Professional Documents
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Acute Lower Gastrointestinal Bleeding
Acute Lower Gastrointestinal Bleeding
Clinical Practice
This Journal feature begins with a case vignette highlighting a common clinical problem. Evidence
supporting various strategies is then presented, followed by a review of formal guidelines, when they exist.
The article ends with the authors’ clinical recommendations.
From the Institute of Gastroenterology A 71-year-old woman with hypertension, hypercholesterolemia, and ischemic heart
and Hepatology (I.M.G.) and Medical disease, who had a cardiac stent placed 4 months earlier, presents to the emergency
Imaging Institute (Z.N.), Emek Medical
Center, Afula, and Rappaport Faculty of department with multiple episodes of red or maroon-colored stool mixed with clots
Medicine, Technion–Israel Institute of Tech during the preceding 24 hours. Current medications include atenolol, atorvastatin,
nology, Haifa (I.M.G.) — both in Israel; aspirin (81 mg daily), and clopidogrel. On physical examination, the patient is dia-
and the Department of Medicine, Divi
sion of Gastroenterology, University of phoretic. While she is in a supine position, the heart rate is 91 beats per minute and
Washington School of Medicine, Seattle the blood pressure is 106/61 mm Hg; while she is sitting, the heart rate is 107 beats
(L.L.S.). Address reprint requests to Dr. per minute and the blood pressure is 92/52 mm Hg. The remainder of the examina-
Gralnek at the Institute of Gastroenterol
ogy and Hepatology, Emek Medical Cen tion is unremarkable, except for maroon-colored stool on digital rectal examination.
ter, 21 Izhak Rabin Blvd., Afula 1834111, The hemoglobin level is 9.3 g per deciliter, the platelet count 235,000 per cubic milli-
Israel, or at ian_gr@clalit.org.il. meter, and the international normalized ratio 1.1. How should this patient’s case be
N Engl J Med 2017;376:1054-63. further evaluated and managed?
DOI: 10.1056/NEJMcp1603455
Copyright © 2017 Massachusetts Medical Society.
The Cl inic a l Probl em
I
n the United States, gastrointestinal bleeding is the most common
cause of hospitalization due to gastrointestinal disease; approximately 30 to 40%
of all cases of gastrointestinal bleeding are from a lower gastrointestinal source.1
In most patients with acute lower gastrointestinal bleeding, the bleeding stops
without intervention, and there are no complications. However, advanced age and
An audio version clinically significant coexisting illnesses are associated with increased morbidity
of this article and mortality.2 Classically, acute lower gastrointestinal bleeding manifests as he-
is available at matochezia (maroon or red blood passed through the rectum). Uncommonly,
NEJM.org
lower gastrointestinal bleeding can manifest as melena (black, tarry stools), or,
conversely, brisk (rapid) upper gastrointestinal bleeding can manifest as hemato-
chezia. Previously, lower gastrointestinal bleeding was defined as bleeding origi-
nating distal to the ligament of Treitz. However, owing to the distinct nature of
small-intestinal bleeding (defined as bleeding originating between the ligament of
Treitz and the ileocecal valve and now referred to as middle gastrointestinal bleed-
ing), acute lower gastrointestinal bleeding is defined as the onset of hematochezia
originating from either the colon or the rectum.3,4 This review focuses on the
management of brisk, large-volume colorectal bleeding.
0.72 to 0.79).5,7-12 (For more on risk-factor mod- bleeding undergoing early colonoscopy (within
els, see Table S1 in the Supplementary Appendix, 12 to 24 hours after presentation) than among
available with the full text of this article at those undergoing colonoscopy at a later time,18-20
NEJM.org.) although two small, randomized trials compar-
ing early with later colonoscopy did not show
Initial Management significant differences in length of stay or in
Intravenous fluid resuscitation with crystalloids rates of rebleeding or surgery.21,22 Adequate
should be started on presentation.3,4,13 A recent preparation of the colon is important for endo-
guideline for the management of acute lower scopic visualization, diagnosis, and treatment;
gastrointestinal bleeding recommends a blood- preparation includes at least 4 liters of a poly-
transfusion approach that minimizes the admin- ethylene glycol solution or the equivalent, admin-
istration of blood — similar to guideline recom- istered over a period of approximately 4 hours.3,4
mendations for upper gastrointestinal bleeding.4,14 Colonoscopy or sigmoidoscopy without prepa-
Although randomized trials of transfusion ration should generally be avoided but can be
thresholds have not included patients with low considered in selected cases (e.g., suspected
er gastrointestinal bleeding, these recommen- bleeding from the distal left colon), with careful
dations for the management of acute lower cleaning and inspection of the colon during the
gastrointestinal bleeding are based on a large, procedure.4,23 In patients with ongoing bleeding
randomized trial and a meta-analysis involving who cannot consume the preparation solution,
patients with acute upper gastrointestinal bleed- the short-term placement of a nasogastric tube
ing that showed both a decreased risk of re- can be considered as long as the risk of aspira-
bleeding and a mortality benefit.15,16 The guide- tion is low. Patients should be without solid
lines recommend transfusion of packed red food for at least 8 hours before colonoscopy;
cells to maintain a hemoglobin level of more clear fluids, including the colonoscopy prepa-
than 7 g per deciliter in most patients, with ration, are permitted up to 2 hours before
consideration of a transfusion threshold of 9 g colonoscopy.
