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):
Stewart R. Craig
Evan W.J. Cameron
William S. Walker
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 Craig, S. R.
Right arrow Articles by Walker, W. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Craig, S. R.
Right arrow Articles by Walker, W. S.

Ann Thorac Surg 1998;66:356-361
© 1998 The Society of Thoracic Surgeons

Original articles: general thoracic

Effect of blood transfusion on survival after esophagogastrectomy for carcinoma1

Stewart R. Craig, FRCSa, Donald J. Adam, FRCSa, Peng Lee Yap, FRCPatha, H. Anne Leaver, PhDa, Robert A. Elton, PhDa, Evan W.J. Cameron, FRCSa, Christopher T.M. Sang, FRCSa, William S. Walker, FRCSa

a Thoracic Surgical Unit, City Hospital, Edinburgh, United Kingdom

Accepted for publication March 9, 1998.

Address reprint requests to Mr Craig, Department of Cardiothoracic Surgery, Royal Infirmary of Edinburgh, Lauriston Place, Edinburgh EH3 9YW, UK


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. There is growing evidence that blood transfusion is associated with clinical factors that can lead to transfusion-induced immunosuppression. This effect can be beneficial or deleterious.

Methods. The effect of perioperative allogeneic blood transfusion on survival was studied retrospectively in 524 patients who were discharged from the hospital after esophagogastrectomy for carcinoma performed in a single unit over a 10-year period.

Results. The median operative blood loss for the series was 500 mL (range, 50 to 3,750 mL). Three hundred thirty-five patients (64%) received a perioperative allogeneic blood transfusion related to esophagogastrectomy, and 189 (36%) did not. The median perioperative blood transfusion administered was 900 mL (range, 300 to 12,950 mL). Perioperative allogeneic blood transfusion was associated with reduced survival for patients in stage III (p < 0.05) at 1 year, but no significant difference was found in this stage at 3 or 5 years after resection. Stage III disease accounted for 250 (48%) of the 524 patients discharged.

Conclusions. Although perioperative allogeneic blood transfusion does not affect long-term survival after esophagogastrectomy for carcinoma, it does have a significant association with short-term survival in a group whose overall survival is often limited after resection. Attention should be directed toward minimizing operative blood loss and transfusing only for factors known to be clinically important, such as oxygen delivery and hemodynamics, not arbitrary hemoglobin levels.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
The risk of blood transfusion in regard to the transmission of viral agents such as hepatitis viruses B, C, and G, human immunodeficiency virus, and cytomegalovirus is well established. There is also increasing evidence that blood transfusion is associated with clinical phenomena that may be attributable to the development of transfusion-induced immunosuppression. The transfusion effect can be favorable; preoperative transfusion in patients requiring dialysis improves the survival of subsequently transplanted renal allografts [1], and patients undergoing bowel resection for Crohn’s disease have reduced recurrence rates if they receive a perioperative blood transfusion [2]. Transfusion-associated immunomodulation, however, can have deleterious effects. After the initial report by Burrows and Tartter [3] in 1982 suggesting a poorer outcome with perioperative allogeneic blood transfusion (PABT) in patients with colorectal cancer, others have confirmed their findings not only for colorectal cancer [4] but also for gastric [5], renal [6], lung [7], and breast cancer [8]. These findings have not been universally supported by others who failed to find such associations in colorectal [9], renal [10], and lung cancer [11]. A metaanalysis [12] of 20 reports comprising 5,236 patients with colorectal cancer revealed a positive association between perioperative blood transfusion and increased rates of recurrence and death. A recent study [13] of the effect of PABT on survival of 316 patients undergoing resection of esophageal cancer over 23 years reported that the association between high-volume (>8 units) blood transfusions and decreased survival reflected more on the circumstances necessitating blood transfusion than the blood transfusion itself. The aim of this investigation was to ascertain the effect of PABT on survival in a large consecutive series of patients with esophageal and gastric cardia carcinoma who underwent resection and were discharged from a single surgical unit over a recent 10-year period.


