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Endoscopic hemostatic devices

      Abbreviations:

      APC (argon plasma coagulator), ASGE (American Society for Gastrointestinal Endoscopy), GAVE (gastric antral vascular ecstasia), HP (heater probe), MPEC (multipolar electrocautery)
      The American Society for Gastrointestinal Endoscopy (ASGE) Technology Committee provides reviews of existing, new, or emerging endoscopic technologies that have an impact on the practice of GI endoscopy. Evidence-based methodology is used, with a MEDLINE literature search to identify pertinent clinical studies on the topic and a MAUDE (US Food and Drug Administration Center for Devices and Radiological Health) database search to identify the reported complications of a given technology. Both are supplemented by accessing the “related articles” feature of PubMed and by scrutinizing pertinent references cited by the identified studies. Controlled clinical trials are emphasized, but, in many cases, data from randomized, controlled trials are lacking. In such cases, large case series, preliminary clinical studies, and expert opinions are used. Technical data are gathered from traditional and Web-based publications, proprietary publications, and informal communications with pertinent vendors.
      Technology Status Evaluation Reports are drafted by 1 or 2 members of the ASGE Technology Committee, reviewed and edited by the committee as a whole, and approved by the Governing Board of the ASGE. When financial guidance is indicated, the most recent coding data and list prices at the time of publication are provided. For this review, the MEDLINE database was searched through September 2008 for articles related to endoscopic hemostatic devices by using the keywords “multipolar electrocautery,” “bipolar electrocautery,” “heater probe,” “hemostatic grasper,” “argon plasma coagulator,” “injection needle,” “endoloop,” “clip,” paired with “complication,” “perforation,” “peptic ulcer disease,” “gastric antral vascular ectasia,” “Dieulafoy lesion,” “Mallory-Weiss tear,” “radiation induced angioectasias,” “diverticular bleeding,” “angiodysplasia,” and “postpolypectomy bleeding.”
      Technology Status Evaluation Reports are scientific reviews provided solely for educational and informational purposes. Technology Status Evaluation Reports are not rules and should not be construed as establishing a legal standard of care or as encouraging, advocating, requiring, or discouraging any particular treatment or payment for such treatment.

      Background

      Endoscopic hemostatic therapy has been shown to improve outcomes in upper GI bleeding.
      • Cook D.J.
      • Guyatt G.H.
      • Salena B.J.
      • et al.
      Endoscopic therapy for acute nonvariceal upper gastrointestinal hemorrhage: a meta-analysis.
      • Sacks H.S.
      • Chalmers T.C.
      • Blum A.L.
      • et al.
      Endoscopic hemostasis. An effective therapy for bleeding peptic ulcers.
      • Sung J.J.
      • Tsoi K.K.
      • Lai L.H.
      • et al.
      Endoscopic clipping versus injection and thermo-coagulation in the treatment of non-variceal upper gastrointestinal bleeding: a meta-analysis.
      Hemostatic devices used for upper GI bleeding have also been applied to the colon.
      • Bloomfeld R.S.
      • Rockey D.C.
      • Shetzline M.A.
      Endoscopic therapy of acute diverticular hemorrhage.
      • Jensen D.M.
      • Machicado G.A.
      • Jutabha R.
      • et al.
      Urgent colonoscopy for the diagnosis and treatment of severe diverticular hemorrhage.
      Therapeutic modalities include contact thermal devices (eg, heater probe [HP], multipolar electrocautery [MPEC] probes, and hemostatic graspers), noncontact thermal devices (eg, argon plasma coagulator [APC]), injection needles, and mechanical devices (eg, band ligators, clips, and loops). Band ligators are the subject of a separate recent Status Evaluation Report.
      • Liu J.
      • Petersen B.T.
      • Tierney W.M.
      • et al.
      Endoscopic banding devices.
      This report describes all other commonly used hemostatic devices currently available in the United States.

      Technology under review

      Thermal hemostatic devices

      Thermal devices generate heat either directly (eg, HP) or indirectly by passage of electrical current through tissue (eg, MPEC probe, APC, hemostatic grasper). Heating leads to edema, coagulation of tissue protein, and contraction of vessels and indirect activation of the coagulation cascade, resulting in a hemostatic bond.
      • Wara P.
      • Berg V.
      • Jacobsen N.O.
      • et al.
      Possible mechanism of hemostasis effected by electrocoagulation.
      Tissue coagulation requires a temperature of approximately 70°C. Contact thermal devices also allow coaptation of vessels, which may contribute to hemostasis.
      • Harrison J.D.
      • Morris D.L.
      Does bipolar electrocoagulation time affect vessel weld strength?.

      Multipolar/bipolar electrocautery

      MPEC probes deliver thermal energy by completion of an electrical circuit between 2 electrodes on the tip of a probe as current flows through nondesiccated tissue. In contrast to monopolar electrocautery, the circuit is completed locally; therefore, no grounding pad is required. As the targeted tissue desiccates, there is a decrease in electrical conductivity, limiting the maximum temperature (100°C) and depth and breadth of tissue injury.
      • Laine L.
      Therapeutic endoscopy and bleeding ulcers. Bipolar/multipolar electrocoagulation.
      A port at the tip delivers water for irrigation, which can help to improve visualization of the target tissue. A foot pedal controls delivery of energy. Power output is in watts (W). Maximum power settings are dependent on the generator used, but usually do not exceed 50 W. A standard setting is 20 W. Irrigation can be controlled by a foot pedal connected to a pump or by simply flushing the irrigation port with a syringe. Pressure is often applied to the target tissue during coagulation to ensure coaptation. Catheters come in several lengths and diameters that must be coordinated with the length and size of the working channel of the endoscope (Table 1).
      Table 1Contact thermal devices
      ManufacturerDevice nameSheath diameter (French)Sheath length (cm)List priceSpecial features
      Multipolar electrocautery probes
       Boston Scientific (Natick, Mass)Gold Probe7, 10300, 350$285 each
      Injector Gold Probe7, 10210$335 eachIntegrated 25-gauge injection needle
       ConMed Endoscopic Technologies (Chelmsford, Mass)Bicap Superconductor, multielectrode bipolar probe5, 7, 10200, 300, 350$310 each
      Palladium tip bipolar hemostasis probe7, 10300$240 each
       Cook Medical (Winston-Salem, NC)Quicksilver bipolar probe7, 10350$271 each
       Olympus America (Center Valley, Pa)SolarProbe7, 10350$235 each
       US Endoscopy (Mentor, Ohio)Bipolar hemostasis probe7, 10350$230 each
      Heater probes
       Olympus AmericaHeatProbe7, 10230, 300$530 eachReusable
      Hemostatic grasper
       Olympus AmericaCoagrasper7165$200 eachRotatable

