1
2
3
4
5
18
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20
21
22
14
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17
9
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11
12
13
6
7
8
28
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31
23
24
25
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32
33
Surgical Technique
Surgical re-exploration after CABG due to postoperative bleeding is rare (<3%) but associated with a 4.5fold higher peri-operative mortality(1,2). Technical reasons are the primary cause for bleeding after surgery and therefore greater attention to surgical techniques is likely to lower morbidity and mortality (3).
Technical refinements in mammary artery harvesting, meticulous haemostasis and use of haemostatic sealants or topical antifibrinolytics are key players in patients on DAPT(4). Off-pump CABG surgery has been associated with significant reduction in blood loss and transfusion requirement when compared with conventional on-pump CABG(5). Despite some evidence of less bleeding events associated with OPCAB, the recent literature yields heterogeneous results regarding time delay from clopidogrel interruption to CABG surgery (Supplement Table 4S).
Blood Salvage Interventions
Haemoconcentration during on-pump CABG by continuous or modified ultrafiltration results in protein-rich haemoconcentrated blood that can be reinfused after cardiopulmonary bypass discontinuation. Available evidence suggests that the addition of modified ultrafiltration is associated with reduced haemodilution and diminishes blood transfusion(6). In addition, cell saver use has been shown to reduce allogeneic blood product exposure (OR 0.63, 95% CI:0.43-0.94; p<0.02) but also red blood cells and the mean volume of total allogeneic blood products transfused per patient (p<0.002)(7).
Pharmacological Strategies
Antifibrinolytic drugs are effective in reducing blood loss, the need for allogenic red cell transfusion, and the need for re-operation due to continued post-operative bleeding in cardiac surgery(8). Aprotinin was shown to decrease postoperative bleeding and the number of transfusions in patients undergoing CABG and treated with clopidogrel < 5 days before surgery and appears more effective than the lysine analogues in minimizing blood loss (9). However, aprotinin was withdrawn in 2008 based on trial findings in on-pump surgery showing a relative risk of death of 1.53 (95% CI 1.06-2.22) as compared with the combined rate for lysine analogues(10). An updated meta-analysis of the randomised trials comparing aprotinin with no treatment does not confirm the evidence from observational studies that aprotinin increases the risks of vascular occlusive events and mortality(11). Despite being potentially less effective than aprotinin, lysine analogues are effective in reducing blood loss during and after surgery and appear to be free of serious
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42
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38
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60
34
35
36
37
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67 adverse effects(11–13). The EMA has recommended lifting the suspension of the marketing authorization for aprotinin-containing medicines in the European Union (EU) after risk/benefit assessment and consideration of alternative treatments (www.ema.europa.eu).
Red blood cell transfusion
Blood transfusion is beneficial in the management of haemorrhagic shock but the number of transfused red blood cell units is an independent risk factor for worse outcomes(14,15). Transfusion trigger to a target haematocrit around 24% is as safe as a liberal strategy of 30% with respect to 30-day mortality and complications(16). In addition, multiple packed red blood cell transfusion is associated with coagulation factor deficit requiring fresh frozen plasma or preferably prothrombin complex concentrate administration and fibrinogen. Preventive fresh frozen plasma administration does not reduce bleeding and is not recommended.
Platelet transfusion
Platelet transfusion is indicated in case of excessive bleeding to maintain a platelet count above 75 x 10 9 /l.
There have been small inconclusive studies that have used platelet transfusion in patients undergoing CABG to reverse platelet inhibition secondary to extracorporeal cardiopulmonary bypass(17) and glycoprotein
IIb/IIIa inhibition from abciximab(18). There is no evidence to support systematic platelet transfusion for perioperative minor bleedings in patients on DAPT. Platelet transfusion (1U/7-10Kg) is indicated when persistent oozing occurs after a full surgical revision of the wound. Persistent chest tube drainage >100cc/h for 6 hours and normal routine coagulation tests in patients with recent P2Y
12
inhibitor exposure may benefit from platelet transfusion if there is a good probability that a surgical cause can be excluded. If not, early surgical revision avoids the higher rate of adverse events associated with delayed re-exploration associated with haemodynamic instability or the need for multiple transfusion (2,19).
