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The Journal of Bone and Joint Surgery. American Volume logoLink to The Journal of Bone and Joint Surgery. American Volume
. 2013 Dec 4;95(23):2105–2110. doi: 10.2106/JBJS.L.00979

The Association Between Perioperative Allogeneic Transfusion Volume and Postoperative Infection in Patients Following Lumbar Spine Surgery

Barrett I Woods 1, Bedda L Rosario 1, Antonia Chen 1, Jonathan H Waters 1, William Donaldson III 1, James Kang 1, Joon Lee 1
PMCID: PMC4098016  PMID: 24306697

Abstract

Background:

Perioperative allogeneic red blood cell transfusion is a risk factor for surgical site infection. The purpose of this study was to determine if the volume of perioperative allogeneic red blood cell transfusion influences the risk of surgical site infection following lumbar spine procedures.

Methods:

A retrospective matched case control study was performed by reviewing all patients who had undergone lumbar spine surgery at our institution from 2005 to 2009. Surgical site infections (spinal or iliac crest) were identified, all within thirty days of the procedure. Controls were matched to the infection cohort according to age, sex, body mass index, diabetic status, smoking status, Charlson Comorbidity Index, length of surgery, and procedure. A conditional logistic regression was performed to examine the association between transfusion volume and surgical site infection. The results were summarized by an odds ratio.

Results:

A total of 1799 lumbar procedures were identified with an infection rate of 3.1% (fifty-six cases). On the basis of the numbers, there was no significant difference in the matched variables between the infection cohort and the matched controls. The volume of transfusion was significantly associated with surgical site infection (odds ratio, 4.00 [95% confidence interval, 1.96 to 8.15]) after adjusting for both unmatched variables of preoperative hemoglobin level and volume of intraoperative blood loss.

Conclusions:

In this retrospective matched case control study, the association between surgical site infection following lumbar spine surgery and volume of perioperative allogeneic red blood cell transfusion was supported.

Level of Evidence:

Prognostic Level III. See Instructions for Authors for a complete description of levels of evidence.

Infections following spinal surgical procedures impart an increased risk of postoperative patient morbidity and mortality. Surgical site infection is the most common nosocomial infection in the early postoperative period1. More importantly, 77% of acute mortality in patients with surgical site infection is directly related to the infection2. The consequences of postoperative infection include loss of instrumentation fixation, pseudarthrosis, osteomyelitis, chronic pain, sepsis, and death3-6. In addition, the economic implications of infection following spinal surgery cannot be overstated. Patients who develop surgical site infection usually require longer postoperative hospitalization, are more likely to be managed in intensive care units, and have higher hospital readmission rates7.

The incidence of surgical site infection following spinal procedures is influenced by a multitude of intrinsic and extrinsic factors. Patient-specific factors identified as increasing the risk for surgical site infection include advanced age6,8,9, corticosteroid use10,11, smoking6,12,13, alcohol abuse6, and diabetes6,10,13,14. Olsen et al. performed a large retrospective case control study in which diabetes was the greatest independent risk factor for spinal surgical site infection15. Schwarzkopf et al. found body mass index (BMI) to significantly influence the risk of surgical site infection following thoracic and lumbar spine surgery16. Intraoperative risk factors identified include the type of surgical approach, the procedure performed, revision procedures, and the length of the surgery6,14. A point of contention in the literature and among surgeons is the relationship between allogeneic perioperative blood product transfusion and morbidity. The rationale for aggressive perioperative red blood cell transfusion following spine surgery has been established17. Additionally, postoperative anemia has been correlated with longer hospital admission and higher readmission rates in patients following open reduction and internal fixation of hip fractures18, although this has been questioned recently19.

In the United States, 14 million units of blood are transfused annually and transfused blood is generally considered to be safe20. However, allogeneic transfusion does have some risks. The association between the development of surgical site infection and transfusion has been reported in the literature21-24. The immunomodulatory effects imparted by allogeneic transfusion are not completely understood. Allogeneic transfusion has been linked not only to an increased risk of nosocomial infection, but also to cancer recurrence and autoimmune diseases25-27. Although allogeneic red blood cell transfusion has been identified as a risk factor for the development of surgical site infection following spinal surgery16, we are unaware of any studies that have evaluated if the volume of transfusion given influences infection risk. The purpose of this study was to determine if there is an association between the volume of perioperative red blood cell transfusion and the risk of surgical site infection following lumbar spine procedures.