      HP

      The HP consists of a Teflon-coated hollow aluminum cylinder with an inner heating coil. A thermocoupling device at the tip of the probe maintains a constant temperature. In contrast to MPEC, the mechanism of tissue coagulation is direct heat transfer. Pressure is usually applied with HP therapy, and there is an irrigation port. A foot pedal controls heat activation and irrigation. HP activation delivers energy to the diode in the probe tip. Once the pulse has been initiated, the duration of activation is predetermined and cannot be stopped until the entire amount of preselected joules is delivered.
      • Fullarton G.M.
      • Birnie G.G.
      • Macdonald A.
      • et al.
      Controlled trial of heater probe treatment in bleeding peptic ulcers.

      Hemostatic grasper

      The hemostatic grasper is a recently developed device similar to monopolar hot biopsy forceps currently used for polypectomy.
      • Barkun A.
      • Liu J.
      • Carpenter S.
      • et al.
      Update on endoscopic tissue sampling devices.
      The grasper operates much like a biopsy forceps, although, unlike biopsy forceps, the jaws are flat instead of cupped and the device is rotatable. The jaws are closed around the target tissue, and then monopolar electrocautery is used to desiccate the tissue. Clinical experience with this device is limited, with one study reporting the use of the hemostatic grasper during a natural orifice transluminal endoscopic surgery cholecystectomy.
      • Meining A.
      • Wilhelm D.
      • Burian M.
      • et al.
      Development, standardization, and evaluation of NOTES cholecystectomy using a transsigmoid approach in the porcine model: an acute feasibility study.

      APC

      An APC is a noncontact electrocoagulation device that uses high-frequency monopolar alternating current conducted to target tissues through ionized argon gas (argon plasma). Electrons flow through a stream of electrically activated ionized argon gas from the probe electrode to the targeted tissue, causing tissue desiccation at the interface. As the tissue surface loses its electrical conductivity as a result of desiccation, the plasma stream shifts to adjacent nondesiccated (conductive) tissue, which limits the depth of injury. If the catheter is not near target tissue (ie, the resistance to electrical current flow is too great), there is no ignition of the gas, and depression of the foot pedal results only in flow of inert argon gas. Coagulation depth is dependent on the generator power setting, duration of application, and distance from the probe tip to the target tissue.
      • Watson J.P.
      • Bennett M.K.
      • Griffin S.M.
      • et al.
      The tissue effect of argon plasma coagulation on esophageal and gastric mucosa.
      The optimal distance between the probe and tissue ranges from 2 to 8 mm.
      • Cipolletta L.
      • Bianco M.A.
      • Rotondano G.
      • et al.
      Prospective comparison of argon plasma coagulator and heater probe in the endoscopic treatment of major peptic ulcer bleeding.
      The available APC systems (ERBE USA, Marietta, Ga; ConMed Electrosurgery, Centennial, Colo; Canady Technology, Pittsburgh, Pa) include a specialized electrosurgical generator capable of high-frequency monopolar current, an activation foot pedal, an argon gas cylinder, disposable grounding pads, and flexible, single-use delivery probes. A gas flow meter adjusts to allow argon flow rates of 0.5 to 7 L/min. These generators can also serve as multipurpose electrosurgical units capable of varying levels of power output with any monopolar or bipolar endoscopic accessory. Probes are composed of Teflon (DuPont, Wilmington, Del) with a ceramic tip encasing the tungsten electrode. They are available in a variety of lengths and widths (Table 2). Probes are available with forward, side, or circumferential ports allowing forward, tangential, or circumferential applications, respectively.
      Table 2Noncontact thermal devices
      ManufacturerDevice nameSheath diameter (French)Sheath length (cm)Fire directionList priceSpecial features
      Canady (Hampton, Va)Canady plasma GI probe5, 7230, 340Straight, side$1550/box of 10
      ConMed Endoscopic Technologies (Chelmsford, Mass)Beamer argon probe5, 7, 10160, 230, 320Straight fire$2550/box of 10
      Beamer argon snare probe7160, 230Straight fire$1750/box of 5Combination APC probe and snare
      ERBE (Marietta, Ga)APC probe5, 7, 10150, 220, 300Straight, side, circumferential$1995-2305/box of 10
      All probes $1995/box of 10 except the side-fire probes ($2050/box of 10) and the 300-cm probes ($2305/box of 10).
      FiAPC probe5, 7, 10150, 220, 300Straight, side, circumferential$2077-2387/box of 10
      All probes $2077/box of 10 except circumferential and side-fire probes ($2132/box of 10) and 300-cm probes ($2387/box of 10).
      Integrated filter
      APC, Argon plasma coagulation.
      All probes $1995/box of 10 except the side-fire probes ($2050/box of 10) and the 300-cm probes ($2305/box of 10).
      All probes $2077/box of 10 except circumferential and side-fire probes ($2132/box of 10) and 300-cm probes ($2387/box of 10).