   Patients and methods
Top
 Footnotes
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Over a 10-year period ending December 1992, 597 consecutive patients underwent resection of a carcinoma of the esophagus or gastric cardia in the Thoracic Surgical Unit, City Hospital, Edinburgh. Twenty-one patients received preoperative transfusions, and as this was mainly because of extensive disease, these patients were excluded from this analysis. The overall in-patient mortality rate was 9.0% (52/576) and was significantly lower in patients who did not receive a PABT (2.6% versus 12.3%; p < 0.001). As there was a possibility that this difference was due to the circumstances necessitating the transfusion rather than the transfusion itself, the patients who died in the hospital were also excluded from the analysis.

Study group
Five hundred twenty-four patients were entered into the study. Of these patients, 189 (36%) did not receive a PABT (group 1). This group consisted of 132 men and 57 women with a median age of 66 years (range, 33 to 85 years). Three hundred thirty-five patients (64%) did receive a PABT (group 2). This group comprised 201 men and 134 women with a median age of 67 years (range, 28 to 87 years).

Tumors were staged after resection according to the American Joint Committee on Cancer guidelines [14]. The two groups were compared with respect to the following clinicopathologic data retrieved from the hospital case notes and shown in Table 1: sex, tumor site, tumor histology, degree of differentiation, depth of tumor penetration, local invasion, lymph node status, visceral metastases, tumor stage, extent of resection, and resection margins. Survival data were obtained from the case notes or by contact with each patient’s general medical practitioner and then cross-checking with the Scottish Cancer Registry data. Death regardless of cause was defined as a negative outcome, as it was not possible to ascertain cause of death or tumor recurrence for all patients.


View this table:
[in this window]
[in a new window]
  		Table 1. Clinicopathologic Data for 524 Patients Discharged After Resectiona

 
Treatment of the majority of patients was by resection alone. Transthoracic resection was performed in 515 patients, and a transhiatal approach was used in 9 patients (3 in group 1 and 6 in group 2). The technique of surgical resection employed in the unit has previously been described [15]. Splenectomy and partial pancreatectomy (8 in group 1 and 21 in group 2) was undertaken when required to achieve tumor clearance. Twenty patients (3.8%) had preoperative radiotherapy (n = 13) or combination radiotherapy and chemotherapy (n = 7) as part of a clinical trial that failed to show a survival benefit [16].

Statistical analysis
Actuarial survival at 1 year, 3 years, and 5 years was calculated by the method of Kaplan and Meier. A Cox proportional hazards regression analysis was used to control for the following clinicopathologic covariates of prognostic significance: sex, tumor site, tumor histology, degree of differentiation, depth of tumor penetration, local invasion, lymph node metastasis, resection margins, blood loss, and PABT. The {chi}2 test, Fisher’s exact test, and Mann-Whitney test were used where appropriate. A probability value of less than 0.05 was regarded as significant.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Two hundred forty-seven patients (47%) had no complications of any sort in the postoperative period. Sixteen patients (3%) had nonfatal anastomotic dehiscence. Twenty-two patients (4%) required assisted ventilation for 24 hours or longer postoperatively (median duration, 5 days; range, 1 to 9 days). The median in-patient stay for all patients was 12 days (range, 6 to 44 days).

The overall median operative blood loss for 510 patients (97%) for whom this information was available was 500 mL (range, 50 to 3,750 mL). The median operative blood loss recorded for 184 of the 189 patients not receiving a transfusion was significantly lower than for 326 of the 335 patients who had a transfusion (350 mL with a range of 50 to 1,000 mL versus 600 mL with a range of 50 to 3,750 mL; p < 0.0001, Mann-Whitney test). The median operative blood loss by tumor stage ranged between 300 and 500 mL (Table 2). The operative blood loss was less than 1,000 mL in 447 (87%) of 510 patients. The overall median transfusion volume in those patients receiving a PABT was 900 mL (range, 300 to 12,950 mL). The use of blood transfusion by tumor stage is listed in Table 3.


View this table:
[in this window]
[in a new window]
  		Table 2. Operative Blood Loss by Tumor Stage in 510 Resections

 

View this table:
[in this window]
[in a new window]
  		Table 3. Perioperative Blood Transfusion by Tumor Stage in 524 Resectionsa

 
The actuarial survival at 1 year, 3 years, and 5 years according to tumor stage and transfusion status in 524 patients discharged after resection is shown in Table 4. There was no difference in short-term and long-term survival for stages I, IIA, IIB, or IV between patients who did and those who did not receive a PABT. However, for patients with stage III disease who were discharged, those in group 1 (no transfusion) had significantly better survival at 1 year (p < 0.05) than those in group 2 (transfusion) (Fig 1). However, this did not translate into improved survival at 3 or 5 years.


View this table:
[in this window]
[in a new window]
  		Table 4. Actuarial Survival at 1, 3, and 5 Years by Stage and Transfusion Status for 524 Patients Discharged After Resection

 


View larger version (15K):
[in this window]
[in a new window]
  		Fig 1. Actuarial survival according to transfusion status for 250 patients with stage III disease who were discharged after resection.

 
Clinicopathologic data for patients with stage III disease who were discharged are shown in Table 5, and a Cox proportional hazards regression analysis of this group is shown in Table 6. Although patients with stage III disease who received a transfusion were more likely to undergo operation for midesophageal carcinoma with local invasion (see Table 5), tumor site, excluding upper-third lesions, and local invasion were not independently associated with a poor prognosis. The absence of a covariate-adjusted association between blood loss and survival in patients with stage III disease who did not have a transfusion is evidence that it is the blood transfusion that has a causative effect on survival and not the blood loss leading to the transfusion or the clinical characteristics causing the blood loss.


View this table:
[in this window]
[in a new window]
  		Table 5. Clinicopathologic Data for 250 Patients With Stage III Disease Who Were Discharged After Resectiona

 

View this table:
[in this window]
[in a new window]
  		Table 6. Ninety-five Percent Confidence Limits for Estimated Risk Ratios From Cox Regression of Survival on Select Prognostic Factors in Patients With Stage III Disease Who Were Discharged From the Hospitala

 
The actual reason for a blood transfusion was rarely mentioned in the case notes. In the operating theater, transfusion was initiated when there was concern about operative blood loss. In the postoperative period, even if there was no ongoing blood loss, a transfusion was usually given if the hemoglobin level fell lower than 10 g/dL. This was by no means consistent, and little correlation between blood transfusion and postoperative symptoms resulting from anemia could be found.


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
We have shown a significant correlation between use of blood in the perioperative period and adverse outcome in terms of survival for patients with stage III disease at 1 year after operation (see Fig 1). It is accepted that there are fundamental limitations of observational studies such as this that attempt to show a cause and effect relationship. However, a multiple regression analysis showed that PABT was a significant independent prognostic factor in patients with stage III disease. Further, the absence of a covariate-adjusted association between blood loss and survival in patients with stage III disease who did not have a transfusion is evidence that blood transfusion has a causative effect on survival that is independent of both the blood loss that led to the transfusion and the clinical characteristics that led to the blood loss.

This effect on survival at 1 year may be the result of two patient subpopulations within this stage, namely, patients with and patients without occult metastases. If blood transfusion does indeed reduce survival at 1 year in patients given a transfusion, then the percentage surviving thereafter would remain relatively unchanged and would explain the absence of a difference in survival at 3 and 5 years. Transfusion therefore could also be expected to have little effect in the other stages, as the presence of occult metastases would be lower in stages I and II and much higher in stage IV. This association with stage III is important, as it comprised almost half of all patients discharged after resection.

The effect of blood transfusion on the immune system has been studied extensively and has been shown to have substantial immunosuppressive effects [17]. The development of immunosuppression in the postoperative period after resection of cancer is important, as the immune system is thought to play a major role in limiting the development of malignant cells [18]. Transfusion of allogeneic whole-blood products reduces natural killer cell activity and T lymphocyte blastogenesis and increases suppressor T lymphocyte activity [19], factors that may be of great importance for host resistance to infection and prevention of dissemination of malignant cells. This effect may last for up to 8 months after transfusion [20]. Transfusion-associated immunosuppression therefore compounds that already produced by malnutrition [21], anesthesia, and the operation itself [22]. Blood transfusion alone may increase the risk of the development of cancer, independent of trauma or operation, for up to 9 years after transfusion [23].

The blood loss in this series was low compared with other series reporting such data, and this is important, as hemorrhage alters function and cytokine production of T cells and their subpopulations [24]. Interleukin-2 and interferon-{gamma} both play a major role in natural killer and T cell cytolysis [10]. Levels of interleukin-2, necessary for the activation of B lymphocytes and regulation of T lymphocyte production, are reduced after blood transfusion [25]. In addition, other mediators such as serum factors and metabolites of the arachidonic acid pathway may be involved in immunomodulation [26]. The increased iron load, which accompanies transfusion, also decreases the lymphocytic response to antigens [27].

Although the use of autologous blood donation has been shown to reduce the incidence of postoperative infectious complications [28], no difference in tumor recurrence rates have been found compared with allogeneic blood transfusion [29].

In thoracic surgical practice, there is strong support for resection being performed with scrupulous attention to minimizing operative blood loss. Indications for blood transfusion should be based on factors known to be clinically important such as oxygen delivery and hemodynamics and not on arbitrary hemoglobin levels, which can lead to unnecessary transfusion. It has been suggested [30] that in patients undergoing operation for colorectal cancer, 25% to 28% receive at least 1 unit of unnecessary blood. The timing of transfusion, should it be required, may also be important. Operation-induced immunosuppression is maximal in the first 48 hours after operation [31–33], and therefore, it would appear that transfusion should be avoided, if clinically possible, until after this period. The practice of normovolemic hemodilution allows safe reduction in hemoglobin levels without an increase in morbidity or mortality [34].

Future attempts to reduce the requirement of transfusion may center on bone marrow stimulants such as erythropoietin [35] and artificial blood substitutes [36]. A randomized trial [37] comparing leukocyte-depleted versus buffy coat–poor blood transfusion in operation for colorectal cancer found significant increases in infectious complications in patients receiving buffy coat–poor blood. The number of immunosuppressive leukocytes in whole blood can be reduced significantly with the use of high-efficiency leukocyte-depleting blood filters. A prospective study to look at infectious complications and survival after transfusion in patients with esophageal cancer would be possible in principle. However, given that a multicenter study involving a large number of patients with a long follow-up would be required, it is unlikely to be performed in the near future. The risk to the transfusion recipient from infectious hazards and transfusion reactions is well documented. If there is a poorer outcome after esophageal cancer resection with transfusion, as we have shown, any unnecessary transfusion cannot be justified.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
1 This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/annals Back