Materials and Methods

Following institutional review board approval, all lumbar spinal surgical procedures performed at the University of Pittsburgh Medical Center from 2005 to 2009 by one senior fellowship-trained spine surgeon (J.K.) were retrospectively reviewed. The surgical procedures included laminectomy, instrumented and non-instrumented fusion, and anterior and posterior interbody fusions. Additional information collected for each procedure included if it was a primary or revision procedure, if allogeneic or autogenous bone graft (iliac crest) was used, and if bone morphogenetic protein 2 (BMP-2) was used. All included patients had a subfascial medium postoperative blood salvage system (Hemovac System; Zimmer, Warsaw, Indiana) placed prior to closure.

Infections were recorded in each group and defined as surgical site infections (spinal or iliac crest) that occurred within thirty days of the procedure as in accordance with the Centers for Disease Control and Prevention definition2. All diagnosed surgical site infections were treated with operative irrigation and debridement and intravenous antibiotics.

The volume of allogeneic red blood cell transfusion for each procedure was obtained from our central blood bank database. All patients who underwent transfusion received blood intraoperatively or in the immediate postoperative period, defined as within twenty-four hours after surgery. Indication for perioperative transfusion was determined by the attending surgeon and anesthesiologist. Factors that influenced transfusion included large-volume blood loss, hypotension, and oliguria. Intraoperative autotransfusion was used in all patients. Intraoperative blood loss was estimated at the conclusion of each procedure and was recorded for all patients included in the study.

Potential risk factors for surgical site infection were identified and were recorded by medical record review. The Charlson Comorbidity Index score was obtained on each patient to summarize preexisting comorbid illness28. The medical record was searched for the presence of the comorbidities listed in the Appendix, and the comorbidity score was a summation of the points associated with each condition. This comorbidity score has been previously validated as a predictor of mortality in patients with a wide range of disease processes (stroke, end-stage renal disease, pneumonia, cancer) and after certain treatments such as coronary artery bypass surgery29-34. Patients who had an incomplete medical record in which a comorbidity score could not be generated were excluded from the study.

The analysis was performed as a matched case-control study. One to five control subjects were matched to each case subject by age, sex, BMI, smoking status, diabetes status, Charlson Comorbidity Index, length of surgery, revisions, iliac crest bone graft, and the use of allograft. These variables were chosen to eliminate them as potential confounders. Subject characteristics and risk data were compared between case and control subjects with use of generalized estimating equations for categorical and continuous variables. The impact of volume of transfusion on the occurrence of surgical infection was examined by conditional logistic regression through the PHREG procedure (SAS, version 9.3; SAS Institute, Cary, North Carolina), with each case and matched controls forming a separate stratum. The volume of transfusion was treated as a continuous variable and surgical infection was treated as a nominal variable (yes or no). To examine the impact of non-matched variables in the association, we further adjusted for possible confounders, specifically the preoperative hemoglobin level and the volume of intraoperative blood. Confounding was assessed by the impact of the potential confounder on the parameter estimate for the main effect (i.e., volume of transfusion). If a removal of a possible confounding variable caused a change of 10% or more in the value of the parameter estimate, that variable was considered to be a confounder and was included in the final model. Pairwise interactions were assessed where relevant. The results were summarized by the odds ratio (OR) and its 95% confidence interval (95% CI). The odds ratio represents the average increase in odds associated with a one-unit increase in the exposure. All analyses were performed with the alpha level set to 0.05.

Source of Funding

The statistical analysis was performed through the Clinical and Translational Science Institute (CTSI) and was funded by the National Institutes of Health (Grant Numbers UL1 RR024153 and UL1TR000005).

Results

A total of 1799 lumbar spine surgical procedures had an infection rate of 3.1% (fifty-six cases). A total of ninety-one lumbar controls were subsequently identified. For the matched data, thirty-one cases had one control, nineteen cases had two controls, four cases had three controls, and two cases had five controls. Of the fifty-six infection cases, thirty-nine involved only the midline surgical incision and seventeen involved the iliac crest.

The average age of all subjects included in this study was sixty-one years (range, twenty-three to eighty-three years). This average and variation were consistent across both infection and control groups. A wide range of procedures were included in this study; however, laminectomy with instrumented fusion was the most frequently performed, accounting for 87.5% (forty-nine of fifty-six) of the infection cases and 89% (eighty-one of ninety-one) of the control cases (p = 0.91).

The length of surgery was, on average, five minutes longer in the infection cohort (272.7 minutes) compared with controls (267.6 minutes) (p = 0.45). The length of surgery was also analyzed separately for primary and revision procedures for the infected and control groups. Revision procedures for both the infection (296 minutes) and control lumbar (287.9 minutes) subgroups required significantly more time (p = 0.001) than primary procedures in the same subgroup; the infection subgroup required 230.9 minutes and the control subgroup required 225 minutes.