      Injection needles

      Injection needles consist of an outer sheath (plastic, Teflon, or stainless steel) and an inner hollow-core needle (19-25 gauge) (Table 3). Using a handle on the end of the needle sheath, the operator can retract the needle into the sheath for safe passage through the working channel of the endoscope. When the catheter is placed near the target tissue, the needle can be extended out of the end of the sheath to a preset distance, and a syringe attached to the handle is used to inject liquid agents into the target tissue. Injection of various solutions achieves hemostasis by both mechanical tamponade and cytochemical mechanisms.
      • Nelson D.B.
      • Bosco J.J.
      • Curtis W.D.
      • et al.
      ASGE technology status evaluation report. Injection needles. February 1999.
      Table 3Injection needles
      ManufacturerDevice nameSheath diameter (French)Sheath length (cm)Needle gaugeNeedle length (mm)List priceSpecial features
      Boston Scientific (Natick, Mass))Interject sclerotherapy needle7200, 24023, 254, 6$37 each
      ConMed Endoscopic Technologies (Chelmsford, Mass)Click-Tip injection needle7180, 23019, 22, 254, 6$580/box of 10
      FlexiTip disposable sclerotherapy needle7160, 230254, 5, 6$255/box of 5
      Sure Shot injection needle7230255$315/box of 5
      Cook Medical (Winston-Salem, NC)AcuJet variable injection needle722023, 25Variable$42 each
      Disposable varices injector7200-32023, 25Variable$48 each
      Injectaflow variable injection needle722023, 25Variable$61 eachFlush port
      Kimberly-Clark (Roswell, Ga)Injection needle catheter7160, 200, 24023, 254, 6$260/box of 10
      Olympus America (Center Valley, Pa)Injector Force injection needle7165-23021, 23, 254, 5, 6, 8$276/box of 6
      TeleMed Systems (Hudson, Mass)Sure-Stop sclerotherapy needle5, 7160-24021, 23, 254, 5$130/box of 5
      US Endoscopy (Mentor, Ohio)Articulator injection needle7160, 230, 350254, 5$250/box of 5
      Carr-Locke injection needle7230255$275/box of 5
      iSnare1023023, 255$625/box of 52.5 × 4-cm integrated snare
      Vari-Safe injection needle7230234, 5, 7$50 each

      Mechanical hemostatic devices

      Endoscopic clipping devices

      All endoscopic clipping devices have 3 main components: a metal double- or triple-pronged preloaded clip, a delivery catheter, and a handle used to operate and deploy the clip. Clips are available in a variety of jaw lengths (Table 4). The delivery catheter consists of a metal cable within a metal coil sheath enclosed within a Teflon catheter. The tip of the metal cable has a hook onto which the clip is attached. The handle consists of 2 sliding components. The first allows advancement of the metal cable holding the clip out of the protective sheath. The second is the plunger that controls opening, closing, and deployment of the clip. After insertion of the catheter through the working channel of the endoscope, the clip is extended out of the sheath. The clip is then positioned over the target and opened with the plunger handle. A rotation mechanism on the handle of some clips allows a change in orientation of the clip jaws. The jaws of the clip are applied with pressure and closed onto the target tissue by using the device handle.
      • Chuttani R.
      • Barkun A.
      • Carpenter S.
      • et al.
      Endoscopic clip application devices.
      Some clips may be reopened and repositioned, whereas others are permanently deployed and released on closure. Similarly, some clips are automatically released on deployment, and others require repositioning of the plunger handle to release the deployed clip from the catheter. Hemostasis is achieved by mechanical compression.
      Table 4Mechanical hemostatic devices
      ManufacturerDevice nameSheath diameter (French)Sheath length (cm)Jaw opening width (mm)List priceSpecial features
      Endoscopic clipping devices
       Boston Scientific (Natick, Mass)Resolution clip7155, 23511$145 each2-prong clip
       Cook Medical (Bloomington, Ind)Triclip7, 820712$316 (box of 3)3-prong clip, 8-French model has flush port
       Olympus America (Center Valley, Pa)QuickClip27165, 2309$95 each (box of 5 or 20)2-prong clip, rotatable
      QuickClip2 long7165, 23011$95 each (box of 5 or 20)2-prong clip, rotatable
      Detachable loop-ligating devices
       Olympus AmericaEndo-Loop7195, 23030
      Loop diameter.
      $330/box of 10 loops, $570 each for catheterNonsterile, reusable catheter
      Poly-Loop723030
      Loop diameter.
      $525/box of 5Sterile, single-use loop and catheter
      Loop diameter.

      Detachable loop ligating devices

      Detachable loop ligating devices consist of a circular- or elliptical-shaped nylon loop preloaded onto a delivery system that includes a hook wire (to which the loop is attached) within a Teflon sheath and an operating handle. Some older devices required preloading of the loop onto the hook wire. The loop is advanced out of the sheath and placed around the target tissue, usually the stalk of a large pedunculated polyp. The loop is tightened with advancement of a silicon rubber stopper by using the handle. When the loop is closed to the desired extent, as evidenced by tissue cyanosis or hemostasis, it is then released from the hook wire. There is a separate loop-cutting device that can be used to cut and release the nylon loop if it is malpositioned or fails to release from the catheter.

      Ease of use

      Thermal hemostatic devices are relatively easy to use because they require only direct or indirect (eg, APC) contact with the target tissue. Use of argon plasma coagulation requires an endoscopist to have fine control of the endoscope because the optimal distance of 2 to 8 mm from the device to the tissue target must be maintained during energy delivery. Power generators for contact thermal probes and APCs are portable and use a standard 110-V outlet. Ten-French probes require an endoscope with a working channel larger than 3.4 mm. Repeated application of thermal energy can result in the buildup of coagulum at the catheter tip, which can impede conductivity, necessitating removal of the probe and cleaning of the tip.
      For mechanical methods of hemostasis, injection needles require only an understanding of how the handle works to extend the needle from the sheath. Both clips and detachable loops have more complex delivery mechanisms and handles that require a high degree of coordination between the endoscopist and endoscopy assistant. Use of an angulated endoscope or a side-viewing endoscope may make deployment of clips and advancement of injection needles difficult. If the position of some targeted lesions limits visualization or results in tangential orientation, clips may be difficult to place. Additionally, if there is a vessel within an ulcer with a large fibrotic base, there may not be adequate tissue to anchor a clip device. Optimal positioning of a clip and loop device before deployment generally requires more experience relative to standard diagnostic endoscopic methods.

