Acute Lower Gastrointestinal Bleeding

Written By Danial Mirza

Definition

Acute Lower Gastrointestinal Bleeding (LGIB) is formally defined as hemorrhage originating from a source anatomically distal to the Ligament of Treitz, with a duration of less than three days. Clinically, it is significant enough to cause hemodynamic instability (shock), a substantial drop in hemoglobin necessitating blood transfusion, or the overt passage of blood per rectum, known as hematochezia (1, 21).

The Ligament of Treitz, a peritoneal fold anchoring the duodenojejunal flexure, is more than a simple anatomical footnote; it is the critical landmark that dictates the entire initial management pathway. Bleeding proximal to it (Upper GI Bleed, or UGIB) is managed with a different paradigm, often involving early administration of proton-pump inhibitors and emergent upper endoscopy (esophagogastroduodenoscopy or EGD). In contrast, bleeding distal to it (LGIB) requires a different diagnostic algorithm, primarily centered on ruling out a UGIB in unstable patients, followed by colonoscopy or advanced radiological imaging. This fundamental distinction prevents critical delays and ensures the correct initial intervention is chosen, directly impacting patient survival and morbidity.

Epidemiology

While comprehensive national incidence data for Malaysia remains an area for further research, a pivotal local study from a major tertiary hospital revealed that LGIB was the leading indication for colonoscopy, comprising 34% of all procedures performed (1). This figure strongly suggests a significant and under-appreciated disease burden within the Malaysian healthcare system. Globally, LGIB is less frequent than UGIB, with a reported annual incidence between 20 and 87 cases per 100,000 adults, making it a common cause for emergency hospital admission (9, 13).

The condition has a strong predilection for older individuals, with the incidence rising dramatically after the age of 60; the mean age of presentation is typically between 63 and 69 years (10, 12). This demographic trend is directly linked to the higher prevalence of age-related colonic pathologies, primarily diverticulosis and angiodysplasia. A concerning epidemiological shift is underway: while UGIB rates are declining due to H. pylori eradication and widespread PPI use, the incidence of LGIB has remained stable or is increasing. This is propelled by two major factors: the aging of the population and, critically, the escalating use of antithrombotic and anti-inflammatory drugs. The widespread prescription of aspirin, dual antiplatelet therapy (e.g., clopidogrel), direct oral anticoagulants (DOACs), and non-steroidal anti-inflammatory drugs (NSAIDs) for cardiovascular and rheumatological diseases has transformed minor mucosal lesions into sources of major hemorrhage, increasing both the frequency and severity of LGIB episodes (12).

Pathophysiology

The underlying mechanisms of LGIB are diverse, and a strong grasp of pathophysiology allows the clinician to form an accurate differential diagnosis from the initial history.

The most common cause of major, acute LGIB, responsible for up to 40% of cases, is Diverticular Disease. The pathophysiology is purely mechanical. Colonic diverticula are outpouchings that occur where the vasa recta—the penetrating arteries supplying the colon—pierce the muscle layer, creating an inherent point of weakness. As these arteries drape over the dome of the diverticulum, they are exposed and vulnerable to erosion from hard, inspissated stool. This leads to asymmetric rupture of the artery, causing an abrupt, large-volume, and characteristically painless arterial hemorrhage (16). Bleeding is more common from right-sided diverticula, which tend to have wider necks and expose the vessel over a larger surface area.

Angiodysplasia, or arteriovenous malformation (AVM), is the second most frequent cause, accounting for roughly 25% of cases. These are acquired, fragile, dilated submucosal blood vessels, most commonly found in the cecum and ascending colon of adults over 60. They are thought to arise from chronic, low-grade obstruction of submucosal veins, leading to capillary dilation and the formation of direct arteriovenous shunts. Their rupture results in painless bleeding that can be acute or chronic (16, 18). There is a well-known association with aortic stenosis (Heyde's syndrome), where high shear stress across the diseased valve is thought to cause an acquired von Willebrand factor deficiency, and with chronic kidney disease, where uremia contributes to platelet dysfunction.

Colitis, or inflammation of the colon, causes bleeding through mucosal damage and ulceration.