   References
Top
 Footnotes
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Glass N.R., Miller D.T., Sollinger H.W., Belzer F.O. A four-year experience with donor transfusion protocols for living-donor renal transplantation. Transplantation 1985;39:615-619.[Medline]
  2. Scott A.D.N., Ritchie J.K., Philips R.K.S. Blood transfusion and recurrent Crohn’s disease. Br J Surg 1991;78:455-458.[Medline]
  3. Burrows L., Tartter P. Effect of blood transfusion on colonic malignancy recurrence rate [Letter]. Lancet 1982;2:662.[Medline]
  4. Busch O.R.C., Hop W.C.J., Hoynck van Papendrect M.A.W., Marquet R.L., Jeekel J. Blood transfusions and prognosis in colorectal cancer. N Engl J Med 1993;328:1372-1376.[Abstract/Free Full Text]
  5. Fong Y., Karpah M., Mayer K., Brennan M.F. Association of perioperative transfusions with poor outcome in resection of gastric adenocarcinoma. Am J Surg 1994;167:256-260.[Medline]
  6. Edna T.-H., Vada K., Hesselberg F., Mjolnerod O.K. Blood transfusion and survival following surgery for renal carcinoma. Br J Urol 1992;70:135-138.[Medline]
  7. Hyman N.H., Foster R.S., DeMeules J.E., Costanza M.C. Blood transfusions and survival after lung cancer resection. Am J Surg 1985;149:502-507.[Medline]
  8. Tartter P.I., Burrows L., Papatestas A.E., et al. Perioperative blood transfusion has prognostic significance for breast cancer. Surgery 1985;97:225-230.[Medline]
  9. Francis D.M.A., Judson R.T. Blood transfusion and recurrence of cancer of the colon and rectum. Br J Surg 1987;74:26-30.[Medline]
  10. Moffat L.E., Sunderland G.T., Lamont D. Blood transfusion and survival following nephrectomy for carcinoma of the kidney. Br J Urol 1987;70:316-319.
  11. Pastorino U., Valente M., Cataldo I., Lequaglie C., Ravasi G. Perioperative blood transfusion and prognosis of resected Ia lung cancer. Eur J Cancer Clin Oncol 1986;22:1375-1378.[Medline]
  12. Chung M., Steinmetz O.K., Gordon P.H. Perioperative blood transfusion and outcome after resection for colorectal carcinoma. Br J Surg 1993;80:427-432.[Medline]
  13. Swisher S.G., Holmes E.C., Hunt K.K., Gornbein J.A., Zinner M.J., McFadden D.W. Perioperative blood transfusions and decreased long-term survival in esophageal cancer. J Thorac Cardiovasc Surg 1996;112:341-348.[Abstract/Free Full Text]
  14. American Joint Committee on Cancer. Manual for staging of cancer, 3rd ed. Philadelphia: Lippincott, 1988:63-71.
  15. Craig S.R., Walker W.S., Cameron E.W.J., Wightman A.J.A. A prospective randomised trial comparing stapled with handsewn oesophagogastric anastomoses. J R Coll Surg Edinb 1996;41:17-19.[Medline]
  16. Arnott S.J., Duncan W., Kerr G.R., et al. Low-dose pre-operative radiotherapy for carcinoma of the oesophagus: result of a randomised clinical trial. Radiother Oncol 1992;24:108-113.[Medline]
  17. Nielsen H.J. Detrimental effects of perioperative blood transfusion. Br J Surg 1995;82:582-587.[Medline]
  18. Cole W.H., Humphrey L. Need for immunologic stimulators during immunosuppression produced by major cancer surgery. Ann Surg 1985;202:9-20.[Medline]
  19. Gafter U., Kalechman Y., Sredni B. Induction of a subpopulation of suppressor cells by a single blood transfusion. Kidney Int 1992;41:143-148.[Medline]
  20. Tartter P.I., Heimann T.M., Aufsus A.H. Blood transfusion, skin test reactivity, and lymphocytes in inflammatory bowel disease. Am J Surg 1986;151:358-361.[Medline]
  21. Villa M.L., Ferrario E., Bergamasco E., Bozzetti F., Cozzaglio L., Clerici E. Reduced natural killer cell activity and IL-2 production in malnourished cancer patients. Br J Cancer 1991;63:1010-1014.[Medline]
  22. Salo M. Effects of anaesthesia and surgery on the immune response. Acta Anaesthesiol Scand 1992;36:201-220.[Medline]
  23. Blomberg J., Moller T., Olsson H., Andersen H., Jonsson M. Cancer morbidity in blood recipients—results of a cohort study. Eur J Cancer 1993;29A:2101-2105.
