, Bailey M, McArthur C, Gillanders L, et al. Supplemental parenteral nutrition versus usual care in critically ill adults: a pilot randomized controlled study. Crit Care. 2018;22:12. doi: 10.1186/s13054-018-1939-7.
    1. Wu W, Zhong M, Zhu DM, Song JQ, Huang JF, Wang Q, et al. Effect of early full-calorie nutrition support following esophagectomy: a randomized controlled trial. JPEN J Parenter Enteral Nutr. 2017;41:1146–1154. doi: 10.1177/0148607116651509.
    1. Oshima T, Heidegger CP, Pichard C. Supplemental parenteral nutrition is the key to prevent energy deficits in critically ill patients. Nutr Clin Pract. 2016;31:432–437. doi: 10.1177/0884533616651754.

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