Monitoring of Haemostasis
There is no reliable and easy strategy by which functional laboratory tests measuring anti- platelet agent effects could predict bleeding complications and guide the use of blood products or antifibrinolytic therapies during CABG(20). Modified thromboelastography(21) can provide information about whether insufficient blood clot formation is related to platelet dysfunction, fibrinogen deficit, lack of coagulation factors, or inadequate heparin reversal and help guide blood products administration leading to reduced chest tube output(22).
Severe intractable bleeding defined as diffuse bleeding from capillary beds at wound surfaces and/or intraoperative or postoperative blood loss exceeding 250 ml/h or 50 ml/10 min over 4 hours or a sudden increase bleeding after the first two hours(23) despite an adequate application of recommended
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74 preventive steps require a stepwise, algorithm-based approach(24). Basic measures and haemostatic management which should be guided by routine coagulation tests, supplemented, if available, by point-ofcare visco-elastic and platelet function tests are summarized in figure 1. In case of antiplatelet therapy and platelet dysfunction ideally confirmed with platelet function tests, platelet concentrates (1U/7-10Kg weight) represent the first therapeutic line. In case of severe bleeding, red blood cells transfusion in association to fresh frozen plasma (and/or prothrombin complex concentrate) and fibrinogen (25-50mg/kg) should be used. Timely reopening of the chest is recommended to exclude a surgical cause, if bleeding persists after correction of coagulation abnormalities and platelet transfusion(2). Recombinant factor VIIa may be considered for patients with intractable bleeding once conventional haemostatic options have been exhausted and a surgical cause has been excluded. Adherence to strict transfusion protocols by all involved stakeholders is associated with lower resource utilization and improved outcomes. This includes the use of decision tree algorithms, higher thresholds for transfusion, laboratory or point-of-care haemostasis tests and multidisciplinary decision making(25).
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1. Mehta RH, Sheng S, O’Brien SM, Grover FL, Gammie JS, Ferguson TB, Peterson ED, Society of Thoracic
Surgeons National Cardiac Surgery Database Investigators. Reoperation for bleeding in patients undergoing coronary artery bypass surgery: incidence, risk factors, time trends, and outcomes. Circ
Cardiovasc Qual Outcomes. 2009;2:583–590.
2. Ranucci M, Bozzetti G, Ditta A, Cotza M, Carboni G, Ballotta A. Surgical reexploration after cardiac operations: why a worse outcome? Ann Thorac Surg. 2008;86:1557–1562.
3. Vivacqua A, Koch CG, Yousuf AM, Nowicki ER, Houghtaling PL, Blackstone EH, Sabik JF 3rd. Morbidity of bleeding after cardiac surgery: is it blood transfusion, reoperation for bleeding, or both? Ann
Thorac Surg. 2011;91:1780–1790.
4. Abrishami A, Chung F, Wong J. Topical application of antifibrinolytic drugs for on-pump cardiac surgery: a systematic review and meta-analysis. Can J Anaesth J Can Anesth. 2009;56:202–212.
5. Lamy A, Devereaux PJ, Prabhakaran D, Taggart DP, Hu S, Paolasso E, Straka Z, Piegas LS, Akar AR, Jain
AR, Noiseux N, Padmanabhan C, Bahamondes J-C, Novick RJ, Vaijyanath P, Reddy S, Tao L,
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Med. 2012;366:1489–1497.
6. Boodhwani M, Williams K, Babaev A, Gill G, Saleem N, Rubens FD. Ultrafiltration reduces blood transfusions following cardiac surgery: A meta-analysis. Eur J Cardiothorac Surg. 2006;30:892–897.
