ATS
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Eric Lim
Ayyaz A. Ali
Steven Tsui
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ali, Z. A.
Right arrow Articles by Tsui, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ali, Z. A.
Right arrow Articles by Tsui, S.
Related Collections
Right arrow Cardiac - pharmacology

Ann Thorac Surg 2004;78:1542-1546
© 2004 The Society of Thoracic Surgeons

Original article: cardiovascular

Allogenic Blood Transfusion Does Not Predispose to Infection After Cardiac Surgery

Ziad A. Ali, MRCSa, Eric Lim, MRCSa,*, Reza Motalleb-Zadeh, MRCSa, Ayyaz A. Ali, MRCSa, Chris J. Callaghan, MRCSa, Caroline Gerrard, MSb, Alain Vuylsteke, MD, FRCAb, Juliet Foweraker, PhD, FRCPc, Steven Tsui, MD, FRCSa

a Department of Cardiothoracic Surgery, Papworth Hospital, Papworth Everard, Cambridge, United Kingdom
b Department of Cardiothoracic Anaesthesia, Papworth Hospital, Papworth Everard, Cambridge, United Kingdom
c Department of Microbiology, Papworth Hospital, Papworth Everard, Cambridge, United Kingdom

Accepted for publication May 7, 2004.

* Address reprint requests to Dr Lim, Department of Cardiothoracic Surgery, Papworth Hospital, Papworth Everard, Cambridge CB3 8RE, UK
eric.lim{at}cvsnet.org


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Many retrospective studies report increased postoperative infection after allogenic blood transfusion. To investigate this phenomenon, we prospectively studied 232 patients undergoing cardiac surgery.

METHODS: Patients were screened daily for evidence of culture positive infections. Wounds were examined daily and defined on the ASEPSIS score. Chest radiographs and white cell counts and differentials were recorded on days 1, 2, and 4. The use of blood products was monitored blindly and independently. Patients were grouped according to transfusion status and compared using {chi}2 or Fisher's test. Logistic regression analyses were performed to identify predictors of transfusion and infection.

RESULTS: Of 232 patients, 116 (50%) received blood product transfusion. Patients receiving blood had lower preoperative hemoglobin, were older, with a greater proportion of urgent/emergency or revision surgery, and were higher risk. Despite this, there were no differences in the frequency of chest infection (20% versus 15%, p = 0.38), urinary infection (3.5% versus 5.3%, p = 0 0.75), wound infection (3.5% versus 8.0%, p = 0.16), or overall infection (28% versus 30%, p = 0.89) comparing the transfused versus untransfused groups. There was no evidence to suggest that administration of blood products was associated with infection (odds ratio 0.92, p = 0.77).

CONCLUSIONS: The administration of blood per se did not lead to increased postoperative infection. Clinicians should reconsider withholding blood transfusion in patients solely owing to concerns of predisposition to infection.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The administration of blood products is common in cardiac surgery. Recent estimates suggest that nearly 20% of packed cell transfusions occur in this context [1]. Along with the proposed benefits, evidence exists that transfusion also acts to suppress immunity contributing to morbidity and delaying postoperative recovery [2].

Since the early 1980s, more than 100 clinical studies have been performed examining the association of blood administration and postoperative infection. The results of these studies are difficult to interpret, as many were weakened by retrospective study design, absence of risk stratification for disease severity, and lack of uniform, rigid criteria to diagnose postoperative infection. While it is known that the risk of infection is higher in patients with increasing severity of illness [3], blood transfusion requirements are also higher in this subgroup [4]. Independent to the risks of transfusion, the inability to dissociate a predisposition to infection from underlying disease severity acts as a strong confounding factor.