Autogenous iliac crest bone graft was harvested from the posterior superior iliac spine through a separate oblique incision. Iliac crest bone graft was incorporated in the fusion construct in a similar number of lumbar infected cases (89.3% [fifty of fifty-six]) and control cases (84.6% [seventy-seven of ninety-one]). There was no significant difference based on the numbers in the percentage of cases that used allograft cancellous bone chips or BMP-2 between infection or control cohorts (p = 0.6). Revision procedures accounted for 64.3% (thirty-six of fifty-six) of the lumbar infection cases and 63.7% (fifty-eight of ninety-one) of the lumbar control cases (p = 0.89). There was no significant difference in the matched variables between infection cases and controls (the p value range was 0.10 to 0.89). There was a significant difference in preoperative hemoglobin level and volume of intraoperative blood loss between cases and controls (p = 0.01). Matched and non-matched variables analyzed between the infection and control groups are summarized in Table I.

TABLE I.

Subject Characteristics for Infection Cases and Their Matched Controls Following Lumbar Surgery

Variables Infection Cases (N = 56) Matched Controls (N = 91) P Value
Matched variables
 Age* (yr) 61.76 ± 12.43 (26 to 83) 60.51 ± 14.87 (23 to 83) 0.84
 Sex† (male) 22 (39.29%) 46 (50.55%) 0.10
 BMI* (kg/m2) 34.00 ± 5.13 (24 to 49) 33.73 ± 4.25 (27 to 49) 0.87
 Smokers† 12 (21.43%) 16 (17.58%) 0.42
 Diabetics† 17 (30.36%) 26 (28.57%) 0.84
 Charlson Comorbidity Index* (points) 3.46 ± 1.43 (1 to 8) 3.40 ± 1.17 (2 to 7) 0.74
 Length of surgery* (min) 272.68 ± 65.55 (176 to 457) 267.60 ± 55.70 (143 to 420) 0.45
 Revision procedure† 36 (64.29%) 58 (63.74%) 0.89
 Iliac crest bone graft† 50 (89.29%) 77 (84.62%) 0.34
 BMP-2 and allograft† 19 (33.93%) 34 (37.36%) 0.60
Non-matched variables*
 Preoperative hemoglobin (g/dL) 13.98 ± 1.62 (10.20 to 16.80) 14.52 ± 1.20 (12.10 to 16.8) 0.01
 Volume of intraoperative blood loss (cm3) 1512.23 ± 477.49 (550 to 2875) 1352.86 ± 369.86 (600 to 2300) 0.01
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*

The values are given as the mean and the standard deviation, with the range in parentheses.

†

The values are given as the number of patients in each group, with the percentages in parentheses.

Overall, there was not a significant difference in the number of patients who received allogeneic transfusion between the infection or control cohorts (p = 0.37). However, of the patients who underwent transfusion, those who developed surgical site infection received nearly one and a half more units of blood than did matched controls. The transfusion data are summarized in Table II.

TABLE II.

Perioperative Transfusion Data for Infection Cases and Matched Controls

Perioperative Transfusion Data Infection Cases (N = 56) Matched Controls (N = 91) P Value
No. of patients undergoing blood transfusion* 43 (76.8%) 66 (72.5%) 0.37
Transfusion volume† (units) 2.89 ± 2.38 (1 to 7) 1.40 ± 1.19 (1 to 4) <0.001
Open in a new tab
*

The values are given as the number of patients, with the percentage in parentheses.

†

The values are given as the mean and the standard deviation, with the range in parentheses.

The volume of transfusion was significantly associated with surgical infection (OR, 2.87 [95% CI, 1.63 to 5.06]). The odds ratio for the association between transfusion volume and surgical site infection after controlling for preoperative hemoglobin level was 3.41 (95% CI, 1.82 to 6.39). Similarly, the odds ratio after adjusting by volume of intraoperative blood loss was 3.38 (95% CI, 1.75 to 6.55). In addition, the volume of transfusion was significantly associated with surgical site infection (OR, 4.00 [95% CI, 1.96 to 8.15]) after adjusting for both unmatched variables (preoperative hemoglobin level and volume of intraoperative blood loss). The association between transfusion volume and surgical site infection remained significant in all models. These models were reassessed along with pairwise interactions; however, no significant interactions were found.