      Efficacy and comparative analysis

      Peptic ulcer disease

      Several meta-analyses including more than 1000 patients have shown that thermal hemostatic devices, injection therapy, and clips either in combination or alone are all highly successful in achieving initial hemostasis in bleeding peptic ulcer disease. Clips and thermal therapy, either alone or paired with injection therapy, are superior to injection therapy alone in preventing rebleeding and the need for surgery. There is no significant difference between clips and thermal therapy in rebleeding rates, the need for surgery, and mortality.
      • Cook D.J.
      • Guyatt G.H.
      • Salena B.J.
      • et al.
      Endoscopic therapy for acute nonvariceal upper gastrointestinal hemorrhage: a meta-analysis.
      • Sacks H.S.
      • Chalmers T.C.
      • Blum A.L.
      • et al.
      Endoscopic hemostasis. An effective therapy for bleeding peptic ulcers.
      • Sung J.J.
      • Tsoi K.K.
      • Lai L.H.
      • et al.
      Endoscopic clipping versus injection and thermo-coagulation in the treatment of non-variceal upper gastrointestinal bleeding: a meta-analysis.
      • Laine L.
      • McQuaid K.R.
      Endoscopic therapy for bleeding ulcers: an evidence-based approach based on meta-analyses of randomized controlled trials.
      Numerous prospective, randomized studies have compared thermal therapies with no treatment, thermal therapies with injection, thermal therapies with each other, and thermal therapies combined with injection. In several studies, the use of an MPEC probe and an HP have been compared with no treatment or sham procedures and show immediate hemostasis rates of 78% to 100%, significantly lower rebleeding rates (0%-18% vs 20%-41%), and a decreased need for surgery, shorter length of hospitalization, and less need for transfusion.
      • Fullarton G.M.
      • Birnie G.G.
      • Macdonald A.
      • et al.
      Controlled trial of heater probe treatment in bleeding peptic ulcers.
      • Jaramillo J.L.
      • Carmona C.
      • Galvez C.
      • et al.
      Efficacy of the heater probe in peptic ulcer with a non-bleeding visible vessel. A controlled, randomised study.
      • Laine L.
      Multipolar electrocoagulation in the treatment of active upper gastrointestinal tract hemorrhage. A prospective controlled trial.
      • Laine L.
      Multipolar electrocoagulation in the treatment of peptic ulcers with nonbleeding visible vessels. A prospective, controlled trial.
      • Tekant Y.
      • Goh P.
      • Alexander D.J.
      • et al.
      Combination therapy using adrenaline and heater probe to reduce rebleeding in patients with peptic ulcer haemorrhage: a prospective randomized trial.
      Comparisons among different thermal modalities show that they are all similar in rebleeding rates, need for surgery, and transfusion requirements.
      • Cipolletta L.
      • Bianco M.A.
      • Rotondano G.
      • et al.
      Prospective comparison of argon plasma coagulator and heater probe in the endoscopic treatment of major peptic ulcer bleeding.
      • Hui W.M.
      • Ng M.M.
      • Lok A.S.
      • et al.
      A randomized comparative study of laser photocoagulation, heater probe, and bipolar electrocoagulation in the treatment of actively bleeding ulcers.
      • Lin H.J.
      • Wang K.
      • Perng C.L.
      • et al.
      Heater probe thermocoagulation and multipolar electrocoagulation for arrest of peptic ulcer bleeding. A prospective, randomized comparative trial.
      Early studies demonstrated that the use of an APC, MPEC probe, and HP have similar efficacy in initial hemostasis and decreasing rebleeding rates compared with injection therapy of epinephrine alone, sclerosant alone, or combined sclerosant and epinephrine.
      • Choudari C.P.
      • Rajgopal C.
      • Palmer K.R.
      Comparison of endoscopic injection therapy versus the heater probe in major peptic ulcer haemorrhage.
      • Laine L.
      Multipolar electrocoagulation versus injection therapy in the treatment of bleeding peptic ulcers. A prospective, randomized trial.
      • Llach J.
      • Bordas J.M.
      • Salmeron J.M.
      • et al.
      A prospective randomized trial of heater probe thermocoagulation versus injection therapy in peptic ulcer hemorrhage.
      • Skok P.
      • Krizman I.
      • Skok M.
      Argon plasma coagulation versus injection sclerotherapy in peptic ulcer hemorrhage—a prospective, controlled study.
      • Waring J.P.
      • Sanowski R.A.
      • Sawyer R.L.
      • et al.
      A randomized comparison of multipolar electrocoagulation and injection sclerosis for the treatment of bleeding peptic ulcer.
      Injection therapy with saline solution alone is significantly less effective than MPEC in treating bleeding ulcers, with rebleeding rates of 29% versus 12% with MPEC.
      • Laine L.
      • Estrada R.
      Randomized trial of normal saline solution injection versus bipolar electrocoagulation for treatment of patients with high-risk bleeding ulcers: is local tamponade enough?.
      MPEC paired with epinephrine injection prevents rebleeding and decreases transfusion requirements compared with epinephrine injection alone, with rebleeding rates of 6.7% versus 30%, respectively.
      • Lin H.J.
      • Tseng G.Y.
      • Perng C.L.
      • et al.
      Comparison of adrenaline injection and bipolar electrocoagulation for the arrest of peptic ulcer bleeding.
      The use of an HP or APC paired with epinephrine injection is equally efficacious in treating high-risk peptic ulcers.
      • Chua T.S.
      • Fock K.M.
      • Ng T.M.
      • et al.
      Epinephrine injection therapy versus a combination of epinephrine injection and endoscopic hemoclip in the treatment of bleeding ulcers.
      Epinephrine injection followed by MPEC also has a higher rate of initial hemostasis than epinephrine injection alone.
      • Bianco M.A.
      • Rotondano G.
      • Marmo R.
      • et al.
      Combined epinephrine and bipolar probe coagulation vs. bipolar probe coagulation alone for bleeding peptic ulcer: a randomized, controlled trial.
      Clips have been compared with thermal therapy, injection therapy alone, and thermal therapy combined with injection in many randomized trials. Clips and APCs have similar efficacy in initial hemostasis, recurrent bleeding, 30-day mortality, and the need for emergency surgery.
      • Cipolletta L.
      • Bianco M.A.
      • Rotondano G.
      • et al.
      Prospective comparison of argon plasma coagulator and heater probe in the endoscopic treatment of major peptic ulcer bleeding.
      One study showed that the rate of recurrent bleeding is higher with an HP than clips (21% vs 1.8%, P < .05).
      • Cipolletta L.
      • Bianco M.A.
      • Marmo R.
      • et al.
      Endoclips versus heater probe in preventing early recurrent bleeding from peptic ulcer: a prospective and randomized trial.
      Another study demonstrated that initial hemostasis was higher with an HP compared with clips (100% vs 85%, P = .01), although no significant difference was seen in rebleeding, transfusion requirements, or 30-day mortality.
      • Lin H.J.
      • Hsieh Y.H.
      • Tseng G.Y.
      • et al.
      A prospective, randomized trial of endoscopic hemoclip versus heater probe thermocoagulation for peptic ulcer bleeding.
      Clips have been compared with an HP paired with epinephrine injection with similar clinical outcomes.
      • Lin H.J.
      • Perng C.L.
      • Sun I.C.
      • et al.
      Endoscopic haemoclip versus heater probe thermocoagulation plus hypertonic saline-epinephrine injection for peptic ulcer bleeding.
      One study showed a higher rebleeding rate in a group with epinephrine injection followed by the use of an HP (33%) relative to clips alone (5%).
      • Lee Y.C.
      • Wang H.P.
      • Yang C.S.
      • et al.
      Endoscopic hemostasis of a bleeding marginal ulcer: hemoclipping or dual therapy with epinephrine injection and heater probe thermocoagulation.
      Clips have also been compared with injection therapy as well as the combination therapy of clips and injection therapy. Clinical outcomes were similar between the groups.
      • Chua T.S.
      • Fock K.M.
      • Ng T.M.
      • et al.
      Epinephrine injection therapy versus a combination of epinephrine injection and endoscopic hemoclip in the treatment of bleeding ulcers.
      • Chung I.K.
      • Ham J.S.
      • Kim H.S.
      • et al.
      Comparison of the hemostatic efficacy of the endoscopic hemoclip method with hypertonic saline-epinephrine injection and a combination of the two for the management of bleeding peptic ulcers.
      • Nishiaki M.
      • Tada M.
      • Yanai H.
      • et al.
      Endoscopic hemostasis for bleeding peptic ulcer using a hemostatic clip or pure ethanol injection.
      • Shimoda R.
      • Iwakiri R.
      • Sakata H.
      • et al.
      Evaluation of endoscopic hemostasis with metallic hemoclips for bleeding gastric ulcer: comparison with endoscopic injection of absolute ethanol in a prospective, randomized study.
      One study found that the rebleeding rate was higher in the epinephrine injection alone group than in the combination therapy group with clips paired with epinephrine injection (21% vs 3.8%, P = .008).
      • Lo C.C.
      • Hsu P.I.
      • Lo G.H.
      • et al.
      Comparison of hemostatic efficacy for epinephrine injection alone and injection combined with hemoclip therapy in treating high-risk bleeding ulcers.