All patients having cardiac surgery undergo careful risk stratification. Accurate assessment of physiologic variables to identify risk factors for postoperative morbidity and mortality prevents bias [5]. Cardiac surgical patients are a homogenous group who commonly receive blood postoperatively and often develop postoperative infection [6]. The frequent use of blood products and well-defined risk stratification make this population a suitable cohort to examine the association of blood transfusion and postoperative infection.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
We performed a prospective observational study consisting of 232 consecutive patients who underwent cardiac surgery at Papworth Hospital over a 3-month period. All patients were preoperatively risk stratified according to the Euroscore, a prospectively validated risk stratification model used specifically for patients undergoing cardiac surgery [7]. The study was performed within the context of a hospital-wide audit on postoperative infection. All nonpenicillin-allergic patients were prescribed intravenous flucloxacillin (1 g at induction and 6 hourly for 24 hours) and gentamicin (2 mg/kg as single dose at induction) as prophylaxis. Penicillin-allergic patients were to receive vancomycin (1 g at induction and a further 1 g after cardiopulmonary bypass) as a substitute for flucloxacillin. Patients with preexisting infection or proceeding to an operation for a complication of infection were excluded to prevent any potential bias of preexisting infection. Patients with hemoglobin of 8.5 g/dL or less, or symptomatic anemia in the range of 8.5 to 10 g/dL, received allogenic leukodeplete red cell transfusion. Fresh-frozen plasma (FFP) was prescribed if the activated partial thromboplastin time (APTT) was more than 48 or the prothrombin time (PT) greater than 21 and if the platelets count dropped below 100 x 109/L.

Primary outcome measures were the development of culture positive chest, sternal wound, leg wound, and urinary tract infections. All other infections identified during the course of the hospital stay were also recorded. Both sternal and leg wound infection were defined according to the ASEPSIS score (Additional treatment, the presence of Serous discharge, Erythema, Purulent exudate, and Separation of deep tissues, the Isolation of bacteria, and the duration of inpatient Stay) detailed in Table 1 [8]. The saphenous vein was harvested using an open approach in all cases.


View this table:
[in this window]
[in a new window]
  		Table 1. Modified ASEPSIS Score

 
All nurses were trained on wound scoring for 1 month and evaluated during a 2-week trial period before the commencement of our study. We assessed agreement by masked and independent validation of wound ASEPSIS scores between the researchers and each scoring nurse. In the case of discrepancy further assessments were performed using photographs of the wound.

A member of the research team collected data prospectively from daily review. Patients were screened for any symptoms or signs suggestive of chest infection (cough and sputum production) or urinary tract infection (frequency or dysuria or hematuria). Sputum, urine samples, or wound swabs were sent on patients with any symptoms, signs or ASEPSIS criteria suggestive of infection and culture results obtained. Further investigations included routine white cell counts (on days 1, 2, and 4) and plain chest radiographs (on days 1, 3, and 5). All chest films were reviewed to document the presence of atelectasis, effusion, and consolidation. At discharge all prescriptions were screened to identify patients who had been started on antibiotics.

Statistical Methods
Descriptive variables are presented as means with standard deviations or medians with interquartile ranges (IQR), and compared with the t test or Mann-Whitney test, respectively. Estimations of precision are presented with 95% confidence intervals (CI). Categorical data and frequencies are expressed as percentage and compared with {chi}2 or Fisher's exact test where appropriate. Conventional levels of significance (0.05) were applied throughout. Logistic regression was performed to identify risk factors for infection and transfusion. Statistical analysis was undertaken using SPSS for windows version 11.0 (Chicago, IL) and S Plus version 6 (Seattle, WA).

Sample Size Calculation
The sample size was powered toward the primary outcome measure. This study required 235 patients to detect a 10% difference in infection rates between the two arms. This was based on the assumption that 15% will develop postoperative infection, a significance level of 0.05, and power of 80%.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Of the 232 patients, 161 (69%) underwent coronary artery bypass surgery, 39 (17%) had heart valve surgery, and 32 (14%) patients underwent a combined procedure. The mean age ± SD of our study participants was 64 ± 10 years old, consisting of 181 males (78%) and 51 females (22%). Baseline characteristics are summarized in Table 2.