Discussion

Surgical site infection following lumbar spine surgery prolongs hospitalization for a median of two weeks, increasing health-care costs by over 300% per patient35. The association between perioperative allogeneic transfusion and surgical site infection has been described16,22,23,36,37; however, this relationship has not been clearly defined. Determining the contribution that transfusion has to the development of surgical site infection is inherently challenging because of the numerous confounding factors often present, which also influences risk. Despite modern screening, the transmission of virulent agents such as hepatitis, human immunodeficiency virus (HIV), Epstein-Barr virus, and others exists with allogeneic transfusion36-38. Allogeneic transfusions expose hosts to foreign antigens such as human leukocyte antigen dendritic presenting cells39. Blood transfusion can result in immune activation or tolerance. Several clinical syndromes associated with immune activation following allogeneic transfusion have been described, including transfusion reactions, transfusion-associated graft-versus-host disease, transfusion-related lung injury, alloimmunization, and the development of autoimmune diseases40. Immune tolerance or suppression following transfusion is demonstrated by the absence of an immune reaction, increased incidence of cancer recurrence in patients who receive chronic transfusions, microchimerism, and increased predisposition to infection26. The immune tolerance that can be imparted by allogeneic transfusion is supported by the enhanced survival of cardiac, renal, and hepatic allografts in patients who receive allogeneic blood compared with those who do not41-45. Similarly, transfusion of allogeneic blood has been associated with a significantly higher rate of surgical site infection following various different procedures46-48. The association between allogeneic blood transfusion and surgical site infection has also been made following spinal surgery15. Proposed mechanisms include defective antigen presentation, decreased natural killer cell function, and a reduction in delayed hypersensitivity and histamine release49,50. Additionally, current storage methods for allogeneic blood may be suboptimal, resulting in structural and functional degradation of the red blood cells. Blood stored for more than fourteen days has a decreased ability to deform and unload oxygen while in circulation51. These deformed cells are more adhesive to endothelial cells, which can cause capillary sludging and obstruction. This can facilitate poor peripheral perfusion and can limit immune response52,53. It is also postulated that these structural changes result in the accumulation of proinflammatory cytokines, which, upon entry in the host, also facilitate an aberrant immune response. Koch et al. specifically evaluated this issue and found that patients who received blood stored for at least two weeks following cardiac surgery had significantly higher postoperative complications and one-year mortality compared with those who received blood stored for shorter periods of time54.

Although the association between blood transfusion and postoperative infection has been described in the literature, it is unclear what, if any, volume of transfusion contributes to that risk. Restrictive transfusion practices have decreased morbidity and mortality in chronically ill patients55,56. However, restrictive transfusion practices are not particularly beneficial in patients who undergo spine surgery. Pull ter Gunne et al. retrospectively reviewed 300 consecutive patients who underwent spinal surgery with at least 2 L of intraoperative blood loss and found that patients with postoperative hemoglobin levels of ≤8 g/dL had a six times higher risk of surgical site infection compared with those with a hemoglobin level of at least 10 g/dL. They concluded that restrictive transfusion practices may not be beneficial for patients undergoing spine surgery17.

The purpose of this study was to specifically determine if the volume of allogeneic red blood cell transfusion influences the risk of surgical site infection following lumbar spine surgery. To our knowledge, no other study has specifically evaluated this topic. Controls were matched with use of several known intrinsic and extrinsic risk factors for surgical site infection and then were randomly selected. Patients who developed postoperative infection following spine surgery received significantly more allogeneic red blood cell volume than those who did not (OR, 2.87 [95% CI, 1.63 to 5.06]). The odds of having a surgical site infection are 2.87 for a one-unit increase in the volume of transfusion. There were two non-matched variables between the infection and control groups that must be taken into account. Preoperative hemoglobin level is an indicator for increased allogeneic red blood cell transfusion following spine surgery57,58. Patients in the infection group had a significantly lower preoperative hemoglobin level (13.98 g/dL) than patients in the control group (14.52 g/dL) (p = 0.01). Additionally, intraoperative blood loss was, on average, 159.4 mL greater for the infection cohort compared with controls (p = 0.01). Both of these non-matched variables are potential explanations why the infection cohort received significantly more allogeneic red blood cell transfusion than matched controls. We are aware of no such association having been made in the literature between either of these non-matched variables and the risk for infection. The volume of transfusion was significantly associated with surgical site infection (OR, 4.00 [95% CI, 1.96 to 8.15]) after adjusting for both unmatched variables of preoperative hemoglobin level and the volume of intraoperative blood. The association between transfusion volume and surgical site infection remained significant in all models.

This study was limited because of its retrospective nature, and thus, from these data, we cannot support or refute restrictive transfusion practices following spine surgery. Specific limitations that should be highlighted include the lack of a specific transfusion algorithm and data on the age of the transfused allogeneic red blood cells.

In conclusion, these data support the premise that allogeneic red blood cell transfusion volume may influence the risk of surgical site infection following lumbar spine surgery, implying that there may be a dose-dependent effect. A more complete understanding of the immunomodulatory effects that allogeneic transfusion has on the host is required. Prospective studies are required to determine if there is a critical volume of allogeneic transfusion that shifts the risk-benefit ratio, and if that volume is influenced by the presence of other surgical site infection risk factors or patients’ comorbid illness. The development of surgical site infection following spinal surgery is clearly a multifactoral issue.