per deciliter in patients with clinically significant
coexisting illness (especially ischemic cardio-
vascular disease) or in the context of delayed
therapeutic intervention. Table 1. Causes of Acute Lower Gastrointestinal Bleeding
in Adults.*
Initial Diagnostic Evaluation
Cause Percentage of Cases
Endoscopy
Diverticulosis 30–65
Colonoscopy is the initial procedure for nearly
all patients presenting with acute lower gastro- Ischemic colitis 5–20
intestinal bleeding because it serves diagnostic Hemorrhoids 5–20
and potentially therapeutic purposes.3,4 Causes Colorectal polyps or neoplasms 2–15
of acute lower gastrointestinal bleeding in adults Angioectasias 5–10
are listed in Table 1. However, hematochezia in
Postpolypectomy bleeding 2–7
the context of hemodynamic instability (tachy-
cardia and hypotension) may represent a brisk Inflammatory bowel disease 3–5
upper gastrointestinal bleeding event; therefore, Infectious colitis 2–5
upper endoscopy must also be considered in Stercoral ulceration 0–5
such patients and can be performed immedi- Colorectal varices 0–3
ately before colonoscopy.3,4 Colonoscopy should
Radiation proctopathy 0–2
generally be performed within 24 hours after
patient presentation, after hemodynamic resus- NSAID-induced colopathy 0–2
citation and adequate colon cleansing.4 Obser- Dieulafoy’s lesion Rare
vational studies have shown a higher frequency
* NSAID denotes nonsteroidal antiinflammatory drug.
of definitive diagnoses and a shorter length of Adapted from Strate and Naumann.17
stay among patients with lower gastrointestinal
In patients with evidence of recurrent lower testinal bleeding caused by ischemic colitis,
gastrointestinal bleeding, repeat colonoscopy inflammatory ulcerative colitis, or colorectal
(with endoscopic hemostasis, if indicated) neoplasms is generally not amenable to durable
should be considered.3,4 Acute lower gastroin- endoscopic hemostasis and is usually treated
A
before surgical resection is critical to prevent the
need for subtotal colectomy and to prevent re-
current bleeding after surgery, owing to a missed
or incorrectly localized lesion. If the upper
bowel and small bowel have been ruled out as
the source of bleeding but the colonic location
of bleeding cannot be identified, a subtotal col-
ectomy may be appropriate. However, subtotal
colectomy is associated with higher morbidity
and mortality than segmental resection.34,35
Table 2. Procedures for the Evaluation and Treatment of Acute Lower Gastrointestinal Bleeding.*
high risk for myocardial infarction and death trointestinal bleeding.44-47 The efficacy of cone-
after discontinuation of dual antiplatelet therapy beam CT technology as an adjunctive diagnostic
and thus are generally advised to continue taking method in selective angiography and the em-
both medications.42 In patients who underwent bolic agent of choice in endovascular therapy are
coronary stenting or had a coronary syndrome unclear.48 In addition, better risk-stratification
less recently, discontinuation of the second anti- tools are needed to improve the triage of patients
platelet agent is recommended for 1 to 7 days, with lower gastrointestinal bleeding.
because discontinuation of the second, nonaspi-
rin antiplatelet agent appears to be associated Guidel ine s
with relatively low risk as long as aspirin therapy
is not interrupted.43 Guidelines for the evaluation and management of
acute lower gastrointestinal bleeding and severe
hematochezia have been published by U.S. profes-
A r e a s of Uncer ta in t y
sional societies of gastroenterologists and radiol-
Randomized trials are needed to better delineate ogists.3,4,24 The recommendations in this article
the most effective timing of colonoscopy, the role are generally concordant with these guidelines.