  24. Abraham E., Chang Y.H. Haemorrhage-induced alterations in function and cytokine production of T cells and T cell subpopulations. Clin Exp Immunol 1992;90:497-502.[Medline]
  25. Wood M.L., Gottschalk R., Monaco A.P. Effect of blood transfusion on IL-2 production. Transplantation 1988;45:930-935.[Medline]
  26. Brunson M.E., Alexander J.W. Mechanisms of transfusion-induced immunosuppression. Transfusion 1990;30:651-658.[Medline]
  27. Matzner Y., Hershko C., Polliack A., et al. Suppressive effect of ferritin on in vitro lymphocyte function. Br J Haematol 1979;41:345-353.
  28. Heiss M.M., Mempel W., Jauch K.W., et al. Beneficial effect of autologous blood transfusion on infectious complications after colorectal cancer surgery. Lancet 1993;342:1328-1333.[Medline]
  29. Ness P.M., Walsh P.C., Zahurak M., Baldwin M.L., Piantadosi S. Prostate cancer recurrence in radical surgery patients receiving autologous or homologous blood. Transfusion 1992;32:31-36.[Medline]
  30. Tartter P.I., Barron D.M. Unnecessary blood transfusion in elective colorectal cancer surgery. Transfusion 1985;25:113-115.[Medline]
  31. Akiyoshi T., Koba F., Arinaga S., Miyazaki S., Wada T., Tsuji H. Impaired production of interleukin-2 after surgery. Clin Exp Immunol 1985;59:45-49.[Medline]
  32. Hammer J.H., Nielsen H.J., Moesgaard F., Kehlet H. Duration of postoperative immunosuppression measured by repeated delayed hypersensitivity (DTH) skin tests. Eur Surg Res 1992;24:133-137.[Medline]
  33. Wakefield C.H., Carey P.D., Foulds S., Monson J.R., Guillou P.J. Changes in major histocompatibility complex class II expression in monocytes and T cells of patients developing infection after surgery. Br J Surg 1993;80:205-209.[Medline]
  34. Spence R.K., Carson J.A., Poses R., et al. Elective surgery without transfusion: influence of preoperative hemoglobin level and blood loss on mortality. Am J Surg 1990;159:320-324.[Medline]
  35. Biesma D.H., Marx J.J.M., Kraaijenhagen R.J., Franke W., Messinger D., van der Wiel A. Lower homologous blood requirement in autologous blood donors after treatment with recombinant human erythropoietin. Lancet 1994;344:367-370.[Medline]
  36. Slanetz P.J., Lee R., Page R., Jacobs E.E., La Raia P.J., Vlahakes G.J. Hemoglobin blood substitutes in extended preoperative autologous blood donation: an experimental study. Surgery 1994;115:246-254.[Medline]
  37. Jensen L.S., Kissmeyer-Nielsen P., Wolff B., Qvist N. Randomised comparison of leucocyte-depleted versus buffy-coat poor blood transfusion and complications after colorectal surgery. Lancet 1996;348:841-845.[Medline]



This article has been cited by other articles:


Home page
 Ann. Thorac. Surg.Home page
A. Eroglu, A. Turkyilmaz, Y. Aydin, A. F. Erdem, M. Tokur, and N. Karaoglanoglu
The Use of the LigaSure Vessel Sealing System in Esophageal Cancer Surgery
Ann. Thorac. Surg., December 1, 2007; 84(6): 2076 - 2079.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
V. Voelter, C. Schuhmacher, R. Busch, C. Peschel, J. R. Siewert, and F. Lordick
Incidence of anemia in patients receiving neoadjuvant chemotherapy for locally advanced esophagogastric cancer
Ann. Thorac. Surg., September 1, 2004; 78(3): 1037 - 1041.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
S. M. Langley, C. Alexiou, D. H. Bailey, and D. F. Weeden
The influence of perioperative blood transfusion on survival after esophageal resection for carcinoma
Ann. Thorac. Surg., June 1, 2002; 73(6): 1704 - 1709.
[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):
Stewart R. Craig
Evan W.J. Cameron
William S. Walker
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 Craig, S. R.
Right arrow Articles by Walker, W. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Craig, S. R.
Right arrow Articles by Walker, W. S.

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