View this table:
[in this window]
[in a new window]
  		Table 2. Baseline Characteristics and Risk Factors for Infection

 
A total of 116 patients (50%) received allogenic leukodeplete red cell transfusion. Of these, 32 (13.8%) also received at least 1 unit of FFP and 33 (14.2%) at least 1 unit of platelets. All patients who received FFP or platelets also had red cell transfusion. The median blood usage was 3.0 units (IQR 2.0 to 6.0 units) per patient. Patients who received transfusion were older, were more likely to undergo revision surgery, had a greater portion of urgent or emergency surgery, and were higher risk according to the Euroscore. In the transfused group, hemoglobin levels were significantly lower before surgery, perioperatively, and before discharge (Table 3).


View this table:
[in this window]
[in a new window]
  		Table 3. Hemoglobin During Hospital Stay

 
The results of postoperative outcome are summarized in Table 4. In total, 29.3% of patients (68 of 232) had a postoperative infection. Respiratory tract pathogens were the most frequent, being cultured in 17.4% (40 of 232) of cases. Culture positive wound infections were present in 5.6% (13 of 232), 11 were leg wound infections (7 of 116 transfused versus 4 of 116 nontransfused, p = 0.35), and 2 sternal wound infections (1 of 116 versus 1 of 116, p = 1.0). Urinary tract infections were diagnosed in 4.3% (10 of 232). Six patients had two concomitant infections. Three had received blood and 3 had not. There was no difference in the frequency of infection or white cell counts between the transfused and nontransfused groups, nor did the effect of receiving blood transfusion influence length of hospital stay.


View this table:
[in this window]
[in a new window]
  		Table 4. Transfusion and Postoperative Outcome

 
There was no evidence to suggest that blood transfusion was associated with infection: the odds ratio was 0.92 per unit received (95% CI: 0.52 to 1.61, p = 0.77; Table 5). Neither red cell (OR 1.03, 95% CI: 0.94 to 1.12, p = 0.54), FFP (OR 0.51, 95% CI: 0.20 to 1.31, p = 0.16), nor platelet administration (OR 0.49, 95% CI: 0.19 to 1.24, p = 0.14) were associated with infection.


View this table:
[in this window]
[in a new window]
  		Table 5. Univariate Logistic Regression Analysis Factors Associated With Infection

 
Risk Factors for Transfusion
The independent risk factors that led to transfusion were lower hemoglobin levels (OR per unit of hemoglobin was 0.28, 95% CI: 0.19 to 0.47, p < 0.001) and increasing Euroscore (OR per additional unit increase was 1.38, 95% CI: 1.12 to 1.50, p < 0.001).


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Blood is always lost after surgery. While there is no argument that transfusion is lifesaving in situations of torrential blood loss, less is known of when and how much to replace for patients with mild to moderate postoperative anemia. When correctly used, blood saves lives and reverses the adverse effects of anemia [1, 9–10]. Survival benefit is increased in critical illness when the effects of anemia are compounded by increased metabolic demand [11]. These effects are particularly important in patients with ischemic heart disease. Observational analyses in more than 75,000 such patients revealed anemia to be associated with significantly higher mortality. In patients with a hematocrit of 27% or less, mortality was near 50% and three times that of controls. Transfusion in patients with significant anemia significantly improved survival [12]. Despite these findings, in the face of recognized and potentially serious complications of blood product administration, a conservative transfusion policy has taken hold in many centers across the world [13].

Aside of the known hazards of transfusion and scarcity of the resource, one theme often arises among opponents of transfusion: concerns of postoperative infection due to the immunomodulatory effects of blood transfusion [14]. Reports have suggested that blood transfusion is the single most important predictor of postoperative infection [15], acting in a dose-dependent manner [4, 15, 16], and increasing the risk of mediastinitis, bacteraemia, mortality, and length of hospital stay [16–19]. In a recent multicenter randomized, controlled trial of transfusion in unselected critically ill patients, a restrictive strategy of red cell transfusion was at least as effective or possibly superior to liberal transfusion in terms of survival [20]. Such findings would suggest that holding off transfusion in critically ill patients may provide benefit. However, the same study failed to show any difference in length of intensive therapy unit stay or mortality among patients with cardiovascular disease. Two large observational cohort studies showed a disproportionate increase in mortality with increasing anemia in patients with ischemic heart disease [21, 22].