  • Ischemic Colitis: Particularly common in the elderly with atherosclerosis, this results from a transient reduction in blood flow to colonic "watershed" areas—regions with tenuous collateral circulation, like the splenic flexure and rectosigmoid junction. This non-occlusive ischemia leads to mucosal sloughing, presenting classically as the acute onset of cramping abdominal pain followed within hours by the passage of bloody diarrhea (9).

  • Inflammatory Bowel Disease (IBD): In Ulcerative Colitis, diffuse inflammation confined to the mucosa leads to widespread friability and continuous bleeding. In Crohn's Disease, deep, transmural, "knife-like" ulcers can erode directly into larger submucosal vessels, potentially causing more significant hemorrhage. The bleeding is typically accompanied by a history of chronic diarrhea, abdominal pain, and weight loss (16).

  • Infectious Colitis: Pathogens like Campylobacter, Salmonella, Shigella, and Shiga toxin-producing E. coli (EHEC) invade the mucosa or produce toxins that cause hemorrhagic inflammation, leading to acute bloody diarrhea, fever, and cramping (9).

Neoplasia, including benign polyps and colorectal cancer, accounts for about 12.5% of cases. While often causing chronic, occult blood loss leading to iron deficiency anemia, larger tumors with friable, ulcerated surfaces can erode into vessels and present as a significant acute bleed (16).

Anorectal disorders like hemorrhoids and anal fissures are the most frequent cause of minor rectal bleeding in patients under 50. Bleeding from internal hemorrhoids is typically painless, bright red, and occurs with defecation. Anal fissures cause similar bleeding but are associated with severe pain. While extremely common, they are a rare cause of hemodynamically significant hemorrhage and should be considered a diagnosis of exclusion in major bleeds (9, 16).

Clinical Presentation

The classic presentation of LGIB is hematochezia—the passage of bright red or maroon blood per rectum (1). However, a meticulous history is paramount to narrowing the differential diagnosis and stratifying risk.

Diagnostic Clues:

  • Painless, large-volume, abrupt-onset hematochezia in an older patient is the hallmark of a vascular etiology like diverticular bleeding or angiodysplasia.

  • Cramping abdominal pain that precedes the bleeding by several hours is highly suggestive of an ischemic process, most commonly ischemic colitis.

  • Chronic diarrhea, tenesmus, and weight loss accompanying the bleed points towards an inflammatory cause like IBD.

  • Fever and acute, profuse bloody diarrhea suggest an infectious colitis.

Common Symptoms (>50%):

  • Hematochezia (bright red or maroon stools) (1)

  • Dizziness, lightheadedness, or weakness (symptoms of intravascular volume loss) (9)

Less Common Symptoms (10-50%):

  • Melena (black, tarry stools) can occur in LGIB if the source is in the right colon or small bowel, where transit time is slow enough for bacterial degradation of hemoglobin (9).

  • Syncope or pre-syncope, indicating significant hypovolemia and cerebral hypoperfusion (9).

  • Abdominal cramping or pain (associated with ischemic, infectious, or inflammatory colitis) (9).

⚠️ Red Flag Signs & Symptoms:

  • Hemodynamic instability (Tachycardia >100 bpm, Hypotension SBP <90 mmHg). This indicates a massive hemorrhage with >30% circulatory volume loss, requiring immediate, aggressive resuscitation.

  • Syncope. This is a powerful predictor of a severe bleed and adverse outcomes, as it signals that cerebral perfusion has been critically compromised (1).

  • Persistent bleeding despite initial fluid resuscitation. This suggests a high-pressure arterial bleed that will not resolve spontaneously and requires urgent intervention.

  • Concomitant use of anticoagulants or dual antiplatelet therapy. These medications can turn a minor bleed into an uncontrollable hemorrhage and complicate management (12).

Complications

  • Cardiovascular: Hypovolemic shock is the most immediate life-threatening complication. Profound anemia and hypotension can also precipitate a Type 2 myocardial infarction (due to supply-demand mismatch) in patients with underlying coronary artery disease, as well as cardiac arrhythmias.

  • Renal: Severe hypovolemia leads to reduced renal perfusion, causing pre-renal acute kidney injury with a rising creatinine level.

  • Iatrogenic: Complications can arise from therapy itself, including transfusion-associated circulatory overload (TACO), bowel perforation during colonoscopy (risk <1%), and post-embolization syndrome or, more seriously, bowel ischemia after radiological intervention (risk ~5%) (36).

Prognosis

While approximately 80% of LGIB episodes resolve spontaneously, this statistic can be misleadingly reassuring. The overall in-hospital mortality rate is between 2% and 4%, but this figure skyrockets to as high as 21% in the high-risk cohort of elderly patients with multiple comorbidities and massive bleeding (1). The risk of re-bleeding after an initial episode is substantial, ranging from 6.7% to 13.5%, highlighting the critical importance of achieving a definitive diagnosis and providing effective therapy to prevent recurrence (1). Risk stratification tools like the Oakland Score can help identify patients at low risk of adverse outcomes who may be suitable for outpatient management.

Differential Diagnosis

A key diagnostic challenge is distinguishing LGIB from a brisk UGIB, as up to 15% of patients presenting with severe hematochezia and shock will be found to have an upper GI source (1).

  • Brisk Upper GI Bleed (e.g., Peptic Ulcer, Varices): This must be the primary consideration in any patient with hematochezia and hemodynamic instability. Rapid transit of a large volume of blood from the stomach or duodenum can overwhelm the bowel, presenting as bright red blood per rectum. Clinical clues include a history of dyspepsia, NSAID use, or known liver disease. A high BUN-to-creatinine ratio (>30) is a strong indicator, as digested blood in the upper tract provides a significant protein load that is absorbed as urea (14). An urgent upper endoscopy is mandatory in this setting to rule out a life-threatening UGIB before committing to a lengthy bowel preparation for colonoscopy (22).

  • Ischemic Colitis: This is a key differential in an elderly patient with cardiovascular risk factors (e.g., atrial fibrillation, peripheral vascular disease) who presents with acute, cramping abdominal pain followed by bleeding. The temporal sequence of pain preceding hematochezia is the classic feature that helps distinguish it from the painless hemorrhage of diverticular disease (9).

  • Infectious Colitis: This diagnosis should be actively considered if the patient presents with fever, tenesmus, and profuse bloody diarrhea. A detailed history regarding recent travel, antibiotic use (risk for C. difficile), or consumption of potentially contaminated food is crucial. Stool cultures and testing for C. difficile toxin are essential to confirm the diagnosis (9).

  • Inflammatory Bowel Disease (IBD): This should be on the differential list for younger patients (<50 years) or those with a history of chronic diarrhea, weight loss, and other systemic or extra-intestinal manifestations (e.g., arthritis, uveitis). The bleeding pattern is typically less massive than a diverticular bleed but is often more persistent and mixed with mucus (16).

Investigations

The diagnostic strategy is dictated entirely by the patient's hemodynamic stability. Resuscitation is not sequential but simultaneous with the diagnostic workup.

Immediate & Bedside Tests

  • Vital Signs & Orthostatics: An immediate and serial assessment of heart rate and blood pressure is crucial. An orthostatic drop in systolic BP of >20 mmHg or an increase in heart rate of >20 bpm upon standing is a sensitive indicator of at least 15% intravascular volume loss (20). The shock index (Heart Rate / Systolic BP), a simple calculation, is a powerful bedside tool; a value >1 is a strong predictor of instability and the need for massive transfusion (20).

  • Digital Rectal Exam (DRE): A DRE is mandatory in every patient with LGIB. It allows the clinician to assess for anorectal masses, tenderness, or fissures and, most importantly, to directly inspect the stool for color (bright red, maroon, melena), which helps guide the subsequent workup (9). Anoscopy can be performed at the bedside to provide direct visualization of the anal canal and distal rectum, which is particularly useful for definitively diagnosing or excluding hemorrhoids as the source.

Diagnostic Workup

For the Hemodynamically UNSTABLE Patient:

  • CT Angiography (CTA): This is the first-line diagnostic test for unstable patients with active, ongoing bleeding. An urgent multiphase CTA is rapid, widely available, non-invasive, and does not require bowel preparation (the action), allowing for rapid and precise localization of a bleeding source (seen as active contrast extravasation into the bowel lumen) at rates as low as 0.3-0.5 mL/min to guide subsequent intervention (the rationale) (27).

  • Upper Endoscopy (EGD): An EGD should be strongly considered and often performed first in any unstable patient with hematochezia (the action) to definitively rule out a life-threatening UGIB source, which is the culprit in up to 15% of such presentations and requires completely different management (the rationale) (22).