Appendix

A table showing the Charlson Comorbidity Index scoring system is available with the online version of this article as a data supplement at jbjs.org.

Supplementary Material

Supporting Data

Disclosure of Potential Conflicts of Interest

Click here for additional data file. (296.3KB, pdf)
Supporting Data

A table showing the Charlson Comorbidity Index scoring system

Click here for additional data file. (396.6KB, pdf)

Acknowledgments

Note: We would like to acknowledge the Clinical and Translational Science Institute (CTSI) at the University of Pittsburgh and Dr. Francis X. Solano for his contributions to the completion of this manuscript.

Footnotes

Disclosure: One or more of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of an aspect of this work. In addition, one or more of the authors, or his or her institution, has had a financial relationship, in the thirty-six months prior to submission of this work, with an entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. No author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.

References

  • 1.Horan TC, Culver DH, Gaynes RP, Jarvis WR, Edwards JR, Reid CR. National Nosocomial Infections Surveillance (NNIS) System. Nosocomial infections in surgical patients in the United States, January 1986-June 1992. Infect Control Hosp Epidemio. 1993 Feb;14(2):73-80. [DOI] [PubMed] [Google Scholar]
  • 2.Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Hospital Infection Control Practices Advisory Committee. Guideline for prevention of surgical site infection, 1999. Infect Control Hosp Epidemiol. 1999 Apr;20(4):250-78, quiz:279-80. [DOI] [PubMed] [Google Scholar]
  • 3.Glassman SD, Dimar JR, Puno RM, Johnson JR. Salvage of instrumental lumbar fusions complicated by surgical wound infection. Spine (Phila Pa 1976). 1996 Sep 15;21(18):2163-9. [DOI] [PubMed] [Google Scholar]
  • 4.Lonstein J, Winter R, Moe J, Gaines D. Wound infection with Harrington instrumentation and spine fusion for scoliosis. Clin Orthop Relat Res. 1973 Oct;(96):222-33. [PubMed] [Google Scholar]
  • 5.Viola RW, King HA, Adler SM, Wilson CB. Delayed infection after elective spinal instrumentation and fusion. A retrospective analysis of eight cases. Spine (Phila Pa 1976). 1997 Oct 15;22(20):2444-50, discussion:2450-1. [DOI] [PubMed] [Google Scholar]
  • 6.Fang A, Hu SS, Endres N, Bradford DS. Risk factors for infection after spinal surgery. Spine (Phila Pa 1976). 2005 Jun 15;30(12):1460-5. [DOI] [PubMed] [Google Scholar]
  • 7.Kirkland KB, Briggs JP, Trivette SL, Wilkinson WE, Sexton DJ. The impact of surgical-site infections in the 1990s: attributable mortality, excess length of hospitalization, and extra costs. Infect Control Hosp Epidemiol. 1999 Nov;20(11):725-30. [DOI] [PubMed] [Google Scholar]
  • 8.Cruse PJ, Foord R. A five-year prospective study of 23,649 surgical wounds. Arch Surg. 1973 Aug;107(2):206-10. [DOI] [PubMed] [Google Scholar]
  • 9.Claesson BE, Holmlund DE. Predictors of intraoperative bacterial contamination and postoperative infection in elective colorectal surgery. J Hosp Infect. 1988 Feb;11(2):127-35. [DOI] [PubMed] [Google Scholar]
  • 10.Gil-Egea MJ, Pi-Sunyer MT, Verdaguer A, Sanz F, Sitges-Serra A, Eleizegui LT. Surgical wound infections: prospective study of 4,468 clean wounds. Infect Control. 1987 Jul;8(7):277-80. [DOI] [PubMed] [Google Scholar]
  • 11.Slaughter MS, Olson MM, Lee JT, Jr, Ward HB. A fifteen-year wound surveillance study after coronary artery bypass. Ann Thorac Surg. 1993 Nov;56(5):1063-8. [DOI] [PubMed] [Google Scholar]
  • 12.Bryan AJ, Lamarra M, Angelini GD, West RR, Breckenridge IM. Median sternotomy wound dehiscence: a retrospective case control study of risk factors and outcome. J R Coll Surg Edinb. 1992 Oct;37(5):305-8. [PubMed] [Google Scholar]
  • 13.Nagachinta T, Stephens M, Reitz B, Polk BF. Risk factors for surgical-wound infection following cardiac surgery. J Infect Dis. 1987 Dec;156(6):967-73. [DOI] [PubMed] [Google Scholar]
  • 14.Olsen MA, Butler AM, Willers DM, Devkota P, Gross GA, Fraser VJ. Risk factors for surgical site infection after low transverse cesarean section. Infect Control Hosp Epidemiol. 2008 Jun;29(6):477-84, discussion:485-6. [DOI] [PubMed] [Google Scholar]
  • 15.Olsen MA, Nepple JJ, Riew KD, Lenke LG, Bridwell KH, Mayfield J, Fraser VJ. Risk factors for surgical site infection following orthopaedic spinal operations. J Bone Joint Surg Am. 2008 Jan;90(1):62-9. [DOI] [PubMed] [Google Scholar]
  • 16.Schwarzkopf R, Chung C, Park JJ, Walsh M, Spivak JM, Steiger D. Effects of perioperative blood product use on surgical site infection following thoracic and lumbar spinal surgery. Spine (Phila Pa 1976). 2010 Feb 1;35(3):340-6. [DOI] [PubMed] [Google Scholar]
  • 17.Pull ter Gunne AF, Skolasky RL, Ross H, van Laarhoven CJ, Cohen DB. Influence of perioperative resuscitation status on postoperative spine surgery complications. Spine J. 2010 Feb;10(2):129-35. Epub 2009 Nov 14. [DOI] [PubMed] [Google Scholar]
  • 18.Halm EA, Wang JJ, Boockvar K, Penrod J, Silberzweig SB, Magaziner J, Koval KJ, Siu AL. The effect of perioperative anemia on clinical and functional outcomes in patients with hip fracture. J Orthop Trauma. 2004 Jul;18(6):369-74. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Carson JL, Terrin ML, Noveck H, Sanders DW, Chaitman BR, Rhoads GG, Nemo G, Dragert K, Beaupre L, Hildebrand K, Macaulay W, Lewis C, Cook DR, Dobbin G, Zakriya KJ, Apple FS, Horney RA, Magaziner J. FOCUS Investigators. Liberal or restrictive transfusion in high-risk patients after hip surgery. N Engl J Med. 2011 Dec 29;365(26):2453-62. Epub 2011 Dec 14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.National Blood Data Resource Center. Report on blood collection and transfusion in the United States in 2001. Bethesda: National Blood Data Resource Center; 2003. [Google Scholar]
  • 21.Talbot TR, D’Agata EM, Brinsko V, Lee B, Speroff T, Schaffner W. Perioperative blood transfusion is predictive of poststernotomy surgical site infection: marker for morbidity or true immunosuppressant? Clin Infect Dis. 2004 May 15;38(10):1378-82. Epub 2004 Apr 28. [DOI] [PubMed] [Google Scholar]
  • 22.Vamvakas EC, Carven JH. Transfusion of white-cell containing allogeneic blood components and postoperative wound infection: effect of confounding factors. Transfus Med. 1998 Mar;8(1):29-36. [DOI] [PubMed] [Google Scholar]
  • 23.Vamvakas EC, Carven JH. Allogeneic blood transfusion, hospital charges, and length of hospitalization: a study of 487 consecutive patients undergoing colorectal cancer resection. Arch Pathol Lab Med. 1998 Feb;122(2):145-51. [PubMed] [Google Scholar]
  • 24.Walz JM, Paterson CA, Seligowski JM, Heard SO. Surgical site infection following bowel surgery: a retrospective analysis of 1446 patients. Arch Surg. 2006 Oct;141(10):1014-8, discussion:1018. [DOI] [PubMed] [Google Scholar]
  • 25.Martin L, Watier H, Vaillant L, Aractingi S. Sjögren’s syndrome and vitiligo in a woman with posttransfusion microchimerism. Am J Med. 2001 Oct 1;111(5):419-21. [DOI] [PubMed] [Google Scholar]
  • 26.Raghavan M, Marik PE. Anemia, allogenic blood transfusion, and immunomodulation in the critically ill. Chest. 2005 Jan;127(1):295-307. [DOI] [PubMed] [Google Scholar]
  • 27.Taylor RW, Manganaro L, O’Brien J, Trottier SJ, Parkar N, Veremakis C. Impact of allogenic packed red blood cell transfusion on nosocomial infection rates in the critically ill patient. Crit Care Med. 2002 Oct;30(10):2249-54. [DOI] [PubMed] [Google Scholar]
  • 28.Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373-83. [DOI] [PubMed] [Google Scholar]
  • 29.Hutchinson TA, Thomas DC, MacGibbon B. Predicting survival in adults with end-stage renal disease: an age equivalence index. Ann Intern Med. 1982 Apr;96(4):417-23. [DOI] [PubMed] [Google Scholar]
  • 30.Liu M, Domen K, Chino N. Comorbidity measures for stroke outcome research: a preliminary study. Arch Phys Med Rehabil. 1997 Feb;78(2):166-72. [DOI] [PubMed] [Google Scholar]
  • 31.Muder RR, Brennen C, Swenson DL, Wagener M. Pneumonia in a long-term care facility. A prospective study of outcome. Arch Intern Med. 1996 Nov 11;156(20):2365-70. [PubMed] [Google Scholar]
  • 32.O’Connor GT, Plume SK, Olmstead EM, Coffin LH, Morton JR, Maloney CT, Nowicki ER, Levy DG, Tryzelaar JF, Hernandez F, Nowicki ER, Levy DG, Tryzelaar JF, Hernandez F, Adrian L, Casey KJ, Bundy D, Soule DN, Marrin CAS, Nugent WC, Charlesworth DC, Clough R, Katz S, Leavitt BJ, Wennberg JE. Northern New England Cardiovascular Disease Study Group. Multivariate prediction of in-hospital mortality associated with coronary artery bypass graft surgery. Circulation. 1992 Jun;85(6):2110-8. [DOI] [PubMed] [Google Scholar]
  • 33.Chaudhry S, Jin L, Meltzer D. Use of a self-report-generated Charlson Comorbidity Index for predicting mortality. Med Care. 2005 Jun;43(6):607-15. [DOI] [PubMed] [Google Scholar]
  • 34.West DW, Satariano WA, Ragland DR, Hiatt RA. Comorbidity and breast cancer survival: a comparison between black and white women. Ann Epidemiol. 1996 Sep;6(5):413-9. [DOI] [PubMed] [Google Scholar]
  • 35.Whitehouse JD, Friedman ND, Kirkland KB, Richardson WJ, Sexton DJ. The impact of surgical-site infections following orthopedic surgery at a community hospital and a university hospital: adverse quality of life, excess length of stay, and extra cost. Infect Control Hosp Epidemiol. 2002 Apr;23(4):183-9. [DOI] [PubMed] [Google Scholar]
  • 36.Goodnough LT, Brecher ME, Kanter MH, AuBuchon JP. Transfusion medicine. Second of two parts—blood conservation. N Engl J Med. 1999 Feb 18;340(7):525-33. [DOI] [PubMed] [Google Scholar]
  • 37.Goodnough LT, Brecher ME, Kanter MH, AuBuchon JP. Transfusion medicine. First of two parts—blood transfusion. N Engl J Med. 1999 Feb 11;340(6):438-47. [DOI] [PubMed] [Google Scholar]
  • 38.Pealer LN, Marfin AA, Petersen LR, Lanciotti RS, Page PL, Stramer SL, Stobierski MG, Signs K, Newman B, Kapoor H, Goodman JL, Chamberland ME. West Nile Virus Transmission Investigation Team. Transmission of West Nile virus through blood transfusion in the United States in 2002. N Engl J Med. 2003 Sep 25;349(13):1236-45. Epub 2003 Sep 18. [DOI] [PubMed] [Google Scholar]
  • 39.Austyn JM. Antigen uptake and presentation by dendritic leukocytes. Semin Immunol. 1992 Aug;4(4):227-36. [PubMed] [Google Scholar]
  • 40.Silliman CC, Boshkov LK, Mehdizadehkashi Z, Elzi DJ, Dickey WO, Podlosky L, Clarke G, Ambruso DR. Transfusion-related acute lung injury: epidemiology and a prospective analysis of etiologic factors. Blood. 2003 Jan 15;101(2):454-62. Epub 2002 Sep 5. [DOI] [PubMed] [Google Scholar]
  • 41.Anderson CB, Brennan D, Keller C, Goss J, Shenoy S, Burton K, Sicard G, Flye MW. Beneficial effects of donor-specific transfusions on long-term renal allograft function. Transplant Proc. 1995 Feb;27(1):991-4. [PubMed] [Google Scholar]
  • 42.Flye MW, Burton K, Mohanakumar T, Brennan D, Keller C, Goss JA, Sicard GA, Anderson CB. Donor-specific transfusions have long-term beneficial effects for human renal allografts. Transplantation. 1995 Dec 27;60(12):1395-401. [DOI] [PubMed] [Google Scholar]
  • 43.Inuzuka S, Koga S, Nishikido M, Miyata Y, Kanda S, Shimokawa I, Tanaka M, Saito Y, Kanetake H. Donor-specific blood transfusion prolongs cardiac allograft survival in rats by low nitric oxide production and elevated serum levels of prostaglandin E(2). Immunol Lett. 2002 Sep 2;83(2):119-24. [DOI] [PubMed] [Google Scholar]
  • 44.Liang J, Yamaguchi Y, Matsuda T, Ohshiro H, Zhang JL, Okabe K, Matsumura F, Ishihara K, Uchino S, Mori K, Yamada S, Ogawa M. Posttransplant infusion of donor-specific blood induces immunological unresponsiveness in rat hepatic allografts. Transplantation. 2000 Nov 15;70(9):1363-71. [DOI] [PubMed] [Google Scholar]
  • 45.Rifle G, Mousson C. Donor-derived hematopoietic cells in organ transplantation: a major step toward allograft tolerance? Transplantation. 2003 May 15;75(9)(Suppl):3S-7S. [DOI] [PubMed] [Google Scholar]
  • 46.van de Watering LM, Hermans J, Houbiers JG, van den Broek PJ, Bouter H, Boer F, Harvey MS, Huysmans HA, Brand A. Beneficial effects of leukocyte depletion of transfused blood on postoperative complications in patients undergoing cardiac surgery: a randomized clinical trial. Circulation. 1998 Feb 17;97(6):562-8. [DOI] [PubMed] [Google Scholar]
  • 47.Edna TH, Bjerkeset T. Association between blood transfusion and infection in injured patients. J Trauma. 1992 Nov;33(5):659-61. [DOI] [PubMed] [Google Scholar]
  • 48.Braga M, Vignali A, Radaelli G, Gianotti L, Di Carlo V. Association between perioperative blood transfusion and postoperative infection in patients having elective operations for gastrointestinal cancer. Eur J Surg. 1992 Oct;158(10):531-6. [PubMed] [Google Scholar]
  • 49.Blajchman MA, Bordin JO. Mechanisms of transfusion-associated immunosuppression. Curr Opin Hematol. 1994 Nov;1(6):457-61. [PubMed] [Google Scholar]
  • 50.Jensen LS, Andersen AJ, Christiansen PM, Hokland P, Juhl CO, Madsen G, Mortensen J, Møller-Nielsen C, Hanberg-Sørensen F, Hokland M. Postoperative infection and natural killer cell function following blood transfusion in patients undergoing elective colorectal surgery. Br J Surg. 1992 Jun;79(6):513-6. [DOI] [PubMed] [Google Scholar]
  • 51.Marik PE, Sibbald WJ. Effect of stored-blood transfusion on oxygen delivery in patients with sepsis. JAMA. 1993 Jun 16;269(23):3024-9. [PubMed] [Google Scholar]
  • 52.Stuart J, Nash GB. Red cell deformability and haematological disorders. Blood Rev. 1990 Sep;4(3):141-7. [DOI] [PubMed] [Google Scholar]
  • 53.Fischer DJ, Torrence NJ, Sprung RJ, Spence DM. Determination of erythrocyte deformability and its correlation to cellular ATP release using microbore tubing with diameters that approximate resistance vessels in vivo. Analyst. 2003 Sep;128(9):1163-8. [DOI] [PubMed] [Google Scholar]
  • 54.Koch CG, Li L, Sessler DI, Figueroa P, Hoeltge GA, Mihaljevic T, Blackstone EH. Duration of red-cell storage and complications after cardiac surgery. N Engl J Med. 2008 Mar 20;358(12):1229-39. [DOI] [PubMed] [Google Scholar]
  • 55.Fakhry SM, Fata P. How low is too low? Cardiac risks with anemia. Crit Care. 2004;8(Suppl 2):S11-4. Epub 2004 Jun 14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Hébert PC, Wells G, Blajchman MA, Marshall J, Martin C, Pagliarello G, Tweeddale M, Schweitzer I, Yetisir E. A multicenter, randomized, controlled clinical trial of transfusion requirements in critical care. Transfusion Requirements in Critical Care Investigators, Canadian Critical Care Trials Group. N Engl J Med. 1999 Feb 11;340(6):409-17. [DOI] [PubMed] [Google Scholar]
  • 57.Nuttall GA, Horlocker TT, Santrach PJ, Oliver WC, Jr, Dekutoski MB, Bryant S. Predictors of blood transfusions in spinal instrumentation and fusion surgery. Spine (Phila Pa 1976). 2000 Mar 1;25(5):596-601. [DOI] [PubMed] [Google Scholar]
  • 58.Nuttall GA, Santrach PJ, Oliver WC, Jr, Horlocker TT, Shaughnessy WJ, Cabanela ME, Bryant S. The predictors of red cell transfusions in total hip arthroplasties. Transfusion. 1996 Feb;36(2):144-9. [DOI] [PubMed] [Google Scholar]

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Disclosure of Potential Conflicts of Interest

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Supporting Data

A table showing the Charlson Comorbidity Index scoring system

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