It is conceivable that patients who are sicker and therefore more at risk of infection are the group that receives more blood transfusion. While numerous studies have confirmed the associations of disease severity and transfusion [19, 23], few have incorporated it into their analyses [3]. Moreover, the immunomodulatory effects of transfusion might not have been related to the blood itself, but rather to other unmeasured clinical variables [24]. In this prospective study, multivariate analysis accounting for baseline characteristics and operative risk, neither transfusion alone nor the volume of transfusion was associated with increased infection, an argument most compelling by the odds ratio of 0.92 for the effect of blood product transfusion on postoperative infection.

There are a number of factors that influence the decision to administer blood to patients postoperatively. Many surgeons would transfuse for symptomatic postoperative anemia, others would also require the support of a numerical hemoglobin cutoff to support this decision. Physiologic tolerance to anemia is largely dependent on the ability to increase cardiac output [25]. Some patients tolerate hemodilution during surgery without morbidity. Evidence exists that in healthy adults, cardiac output is not affected until the hemoglobin drops well below 7 g/dL [26]. Conversely, in elderly, more fragile patients with cardiovascular disease, recruitment of physiologic reserve my be limited and anemia less well tolerated [27–29].

At our institution, transfusion triggers are hemoglobin level of 8.5 g/dL or less, or symptomatic anemia in the range of 8.5 to 10 g/dL. Although there is no clinical evidence to support these values, they were chosen based on consensus opinion and to facilitate comparison with other clinical trials [16, 30, 31]. Low hemoglobin level was a strong independent risk factor for transfusion. Interestingly, increasing operative risk also had a positive effect on infection with an odds ratio of 1.1 (0.96 to 1.25, p = 0.20).

Potential Limitations
Despite studies suggesting an increased risk of infection from allogenic red cell transfusion [16, 19, 32–36], cardiac surgery is considered to be relatively "clean" operation. Therefore, extrapolation of the results to the general surgical population requires confirmation. The risk of developing infection after cardiac surgery is high [6]. This may be at least partly attributed to confounding variables such as frequency of diabetes mellitus, frequency of reoperation, history of smoking, volume of blood loss, age, and the use of cardiopulmonary bypass. However, in our study the findings persisted after statistical adjustment for such factors. Lastly, since November 1999 all allogenic blood products in the United Kingdom have been subjected to a leukocyte depletion process. Thus, the findings of our study may not be applicable in countries where blood is not leukocyte depleted.