of colonoscopy versus radiography as the initial
diagnostic method, the choice among radio- C onclusions a nd
graphic imaging studies, and the efficacy and R ec om mendat ions
safety of endoscopic hemostasis treatments (in-
cluding topical powders, band ligation, over-the- Diverticular hemorrhage is the most likely cause
scope clips, and Doppler ultrasonography as an of the acute lower gastrointestinal bleeding in
adjunct to endoscopic hemostasis) in lower gas- the patient described in the vignette. This patient
is at increased risk for a poor outcome owing to response to fluid resuscitation and cannot under-
her advanced age, coexisting conditions, hemo- go colonoscopy, we would perform radiographic
dynamic instability at presentation, fresh blood evaluation, initially using multidetector CT angi-
on rectal examination, and use of dual antiplate- ography and then angiography and embolization
let therapy. Volume resuscitation with crystalloid if indicated. Her low-dose aspirin should be con-
fluids should be initiated immediately. The hemo- tinued without interruption. Because the patient’s
globin level should be reevaluated after hemody- coronary stent was placed more than 30 days
namic resuscitation to assess the need for trans- ago, we would stop clopidogrel temporarily and
fusion. If hemodynamic stability is achieved, resume its use 1 to 7 days after the cessation of
the patient should undergo colonoscopy within bleeding.
24 hours after presentation, after adequate colon
Dr. Gralnek reports receiving fees for serving on an advisory
preparation. Given her initial hemodynamic in- board from MOTUS GI, receiving consulting fees from Endo-
stability and use of dual antiplatelet therapy, Choice, MOTUS GI, and GI-View, receiving honoraria from Endo-
upper endoscopy should be performed immedi- Choice, MOTUS GI, Boston Scientific, Takeda Pharmaceuticals,
and GI-View, receiving grant support from MOTUS GI and Endo-
ately before colonoscopy to rule out an upper Aid, receiving an endoscopy workstation from EndoChoice, serv-
gastrointestinal source of bleeding. Endoscopic ing as an unpaid consultant to EndoAid, and serving on a data
hemostasis therapy may be applied if a definitive and safety monitoring board for Intec Pharma. No other potential
conflict of interest relevant to this article was reported.
bleeding lesion is identified. If the patient has Disclosure forms provided by the authors are available with
ongoing bleeding or an inadequate hemodynamic the full text of this article at NEJM.org.
References
1. Peery AF, Crockett SD, Barritt AS, et al. an artificial neural network: internal and colonoscopy and radiological procedures
Burden of gastrointestinal, liver, and pan- external validation of a predictive model. in the management of acute lower intesti-
creatic diseases in the United States. Gas- Lancet 2003;362:1261-6. nal bleeding. Clin Gastroenterol Hepatol
troenterology 2015;149(7):1731-1741.e3. 10. Strate LL, Orav EJ, Syngal S. Early pre- 2010;8:333-43.
2. Strate LL, Ayanian JZ, Kotler G, Syngal dictors of severity in acute lower intesti- 18. Jensen DM, Machicado GA. Diagnosis
S. Risk factors for mortality in lower intes- nal tract bleeding. Arch Intern Med 2003; and treatment of severe hematochezia: the
tinal bleeding. Clin Gastroenterol Hepatol 163:838-43. role of urgent colonoscopy after purge.
2008;6:1004-10. 11. Strate LL, Saltzman JR, Ookubo R, Gastroenterology 1988;95:1569-74.
3. Pasha SF, Shergill A, Acosta RD, et al. Mutinga ML, Syngal S. Validation of a 19. Jensen DM, Machicado GA, Jutabha R,
The role of endoscopy in the patient with clinical prediction rule for severe acute Kovacs TOG. Urgent colonoscopy for the
lower GI bleeding. Gastrointest Endosc lower intestinal bleeding. Am J Gastroen- diagnosis and treatment of severe diver-
2014;79:875-85. terol 2005;100:1821-7. ticular hemorrhage. N Engl J Med 2000;
4. Strate LL, Gralnek IM. ACG clinical 12. Velayos FS, Williamson A, Sousa KH, 342:78-82.
guideline: management of patients with et al. Early predictors of severe lower gas- 20. Strate LL, Syngal S. Timing of colo-
acute lower gastrointestinal bleeding. Am trointestinal bleeding and adverse out- noscopy: impact on length of hospital stay
J Gastroenterol 2016;111:459-74. comes: a prospective study. Clin Gastro- in patients with acute lower intestinal
5. Newman J, Fitzgerald JE, Gupta S, von enterol Hepatol 2004;2:485-90. bleeding. Am J Gastroenterol 2003;98:317-
Roon AC, Sigurdsson HH, Allen-Mersh TG. 13. Baradarian R, Ramdhaney S, Chapal- 22.
Outcome predictors in acute surgical ad- amadugu R, et al. Early intensive resusci- 21. Green BT, Rockey DC, Portwood G,
missions for lower gastrointestinal bleed- tation of patients with upper gastrointes- et al. Urgent colonoscopy for evaluation
ing. Colorectal Dis 2012;14:1020-6. tinal bleeding decreases mortality. Am J and management of acute lower gastroin-
6. Srygley FD, Gerardo CJ, Tran T, Fisher Gastroenterol 2004;99:619-22. testinal hemorrhage: a randomized con-
DA. Does this patient have a severe upper 14. Gralnek IM, Dumonceau JM, Kuipers trolled trial. Am J Gastroenterol 2005;100:
gastrointestinal bleed? JAMA 2012;307: EJ, et al. Diagnosis and management of 2395-402.
1072-9. nonvariceal upper gastrointestinal hemor- 22. Laine L, Shah A. Randomized trial of
7. Aoki T, Nagata N, Shimbo T, et al. De- rhage: European Society of Gastrointesti- urgent vs. elective colonoscopy in patients
velopment and validation of a risk scoring nal Endoscopy (ESGE) guideline. Endos- hospitalized with lower GI bleeding. Am J
system for severe acute lower gastrointes- copy 2015;47:a1-a46. Gastroenterol 2010;105:2636-42.
tinal bleeding. Clin Gastroenterol Hepatol 15. Villanueva C, Colomo A, Bosch A. 23. Lhewa DY, Strate LL. Pros and cons of
2016;14(11):1562-1570.e2. Transfusion for acute upper gastrointes- colonoscopy in management of acute lower
8. Kollef MH, O’Brien JD, Zuckerman tinal bleeding. N Engl J Med 2013;368: gastrointestinal bleeding. World J Gastro-
GR, Shannon W. BLEED: a classification 1362-3. enterol 2012;18:1185-90.
tool to predict outcomes in patients with 16. Wang J, Bao YX, Bai M, Zhang YG, Xu 24. American College of Radiology (ACR)
acute upper and lower gastrointestinal WD, Qi XS. Restrictive vs liberal transfu- Appropriateness Criteria:radiologic man-
hemorrhage. Crit Care Med 1997;25:1125- sion for upper gastrointestinal bleeding: agement of lower gastrointestinal tract
32. a meta-analysis of randomized controlled bleeding (updated 2014) (https://acsearch
9. Das A, Ben-Menachem T, Cooper GS, trials. World J Gastroenterol 2013; 19: .acr.org/docs/69457/Narrative/).
et al. Prediction of outcome in acute lower- 6919-27. 25. Gunderman R, Leef J, Ong K, Reba R,
gastrointestinal haemorrhage based on 17. Strate LL, Naumann CR. The role of Metz C. Scintigraphic screening prior to
visceral arteriography in acute lower gas- intestinal hemorrhage: results from a et al. ACCF/ACG/AHA 2008 expert consen-
trointestinal bleeding. J Nucl Med 1998; single-institution study. J Vasc Interv Ra- sus document on reducing the gastroin-
39:1081-3. diol 2010;21:477-83. testinal risks of antiplatelet therapy and
26. Zink SI, Ohki SK, Stein B, et al. Non- 34. Farner R, Lichliter W, Kuhn J, Fisher T. NSAID use. Am J Gastroenterol 2008;103:
invasive evaluation of active lower gastro- Total colectomy versus limited colonic 2890-907.
intestinal bleeding: comparison between resection for acute lower gastrointestinal 42. Ho PM, Peterson ED, Wang L, et al.
contrast-enhanced MDCT and 99mTc- bleeding. Am J Surg 1999;178:587-91. Incidence of death and acute myocardial
labeled RBC scintigraphy. AJR Am J Roent- 35. Bender JS, Wiencek RG, Bouwman DL. infarction associated with stopping clopi-
genol 2008;191:1107-14. Morbidity and mortality following total dogrel after acute coronary syndrome.
27. Jacovides CL, Nadolski G, Allen SR, et abdominal colectomy for massive lower JAMA 2008;299:532-9.
al. Arteriography for lower gastrointestinal gastrointestinal bleeding. Am Surg 1991; 43. Eisenberg MJ, Richard PR, Libersan D,
hemorrhage: role of preceding abdominal 57:536-41. Filion KB. Safety of short-term discontin-
computed tomographic angiogram in diag 36. Casado Arroyo R, Polo-Tomas M, Ron- uation of antiplatelet therapy in patients
nosis and localization. JAMA Surg 2015; calés MP, Scheiman J, Lanas A. Lower GI with drug-eluting stents. Circulation 2009;
150:650-6. bleeding is more common than upper 119:1634-42.
28. Kaltenbach T, Watson R, Shah J, et al. among patients on dual antiplatelet ther- 44. Barkun AN, Moosavi S, Martel M.
Colonoscopy with clipping is useful in the apy: long-term follow-up of a cohort of Topical hemostatic agents: a systematic
diagnosis and treatment of diverticular patients commonly using PPI co-therapy. review with particular emphasis on endo-
bleeding. Clin Gastroenterol Hepatol 2012; Heart 2012;98:718-23. scopic application in GI bleeding. Gastro-
10:131-7. 37. Abraham NS, Hartman C, Richardson intest Endosc 2013;77:692-700.
29. Diggs NG, Holub JL, Lieberman DA, P, Castillo D, Street RL Jr, Naik AD. Risk 45. Ishii N, Setoyama T, Deshpande GA,
Eisen GM, Strate LL. Factors that contrib- of lower and upper gastrointestinal bleed- et al. Endoscopic band ligation for colonic
ute to blood loss in patients with colonic ing, transfusions, and hospitalizations diverticular hemorrhage. Gastrointest En-
angiodysplasia from a population-based with complex antithrombotic therapy in dosc 2012;75:382-7.
study. Clin Gastroenterol Hepatol 2011;9: elderly patients. Circulation 2013; 128: 46. Manta R, Galloro G, Mangiavillano B,
415-20. 1869-77. et al. Over-the-scope clip (OTSC) repre-
30. Olmos JA, Marcolongo M, Pogorelsky 38. Sung JJ, Lau JY, Ching JY, et al. Con- sents an effective endoscopic treatment
V, Herrera L, Tobal F, Dávolos JR. Long- tinuation of low-dose aspirin therapy in for acute GI bleeding after failure of con-
term outcome of argon plasma ablation peptic ulcer bleeding: a randomized trial. ventional techniques. Surg Endosc 2013;
therapy for bleeding in 100 consecutive Ann Intern Med 2010;152:1-9. 27:3162-4.
patients with colonic angiodysplasia. Dis 39. Chan FKL, Leung Ki EL, Wong GLH, 47. Jensen DM, Ohning GV, Kovacs TO,
Colon Rectum 2006;49:1507-16. et al. Risks of bleeding recurrence and et al. Natural history of definitive diver-
31. Koh DC, Luchtefeld MA, Kim DG, et al. cardiovascular events with continued ticular hemorrhage based on stigmata of
Efficacy of transarterial embolization as aspirin use after lower gastrointestinal recent hemorrhage and colonoscopic Dop-
definitive treatment in lower gastrointesti- hemorrhage. Gastroenterology 2016;151: pler blood flow monitoring for risk strati-
nal bleeding. Colorectal Dis 2009;11:53-9. 271-7. fication and definitive hemostasis. Gastro-
32. Yi WS, Garg G, Sava JA. Localization 40. Baigent C, Blackwell L, Collins R, et al. intest Endosc 2016;83:416-23.
and definitive control of lower gastrointes- Aspirin in the primary and secondary pre- 48. Ierardi AM, Urbano J, De Marchi G,
tinal bleeding with angiography and em- vention of vascular disease: collaborative et al. New advances in lower gastrointes-
bolization. Am Surg 2013;79:375-80. meta-analysis of individual participant data tinal bleeding management with embolo-
33. Kim CY, Suhocki PV, Miller MJ Jr, from randomised trials. Lancet 2009;373: therapy. Br J Radiol 2016 February 4 (Epub
Khan M, Janus G, Smith TP. Provocative 1849-60. ahead of print).
mesenteric angiography for lower gastro- 41. Bhatt DL, Scheiman J, Abraham NS, Copyright © 2017 Massachusetts Medical Society.