7. Wang G, Bainbridge D, Martin J, Cheng D. The efficacy of an intraoperative cell saver during cardiac surgery: a meta-analysis of randomized trials. Anesth Analg. 2009;109:320–330.
8. McIlroy DR, Myles PS, Phillips LE, Smith JA. Antifibrinolytics in cardiac surgical patients receiving aspirin: a systematic review and meta-analysis. Br J Anaesth. 2009;102:168–178.
9. Linden J van der, Lindvall G, Sartipy U. Aprotinin decreases postoperative bleeding and number of transfusions in patients on clopidogrel undergoing coronary artery bypass graft surgery: a doubleblind, placebo-controlled, randomized clinical trial. Circulation. 2005;112:I276–280.
10. Fergusson DA, Hébert PC, Mazer CD, Fremes S, MacAdams C, Murkin JM, Teoh K, Duke PC, Arellano R,
Blajchman MA, Bussières JS, Côté D, Karski J, Martineau R, Robblee JA, Rodger M, Wells G, Clinch J,
Pretorius R, BART Investigators. A comparison of aprotinin and lysine analogues in high-risk cardiac surgery. N Engl J Med. 2008;358:2319–2331.
11. Henry DA, Carless PA, Moxey AJ, O’Connell D, Stokes BJ, Fergusson DA, Ker K. Anti-fibrinolytic use for minimising perioperative allogeneic blood transfusion. Cochrane Database Syst Rev. 2011;CD001886.
12. Karski J, Djaiani G, Carroll J, Iwanochko M, Seneviratne P, Liu P, Kucharczyk W, Fedorko L, David T,
Cheng D. Tranexamic acid and early saphenous vein graft patency in conventional coronary artery bypass graft surgery: a prospective randomized controlled clinical trial. J Thorac Cardiovasc Surg.
2005;130:309–314.
13. Murphy GJ, Mango E, Lucchetti V, Battaglia F, Catapano D, Rogers CA, Angelini GD. A randomized trial of tranexamic acid in combination with cell salvage plus a meta-analysis of randomized trials
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14. Kumbhani DJ, Bhatt DL. Platelet activation: yet another strike against routine TRANSFUSION. Eur
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15. Silvain J, Pena A, Cayla G, Brieger D, Bellemain-Appaix A, Chastre T, Vignalou JB, Beygui F, Barthelemy
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2821.
16. Hajjar LA, Vincent J-L, Galas FRBG, Nakamura RE, Silva CMP, Santos MH, Fukushima J, Kalil Filho R,
Sierra DB, Lopes NH, Mauad T, Roquim AC, Sundin MR, Leão WC, Almeida JP, Pomerantzeff PM,
Dallan LO, Jatene FB, Stolf NAG, Auler JOC Jr. Transfusion requirements after cardiac surgery: the
TRACS randomized controlled trial. JAMA J Am Med Assoc. 2010;304:1559–1567.
17. Simon TL, Akl BF, Murphy W. Controlled trial of routine administration of platelet concentrates in cardiopulmonary bypass surgery. Ann Thorac Surg. 1984;37:359–364.
18. Juergens CP, Yeung AC, Oesterle SN. Routine platelet transfusion in patients undergoing emergency coronary bypass surgery after receiving abciximab. Am J Cardiol. 1997;80:74–75.
19. Karthik S, Grayson AD, McCarron EE, Pullan DM, Desmond MJ. Reexploration for bleeding after coronary artery bypass surgery: risk factors, outcomes, and the effect of time delay. Ann Thorac Surg.
2004;78:527–534.
20. Gurbel PA, Mahla E, Tantry US. Peri-operative platelet function testing: the potential for reducing ischaemic and bleeding risks. Thromb Haemost. 2011;106:248–252.
21. Perry DJ, Fitzmaurice DA, Kitchen S, Mackie IJ, Mallett S. Point-of-care testing in haemostasis. Br J
Haematol. 2010;150:501–514.
22. Wasowicz M, McCluskey SA, Wijeysundera DN, Yau TM, Meinri M, Beattie WS, Karkouti K. The incremental value of thrombelastography for prediction of excessive blood loss after cardiac surgery: an observational study. Anesth Analg. 2010;111:331–338.
23. Hall TS, Brevetti GR, Skoultchi AJ, Sines JC, Gregory P, Spotnitz AJ. Re-exploration for hemorrhage following open heart surgery differentiation on the causes of bleeding and the impact on patient outcomes. Ann Thorac Cardiovasc Surg. 2001;7:352–357.
24. Kozek-Langenecker SA, Afshari A, Albaladejo P, Santullano CAA, Robertis E De, Filipescu DC, Fries D,
Görlinger K, Haas T, Imberger G, Jacob M, Lancé M, Llau J, Mallett S, Meier J, Rahe-Meyer N, Samama
CM, Smith A, Solomon C, Linden P Van der, Wikkelsø AJ, Wouters P, Wyffels P. Management of severe perioperative bleeding: guidelines from the European Society of Anaesthesiology. Eur J Anaesthesiol.
2013;30:270–382.
25. Despotis G, Eby C, Lublin DM. A review of transfusion risks and optimal management of perioperative bleeding with cardiac surgery. Transfusion (Paris). 2008;48:2S–30S.
26. Ferraris VA, Saha SP, Oestreich JH, Song HK, Rosengart T, Reece TB, Mazer CD, Bridges CR, Despotis
GJ, Jointer K, Clough ER, Society of Thoracic Surgeons. 2012 update to the Society of Thoracic
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28. Dunning J, Versteegh M, Fabbri A, Pavie A, Kolh P, Lockowandt U, Nashef SAM, EACTS Audit and
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29. Hillis LD, Smith PK, Anderson JL, Bittl JA, Bridges CR, Byrne JG, Cigarroa JE, Disesa VJ, Hiratzka LF,
Hutter AM Jr, Jessen ME, Keeley EC, Lahey SJ, Lange RA, London MJ, Mack MJ, Patel MR, Puskas JD,
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30. Hamm CW, Bassand J-P, Agewall S, Bax J, Boersma E, Bueno H, Caso P, Dudek D, Gielen S, Huber K,
Ohman M, Petrie MC, Sonntag F, Uva MS, Storey RF, Wijns W, Zahger D, Bax JJ, Auricchio A,
Baumgartner H, Ceconi C, Dean V, Deaton C, Fagard R, Funck-Brentano C, Hasdai D, Hoes A, Knuuti J,
Kolh P, McDonagh T, Moulin C, Poldermans D, Popescu BA, Reiner Z, Sechtem U, Sirnes PA, Torbicki A,
Vahanian A, Windecker S, Achenbach S, Badimon L, Bertrand M, Botker HE, Collet JP, Crea F, Danchin
N, Falk E, Goudevenos J, Gulba D, Hambrecht R, Herrmann J, Kastrati A, Kjeldsen K, Kristensen SD,
Lancellotti P, Mehilli J, Merkely B, Montalescot G, Neumann FJ, Neyses L, Perk J, Roffi M,Romeo F,
Ruda M, Swahn E, Valgimigli M, Vrints CJ, Widimsky P. ESC Guidelines for the management of acute coronary syndromes in patients presenting without persistent ST-segment elevation: The Task Force for the management of acute coronary syndromes (ACS) in patients presenting without persistent STsegment elevation of the European Society of Cardiology (ESC). Eur Heart J. 2011;32:2999–3054.
31. Purkayastha S, Athanasiou T, Malinovski V, Tekkis P, Foale R, Casula R, Glenville B, Darzi A. Does clopidogrel affect outcome after coronary artery bypass grafting? A meta-analysis. Heart Br Card Soc.
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32. Pickard AS, Becker RC, Schumock GT, Frye CB. Clopidogrel-associated bleeding and related complications in patients undergoing coronary artery bypass grafting. Pharmacotherapy.
2008;28:376–392.
33. Nijjer SS, Watson G, Athanasiou T, Malik IS. Safety of clopidogrel being continued until the time of coronary artery bypass grafting in patients with acute coronary syndrome: a meta-analysis of 34 studies. Eur Heart J. 2011;32:2970–2988.
34. Au AG, Majumdar SR, McAlister FA. Preoperative thienopyridine use and outcomes after surgery: a systematic review. Am J Med. 2012;125:87–99.e1.
35. Biancari F, Airaksinen KEJ, Lip GYH. Benefits and risks of using clopidogrel before coronary artery bypass surgery: systematic review and meta-analysis of randomized trials and observational studies. J
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36. Shim JK, Choi YS, Oh YJ, Bang SO, Yoo KJ, Kwak YL. Effects of preoperative aspirin and clopidogrel therapy on perioperative blood loss and blood transfusion requirements in patients undergoing offpump coronary artery bypass graft surgery. J Thorac Cardiovasc Surg. 2007;134(1):59–64.
37. Song SW, Youn YN, Lee S, Yoo KJ. ffects of continuous administration of clopidogrel before off-pump
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38. Kapetanakis EI, Medlam DA, Petro KR, Haile E, Hill PC, Dullum MK, Bafi AS, Boyce SW, Corso PJ. Effect of clopidogrel premedication in off-pump cardiac surgery: are we forfeiting the benefits of reduced hemorrhagic sequelae? Circulation. 2006;113(13):1667–1674.
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40. Maltais S, Perrault LP, Do QB. Effect of clopidogrel on bleeding and transfusions after off-pump coronary artery bypass graft surgery: impact of discontinuation prior to surgery. Eur J Cardiothorac
Surg. 2008;34(1):127–131.
7

Table 1S: Guidelines on antiplatelet therapy in patients undergoing CABG
12
Discontinuation in high-risk patients such as those who refuse blood transfusion for religious reasons (Jehovah’s Witness) is reasonable.
Discontinuation before purely elective operations in patients without ACS is reasonable to decrease the risk of bleeding.
Discontinuation of P2Y
12
inhibitors for a few days before cardiovascular operations is recommended to reduce bleeding and blood transfusion, especially in high-risk patients.
The interval between discontinuation of antiplatelet drugs and operation is uncertain and depends on multiple factors mostly related to patient drug responsiveness and thrombotic risk.
Continue up to and beyond time of CABG
Interrupt 5 days
DAPT in BMS<6 weeks
DAPT in DES<12 month
Elective: stop 2-10 days
Urgent for ACS: Continue till surgery
Urgent Surgery: stop 5-7 days if clinical condition allows
Administer preoperatively
Clopidogrel and ticagrelor stop at least
5 days before surgery. Prasugrel stop at least 7 days.
In patients pre-treated with P2Y
12 inhibitors who need to undergo nonemergent major surgery (including
CABG), postponing surgery at least for
5 days after cessation of ticagrelor or clopidogrel, and 7 days for prasugrel, if clinically feasible and unless the patient is at high risk of ischaemic events should be considered (IIaC)
8

Table 2S: P2Y
12
Inhibitors with mode of action
P2Y
12 inhibitor
Type Route Action
Clopidogrel
Prasugrel
Ticagrelor
Cangrelor
Thienopyridine
(Second generation)
Thienopyridine
(Third generation)
Cyclopentyltriazolopyrimidine
ATP analogue
Oral
Oral
Oral
IV
Hepatic transformation to active metabolite
Irreversible blockade
Hepatic transformation to active metabolite
Irreversible blockade
Direct and reversible inhibition
Non-competitive binding
Direct and reversible inhibition
Semi-competitive binding
ATP = adenosine triphosphate; IV = intravenous
Loading dose
300-600 mg
60 mg
180 mg
30µg/kg bolus
Maintenance dose
75 mg
5-10 mg
90 mg twice daily
0.75-4
µg/kg/min
9

Table 3S: Clopidogrel before CABG: Meta-Analyses and Systematic Reviews
Reference Period
Nº Pts/
Studies
Inclusion Criteria Main Results
Purkayastha S
(31)
Pickard AS (32)
Nijjer SS(33)
Au AG(34)
1999-2004
1990-2007
1980-2011
1980-2010
4002/11
3505/23
22584/34
19849/26
Biancari F(35)
Up to 7/2010
1234/3RCT
17 Observational
Clopidogrel vs control
Clopidogrel increases blood loss, transfusion, adverse outcomes, reoperation and length of stay.
Mortality not significantly different.
Clopidogrel exposure within 7 days of surgery
Clopidogrel exposure < 7 days increased risk of major bleeding, reoperation, transfusion.
Aprotinin mitigated haemorrhagic risk.
Clopidogrel use prior to
CABG vs Clopidogrel naive or drug free period before surgery
Clopidogrel increases mortality but not in ACS patients.
Reoperation rates and chest drain output are increased but have reduced over time. No difference in MACE rates.
Clopidogrel use within 5 days vs comparator not exposed
Clopidogrel increased risk of stroke, reoperation for bleeding and all-cause mortality and NOT associated with reduction in MI.
DAPT versus aspirin.
Exclusion if exposure in control group even if discontinuation 5-7 days and aprotinin use
RCT: non-significant reduced risk of composite end point (death, myocardial infarction, or stroke) in the clopidogrel group.
Observational: clopidogrel associated with increased risk of death, reoperation for bleeding, need of packed red blood cell transfusion and increased use of blood products but significantly reduced risk of postoperative myocardial infarction.
10

Table 4S: Effect of ASA + Clopidogrel in Off-Pump CABG
Shim JK(36)
Song SW(37)
Kapetanakis
EI(38)
Vaccarino
GN(39)
Maltais S(40)
Retrospective : 3 Groups according to exposure to
DAPT: >6d, 3-5d, <2d
Retrospective : DAPT untill surgery vs Surgery delayed>3d
Retrospective : Propensity score match pair analysis No
Clopidogrel/exposure<7d
/exposure<7d
106 non emergent
No difference between groups in blood loss, RBC transfusion and
Platelet transfusion, FFP amounts
172 ACS
1572
Similar blood loss, reexploration, blood transfusion, platelet transfusion
Clopidogrel<7d: higher likelihood of reoperation for bleeding
(p<0.01), pRBC (p<0.01), multiple unit (p=0.02) platelet transfusions
(p<0.01)
Retrospective of prospectively collected data. Propensity score matching
1104 (88 vs 166 propensity matched)
Clopidogrel<7d: FFP (18.1% vs
8.5%;p=0.02), reoperation for bleeding (5.6% vs 0.5%; p=0.009), trend toward more major adverse events
Retrospective of prospectively collected data

Clopidogrel use is associated with more blood loss, pRBC and platelet transfusion
101 on-clopidogrel
(</=72h vs >72h)
No Clopidogrel: 352

Blood loss higher in
Clopidogrel<72h vs >72h

Blood loss similar in off
Clopidogrel>72h vs control
11

Table 5S: Strategies to reduce bleeding during CABG-surgery
Use of cell savage, off pump CABG or, alternatively, mini CPB circuits is recommended
Platelet transfusions should be considered in patients receiving dual antiplatelet drugs who require urgent operation and have excessive perioperative bleeding.
Antifibrinolytics with lysine analogs (tranexamic acid) to reduce perioperative bleeding are recommended
The use of decision tree algorithms, higher thresholds for red blood cell transfusion, and multidisciplinary decision making for blood product administration is recommended
Point of care haemostasis tests may be used to to guide haemostatic interventions in patients on P2Y
12
inhibitors
I
IIa
I
I
IIb
C
C
A
C
B
(5)
(16,17)
(8)
(22,24,26)
(19) , (22)
12

Figure 1: Algorith-based approach for the management of peri-operative severe bleeding
13