Conclusions
In this prospective study, using a validated wound score, clear endpoints, and stratification for severity of disease, we did not find an association between blood transfusion and postoperative infection. Blood is a precious resource, with known risks of death from incompatibility, defined risk of transmission of infection, and other adverse events. While many good reasons exist to limit the use of blood products, we challenge the opinion of withholding blood transfusion in patients solely because of concerns of predisposition to infection.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
The authors gratefully acknowledge the support of the surgical assistants and intensive care and surgical ward nurses of Papworth Hospital for their contribution to the conduct of this study.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Gattinoni L, Brazzi L, Pelosi P, et al. A trial of goal-oriented hemodynamic therapy in critically ill patients. N Engl J Med. 1995;333:1025–1032[Abstract/Free Full Text]
  2. Franson E, Maessen J, Dentener M, Senden N, Buurman W. Impact of blood transfusions on inflammatory mediator release in patients undergoing cardiac surgery. Chest. 1999;116:1233–1239[Abstract/Free Full Text]
  3. Vamvakas EC, Blajchman MA. Deleterious clinical effects of transfusion-associated immunomodulation: fact or fiction? Blood. 2001;97:1180–1195[Free Full Text]
  4. Vincent JL, Baron JF, Reinhart K, et al. Anemia and blood transfusion in critically ill patients. JAMA 2002 25;288:1499–507
  5. Jones HJ, de Cossart L. Risk scoring in surgical patients. Br J Surg. 1999;86:149–157[Medline]
  6. Mehta G, Khanna SK, Trehan H, Gupta V. Postoperative infection in cardiac surgery: the influence of a change in prophylactic antibiotic regimen. J Hosp Infect. 1990;15:353–362[Medline]
  7. Roques F, Nashef SA, Michel P, et al. Risk factors and outcome in European cardiac surgery: analysis of the EuroSCORE multinational database of 19030 patients. Eur J Cardiothorac Surg. 1999;15:816–823[Abstract/Free Full Text]
  8. Wilson AP, Treasure T, Sturridge MF, Gruneberg RN. A scoring method (ASEPSIS) for postoperative wound infections for use in clinical trials of antibiotic prophylaxis. Lancet. 1986;1:311–313[Medline]
  9. Boyd O, Grounds RM, Bennett ED. A randomized clinical trial of the effect of deliberate perioperative increase of oxygen delivery on mortality in high-risk surgical patients. JAMA. 1993;270:2699–2707[Abstract/Free Full Text]
  10. Shoemaker WC, Appel PL, Kram HB, Waxman K, Lee TS. Prospective trial of supranormal values of survivors as therapeutic goals in high-risk surgical patients. Chest. 1988;94:1176–1186[Abstract/Free Full Text]
  11. Nelson AH, Fleisher LA, Rosenbaum SH. Relationship between postoperative anemia and cardiac morbidity in high-risk vascular patients in the intensive care unit. Crit Care Med. 1993;21:860–866[Medline]
  12. Wu W-C, Rathore SS, Wang Y, Radford MJ, Krumholz HM. Blood transfusion in elderly patients with acute myocardial infarction. N Engl J Med. 2001;345:1230–1236[Abstract/Free Full Text]
  13. Goodnough LT, Brecher ME, Kanter MH, AuBuchon JP. Blood transfusion. N Engl J Med. 1999;340:438–447[Free Full Text]
  14. Greenberg AG. Benefits and risks of blood transfusion in surgical patients. World J Surg. 1996;20:1189–1193[Medline]
  15. Leal-Noval SR, Rincon-Ferrari MD, Garcia-Curiel A, et al. Transfusion of blood components and postoperative infection in patients undergoing cardiac surgery. Chest. 2001;119:1461–1468[Abstract/Free Full Text]
  16. Blumberg N, Heal JM. Immunomodulation by blood transfusion: an evolving scientific and clinical challenge. Am J Med. 1996;101:299–308[Medline]
  17. Goodnough LT, Despostis GJ, Hogue CW Jr, Ferguson TB Jr. On the need for improved transfusion indicators in cardiac surgery. Ann Thorac Surg. 1995;60:473[Abstract/Free Full Text]
  18. Fernández LA, MacSween JM, Choong K, et al. Immunologic changes after blood transfusion in patients undergoing vascular surgery. Am J Surg. 1992;163:263–269[Medline]