      Gastric antral vascular ectasia

      APC is the most commonly reported modality for the ablation of gastric antral vascular ectasia (GAVE). Multiple sessions are usually required, but transfusion requirements can be eliminated in more than 70% of patients.
      • Herrera S.
      • Bordas J.M.
      • Llach J.
      • et al.
      The beneficial effects of argon plasma coagulation in the management of different types of gastric vascular ectasia lesions in patients admitted for GI hemorrhage.
      • Kwan V.
      • Bourke M.J.
      • Williams S.J.
      • et al.
      Argon plasma coagulation in the management of symptomatic gastrointestinal vascular lesions: experience in 100 consecutive patients with long-term follow-up.
      • Pavey D.A.
      • Craig P.I.
      Endoscopic therapy for upper-GI vascular ectasias.
      MPEC and HP have also been described for the ablation of GAVE.
      • Binmoeller K.F.
      • Katon R.M.
      Bipolar electrocoagulation for watermelon stomach.
      • Petrini Jr., J.L.
      • Johnston J.H.
      Heat probe treatment for antral vascular ectasia.
      Long-term sequelae of ablation include antral scarring and hyperplastic polyps.
      • Dulai G.S.
      • Jensen D.M.
      Treatment of watermelon stomach.
      A recent retrospective study of thermal therapy (APC or MPEC probe) compared with band ligation found that band ligation required fewer sessions for cessation of bleeding.
      • Wells C.D.
      • Harrison M.E.
      • Gurudu S.R.
      • et al.
      Treatment of gastric antral vascular ectasia (watermelon stomach) with endoscopic band ligation.
      Newer mucosal ablation techniques
      • Rodriguez S.A.
      • Adler D.G.
      • Chand B.
      • et al.
      Mucosal ablation devices: Status Evaluation Report.
      such as radiofrequency ablation and cryotherapy have also been used to ablate GAVE in small pilot studies. A study of 26 patients with a variety of bleeding lesions (eg, GAVE, arteriovenous malformations, radiation proctitis, radiation gastritis) were treated with cryotherapy with a mean of 3.6 sessions.
      • Kantsevoy S.V.
      • Cruz-Correa M.R.
      • Vaughn C.A.
      • et al.
      Endoscopic cryotherapy for the treatment of bleeding mucosal vascular lesions of the GI tract: a pilot study.
      These patients had previously undergone treatment with MPEC and HP but continued to have bleeding. Cryotherapy with nitrous oxide was efficacious in causing hemostasis in 77% overall, with follow-up of 6 months. In another recent report of 12 patients, including 8 patients in whom the use of an APC failed, cryotherapy resulted in a decrease in transfusion requirement and an increase in hemoglobin.
      • Cho S.
      • Zanati S.
      • Yong E.
      • et al.
      Endoscopic cryotherapy for the management of gastric antral vascular ectasia.
      A pilot study of 6 patients with GAVE treated with the HALO90 device (Barrx Medical, Sunnyvale, Calif) showed improved hemoglobin concentrations in all patients after 1 to 3 treatments. Five of 6 patients were no longer transfusion dependent.
      • Gross S.A.
      • Al-Haddad M.
      • Gill K.R.
      • et al.
      Endoscopic mucosal ablation for the treatment of gastric antral vascular ectasia with the HALO90 system: a pilot study.

      Angiodysplasia

      MPEC probes, HPs, and APCs have all been described in treating angiodysplasia encountered in the GI tract during upper endoscopy, enteroscopy, and colonoscopy.
      • Hayat M.
      • Axon A.T.
      • O'Mahony S.
      Diagnostic yield and effect on clinical outcomes of push enteroscopy in suspected small-bowel bleeding.
      • Hsu C.M.
      • Chiu C.T.
      • Su M.Y.
      • et al.
      The outcome assessment of double-balloon enteroscopy for diagnosing and managing patients with obscure gastrointestinal bleeding.
      • Vargo J.J.
      Clinical applications of the argon plasma coagulator.
      One series of 16 patients showed that thermal ablation of angiodysplasia decreased transfusion requirements in 76% of patients and that only 1 to 2 sessions were needed for ablation compared with a mean of 6 sessions needed to ablate GAVE.
      • Pavey D.A.
      • Craig P.I.
      Endoscopic therapy for upper-GI vascular ectasias.
      In contrast to treating bleeding peptic ulcers, lower power settings and lower appositional forces are used with MPEC and HP treatment of angiodysplasia.

      Dieulafoy lesions

      Injections of epinephrine, ethanol, or histoacryl have been described as successful in stopping bleeding from Dieulafoy lesions. Epinephrine injection followed by thermal therapy (eg, MPEC, HP) or clip placement has also been effective in small case series.
      • Casella G.
      • Bonforte G.
      • Corso R.
      • et al.
      Rectal bleeding by Dieulafoy-like lesion: successful endoscopic treatment.
      • Cheng C.L.
      • Liu N.J.
      • Lee C.S.
      • et al.
      Endoscopic management of Dieulafoy lesions in acute nonvariceal upper gastrointestinal bleeding.
      • Norton I.D.
      • Petersen B.T.
      • Sorbi D.
      • et al.
      Management and long-term prognosis of Dieulafoy lesion.
      • Parra-Blanco A.
      • Takahashi H.
      • Mendez Jerez P.V.
      • et al.
      Endoscopic management of Dieulafoy lesions of the stomach: a case study of 26 patients.
      A prospective, randomized trial of 24 patients compared mechanical devices (clips or band ligation) and injection of hypertonic saline solution for Dieulafoy lesions.
      • Chung I.K.
      • Kim E.J.
      • Lee M.S.
      • et al.
      Bleeding Dieulafoy's lesions and the choice of endoscopic method: comparing the hemostatic efficacy of mechanical and injection methods.
      The rate of rebleeding was significantly lower in the mechanical group (8%) than in the injection group (33%).

      Mallory-Weiss tears

      Studies of endoscopic therapy for Mallory-Weiss tears have focused on actively bleeding lesions. A randomized, controlled trial of 44 patients undergoing MPEC versus sham MPEC in active upper GI bleeding revealed that in a subgroup of 17 patients with Mallory-Weiss tears, there was a significant improvement in the MPEC group with regard to initial hemostasis (100% vs 13%) and emergency surgery or other intervention and a trend toward less need for transfusions.
      • Laine L.
      Multipolar electrocoagulation in the treatment of active upper gastrointestinal tract hemorrhage. A prospective controlled trial.
      A prospective, randomized study of 41 patients with actively bleeding Mallory-Weiss tears randomized to clips or band ligation showed that all patients had immediate hemostasis, and only 1 patient rebled in the clip group and 2 in the banding group.
      • Cho Y.S.
      • Chae H.S.
      • Kim H.K.
      • et al.
      Endoscopic band ligation and endoscopic hemoclip placement for patients with Mallory-Weiss syndrome and active bleeding.
      A study of 35 patients with actively bleeding or oozing Mallory-Weiss tears were prospectively randomized to either clip application or epinephrine injection.
      • Huang S.P.
      • Wang H.P.
      • Lee Y.C.
      • et al.
      Endoscopic hemoclip placement and epinephrine injection for Mallory-Weiss syndrome with active bleeding.
      There was no difference in immediate hemostasis or rebleeding.

      Radiation-induced angioectasias

      The use of MPEC, HP, and APC has been described in small case series as successful treatments for bleeding from radiation-induced angioectasias, usually in the rectum. Multiple sessions were typically required for complete ablation.
      • Jensen D.M.
      • Machicado G.A.
      • Cheng S.
      • et al.
      A randomized prospective study of endoscopic bipolar electrocoagulation and heater probe treatment of chronic rectal bleeding from radiation telangiectasia.
      • Maunoury V.
      • Brunetaud J.M.
      • Cortot A.
      Bipolar electrocoagulation treatment for hemorrhagic radiation injury of the lower digestive tract.
      • Postgate A.
      • Saunders B.
      • Tjandra J.
      • et al.
      Argon plasma coagulation in chronic radiation proctitis.
      • Tjandra J.J.
      • Sengupta S.
      Argon plasma coagulation is an effective treatment for refractory hemorrhagic radiation proctitis.
      Other mucosal ablation therapies such as cryotherapy and radiofrequency ablation have also been used for radiation-induced angioectasias.
      • Kantsevoy S.V.
      • Cruz-Correa M.R.
      • Vaughn C.A.
      • et al.
      Endoscopic cryotherapy for the treatment of bleeding mucosal vascular lesions of the GI tract: a pilot study.
      • Gross S.A.
      • Al-Haddad M.
      • Gill K.R.
      • et al.
      Endoscopic mucosal ablation for the treatment of gastric antral vascular ectasia with the HALO90 system: a pilot study.

      Diverticular bleeding

      Epinephrine injection with or without MPEC has been described in observational studies as an effective measure to obtain initial hemostasis in diverticular bleeding.
      • Bloomfeld R.S.
      • Rockey D.C.
      • Shetzline M.A.
      Endoscopic therapy of acute diverticular hemorrhage.
      • Jensen D.M.
      • Machicado G.A.
      • Jutabha R.
      • et al.
      Urgent colonoscopy for the diagnosis and treatment of severe diverticular hemorrhage.
      Case reports also describe the use of clips in diverticular bleeding.
      • Binmoeller K.F.
      • Thonke F.
      • Soehendra N.
      Endoscopic hemoclip treatment for gastrointestinal bleeding.
      • Hokama A.
      • Kinjo F.
      • Fujita J.
      Hemoclip application for colonic diverticular hemorrhage.
      • Rino Y.
      • Imada T.
      • Iwasaki H.
      • et al.
      Hemostasis of colonic diverticular bleeding with hemoclips under endoscopic control: report of a case.

      Postpolypectomy bleeding

      Various combinations of epinephrine injection, MPEC, and HP application to postpolypectomy bleeding sites have been described.
      • Rex D.K.
      • Lewis B.S.
      • Waye J.D.
      Colonoscopy and endoscopic therapy for delayed post-polypectomy hemorrhage.
      Clips have also been used to stop postpolypectomy bleeding.
      • Binmoeller K.F.
      • Thonke F.
      • Soehendra N.
      Endoscopic hemoclip treatment for gastrointestinal bleeding.
      • Parra-Blanco A.
      • Kaminaga N.
      • et al.
      Hemoclipping for postpolypectomy and postbiopsy colonic bleeding.
      Detachable loops were developed for the prevention of postpolypectomy bleeding. Small case series have described the feasibility of placing loops before polypectomy.
      • Matsushita M.
      • Hajiro K.
      • Takakuwa H.
      • et al.
      Ineffective use of a detachable snare for colonoscopic polypectomy of large polyps.
      • Rey J.F.
      • Marek T.A.
      Endo-loop in the prevention of the post-polypectomy bleeding: preliminary results.
      Several prospective, randomized studies evaluated the role of detachable loops, clips, and injection therapy in the prevention of postpolypectomy bleeding after removal of large polyps. A study of 159 patients showed that the application of a detachable loop with epinephrine injection resulted in a significant decrease in immediate bleeding compared with epinephrine injection alone (1% vs 9%), although there was no difference in delayed bleeding.
      • Paspatis G.A.
      • Paraskeva K.
      • Theodoropoulou A.
      • et al.
      A prospective, randomized comparison of adrenaline injection in combination with detachable snare versus adrenaline injection alone in the prevention of postpolypectomy bleeding in large colonic polyps.
      A study comparing loop placement, epinephrine injection, and no therapy showed that there is a significant increase in postpolypectomy bleeding with the removal of large polyps (>2 cm) when no therapy is used (2.7% vs 2.9% vs 15.1%, respectively).
      • Di Giorgio P.
      • De Luca L.
      • Calcagno G.
      • et al.
      Detachable snare versus epinephrine injection in the prevention of postpolypectomy bleeding: a randomized and controlled study.
      One study in patients undergoing saline solution lift polypectomy showed that the addition of epinephrine had no effect on the rate of postpolypectomy bleeding.
      • Lee S.H.
      • Chung I.K.
      • Kim S.J.
      • et al.
      Comparison of postpolypectomy bleeding between epinephrine and saline submucosal injection for large colon polyps by conventional polypectomy: a prospective randomized, multicenter study.
      Another study demonstrated no decrease in postpolypectomy bleeding with prophylactic clip placement.
      • Shioji K.
      • Suzuki Y.
      • Kobayashi M.
      • et al.
      Prophylactic clip application does not decrease delayed bleeding after colonoscopic polypectomy.
      The data to date, therefore, reveal no clear benefit of routine prophylactic therapy with the possible exception of the use of detachable loops and epinephrine injection in large pedunculated polyps.

      Safety

      Thermal hemostatic devices

      Rare perforations of peptic ulcers treated with MPEC and precipitation of bleeding (the majority stopped with further application of MPEC) in as many as 18% of patients have been reported.
      • Laine L.
      Multipolar electrocoagulation in the treatment of peptic ulcers with nonbleeding visible vessels. A prospective, controlled trial.
      Colonic perforation after treatment of angiodysplasia, particularly in the right colon, has been reported in as many as 2.5% of cases.
      • Foutch P.G.
      Angiodysplasia of the gastrointestinal tract.
      The rate of perforation after treatment of GI bleeding with HP has been reported to be as high as 1.8% to 3%, and precipitation of bleeding has been reported in as many as 5% of patients.
      • Cook D.J.
      • Guyatt G.H.
      • Salena B.J.
      • et al.
      Endoscopic therapy for acute nonvariceal upper gastrointestinal hemorrhage: a meta-analysis.
      • Chung S.C.
      • Leung J.W.
      • Sung J.Y.
      • et al.
      Injection or heat probe for bleeding ulcer.
      • Matthewson K.
      • Swain C.P.
      • Bland M.
      • et al.
      Randomized comparison of Nd YAG laser, heater probe, and no endoscopic therapy for bleeding peptic ulcers.
      Colonic perforation with application of an HP to angiodysplasia in the cecum has also been reported.

      U.S. Food and Drug Administration. Available at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfMAUDE/search.CFM. Accessed September 1, 2008.

      Complications from an APC are rare and include distention of the GI tract with argon gas, submucosal emphysema, pneumomediastinum, and pneumoperitoneum.
      • Cipolletta L.
      • Bianco M.A.
      • Rotondano G.
      • et al.
      Prospective comparison of argon plasma coagulator and heater probe in the endoscopic treatment of major peptic ulcer bleeding.
      • Johanns W.
      • Luis W.
      • Janssen J.
      • et al.
      Argon plasma coagulation (APC) in gastroenterology: experimental and clinical experiences.
      • Wahab P.J.
      • Mulder C.J.
      • den Hartog G.
      • et al.
      Argon plasma coagulation in flexible gastrointestinal endoscopy: pilot experiences.
      Perforation has been described after the use of an APC in the duodenum and colon.

      U.S. Food and Drug Administration. Available at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfMAUDE/search.CFM. Accessed September 1, 2008.

      These complications may be related to the power setting, duration of application, and distance of the probe tip to the target tissue.
      • Watson J.P.
      • Bennett M.K.
      • Griffin S.M.
      • et al.
      The tissue effect of argon plasma coagulation on esophageal and gastric mucosa.
      Cases of intracolonic gas explosion caused by ignition of accumulated oxygen, hydrogen, and methane have also been described. These explosions occurred in patients with incomplete or inadequate colonic cleansing or when malabsorbed carbohydrates were used as a bowel preparation.
      • Ladas S.D.
      • Karamanolis G.
      • Ben-Soussan E.
      Colonic gas explosion during therapeutic colonoscopy with electrocautery.
      • Manner H.
      • Plum N.
      • Pech O.
      • et al.
      Colon explosion during argon plasma coagulation.
      Therefore, complete colonic cleansing with a polyethylene glycol- or saline solution-based laxative should be used before using APC in the colon.

      Injection needles

      Complications of injection therapy are usually related to the substance injected rather than the needle itself. However, there are reports of needles failing to extend from their sheaths and of needles separating from the catheter in the patient and requiring retrieval. No direct patient harm has been reported from either of these device failures.

      U.S. Food and Drug Administration. Available at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfMAUDE/search.CFM. Accessed September 1, 2008.

      Cardiac arrhythmias and hypertension have been reported after epinephrine injection.
      • Stevens P.D.
      • Lebwohl O.
      Hypertensive emergency and ventricular tachycardia after endoscopic epinephrine injection of a Mallory-Weiss tear.
      Most complications occurring from injection therapy are complications related to esophageal variceal sclerotherapy.
      • Croffie J.
      • Somogyi L.
      • Chuttani R.
      • et al.
      Sclerosing agents for use in GI endoscopy.
      Sclerotherapy complications may occur in as many as 50% of patients and can be separated into local complications including retrosternal pain, dysphagia, odynophagia, ulcerations, strictures, bleeding, perforation, and systemic complications including fever, bacteremia, sepsis, pleural effusions, pneumonia, and adult respiratory distress syndrome.
      • D'Amico G.
      • Pagliaro L.
      • Bosch J.
      The treatment of portal hypertension: a meta-analytic review.
      • Elsayed S.S.
      • Shiha G.
      • Hamid M.
      • et al.
      Sclerotherapy versus sclerotherapy and propranolol in the prevention of rebleeding from oesophageal varices: a randomised study.
      • Sung J.J.
      • Chung S.C.
      • Lai C.W.
      • et al.
      Octreotide infusion or emergency sclerotherapy for variceal haemorrhage.

      Mechanical hemostatic devices

      There are numerous reports of handle malfunction, the inability to separate the clip from the catheter after deployment, and premature deployment of the clip. There is one report of inadvertent colon perforation while attempting to deploy a clip for a postpolypectomy bleed. Interestingly, this small perforation was closed with another clip. One reported incident of a clip failing to detach from the catheter led to additional bleeding that was successfully treated with another clip.

      U.S. Food and Drug Administration. Available at: http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfMAUDE/search.CFM. Accessed September 1, 2008.

      Clips are complex mechanical devices, and whether these reports represent device failure or operator inexperience with the device is not discernible. Although most clips detach and pass without incident within days, there have been reports of clips retained at the site of deployment for prolonged periods.
      • Chuttani R.
      • Barkun A.
      • Carpenter S.
      • et al.
      Endoscopic clip application devices.
      • Shin E.J.
      • Ko C.W.
      • Magno P.
      • et al.
      Comparative study of endoscopic clips: duration of attachment at the site of clip application.
      The clinical significance of clip retention is unknown, but there have been no adverse consequences reported. None of the clips described in this review are magnetic resonance imaging safe.
      Detachable loop ligating devices have been associated with loop entanglement with snare complicating polypectomy, slippage of the loop resulting in delayed bleeding, and inadvertent transection of the polyp stalk leading to immediate bleeding.
      • Katsinelos P.
      • Kountouras J.
      • Paroutoglou G.
      • et al.
      Endoloop-assisted polypectomy for large pedunculated colorectal polyps.

      Financial considerations

      Commonly used CPT
      CPT (Current Procedural Terminology) is a registered trademark of the American Medical Association. CPT codes © 2008 American Medical Association. All rights reserved.
      (Current Procedural Terminology) codes for endoscopic hemostasis are shown in the Table 5, and the detailed instructions for use of these numerous individual codes are provided elsewhere.
      • American Medical Association
      CPT® Guide 2009, Professional Edition.
      Table 1, Table 2, Table 3, Table 4 contain the list price of frequently used hemostatic devices available in the United States. The costs vary greatly among the different devices. Thermal probes are the most expensive devices, costing typically several hundred dollars each. The HP is more expensive but is reusable, whereas MPEC probes and APC catheters are single use. Clips and loops are approximately $100 each, although a mean use of 3 clips per patient for peptic ulcer bleeding has been reported.
      • Binmoeller K.F.
      • Thonke F.
      • Soehendra N.
      Endoscopic hemoclip treatment for gastrointestinal bleeding.
      Injection needles are the least expensive devices, costing approximately $50 each, although they are commonly used in conjunction with thermal probes or clips. All prices were obtained from the vendors as of September 1, 2008. Two cost identification studies have shown that in patients with bleeding peptic ulcers, the mean cost of hospitalization in patients treated with endoscopic therapy is less than half of the cost for patients treated with medical-surgical therapy.
      • Laine L.
      Multipolar electrocoagulation in the treatment of active upper gastrointestinal tract hemorrhage. A prospective controlled trial.
      • Gralnek I.M.
      • Jensen D.M.
      • Kovacs T.O.
      • et al.
      An economic analysis of patients with active arterial peptic ulcer hemorrhage treated with endoscopic heater probe, injection sclerosis, or surgery in a prospective, randomized trial.
      Table 5CPT codes for endoscopic hemostasis
      CPT code descriptionEsophagoscopyEGDEnteroscopyStomaFlex sigColonoscopy
      Control of bleeding, any method
      Any method may include, but is not limited to, the following hemostasis techniques: injection, bipolar cautery, unipolar cautery, laser, heater probe, clip, or argon plasma coagulator.
      432274325544366443914533445382
      Injection sclerosis4320443243
      Removal by ablation technique432284325844369443934533945383
      CPT (Current Procedural Terminology) is a registered trademark of the American Medical Association. CPT codes © 2008 American Medical Association. All rights reserved.
      Flex sig, Flexible sigmoidoscopy.
      Any method may include, but is not limited to, the following hemostasis techniques: injection, bipolar cautery, unipolar cautery, laser, heater probe, clip, or argon plasma coagulator.

      Areas for future research

      The optimal device for ablation of GAVE and angiodysplasia remains unclear. New technologies using radiofrequency ablation and cryotherapy may also hold promise in ablating GAVE,
      • Kantsevoy S.V.
      • Cruz-Correa M.R.
      • Vaughn C.A.
      • et al.
      Endoscopic cryotherapy for the treatment of bleeding mucosal vascular lesions of the GI tract: a pilot study.
      • Cho S.
      • Zanati S.
      • Yong E.
      • et al.
      Endoscopic cryotherapy for the management of gastric antral vascular ectasia.
      • Gross S.A.
      • Al-Haddad M.
      • Gill K.R.
      • et al.
      Endoscopic mucosal ablation for the treatment of gastric antral vascular ectasia with the HALO90 system: a pilot study.
      but require further study. The role of endoscopic therapy in diverticular bleeding remains unclear, as does the optimal modality for hemostasis. The patient group most likely to benefit from the use of mechanical hemostatic devices such as clips and loops in the prevention of immediate or delayed postpolypectomy bleeding requires further study.

      Summary

      Endoscopic therapy improves clinical outcomes for many causes of GI bleeding. There are many safe and effective devices available for endoscopic hemostatic therapy. Although there are few compelling data favoring a particular device for treatment of various etiologies of GI bleeding, patients with peptic ulcer disease requiring intervention will benefit from the combination of thermal therapy or clips and injection therapy compared with injection therapy alone. Selection of the optimal hemostatic device depends on characteristics of the lesion, local expertise, equipment availability, and cost.

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