  • Catheter Angiography: This is indicated for patients with a positive CTA or for those who are too unstable to even be moved to the CT scanner. It serves as both a diagnostic tool and a therapeutic one (the action), as it allows for immediate transcatheter arterial embolization (TAE) with microcoils or other agents once the bleeding vessel is identified (the rationale) (31).

For the Hemodynamically STABLE Patient:

  • Colonoscopy: This is the gold standard investigation for stable patients. After an adequate bowel purge to clear blood and stool, colonoscopy provides a high diagnostic yield (75-90%) and, crucially, allows for immediate therapeutic intervention like clipping, thermal coagulation, or band ligation (the action), which can achieve definitive hemostasis, identify stigmata of recent hemorrhage, and prevent re-bleeding (the rationale) (32). Guidelines recommend performing the colonoscopy within 24 hours of presentation for optimal yield (22).

Monitoring & Staging

  • Full Blood Count (FBC): An initial FBC is essential to establish a baseline hemoglobin and platelet count, but it can be falsely reassuring initially before hemodilution occurs. Serial FBCs are then performed every 4-8 hours depending on severity (the action) to assess for ongoing blood loss, monitor the response to resuscitation, and guide transfusion therapy (the rationale) (1).

  • Coagulation Profile (PT/INR, aPTT): This is critical to identify any underlying or iatrogenic coagulopathy (e.g., from warfarin or liver disease) (the action), which must be identified and corrected to allow for effective clot formation and achieve hemostasis (the rationale) (1).

  • Renal Function & Electrolytes (BUN/Creatinine): This assesses for acute kidney injury from hypoperfusion and can provide vital diagnostic clues (the action), as a disproportionately elevated BUN relative to creatinine strongly suggests a UGIB source due to the digestion of a large protein load from blood (the rationale) (14).

  • Group & Screen / Crossmatch: Blood must be typed and crossmatched immediately upon patient arrival (the action) to ensure that packed red blood cells and other blood products are available for transfusion without life-threatening delay (the rationale) (1).

Management

Management Principles

The management of acute LGIB is a dynamic process centered on three core principles: prompt and aggressive hemodynamic resuscitation, accurate localization of the bleeding source, and application of definitive hemostasis to prevent recurrence.

Acute Stabilisation (The First Hour)

  • Airway/Breathing: Administer high-flow oxygen via a non-rebreather mask to maintain SpO2 >94% (the action), which is crucial to maximize arterial oxygen content and prevent tissue hypoxia driven by a depleted circulatory volume (the rationale). Patients with altered mental status may require intubation for airway protection.

  • Circulation: Secure two large-bore (16-gauge or larger) IV cannulas and administer a stat fluid bolus of an isotonic crystalloid, such as Normal Saline or a balanced solution (e.g., Lactated Ringer's), at 20mL/kg (the action) to rapidly expand intravascular volume, correct hypotension, and restore end-organ perfusion (the rationale) (1). In cases of refractory shock, activate the hospital's massive transfusion protocol.

  • Disability: Assess mental status using the Glasgow Coma Scale (GCS); a decreased GCS may indicate cerebral hypoperfusion or an impending need for airway protection.

  • Exposure: Fully expose the patient to perform a thorough secondary survey, assessing for signs of trauma or other sources of bleeding, while taking care to prevent hypothermia with warming blankets.

Definitive Therapy

Definitive therapy is tailored to the bleeding source identified.

  • Endoscopic Therapy: For diverticular bleeding or post-polypectomy bleeding, mechanical methods like through-the-scope clips are preferred for their safety and efficacy in achieving mechanical coaptation of the vessel (22). For broad, flat vascular lesions like angiodysplasia or radiation proctitis, thermal coagulation (e.g., Argon Plasma Coagulation) is effective for ablating the superficial vessels (22). Epinephrine injection is never used as monotherapy due to high re-bleeding rates but is a useful adjunct to temporarily slow bleeding via vasoconstriction, thereby improving visualization for a definitive second modality like clipping (22).

  • Radiological Therapy: Transcatheter Arterial Embolization (TAE) is a life-saving intervention for patients who fail or are not candidates for endoscopy. Using a superselective technique, a microcatheter is advanced into the culprit artery, and embolic agents (e.g., microcoils) are deployed to occlude the vessel. This is highly effective, with technical success rates of 80-90% (28, 36).

  • Surgical Therapy: Surgery is now a last resort, reserved for the small subset of patients with life-threatening hemorrhage unresponsive to aggressive endoscopic and radiological control (18, 37). A directed segmental colectomy based on accurate pre-operative localization (from CTA or endoscopy) is the procedure of choice. A "blind" subtotal colectomy, performed without a known source, is an act of desperation associated with extremely high morbidity and mortality and should be avoided whenever possible (37).

Supportive & Symptomatic Care

  • Blood Transfusion: Modern evidence supports a restrictive transfusion strategy. Transfuse packed red blood cells only when hemoglobin drops below 7 g/dL in most hemodynamically stable patients (22). This approach avoids the risks of over-transfusion, such as volume overload and immunomodulation. A more liberal threshold of <8 g/dL may be considered for patients with known significant underlying cardiovascular disease (e.g., recent MI) where higher oxygen-carrying capacity might be beneficial (22).

  • Reversal of Anticoagulation: This high-risk intervention is reserved only for patients with life-threatening, hemodynamically compromising hemorrhage that is unresponsive to initial resuscitation efforts (21). Routine reversal is not recommended. If deemed necessary, use targeted agents: for warfarin, 4-factor prothrombin complex concentrate (PCC) is superior to FFP. For DOACs, use specific reversal agents if available (e.g., idarucizumab for dabigatran; andexanet alfa for apixaban/rivaroxaban) (21). Tranexamic acid is not recommended in LGIB; studies have shown it provides no benefit and may increase the risk of thromboembolic events (9).

Key Nursing & Monitoring Instructions

  • Strict hourly monitoring of vital signs (HR, BP, SpO2, RR) until the patient is hemodynamically stable for at least 4-6 hours.

  • Maintain a strict input/output chart to closely monitor fluid balance and ensure urine output remains >0.5mL/kg/hr as an indicator of adequate renal perfusion.

  • Monitor for any further episodes of hematochezia, melena, or new symptoms like dizziness, palpitations, or chest pain, and report immediately.

  • Inform the medical officer immediately if systolic BP drops below 100 mmHg, heart rate rises above 100 bpm, or there is any deterioration in the patient's mental status.

  • Ensure the patient is kept strictly nil by mouth (NBM) in preparation for a potential urgent endoscopic or radiological procedure.

Long-Term Plan & Patient Education

  • Secondary Prevention: Patient education is crucial. Patients should be counseled to permanently avoid NSAIDs after an episode of bleeding from diverticulosis or angiodysplasia, as these drugs directly cause mucosal injury and significantly increase the risk of a recurrent, often more severe, bleed (9).

  • Antithrombotic Resumption: This is a critical decision requiring a multidisciplinary discussion. For patients on aspirin for secondary cardiovascular prevention, guidelines strongly recommend that it be continued or resumed as soon as possible (ideally within 7 days) after bleeding ceases, as the risk of a major adverse cardiac event from stopping it outweighs the risk of re-bleeding (21, 25). The decision to resume other potent antiplatelets or anticoagulants requires careful weighing of the thrombotic vs. re-bleeding risk, typically resuming within 7-14 days for strong indications like atrial fibrillation or a mechanical heart valve (21).

  • Follow-up: All patients require follow-up in the gastroenterology clinic to discuss the results of investigations, ensure clinical resolution, and plan for future surveillance, especially if a neoplastic lesion was found or if the source of bleeding was not definitively identified.

When to Escalate

A house officer must recognize signs of deterioration and escalate care immediately.

Call Your Senior (Medical Officer/Specialist) if:

  • The patient remains hemodynamically unstable (tachycardic or hypotensive) despite an initial 1-2 liters of crystalloid resuscitation.

  • The patient has a significant drop in hemoglobin (>2 g/dL in a few hours) or requires ongoing blood transfusions (i.e., >2 units of packed cells transfused with continued instability).

  • The patient develops new signs of end-organ hypoperfusion, such as chest pain (potential MI), altered mental status, or oliguria/anuria.

  • You are considering the reversal of anticoagulation, as this is a major decision with significant risks.

  • The serum lactate is >4 mmol/L or fails to clear by at least 50% after 2 hours of resuscitation, indicating persistent tissue hypoperfusion.

Referral Criteria:

  • Refer to Gastroenterology: All patients admitted with acute LGIB require an urgent referral for consultation and consideration of endoscopy. Clearly communicate the patient's stability, suspected etiology, and transfusion requirements.

  • Refer to Interventional Radiology: Refer urgently if the patient is unstable with active bleeding confirmed on CTA, or if endoscopy has failed to control the hemorrhage. Provide the CTA report and images.

  • Refer to Surgery: An urgent surgical consultation is mandatory for patients with life-threatening hemorrhage who have failed or are not candidates for endoscopic and radiological interventions. This is a time-critical referral.

References

(1) Ministry of Health Malaysia. (2017). Management of Non-Variceal Upper Gastrointestinal Bleeding. Putrajaya: MOH. [Note: While this CPG is for UGIB, it contains relevant definitions and local context referenced in the text. A specific Malaysian LGIB CPG was not identified, hence reliance on international guidelines and the provided source document.]

(9) Strate, L. L., & Gralnek, I. M. (2020). Acute Lower Gastrointestinal Bleeding: Evaluation and Management. American Family Physician, 101(4), 206–216.

(10) Oakland, K. (2019). Assessment of lower gastrointestinal bleeding. BMJ Best Practice. Retrieved from https://bestpractice.bmj.com/topics/en-gb/457

(12) Lanas, A., & García-Rodríguez, L. A. (2019). Changing epidemiology and etiology of upper and lower gastrointestinal bleeding. Gastroenterology, 156(6), 1577-1579.

(13) Strate, L. L., & Naumann, C. R. (2010). Epidemiology of lower gastrointestinal bleeding. Gastrointestinal Endoscopy Clinics of North America, 20(4), 541-551.

(14) Upper Gastrointestinal Bleeding. In StatPearls. StatPearls Publishing.

(16) Lower GI bleed: Symptoms, causes, treatment, and recovery. (2023). Medical News Today.

(18) American College of Gastroenterology. (n.d.). Lower Gastrointestinal (GI) Bleeding. Retrieved from https://gi.org/topics/lower-gi-bleeding/

(20) Diagnosis and management of acute lower gastrointestinal bleeding. (2020). BINASSS.

(21) Sengupta, N., Feuerstein, J. D., Jairath, V., et al. (2023). Management of patients with acute lower gastrointestinal bleeding: An updated ACG guideline. The American Journal of Gastroenterology, 118(2), 208-231. https://doi.org/10.14309/ajg.0000000000002130

(22) Strate, L. L., Gralnek, I. M., et al. (2016). ACG Clinical Guideline: Management of Patients With Acute Lower Gastrointestinal Bleeding. The American Journal of Gastroenterology, 111(4), 459-474. https://doi.org/10.1038/ajg.2016.41

(25) emDocs. (2023). Guideline Update: Acute Lower GI Bleeding. Retrieved from http://www.emdocs.net/guideline-update-acute-lower-gi-bleeding/

(27) Winter, M., & Nural, M. S. (2017). Lower gastrointestinal bleeding-Computed Tomographic angiography. World journal of radiology, 9(1), 1–5. https://doi.org/10.4329/wjr.v9.i1.1

(28) Yu, H., et al. (2016). New advances in lower gastrointestinal bleeding management with embolotherapy. Gastroenterology Research and Practice, 2016, 8943138. https://doi.org/10.1155/2016/8943138

(31) Foley, T. R., & Waltman, A. C. (2015). Angiographic Evaluation and Management of Nonvariceal Gastrointestinal Hemorrhage. American Journal of Roentgenology, 205(4), 741-755. https://doi.org/10.2214/AJR.15.14803

(32) Jensen, D. M., & Machicado, G. A. (2012). Pros and cons of colonoscopy in management of acute lower gastrointestinal bleeding. Gastrointestinal Endoscopy Clinics of North America, 22(4), 599-614. https://doi.org/10.1016/j.giec.2012.07.003

(36) Embolization of lower GI bleed. (n.d.). UConn Health.

(37) Lee, Y. S. (2018). Role of surgery in gastrointestinal bleeding. Gastrointestinal Intervention, 7(2), 65-68. https://doi.org/10.18528/gii180029

Danial Mirza
Previous

Urolithiasis: A Comprehensive Clinical Review
Next

Upper Gastrointestinal Bleeding (UGIB)