  19. Ottino G, Paulis R, Pansini S. Major sternal wound infection and open-heart surgery: a multi-variant analysis of risk factors in 2579 consecutive operative procedures. Ann Thorac Surg. 1995;60:473–480[Abstract/Free Full Text]
  20. Hebert PC, Wells G, Blajchman MA, et al. A multicenter randomized controlled clinical trial of transfusion requirements in critical care. N Engl J Med. 1999;340:409–417[Abstract/Free Full Text]
  21. Carson JL, Duff A, Poses RM, et al. Effect of anaemia and cardiovascular disease on surgical mortality and morbidity. Lancet. 1996;348:1055–1060[Medline]
  22. Hebert PC, Wells G, Tweeddale M, et al. Does transfusion practice affect mortality in critically ill patients? Am J Respir Crit Care Med. 1997;155:1618–1623[Abstract]
  23. Kuhn C, Muller-Werdan U, Schmitt DV, et al. Improved outcome of APACHE II score-defined escalating systemic inflammatory response syndrome in patients post cardiac surgery in 1996 compared to 1998–1990: the ESSICS-study pilot project. Eur J Cardiothorac Surg. 2000;17:30–37[Abstract/Free Full Text]
  24. Vamvakas EC. Transfusion associated cancer-recurrence and postoperative infection: meta-analysis of randomised, controlled trials. Transfusion. 1996;36:175–186[Medline]
  25. Goodnough LT, Bach GR. Anemia, transfusion and mortality. N Engl J Med. 2001;345:1272–1273[Free Full Text]
  26. D'Ambra MN, Kaplan DK. Alternatives to allogenic blood use in surgery: acute normovolemic hemodilution and preoperative autologous donation. Am J Surg. 1995;170(Suppl):49–52
  27. Jovic ME, Calija BM, Radomir BJ, et al. The use of acute normovolemic hemodilution in patients undergoing cardiac surgery. Cardiovasc Surg. 2003;11:201–205[Medline]
  28. Duke M, Abelmann WH. The hemodynamic response to chronic anemia. Circulation. 1960;39:503–515
  29. Levy PS, Kim SJ, Eckel PK, et al. Limit to cardiac compensation during acute isovolumic hemodilution: influence of coronary stenosis. Am J Physiol. 1993;265:H340–349[Medline]
  30. American College of Physicians. Practice strategies for elective RBC transfusion. Ann Intern Med. 1992;116:403–406[Abstract/Free Full Text]
  31. Consensus Conference. Perioperative red blood cell transfusion. JAMA. 1988;260:2700–2703[Abstract/Free Full Text]
  32. Vamvakas EC, Carven JH. Transfusion and post-operative pneumonia in coronary artery bypass graft surgery: effect of the length of storage of red cells. Transfusion. 1999;39:701–710[Medline]
  33. Miholic J, Hudec M, Domanig E. Risk factors for severe bacterial infection after valve replacement and aortocoronary bypass operations: analysis of 246 cases by logistic regression. Ann Thorac Surg. 1985;40:224–228[Abstract]
  34. El Oakley R, Paul E, Wong PS, Yohana A, Magee P, Walesby R. Mediastinitis in patients undergoing cardiopulmonary bypass: risk analysis and midterm results. J Cardiovasc Surg. 1997;38:595–600[Medline]
  35. Zacharias A, Habib RH. Factors predisposing to median sternotomy complications: deep vs. superficial infection. Chest. 1996;110:1173–1178[Abstract/Free Full Text]
  36. Ryan T, McCarthy JF, Rady MY, et al. Early bloodstream infection after cardiopulmonary bypass: frequency rate, risk factors, and implications. Crit Care Med. 1997;25:2009–2014[Medline]



This article has been cited by other articles:


Home page
 Ann. Thorac. Surg.Home page
G. J. Murphy and G. D. Angelini
Indications for Blood Transfusion in Cardiac Surgery
Ann. Thorac. Surg., December 1, 2006; 82(6): 2323 - 2334.
[Abstract] [Full Text] [PDF]

Home page
 Eur. J. Cardiothorac. Surg.Home page
A. Michalopoulos, S. Geroulanos, E. S. Rosmarakis, and M. E. Falagas
Frequency, characteristics, and predictors of microbiologically documented nosocomial infections after cardiac surgery.
Eur. J. Cardiothorac. Surg., April 1, 2006; 29(4): 456 - 460.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Eric Lim
Ayyaz A. Ali
Steven Tsui
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ali, Z. A.
Right arrow Articles by Tsui, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ali, Z. A.
Right arrow Articles by Tsui, S.
Related Collections
Right arrow Cardiac - pharmacology

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS